EFSA Journal 2010; 8 (5):1595

SCIENTIFIC OPINION

Scientific Opinion on Q fever1
EFSA Panel on Animal Health and Welfare (AHAW)2, 3
EFSA Panel on Biological Hazards (BIOHAZ)2, 3 (Chapter 4 on Food Safety)
European Food Safety Authority (EFSA), Parma, Italy

ABSTRACT
Following a request from the European Commission, a scientific opinion was prepared by EFSA‘s
Animal Health and Welfare Panel to determine the magnitude, distribution, impact and significance of
infection and disease in domestic ruminants and humans, risk factors for the maintenance (in domestic
ruminant populations) and spillover (from these populations to humans) of Coxiella burnetii (the
causative agent of Q fever), and control options in domestic ruminant populations. A range of
approaches were used, including an assessment of monitoring/surveillance data, the development of a
simple conceptual model, a critical review of available literature, and several country case studies.
Control options for C. burnetii infection in small ruminants were qualitatively assessed. Infection is
endemic in domestic ruminants in most, if not all, EU member states, however, disease is rare and
impact is limited. In the EU, Q fever is a zoonotic disease with limited public health impact, except
under certain epidemiological circumstances and for particular risk groups. Human cases are often
associated with proximity to small ruminants (particularly at parturition or during abortions) and dry,
windy weather. Currently, there is no clear evidence of an association between bacterial
genotypes/isolates and virulence. A number of longer-term options to control C. burnetii infection in
domestic ruminants were identified; these should be considered in those situations where the public
health risk is considered unacceptable. Some additional options were not considered sustainable for
long-term control, but may have a role in the face of an outbreak. Persistent environmental
contamination may confound animal-based control efforts. Vaccination should be considered a longterm control option, noting that effectiveness may not be observed in the short-term. Antibiotic
treatment of animals is not recommended. There is no conclusive evidence that the consumption of
milk and milk products containing C. burnetii has resulted in clinical Q fever in humans.
KEY WORDS: Q fever, EU, Coxiella burnetii, domestic ruminants, public health, risk factors, control options

1 On request from European Commission, Question No EFSA-Q-2010-00010, adopted on 27 April, 2010 by AHAW Panel
and Question No EFSA-Q-2010-00772 (Chapter 4), adopted on 22 April, 2010 by BIOHAZ.
2 Panel members AHAW: Anette Bøtner, Donald Broom, Marcus G. Doherr, Mariano Domingo, Jörg Hartung, Linda
Keeling, Frank Koenen, Simon More, David Morton, Pascal Oltenacu, Albert Osterhaus, Fulvio Salati, Mo Salman, Moez
Sanaa, James M. Sharp, Jan A. Stegeman, Endre Szücs, Hans-H. Thulke, Philippe Vannier, John Webster and Martin
Wierup. Correspondence: ahaw@efsa.europa.eu.
Panel members BIOHAZ: Olivier Andreoletti, Herbert Budka, Sava Buncic, John D. Collins, John Griffin, Arie Havelaar,
James Hope, Günter Klein, Tine Hald, Winy Messens, James McLauchlin, Christine Mueller-Graf, Christophe NguyenThé, Birgit Noerrung, Miguel Prieto Maradona, Luisa Peixe, Antonia Ricci, John Sofos, John Threlfall, Ivar Vågsholm,
Emmanuel Vanopdenbosch. Correspondence: biohaz@efsa.europa.eu.
3 Acknowledgement: The AHAW Panel wishes to thank the members of the Working Group on Q fever for the preparation
of this opinion: Simon More (Chair), Jan Arend Stegeman, Annie Rodolakis, Hendrik-Jan Roest, Piet Vellema, Richard
Thiéry, Heinrich Neubauer, Wim van der Hoek, Katharina Staerk, Howard Needham (ECDC) and the EFSA staff members
Ana Afonso, Milen Georgiev and Jane Richardson for the support provided to this EFSA scientific output. Thank you also
for the valuable information made available by the Zoonoses task force, the EFSA Animal Health and Welfare network,
Prof. S. Martinov and I. Yordanov.This opinion was the result of a fruitful collaboration with ECDC in relation to public
health aspects. The BIOHAZ Panel wishes to thank the EFSA staff member Bart Goossens for the support provided to
Chapter 4 of this EFSA scientific output.
For citation purposes: EFSA Panel on Animal Health and Welfare (AHAW); Scientific Opinion on Q Fever. EFSA Journal
2010; 8(5):1595. [114 pp.]. doi:10.2903/j.efsa.2010.1595. Available online: www.efsa.europa.eu

© European Food Safety Authority, 2010

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Q fever

SUMMARY
The recent developments in the EU, especially the increase in confirmed human cases of Q fever in the
Netherlands, call for special consideration as regards the risks posed by Q fever for humans and
animals. The European Commission requested further scientific advice and risk assessment, as regards
Q fever in animals. The mandate posed three questions:
to assess the significance of the occurrence of Q fever in the EU Member States for a better
understanding of the scale and distribution of the disease and infection (with the focus on farm
animals and humans)
to assess the risk factors for Q fever occurrence and persistence in animal husbandry and the
related risks for humans, and
to assess the effectiveness and efficiency of disease control options.
An opinion, in response to the mandate, was prepared by the EFSA Panel on Animal Health and
Welfare, with input from EFSA‘s Panel on Biological Hazards (BIOHAZ) and the Zoonoses and
Assessment Methodologies Unit, and in close collaboration with the European Centre for Disease
Prevention and Control (ECDC).
Several approaches were adopted during the preparation of this scientific opinion. An assessment of
the magnitude and distribution of infection and disease in domestic ruminants and in humans was
conducted after considering diagnostic methods for Coxiella burnetii infection (the causal agent of
Q fever) and monitoring/surveillance for C. burnetii infection in different member states of the
European Union (MS). Impact and significance was assessed, based on expert opinion. Several
methods were used to clarify risk factors for maintenance of C. burnetii infection in domestic
ruminants and spillover of infection from domestic ruminants to humans, including the development
of a simple conceptual model, a critical review of available literature, and several country case studies.
Control options for C. burnetii infection in domestic ruminant populations were evaluated, following
the development of a generic framework for the control of infectious diseases, and based on available
data about individual control interventions.
Infection with Coxiella burnetii (the causal agent of Q fever) is endemic in domestic ruminants (cattle,
sheep, goats) in most, if not all, EU MS. Although infection in domestic ruminants is common, disease
is rare. The overall impact of C. burnetii infection on the health of domestic ruminants in EU MS is
limited. In humans, C. burnetii infection is present in most, if not all, EU MS. Q fever is a zoonotic
disease with limited public health impact in the EU, however, in certain epidemiological
circumstances and for particular risk groups the public health impact can be significant. As yet, the
Q fever burden of disease in humans has not been determined.
It seems likely that C. burnetii infection can be maintained in domestic ruminants in a wide range of
husbandry systems. There is considerable uncertainty about the relative importance of risk factors for
maintenance of C. burnetii infection in domestic ruminant populations, and for spillover from
domestic ruminants to humans. Nonetheless, maintenance of C. burnetii infection within farms might
be favoured by persistently infected animals, other animal reservoirs of infection, ticks, husbandry
practices that favour within-herd transmission and/or environmental contamination. Currently, there is
no clear evidence of an association between bacterial genotypes/isolates and virulence. The common
risk factors associated with spillover of infection from domestic ruminants to humans in different EU
MS include an association between human infection and small ruminants (sheep and goats), an
indication of proximity between animals and human populations, particularly in association with
parturition in animals (and to abortions, in the case of goats), and specific climatic conditions, in
particular dry, windy weather. In humans, the risk of exposure to C. burnetii is increased, either
following close contact to animals infected with C. burnetii, or following community-based exposure
(caused by an elevation of C. burnetii in the wider environment following release and dissemination
from infected animal hosts). There is no conclusive evidence in support of a link between an increased
density of animals and/or farms and spillover of C. burnetii from infected farms to humans. The
factors leading to outbreaks of Q fever in the human population are not fully understood.

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Regarding disease control, the opinion focused on control options applicable to domestic ruminants,
and on the effectiveness of these options to reduce within-herd transmission, between-herd spread
(each in domestic ruminant populations), and/or the spillover of infection from domestic ruminants to
humans. For almost all of the control options, there is a medium to high level of uncertainty associated
with estimates of control effectiveness, as little relevant published information is available. It is likely
that control methods would need to be used in combination. There is variation in the sustainability of
the assessed control options. A number of long-term control options were identified, including
preventive vaccination, manure management, changes to farm characteristics, wool shearing
management, a segregated lambing/kidding area, removal of risk material, visitor ban, control of other
animal reservoirs and tick control. All but the latter two relate specifically to small ruminants. These
options are ranked according to effectiveness, as assessed by expert opinion, in reducing spillover
from domestic ruminants to humans. Several options were not considered sustainable for long-term
control, but may have a role in the face of an outbreak, including the culling of pregnant animals, a
temporary breeding ban, stamping out, identification and culling of shedders, control of animal
movements and stand still. These options all relate specifically to small ruminants. C. burnetii is
highly resistant in the environment; consequently, persistent environmental contamination is a matter
of concern. Vaccination can be used both to reduce the risk of future outbreaks (preventive
vaccination) and in the face of an outbreak (outbreak vaccination), noting that preventive vaccination
is more effective than outbreak vaccination, phase I is more effective than phase II vaccination,
vaccination is more effective in non-infected than infected animals, vaccination does not appear to be
effective if used in pregnant females, and effectiveness may not be observed in the short-term.
The Animal Health and Welfare Panel recommended harmonized field and laboratory data collection
about C. burnetii infection in animals in EU MS, to allow comparison of prevalence/incidence
estimates over time and between countries. Further, there is a need to strengthen systems to promote
rapid identification and reporting of Q fever outbreaks in animals (abortion episodes). Consideration
should be given for support of early information exchange between veterinarians and public health
counterparts regarding potential events with zoonotic potential, including Q fever. Further studies on
the estimation of Q fever burden of disease in humans are needed. Prevalence and incidence studies in
domestic ruminants should place emphasis on small ruminants, rather than cattle, to provide a clearer
picture of the risk of exposure for humans. Further investigations and research are needed to clarify
the relationship between genotype and virulence, the molecular basis for virulence, and the
relationship between mice models and virulence studies in domestic ruminants, determine the host
specificity of different bacterial isolates, identify factors influencing the maintenance of infection,
including an improved understanding of transmission pathways, quantify the number of bacteria
excreted under different conditions, quantify survival of C. burnetii in the environment, clarify the role
of environmental contamination and climatic factors in the spillover of infection from animals to
humans, and clarify the trade off between farm density and farm size in the maintenance and spillover
of infection. Future investigations are needed to objectively assess the effectiveness of control options
for C. burnetii infection in domestic ruminant populations. Assessment should focus on relevant
epidemiological parameters, including rates of within-herd transmission, between-herd spread and
spillover from animal populations to humans. Control options should generally be used in
combination, given that within-herd transmission, between-herd spread and spillover to humans are
each likely to involve more than one transmission pathway, and that no control option is likely to be
completely effective in limiting within-herd transmission, between-herd spread and spillover to
humans. Longer-term options to control C. burnetii infection in domestic ruminants should be
considered in those situations where the public health risk is considered unacceptable. Control options
where effectiveness at reducing spillover was assessed as either high or medium include preventive
vaccination, appropriate manure management, changes to farm characteristics, wool shearing
management, segregated lambing/kidding area, removal of risk material and visitor ban. Control
options to address proximity between humans and small ruminants, particularly around the time of
lambing/kidding, would be expected to meaningfully contribute to a reduction in spillover from animal
populations to humans. There is a need to build awareness among farmers and veterinarians of
C. burnetii infection in farmed ruminants, including risk factors for spillover from domestic ruminant
populations to humans. Short term options such as the culling of pregnant animals, a temporary
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breeding ban, stamping out, identification and culling of shedders, control of animal movements and
stand still could be used to reduce shedding from infected animals. However, other options (including
preventive vaccination, manure management, wool shearing management, segregated lambing/kidding
area, removal of risk material) should be considered to reduce human exposure through environmental
contamination. Vaccination should be considered as a long-term control option. In order to better
assess vaccine efficacy, it is recommended that field and experimental data are gathered, to improve
our understanding of the epidemiology of C. burnetii infection in, and between, infected flocks, both
prior to and following vaccination. Antibiotic treatment is not effective in substantially reducing either
the level or duration of bacterial shedding in domestic ruminant populations; therefore the use of
antibiotics cannot be recommended.
The widespread distribution of C. burnetii in food producing animals and its occurrence in the milk
supply necessitates questioning the role of food as a vehicle for the transmission of this zoonotic
bacterium to humans. C. burnetii infection in occupationally or otherwise exposed people is mainly
due to inhalation of infected aerosols rather than consumption of contaminated food (e.g. dairy, meat)
products. However, C. burnetii is excreted in milk of infected animals (cattle, sheep and goats) for
variable periods during lactation irrespective whether these animals are showing clinical signs or not
and in addition, milk can be contaminated with C. burnetii by faecal materials or from sites of
infection in the periparturient and/or lactating animal. Consumption of raw milk and raw milk
products represent a relatively greater risk of human exposure to C. burnetii than the consumption of
both milk and dairy products made with milk that has undergone appropriate heat treatment. There are
epidemiological indications that consumption of milk and/or milk products containing C. burnetii has
been associated with sero-conversion in humans. However, there is no conclusive evidence that the
consumption of milk and milk products containing C. burnetii has resulted in clinical Q fever in
humans.
The scientific opinion was adopted by the Scientific Panel on Animal Health and Welfare (AHAW) on
27 April 2010. Chapter 4 (focusing on food safety issues) and related conclusions were adopted by the
Scientific Panel on Biological Hazards (BIOHAZ) on 22 April 2010.

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TABLE OF CONTENTS
Abstract .................................................................................................................................................... 1
Summary .................................................................................................................................................. 2
Table of contents ...................................................................................................................................... 5
List of Tables ............................................................................................................................................ 6
List of Figures .......................................................................................................................................... 6
Background as provided by European Commission ................................................................................ 7
Terms of reference as provided by European Commission ...................................................................... 8
Assessment ............................................................................................................................................... 9
1. Introduction ..................................................................................................................................... 9
1.1.
Context .................................................................................................................................... 9
1.2.
Approaches ............................................................................................................................. 9
1.2.1. Magnitude and distribution of infection and disease .......................................................... 9
1.2.2. Risk factors for Q fever maintenance and spillover ......................................................... 11
1.2.3. Control options in domestic ruminant populations ........................................................... 11
2. Magnitude and distribution of Q fever in the EU Member States ................................................. 12
2.1.
Magnitude and distribution of C. burnetii infection and Q fever in domestic ruminant ....... 12
2.1.1. Diagnosis of C. burnetii infection .................................................................................... 12
2.1.2. Q fever monitoring and surveillance ................................................................................ 16
2.1.3. Infection and disease information in domestic ruminants ................................................ 20
2.1.4. Interpretation/evaluation of the surveillance data ............................................................. 24
2.2.
Magnitude and distribution of Q fever in humans ................................................................ 25
2.2.1. Q fever diagnosis in humans ............................................................................................ 25
2.2.2. Q fever monitoring and surveillance in humans ............................................................... 26
2.2.3. Infection and disease information in humans ................................................................... 28
2.2.4. Interpretation/evaluation of the surveillance data ............................................................. 31
2.3.
Significance and impact of Q fever....................................................................................... 32
2.3.1. Significance and impact on public health ......................................................................... 32
2.3.2. Significance and impact on animal health ........................................................................ 37
3. Risk factors for C. burnetii maintenance and spillover ................................................................. 38
3.1.
Transmission routes .............................................................................................................. 38
3.2.
A review of published literature............................................................................................ 39
3.2.1. Factors affecting the maintenance of C. burnetii infection in domestic ruminants .......... 39
3.2.2. Factors affecting the spillover of C. burnetii from domestic ruminants to humans ......... 42
3.3.
Country case studies ............................................................................................................. 44
3.3.1. Bulgaria ............................................................................................................................ 44
3.3.2. France ............................................................................................................................... 48
3.3.3. Germany ........................................................................................................................... 52
3.3.4. The Netherlands................................................................................................................ 55
4. Food safety aspects ........................................................................................................................ 61
4.1.
Introduction ........................................................................................................................... 61
4.2.
Risk factors for foodborne C. burnetii infection ................................................................... 62
4.3.
Milk and dairy products as a source of C. burnetii for the consumer ................................... 64
4.4.
Heat treatment as a means of controlling C. burnetii in milk and dairy products. ................ 65
5. Control options in domestic ruminant populations ........................................................................ 66
5.1.
Infectious disease epidemiology (concepts and applications) .............................................. 66
5.2.
Available control strategies................................................................................................... 67
5.2.1. The importance of surveillance/monitoring and case ascertainment ................................ 67
5.2.2. General considerations ..................................................................................................... 68
5.2.3. Specific control options .................................................................................................... 69
5.2.4. Effectiveness and sustainability of potential control options ........................................... 75
Conclusions and recommendations ........................................................................................................ 80
References .............................................................................................................................................. 85
Appendices ............................................................................................................................................. 98
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Appendix A - Literature Search ............................................................................................................. 98
Appendix B - Ad hoc EFSA consultation (2010) ................................................................................. 100
Appendix C - Infection and disease information .................................................................................. 102
Glossary and abbreviations .................................................................................................................. 113

LIST OF TABLES
Table 1: Overview of laboratory tests used for diagnosis of C. burnetii infection in domestic ruminants
............................................................................................................................................................... 15
Table 2: The notification status of Q fever in European countries, in domestic ruminants .................. 17
Table 3: National reference laboratories for C burnetii diagnosis in animals in EU MS ...................... 18
Table 4: Monitoring/surveillance for C. burnetii infection/Q fever in domestic ruminants in European
countries ................................................................................................................................................ 19
Table 5: Prevalence of C. burnetii (animal and herd level) in domestic ruminants in Europe and
neighbouring countries. ......................................................................................................................... 21
Table 6: EU harmonised Q fever case definition (adapted from CD 2008/426/EC) ............................. 26
Table 7: Q fever - EU surveillance systems overview in humans (from ECDC Annual Epidemiological
Report 2009) .......................................................................................................................................... 27
Table 8: Reported confirmed Q fever cases in humans reported to the ECDC, 2007-2008.................. 28
Table 9: Prevalence for C burnetii in human populations in Europe and neighbouring countries........ 30
Table 10: Seroprevalence of C burnetii in occupational groups and the general populations............... 34
Table 11: Human outbreaks of Q fever in European countries ............................................................. 35
Table 12: Longest observed duration of excretion during the follow up of naturally or experimentally
infected animals (from Arricau-Bouvery, 2005) ................................................................................... 41
Table 13 : Overview of legislation concerning Q-fever in the Netherlands .......................................... 59
Table 14: Effectiveness, sustainability of potential control options for C burnetii infection in domestic
ruminant populations ............................................................................................................................. 77
Table 15 : Number of laboratory tests conducted in European countries for C. burnetii in domestic
ruminants and number (%) positive, by species, based on data collected in the EFSA/ECDC zoonoses
database about 2006-2008 and collected from ad hoc EFSA consultation (2010) about data in 2009 102
Table 16 : Details of tests conducted in European countries during 2009 as part of a clinical
investigation for C. burnetii in domestic ruminants, by species and country, based on data collected
from ad hoc EFSA consultation (2010) .............................................................................................. 104
Table 17 : Details of tests conducted in European countries during 2009 as part of a monitoring and/or
surveillance activities for C. burnetii in domestic ruminants, by species and country, based on data
collected from ad hoc EFSA consultation (2010) ............................................................................... 107
Table 18: Selected number of human outbreaks of Q fever in Germany ............................................ 109
Table 19: C. burnetii infection in animals -Germany.......................................................................... 111

LIST OF FIGURES
Figure 1: European countries where clinical investigation activities for Q fever in domestic ruminants
were conducted in 2009.
20
Figure 2: European countries where monitoring and/or surveillance investigation activities for
Coxiella burnetii infection in domestic ruminants were conducted in 2009
21
Figure 3: Transmission routes for Coxiella burnetii infection in humans and animals (adapted from
Roest 2010)
38
Figure 4: A conceptual model for maintenance of C. burnetii infection in domestic ruminant
populations, and spillover from animals to humans (A, animal, H, human)
39

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BACKGROUND AS PROVIDED BY EUROPEAN COMMISSION
Q fever is a highly contagious zoonotic disease caused by the pathogen Coxiella burnetii which is
commonly present in all countries worldwide, except in New Zealand. It is listed within the category
of multiple species diseases in the OIE (World Organisation for Animal Health) list (Article 1.2.3. of
the OIE terrestrial Animal Health Code) and many domesticated and wild animals including
mammals, birds, reptiles and arthropods can be carriers of the pathogen but cattle, goats and sheep are
the main reservoirs. In these animals, infection is mostly asymptomatic except for the increase of
abortions or stillbirths.
Both symptomatic and asymptomatic animals shed C. burnetii in large quantities when giving birth.
Shedding can also occur in faeces, milk and urine. C. burnetii is highly resistant to environmental
conditions and can be resistant to heat, drying, and many common disinfectants. These features enable
the bacteria to survive for long periods in the environment and to be spread by the wind. Ticks may be
important in transmission among wildlife, and can also spread infections to domesticated ruminants.
Little is known about the therapeutical treatment of ruminants or other domestic animals. Prophylactic
antibiotic treatment is sometimes recommended to reduce the risk of abortion. Antibiotics may
suppress rather than eliminate infections. Vaccines are available and may prevent infections in calves,
decrease shedding of organisms and improve fertility in infected animals. They do not eliminate
shedding of the organism. As a general rule, in an infected flock, isolating infected pregnant animals
and burning or burying the reproductive membranes and placenta can decrease transmission.
In humans, Q fever occurs in either an acute form (pneumonia, hepatitis) or a severe chronic form
(endocarditis) following an early infection that may have passed unnoticed. In rare cases, Q fever can
be fatal, although the disease is usually treatable with antibiotics. Most human cases are associated
with exposure to ruminants, particularly when the animals have given birth. Human outbreaks
generally involve farmers or other occupationally exposed people (veterinarians, slaughterhouse
personnel). Humans are mainly infected via aerosols, but transmission may also occur by the ingestion
of unpasteurised milk or other contaminated material.
In the EU, there are no harmonized rules or recommendations for the monitoring and reporting of
Q fever in animals. Q fever is not explicitly listed in Annex I to Directive 2003/99/EC of the European
Parliament and of the Council on the monitoring of zoonoses and zoonotic agents, amending Council
Decision 90/424/EEC and repealing Council Directive 92/117/EEC.
Q fever (in humans) is listed in Annex I of Commission Decision 2000/96/EC of 22 December 1999
on the communicable diseases to be progressively covered by the Community network under Decision
No 2119/98/EC of the European Parliament and of the Council. For the communicable diseases and
special health issues listed in this Annex, epidemiological surveillance within the Community network
is to be performed by the standardised collection and analysis of data in a way that is to be determined
for each communicable disease and special health issue when specific surveillance networks are put in
place.
Disease control measures are normally taken on national, regional or even farm level. Currently,
EFSA is working on a guidance document for the harmonized reporting of Q fever and rabies. The
outcome of this work should be available by the end of this year.
As regards the infection in animals, the information provided by the EU Member States in the context
of Directive 2003/99/EC on Q fever in animals for the years 2008 (18 EU MS's) and 2007 (17 EU
MS's) show that the proportion of reported positive cases in cattle, sheep and goats increased from
7.4% to 10.0% in 2008 at the EU level. The highest proportion of positive cases was reported for
goats: 9.7% and 15.7% in 2007 and 2008, respectively. In particular, the Netherlands reported a threefold increase in 2008 from 9.5% to 31.9%. The proportion of positive cases in sheep was 6.3% in 2008
and 7.9% in 2007.

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In the EU Member States, Q fever appears to be present in cattle, sheep and goat holdings.
Nevertheless, human cases of Q fever were rarely known until 2007. In 2008, a total of 1554
confirmed cases of Q fever were reported in the EU. This figure represents a 165.5% increase
compared with the number of confirmed cases reported in 2007. The Netherlands and Germany
accounted for the majority of this increase. In the Netherlands, for the year 2009, the number of human
cases appears to have already doubled to almost 2300.
It is not clear what has caused this major increase of reported human outbreaks in the Netherlands. It
appears that the majority of the human cases are not linked to farm-visits or occupational exposure.
The geographical locations of the human cases indicate that there might be a connection with the
presence of dairy goat holdings in the area, where this particular type of milk production has
developed rapidly over the past decade.
In response to this unusually large number of human cases, special preventive and control measures
have been taken to control Q fever in the Netherlands, in particular in dairy goats and dairy sheep:
The culling of all pregnant animals and infected male animals on infected farms;
Q fever in 2010, vaccination will be compulsory nationwide;
all dairy goat and dairy sheep farms are obliged to participate in a regular milk test for
Q fever;
Special measures are imposed on farms where the bacterium is found in milk, such as
restrictions on movements of animals and compulsory composting of manure.
The recent developments in the EU, especially in the Netherlands call for special consideration as
regards the risks posed by Q fever for humans and animals. The Commission is in need of further
scientific advice and risk assessment, as regards Q fever in animals.

TERMS OF REFERENCE AS PROVIDED BY EUROPEAN COMMISSION
In view of the above, and in accordance with Article 29 of Regulation (EC) 178/2002, the Commission
asks EFSA for a scientific opinion and specifically:

1. to assess the significance of the occurrence of Q fever in the EU Member States for a better
understanding of the scale and distribution of the disease and infection (with the focus on
farm animals and humans);

2. to assess the risk factors for Q fever occurrence and persistence in animal husbandry, and the
related risks for humans, taking into account at least the presence and density of susceptible
livestock and the type of husbandry in which they are kept;

3. to assess the effectiveness and efficiency of disease control options such as vaccination,
pharmaceutical treatments, establishing animal movement restrictions, the culling of animals,
etcetera.

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ASSESSMENT
1.

Introduction
1.1.

Context

Q fever has emerged as an important public health problem in the Netherlands. In May 2007, the first
community Q fever outbreak was reported around a single village in the province of Noord-Brabant
(Schimmer et al., 2010). Subsequently, human outbreaks of unprecedented size have occurred in the
Netherlands during 2007 (Karagiannis et al., 2007), 2008 (Schimmer et al., 2008) and 2009
(Schimmer et al., 2009). Further, there is early evidence of ongoing transmission of Coxiella burnetii
(the causative agent of Q fever) to humans in 2010 (van Duynhoven et al., 2010).
In response to these public health concerns, the European Commission has sought scientific advice
from the European Food Safety Authority. The current EFSA report focuses on three broad areas, to
address the above-mentioned terms of reference:
Chapter 2: The magnitude and distribution of both infection and disease, and associated
impact and significance, in human and animal populations in Europe; the focus regarding
animal population was on domestic ruminants (cattle, sheep and goats).
Chapters 3: Risk factors for C. burnetii maintenance of infection in domestic ruminants, and
spillover of infection to humans. Risk factors relating to food safety are addressed in Chapter
4; and
Chapter 5: Potential animal-focused control options, to limit adverse impact on both animal
health (reducing within-herd transmission, reducing between-herd spread) and public health
(reducing spillover to humans), assessed on the basis of effectiveness, certainty with respect to
this estimate, sustainability and limitations. Control options relating to food safety are
addressed in Chapter 4.
This Chapter 4 and conclusions and recommendations related with food safety have been adopted by
EFSA-BIOHAZ Panel.
1.2.

Approaches

Several approaches were adopted during the preparation of this scientific opinion, after considering
important constraints, as discussed below. The drafting of this opinion was substantially constrained
by the time available which limited the choices of methodologies that could be applied. In particular it
was not possible to complete a formal systematic review of the literature and meta analysis of risk
factors and control options.
1.2.1.

Magnitude and distribution of infection and disease

A number of important constraints were identified during project design, as follows:
o In the EU, there are no harmonized rules or recommendations for either monitoring or
reporting of C. burnetii infection and Q fever in animals. Further, comparability of data
between EU MS will be affected by variations in regulatory aspects (including case
definitions), laboratory capacity and monitoring/surveillance intensity. These concerns are
more problematic for C. burnetii infection and Q fever in animals compared to humans; and
o

In its current form, EU-level data (as compiled in the EFSA/ECDC zoonoses database) needs
to be interpreted with considerable care, for a range of reasons including incomplete and
uneven reporting, the use of inconsistent case definitions, and difficulties in distinguishing
active and passive data collection.

EFSA Journal 2010; 8 (5):1595

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Q fever

After considering each of the above-mentioned concerns, this opinion has utilised the following
methodology to determine the magnitude and distribution of infection and disease in both domestic
ruminants and humans:
A brief review of the diagnosis of C. burnetii, based on a review of the published literature,
and a recent report commissioned by EFSA under Article 36 (Sidi-Boumedine et al., 2010);
A descriptive assessment of monitoring and surveillance for C. burnetii infection in different
EU MS. For animals, this was based on an evaluation of notification, laboratory capacity and
monitoring/surveillance intensity. A range of data sources were used, including the recent
Article 36 report (Sidi-Boumedine et al., 2010), monitoring/surveillance data collected from
the annual EFSA/ECDC Zoonoses Reports for 2006 to 2008 (EFSA/ECDC, 2007, 2009,
2010), and feedback from an ad hoc EFSA consultation in 2010 of C. burnetii testing that was
conducted in EU MS during 2009. Additional information from WG members was also taken
into account. For humans, a review was conducted of notification (including case definition)
and monitoring/surveillance programmes in EU MS.
Insights into the magnitude and distribution of infection and disease. For animals, this was
based on an understanding of testing intensity (irrespective of whether the tests were
conducted in association with active or passive data collection), of clinical investigation (a
disease event in animals that was initially triggered by passive data collection), and of animaland herd-level seroprevalence (active data collection). For the first of these two points [testing
intensity, clinical investigation], data were obtained from the annual EFSA/ECDC Zoonoses
Reports for 2006 to 2008 (EFSA/ECDC, 2007, 2009, 2010) and from feedback from an ad hoc
EFSA consultation in 2010 of C. burnetii testing that was conducted in EU MS during 2009
(the questionnaire is included in appendix D, responses were received from 24 of 29 countries
[27 EU MS, plus Norway and Switzerland]). For the final point [seroprevalence], an earlier
review (Arricau-Bouvery and Rodolakis, 2005) was updated after considering all relevant
literature published after 2004 (the literature search protocol is included in appendix A). For
humans, an analysis was undertaken of data collected under the European Surveillance
System. Note that Q fever incidence in human populations for 2009 was not available entirely
at the time of drafting of this opinion.
A critical evaluation of impact and significance. The evaluation of impact and significance of
C. burnetii infection on human and on animal health in EU MS was prepared, drawing on
expert opinion, and after considering each of the issues listed previously, including diagnosis,
monitoring and surveillance, and estimates of magnitude and distribution. The impact of
C. burnetii infection on other issues, such as the economic impact following the imposition of
control options by authorities was not considered. Relevant literature was also considered. A
summary of human outbreaks was prepared, updating an earlier review (Arricau-Bouvery and
Rodolakis, 2005) with all relevant literature published after 2004.
The first term of reference (significance of the occurrence of infection and disease, for both
domestic ruminants and humans) was addressed, after considering:
A brief review of the diagnosis of C. burnetii infection,
A descriptive assessment of measures of monitoring/surveillance of C. burnetii infection in
different MS,
Insights into the magnitude and distribution of infection and disease, and
A critical qualitative evaluation of impact and significance.

EFSA Journal 2010; 8 (5):1595

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Q fever

1.2.2.

Risk factors for Q fever maintenance and spillover

A number of important constraints were identified during project design, as follows:
There is considerable variation in the degree (depth, intensity) to which reported outbreak
investigations have been conducted, both in terms of epidemiological methods and laboratory
support;
Risk factor identification/assessment has generally been conducted using qualitative methods,
including implication on the basis of association and consistency with previous reports. The
level of scientific certainty associated with study conclusions is often relatively low; and
The published literature on Q fever outbreaks (and associated risk factors) is fragmented, with
a particular focus on the large and the unusual outbreaks.
After considering each of the above-mentioned concerns, this opinion has utilised the following
methodology:
The development of a simple conceptual model, separately highlighting the maintenance of
infection in animal populations (focusing on domestic ruminants), and the spillover of
infection from animal populations to humans through a process of amplification, transmission
and exposure;
A critical review of available literature, identifying risk factors for C. burnetii maintenance
and for spillover. Limits to the literature search are presented in Appendix A; and
Several country case studies (overview, magnitude and distribution, risk factors for
maintenance and spillover, control options, implications/lessons learned), based on a detailed
review of relevant published literature, and based on expert knowledge and opinion.
The second term of reference (risk factors for Q fever maintenance and spillover) was addressed,
after considering:
The development of a simple conceptual model;
A critical review of available literature; and
Several country case studies.
1.2.3.

Control options in domestic ruminant populations

The third TOR requested the assessment of possible options to control the maintenance of infection in
domestic ruminants and spillover from animal to human populations. A number of important
constraints were identified during project design, as follows:
There is limited published information about animal-based control options adopted in
response to outbreaks of disease in humans;
With most outbreaks, there has been little to no robust evaluation of control effectiveness.
Further, available information is rarely quantitative; and
The published literature on Q fever outbreaks (and associated control options) is fragmented,
with a particular focus on the large and the unusual.
After considering each of the above-mentioned concerns, this opinion has utilised the following
methodology:

EFSA Journal 2010; 8 (5):1595

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Q fever

The development of a generic framework for the control of infectious diseases, based on a
brief review of concepts and applications in infectious disease epidemiology. This framework
was then used as the basis for a critical evaluation of available control options, as outlined
below. Further, control options focused specifically on small ruminants (goats, sheep), given
that cattle appear to have a very minor role in the spillover of C. burnetii infection from
domestic ruminants to humans;
A critical evaluation of available control options, based on expert opinion within the WG,
after considering all available information in both the published and grey literature. For each
option, each of the following were undertaken:
o

A description;

o

A qualitative assessment of effectiveness (high, very effective; medium, moderately
effective; low, very limited effect; none, no effect):
To influence animal health through reduced within-herd transmission and between-herd
spread;
To influence spillover from domestic ruminant populations to humans;

o

The qualitative assessment of the level of uncertainty associated with each of these estimates
of effectiveness:
High: Scarce or no data available; evidence provided in unpublished reports, or few
observations and personal communications, and/or authors‘ or experts‘ conclusions vary
considerably
Medium: Some or only incomplete data available; evidence provided in small number of
references; authors‘ or experts‘ conclusions vary, or limited evidence from field
observations, or solid and complete data available from other species which can be
extrapolated to the species being considered
Low: Solid and complete data available; strong evidence in multiple references with most
authors coming to the same conclusions, or considerable and consistent experience from
field observations.

o

A qualitative assessment of sustainability (high, sustainable in the long-term; medium,
sustainable only in the short-to-medium term; low, sustainable only in the short term.); and

o

Associated limitations.

The third term of reference (effectiveness and efficiency of disease control options in farmed
animal populations) was addressed, after considering:
The development of a generic framework for the control of infectious diseases; and
A critical evaluation of available control options.
2.

Magnitude and distribution of Q fever in the EU Member States
2.1.

Magnitude and distribution of C. burnetii infection and Q fever in domestic ruminant
2.1.1.

Diagnosis of C. burnetii infection

Several assays have been described for the diagnosis of C. burnetii in animals, including both direct
identification of the agent and serological testing (OIE, 2009; Table 1).
EFSA Journal 2010; 8 (5):1595

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Q fever

Direct identification of the agent
Samples should be collected from aborted fetuses, placenta and vaginal discharges soon after abortion
or parturition. Milk (bulk tank milk; milk or colostrum from individual cows), and faeces samples can
also be taken. Conventional staining techniques (Stamp, Gimenez, Macchiavello, Giemsa and
modified Koster) are available within the context of the diagnostic of abortion and are used on tissues
from fetus or placenta and on vaginal discharge. However these tests have low diagnostic sensitivities
and specificities. Attention must be taken in the interpretation of the results as, microscopically,
C. burnetii can be confused with Chlamydophila abortus or Brucella spp.
Isolation of C. burnetii can be done by cell or embryonated chicken egg culture. Such isolation is
possible when microscopic examination indicates a large number of C. burnetii and a low level of
contamination. However, such methods are labour intensive and are not usually used in routine
diagnostics laboratories. In addition, level 3 containment facilities are required. With heavily
contaminated samples, such as placentas, vaginal discharges, faeces or milk, the inoculation of
laboratory animals may be necessary. Mice and guinea pigs are the most appropriate, but infected
animals also have to be manipulated in level 3 biocontainment facilities.
Detection of C. burnetii can also be achieved by immunohistochemistry (IHC). Immunohistology may
be used with paraffin-embedded tissues or on acetone fixed smears (Raoult et al., 1994a). The method
uses either indirect immunofluorescence or an immunoperoxidase assay, using polyclonal C. burnetii
antibodies (either a well characterized antiserum of human origin or a specific antiserum produced in
either rabbits or guinea pigs). An anti-species (human, rabbit or guinea pig) anti-IgG conjugate labeled
with Fluorescein isothiocyanate (FITC) or peroxidase is then used to visualize the bacteria. No
specific antibodies for immunohistochemistry are commercially available (OIE, 2009).
Currently, the polymerase chain reaction (PCR) is one of the most analytically sensitive and rapid
means for both the direct detection of C. burnetii and the identification of shedders. PCR can be used
on a wide range of samples (vaginal discharge, abortion material, faeces and milk [bulk or
individual]). It has become increasingly common in diagnostic laboratories (Berri et al., 2000; Nicollet
and Valognes, 2007). The level of detection of conventional PCR is related to the sample under
investigation (1–500 bacteria/ml of milk; 1 bacteria/mg of faeces). Several target genes have been
used, such as the multicopy insertion sequence (IS1111) or single copy genes encoding various
proteins (e.g dismutase [sodB]; com1 encoding a 27 kDa outer membrane protein; heat shock proteins
[htpA and htpB]; isocitrate dehydrogenase [icd]; macrophage infectivity potentiator protein [cbmip]).
Real-time PCR techniques have also been described (Kim et al., 2005; Klee et al., 2006; Stemmler and
Meyer, 2002). For routine diagnostics, it is widely accepted that real-time PCR technology is
preferable to conventional gel-based detection methods. It allows high sample throughput, has a
reduced potential for carry-over contamination and is best suited for quantification of C. burnetii in
biological samples. As with conventional PCR, various target genes are used, including IS1111, com1
and icd. Quantitative PCR kits are now commercially available.
Several typing methods have been used for the characterisation of C. burnetii strains, including
restriction endonucleae of genomic DNA (Hendrix et al., 1991), PFGE (pulsed-field gel
electrophoresis) (Heinzen et al., 1990; Jager et al., 1998), and sequence and/or PCR-RFLP (restriction
fragment length polymorphism) analysis of icd, com1 and mucZ genes. More recently, two PCR-based
typing methods have been described, MLVA (multi-locus variable number of tandem repeats analysis)
(Arricau-Bouvery et al., 2006; Svraka et al., 2006) and multispacer sequence typing (MST)
(Glazunova et al., 2005) that each permit the typing of C. burnetii without the need for isolation of the
organism. To date, MLVA and MST are considered to be the most discriminating methods for
C. burnetii, allowing the identification of up to 36 distinct genotypes. Moreover, databases have been
established (http://minisatellites.u-psud.fr/MLVAnet/ and http://ifr48.timone.univ-mrs.fr for MLVA
and MST, respectively). The availability of such databases allows for easy interlaboratory
comparisons, leading to a better understanding of different C. burnetii isolates. Furthermore, their use
in the characterisation of field samples or isolates is increasing (Chmielewski et al., 2009; Klaassen
EFSA Journal 2010; 8 (5):1595

13

Q fever

et al., 2009), and efforts to produce a standardised scheme for MLVA (based on common decisions for
allele calling and marker panels) are in progress and should be available in the near future. These tools
will be very useful for epidemiological investigation, particularly toclarify linkages regarding source
of infection.
Serological testing
Although there is no officially (OIE) designated serological test for Q fever, the complement fixation
(CFT) was considered the reference test for historical reasons. However, there is increasing use of
indirect immunofluorescence assay (IFA) and ELISAs (commercial and in-house assays). Serological
assays are suitable for screening herds, but interpretation at the individual animal level can be difficult.
Indeed, animals may remain seropositive for several years following an acute infection, some animals
may shed C. burnetii and pose a risk for infection prior to the development of antibodies, and some
infected animals seem not to seroconvert. Three ELISA commercial kits for the diagnosis of Q fever
in ruminants are currently available. Comparative analyses of available serological methods has been
conducted during ring trials assessments as part of a EU-funded, Framework 6 project (MedVetNet; a
European network of excellence working for the prevention and control of zoonoses and food borne
diseases; www.medvetnet.org). The IFA and commercially available ELISAs were each reproducible,
with comparable diagnostic sensitivity. In contrast, the diagnostic sensitivity of the CFT was highly
variable (Roest et al., 2009). The analytical sensitivity of the ELISA was found to be 8-16 times higher
than that of the best CFTs (Roest et al., 2009). Based on recent work, it was found that two
commercial ELISAs can display different diagnostic sensitivities (81 and 95%, respectively) using a
panel of sera from cattle, goat and sheep (Kittelberger et al., 2009). ELISA tests showed higher
diagnostic sensitivities that the CFT. An ELISA test based on antigens of C. burnetii isolated from
ruminants was found to have a higher diagnostic sensitivity than ELISAs based on antigens from the
Nine Mile reference strain isolated from ticks, as assessed on goat sera, and may allow premature
detection of infection (Rousset et al., unpublished).
Serological testing is useful in clarifying the infection status in herds but provides less certainty about
the infection status of individuals (Kennerman et al., 2010). A seronegative result does not provide
assurance that the animal is not infected. Indeed, this state may be associated with both early and longterm C. burnetii infection. In humans, tests are available (based on detection of antibodies to phase I
and phase II antigens) to distinguish acute and chronic infection (see section 2.2.1). Such tests are not
yet available for animals. Serological methods do not allow the identification of C. burnetii-shedding
animals (Rodolakis, 2006; Rousset 2009). Currently, there is no serological test which can distinguish
between vaccinated and naturally infected animals, although skin tests are recently being developed to
select negative animals for vaccination (Guatteo et al., unpublished).

EFSA Journal 2010; 8 (5):1595

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Q fever

Table 1: Overview of laboratory tests used for diagnosis of C. burnetii infection in domestic
ruminants
Detects
Direct
Culture

Analytical
Se

viable
bacteria

Staining

bacteria

IHC

bacteria
in situ

PCR

DNA

Serology
CFT

Ab

ELISA

Ab

IFA

Ab

Comparative
Se

Comparative
Sp

Used for

Remarks

Culture
<staining
Staining <
IHC
IHC << PCR

Culture <
staining
Staining <
IHC
IHC << PCR

Research/
Clinical
investigation
Clinical
investigation
Clinical
investigation

Pathology diagnosis,
skills are important.

Clinical
investigation/
Bulk milk tank

Multicopy target
more sensitive than
single copy target.

1-10
bacteria
[99,99%]
CFT < ELISA
ELISA = IFA

CFT < ELISA
ELISA = IFA

Herd/
Individual
testing
Herd/
Individual
testing
Herd/
Individual
testing

The differentiation
between antibodies to
phase I and phase II
antigens is possible,
however, such tests
for animals are not
commercially
available.

Se: Sensitivity, Sp: Specificity, IHC: immunohistochemical staining, PCR: Polymerase Chain Reaction (conventional as well
as real time), CFT: Complement Fixation Test, IFA: immunofluorescent assay.

EFSA Journal 2010; 8 (5):1595

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Q fever

Several methods are available for diagnosis of C. burnetii infection in animals,
including both direct identification of the agent and serological testing.
Direct identification of the agent:
o There is no officially designated test for the direct identification of C. burnetii in
domestic ruminants.
o Immunohistochemistry can be very useful when considering potential causes of
abortion in domestic ruminants.
o In animals, multicopy polymerase chain reaction (PCR) is currently the most
sensitive and rapid mean for the direct detection of C. burnetii, and the
identification of shedders.
o Currently it is not possible to reliably detect infected animals which are not
shedding.
o PCR can be used on a wide range of samples, including vaginal discharges,
abortion material, faeces and milk (either bulk or individual).
o Two PCR-based typing methods have been described (multi-locus variable number
of tandem repeats analysis, MLVA; multispacer sequence typing, MST). These
methods may become very useful for epidemiological investigations.
Serological testing:
o There is no officially designated serologic test for C. burnetii infection in domestic
ruminants.
o Serological assays are suitable for screening herds, but interpretation at the
individual animal level can be difficult.
Current serological methods provide limited information about stage of disease,
whether infection is recent or latent, or whether the animal is currently shedding/
infectious. The present serological methods do not allow for differentiation between
vaccinated or naturally infected animals.

2.1.2.

Q fever monitoring and surveillance

Notification
There are no EU rules about the notification (i.e. the disease is not listed in Directive 82/849/EEC) or
monitoring/surveillance of C. burnetii infection and/or Q fever in domestic ruminants. There are also
no EU rules, relevant to Q fever, concerning control options, intra-community trade or import. In
many European countries, there is also no national requirement for notification of Q fever in
ruminants. The notification status of Q fever in selected European countries, based on a questionnaire
by the recent Article 36 review (Sidi-Boumedine et al., 2010), is presented in Table 2. No data were
specifically sought about the criteria for notification in different EU MS. Nonetheless, it is likely that
there is considerable variation between EU MS, both in the notification criteria and the animal species
for which disease is notifiable.

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Q fever

Table 2: The notification status of Q fever in European countries, in domestic ruminants
Country
Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
UK
Norway
Switzerland

Notifiable in domestic ruminants
NR
NN

NN


NN

NN


NN
NR



NN
NR
*

NN
NN
NN



NN
NN


*Notifiable in dairy sheep and goats from 2008
NN Not notifiable
NR No response to the questionaire

National reference laboratories
The answers to a questionnaire (Sidi-Boumedine et al., 2010) concerning the presence of a national
reference laboratory for Q fever diagnosis in animals are presented in Table 3. A national reference
laboratory (NRL) for Q fever detection is reported in all but 4 of the 24 EU MS that participated in the
survey (Czech Republic, Estonia, Slovakia and Slovenia). Note that the lack of a NRL does not
necessarily reflect a lack of laboratory capacity for monitoring/surveillance.

EFSA Journal 2010; 8 (5):1595

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Q fever

Table 3: National reference laboratories for C burnetii diagnosis in animals in EU MS
Country

NRL

Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
UK
Norway
Switzerland

NR



No NRL

No NRL




No NRL
NR

No NRL


NR
*



No NRL
No NRL






*Central Veterinary Institute (CVI) is the NRL for all notifiable animal diseases in the Netherlands, including Q fever
NR No response to the questionaire

Monitoring/surveillance intensity
Q fever is included as a list B disease („Other zoonoses and zoonotic agents that shall be monitored
according to the epidemiological situation in a MS‟) in Annex I of Directive 2003/99/EC. The disease
is not specifically listed in Regulation 2160/2003/EC for zoonosis control options. In the EFSA/ECDC
Zoonoses Report, data on C. burnetii infection and Q fever have been available since 2005. In 2005,
data were available from only 2 countries, however, this has progressively increased to include data in
2008 from 17 EU MS and 2 non-EU MS. However, disease reporting from EU MS is not harmonized,
and data completeness varies considerably.
Limited monitoring/surveillance programmes are conducted in European countries. Table 4
summarises all monitoring activities for Q fever in domestic ruminants in European countries, based
on data from the EFSA/ECDC Zoonoses Reports (2006, 2007, 2008), an ad hoc consultation with EU
MS in association with the current opinion (see Table 17), the published scientific literature (see Table
5) and additional information provided by the Q fever WG. It does not include data about clinical
investigation, which is presented in Table 16. Testing for Q fever is generally conducted as part of the
differential diagnosis for abortion.

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Q fever

Table 4: Monitoring/surveillance for C. burnetii infection/Q fever in domestic ruminants in
European countries
European
countries
Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
United Kingdom
Norway
Switzerland

Information
source(s)a
N/Ac
R
R, L
L
R
R, L
R
R
R, L
R
R, L
R
R, L
R
N/A
N/A
R
N/A
R, L
R
R
N/A
N/A
R
L
R
R
R
R

Monitoring/surveillance in domestic ruminants b
2005
2006
2007
2008
2009

c, s (R, L)

c
c, s, g, (R)

c, s, (R, L)
c, s, g

Nod
c (R)

g (L)

g (L)

s, g (R)

s, g (R)

c (R, L)

g (L)
c, s, g

Nod
c
g (R)

s, g (L)
Nod
c, s,

c, s, g

c, s, g

c, s, g

g

s

s

c, s, g

c, s, g

c, s, g

c, s, g
c
s

s, g

c, s, g
c, s, g
c
c
c

c
c, s, g
c
s, g
c, s, g

a. R: as reported to EFSA (EFSA/ECDC Zoonoses Reports or in response to an ad hoc consultation with member states in
2010 in association with the current opinion), L: as reported in the scientific literature (source Table 5)
b. c: cattle, s: sheep, g: goats
c. N/A: no information available, either as reported to EFSA or in the scientific literature
d. No: no monitoring/ surveillance for Q fever

There are currently no EU rules concerning notification and monitoring/surveillance of
C. burnetii infection and/or Q fever in domestic ruminants. In many European countries,
there are also no national notification requirements.
There is also variable laboratory capacity in European countries for diagnosis of C. burnetii
infection.
There is limited monitoring/surveillance for C. burnetii infection in domestic ruminants in
European countries, based on available data.
Disease reporting from EU MS is not harmonized, and the level of reporting is highly
variable. It is not currently possible, with any confidence, to provide accurate, comparative
information about the occurrence of C. burnetii infection and Q fever in domestic ruminant
populations among EU MS.

EFSA Journal 2010; 8 (5):1595

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Q fever

2.1.3.

Infection and disease information in domestic ruminants

Testing intensity
Based on feedback from an ad hoc EFSA consultation with EU MS in 2010, in association with the
current opinion (as detailed in section 1.2.1), testing for C. burnetii infection was conducted during
2009 in 16 (in cattle) 11 (in sheep) and 13 (in goats) of 23 European countries that replied to the
consultation. Detailed data about testing for C. burnetii infection within Europe, by animal species, is
presented in Table 15 (Appendix C).
Clinical investigations
Based on feedback from an ad hoc EFSA consultation with EU MS in 2010, in association with the
current opinion (as detailed in section 1.2.1), Q fever testing in association with clinical investigations
was conducted during 2009 in 15 (in cattle), 9 (in sheep) and 9 (in goats) of 23 European countries that
replied to the consultation, as highlighted in Figures 1. Details of tests conducted in European
countries during 2009 as part of a clinical investigation for Q fever in domestic ruminants, by species
and countries, is presented in Table 16 (Appendix C).

Figure 1: European countries where clinical investigation activities for Q fever in domestic
ruminants were conducted in 2009.
Monitoring/surveillance activities
Based on feedback from an ad hoc EFSA consultation in 2010, in association with the current opinion
(as detailed in section 1.2.1), testing for C. burnetii infection as part of a monitoring and/or
surveillance activities was conducted during 2009 in 8 (in cattle), 4 (in sheep) and 6 (in goats) of 23
European countries that replied to the consultation, as highlighted in Figures 2. A detailed presentation
of available data, by species and country, are presented in Table 17 (Appendix C). Animal- and herdlevel seroprevalence for C. burnetii infection in domestic ruminants in European and neighbouring
countries, by species and country, is also presented in Table 5. These data were initially presented in a
2005 publication by Arricau Bouvery and Rodolakis (2005), but have been updated following a review
of literature published since 2004. Seroprevalence estimates are based on antibody detection.

EFSA Journal 2010; 8 (5):1595

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Q fever

Figure 2: European countries where monitoring and/or surveillance investigation activities for
Coxiella burnetii infection in domestic ruminants were conducted in 2009
Table 5: Prevalence of C. burnetii (animal and herd level) in domestic ruminants in Europe and
neighbouring countries.
CATTLE
Country
Albania
Bulgaria

Cyprus
Denmark

% positive
Cattle
Herds

Testa

Reference

552
311
3,006
3,714
120
3,188

8.5
10.9
8.2
6.5
20.8*
9.7

ELISA
ELISA
CFT
CFT
IFA
CFT

Cekani et al., 2008
Cekani et al., 2008
Martinov 2007a
Martinov 2007a
Panaiotov et al., 2009
Martinov 2007a

3,026
2,932
95,737
20,086
4,749
75

8.1
10.6
5.4
11.8
19.8
24.0

Martinov 2007a
Martinov 2007a
Martinov 2007a
Martinov 2007a
Martinov 2007a
Psaroulaki et al., 2006a
Agger et al., 2010

Year of
study

No. tested
Cattle

1999
1995-1997
2002
2003
2004
2004
2005
2006
1989-2006
1977-1988
1950-1976
NA
2008

544***

21

13

nd

CFT
CFT
CFT
CFT
CFT
IFA
ELISAmilk
ELISAmilk
IFA

155***

6

2

nd

IFA

486

26

20

nd

IFA

44.9**
22.0
1.4 to
2**
8

nd

ELISA
ELISA
ELISA

Bodker and
Christoffersen, 2008
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
Cabassi et al., 2006
Cabassi et al., 2006
Sting et al., 2002

nd

ELISA

In Arricau-Bouvery 2005

2007
Italy

Germany

1998

Herds

100

59.0

742

57

NA
NA
1998-2000

650
600
1,167

105

1998

21,191

544

EFSA Journal 2010; 8 (5):1595

21

Q fever

Netherlands
Spain

Turkey

UK (NI)

1996-1997

826

38

1992-1993

500
665
383**
612 Bulls
1,095
3,500
1,160**
79
626

NA
39
33
1
21
155
234

1991
1989-1990
1987
2006-2007
2008-2009?
2008-2009?
2006-2008
2005
1998
2009
2009

nd

ELISA

Sting et al., 2000

nd
76.9
78.8
100
81
57.4
37

CFT

Wittenbrink et al., 1994

ELISA
ELISA
ELISA
IFA
ELISA
ELISA
ELISA
ELISA
ELISA
ELISA

Rehacek et al., 1993
Klemt and Krauss, 1991
Muskens et al., 2007
Ruiz-Fons et al., 2008
Ruiz-Fons et al., 2010
Ruiz-Fons et al., 2010
Ceylan et al., 2009
Seyitoglu et al., 2005
In Arricau-Bouvery and
Rodolakis 2005
McCaughey et al., 2010
McCaughey et al., 2010

%
positive

Test

Reference

14.3**
0.6
7.6
9.6
19.3
5.6
11.8
13.3
21
35.4
6.7

42
92
230
416

48

5,182

42.9
16.3
9.6
6

nd

6.2
273

48.4
SHEEP

Country

Year

No. tested
Sheep

Herds

1999
1995-1997
2002
2003
2004
2004

292
350
1,819
1,811
100
1,258

12.3
8.9
12.7
8.3
21.0*
14.1

ELISA
ELISA
CFT
CFT
IFA
CFT

Cekani et al., 2008
Cekani et al., 2008
Martinov 2007a
Martinov 2007a
Panaiotov et al., 2009
Martinov 2007a

2005
2006
1950-1976
1977-1988
1989-2006
NA 2006??
2004
NA
NA
1998

1,911
1,925
17,088
16,593
99,189
153
182
481

15.2
8.4
16.7
18.8
4.8
56.9**
11.0*
18.9

CFT
CFT
CFT
CFT
CFT
CFT
CFT
IFA

1999

100

Greece
Italy

NA
1999-2002

3,460
554
7,194

Netherlands

1987
2008

3,603
12,363

Spain

1999-2003
1999-2003
1999-2003
2005
2005
2005
2007-2008

38
34
1,011

NA

465

Martinov 2007a
Martinov 2007a
Martinov 2007a
Martinov 2007a
Martinov 2007a
Martinov. 2007b
Medic et al., 2005
Psaroulaki et al., 2006
Runge and Ganter, 2008
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
Sting et al., 2002
Pape et al., 2009a
In Arricau-Bouvery and
Rodolakis 2005
In Muskens et al., 2007
Van den Brom and P.
Vellema, 2009
Oporto et al., 2006
Oporto et al., 2006
Oporto et al., 2006
Garcia-Perez et al., 2009
Garcia-Perez et al., 2009
Garcia-Perez et al., 2009
Ruiz-Fons et al., 2010
Ruiz-Fons et al., 2010
Karaca et al., 2009

Albania
Bulgaria

Croatia
Cyprus
Germany

95
1,346

ELISA

1

57

ELISA

675

8.7
10.5
9/38

ELISA
IFA
ELISA

3.5
2.4

ELISA
ELISA

8.8**
2.7**
42.1**
67.6**
8.9
22.1
11.7
34
21.1**

PCR
CFT
CFT
ELISA
ELISA
ELISA
ELISA
ELISA
ELISA

148
148

154
1,379
46

Turkey

EFSA Journal 2010; 8 (5):1595

2.7
1.3

22

Q fever

UK (NI)

2001-2004
1998

743
411

NA 2009?
NA 2009?

1,022

42

58

ELISA
ELISA

Kennerman et al., 2010
In Arricau-Bouvery and
Rodolakis 2005
McCaughey et al., 2010
McCaughey et al., 2010

%
positive

Test (a)

Reference

20
10.5

83

12.3
62.1

ELISA
IFA

GOATS
Country

Year

No. tested
Goats

Herds

1999
1995-1997
2002
2003
2004
2004

260
443
677
1,044
50
1,016

4.2
8.8
11.8
7.4
40.0*
21.7

ELISA
ELISA
CFT
CFT
IFA
CFT

Cekani et al., 2008
Cekani et al., 2008
Martinov, 2007a
Martinov, 2007a
Panaiotov et al., 2009
Martinov, 2007a

832
359
1,417
1,791
54,175
417
359

Germany

2005
2006
1950-1976
1977-1988
1989-2006
NA
2006
2006
2006
2008
2008
1998

11.1
19.2
20.5
10.8
7.6
48.2
36.0
88.1
65.3**
32.0
88.1
2.5

CFT
CFT
CFT
CFT
CFT
IFA
ELISA
ELISA
ELISA
ELISA
ELISA
ELISA

Greece
Italy

NA
1999-2002

61
2,155

Netherlan
ds

1987

498

1 goat

ELISA

Martinov, 2007a
Martinov, 2007a
Martinov, 2007a
Martinov, 2007a
Martinov, 2007a
Psaroulaki et al.2006a
Dubuc-Forfait et al., 2009
Dubuc-Forfait et al., 2009
Chaillon et al., 2008
Dubuc-Forfait et al., 2009
Dubuc-Forfait et al., 2009
In Arricau-Bouvery and
Rodolakis 2005
Pape et al., 2009a
In Arricau-Bouvery and
Rodolakis 2005
Muskens et al., 2007

2008

3,409

7.8

ELISA

NA, ML
after 1997
2007-2008
2007-2008
2006-2008
NA, ML
2008-2009?
NA, ML
2008-2009?

98

79.6**

MAT

Van den Brom and P.
Vellema, 2009
Platt-Samoraj et al., 2005

ELISA
ELISA
ELISA
ELISA

Ruiz-Fons et al., 2010
Ruiz-Fons et al., 2010
Ceylan et al., 2009
McCaughey et al., 2010

ELISA

McCaughey et al., 2010

Albania
Bulgaria

Cyprus
France

Poland
Spain
Turkey
UK (NI)

42
75
1,057
42
278
104

115

6.6
13

47

8.7
11

92
54

45.5
5.4
9.3

7

42.9

IFA
ELISA

(a) Indirect Immunofluorescence assay (IFA), Enzyme Linked Immunosorbent assay (ELISA), Complement fixation test
(CFT), Microagglutination test (MAT)
* Investigation in relation to a human outbreak
** Investigation in relation to clinical symptoms in the population (animals)
*** The study was conducted to compare animals kept indoors (544) and outdoors (155)
NA - not available; ML- most likely

EFSA Journal 2010; 8 (5):1595

23

Q fever

There were differences between European countries in testing intensity, and in the reported
level of clinical investigations and monitoring/surveillance activities, for C. burnetii infection
and Q fever
C. burnetii infection is prevalent in domestic ruminants (cattle, sheep, and goats) in a wide
range of European and neighbouring countries, based on the results of serological testing
over the last several decades. These results are indicative of infection, but not necessarily
disease.
2.1.4.

Interpretation/evaluation of the surveillance data

Information of the incidence and prevalence of C. burnetii infection and Q fever in the animal
population in EU is based either on passively collected data (the animal owner or veterinarian reports a
case or outbreak to the authorities) or on a combination of data collected passively and actively (that
is, samples are collected according to a planned framework). The latter is, without doubt, the best way
to get a sound picture of the disease situation in animals, provided:
There is a clear case definition,
There is a commitment among farmers and veterinarians to report suspect (and confirmed)
cases, and
a well designed active monitoring protocol is implemented, including formal random sampling
protocols (sample size based on predefined accuracy and precision, taking into account
clustering of infection in herds and possibly regions) and information on the diagnostic
performance (sensitivity and specificity) of the test(s) being used.
Interpretation of the annual EFSA/ECDC Zoonoses Reports (2006, 2007 and 2008) is currently
problematic. It is difficult to make comparisons between species, countries and years as there are
considerable differences in testing protocol and data availability. Factors such as the reason for testing
(e.g. an abortion/outbreak investigation, milk controls programme, prevalence survey), number of
animals tested, type of tissue sampled (in particular bulk milk or individual animal samples) and
laboratory technique (some animals testing positive for ELISA then test negative for PCR) can each
have a significant effect on the number of animals testing positive. Herd prevalence is higher than
animal prevalence, highlighting concerns about data collection, including the completeness of herdlevel data. In many EU MS, notification is not mandatory. In those EU MS where notification is
mandatory, the differences in the relative number of Q fever tests that have been performed (number
of tests relative to the ruminant population) suggest that compliance to notification is quite variable.
This is to be expected, noting that the clinical signs of Q fever in animals are not very specific, the
causative agent seems to be present in most EU MS, and diagnosis does not result in specific
intervention measures in most EU MS. In addition, there is quite a broad variation in tests being used
for the diagnosis, while at the same time there is a lack of sound information on the diagnostic
sensitivity and specificity of these tests. For the active monitoring and surveillance programmes,
comparison between EU MS is hampered by more or less the same problems. It is not performed in
most EU MS, the sampling design is not consistent among EU MS where it has been implemented and
sound information on diagnostic sensitivity and specificity is lacking (section 2.1.1.). In conclusion, it
is not possible to make a sound comparison of outbreak data or of measures of Q fever occurrence
such as incidence or prevalence.
From the available information and the above, we can conclude that C. burnetii is present in most, if
not all, EU MS. However, because of the lack of harmonization of the monitoring programme and
tests being used in the various EU MS, a comparison of the occurrence of C. burnetii infection in
animal populations between different EU MS is subject to considerable bias and therefore associated
with considerable uncertainty. Within EU MS, however, the monitoring is likely more comparable
over the years (although the variation in tested samples also varies within EU MS, this variation is less
than the variation between EU MS), with a possible exception of 2009 when the Dutch problem may
have boosted Q fever interest in other EU MS as well. Based on the information in the Annex, there
are no indications for an obvious upward trend in Q fever incidence/prevalence within EU MS
although some increase in seroprevalence has been observed in some EU MS.
EFSA Journal 2010; 8 (5):1595

24

Q fever

Questions could be raised about the potential value of a shift towards mandatory Q fever notification
in animal populations in EU MS. However, such a change could be counterproductive in the absence
of clear advantages, such as compensation for affected farmers. If genuinely comparable data from
different EU MS were needed, a range of issues (including case definitions, diagnostic methods and
sampling plans) need to be harmonised and standardised. In addition, laboratories need to operate
under agreed quality management systems.

Based on available data, C. burnetii is present in most, if not all, MS.
Interpretation of the annual EFSA/ECDC Zoonoses Reports is currently problematic,
specifically because data collection between MS is not harmonised. Consequently, it is not
possible to conduct an unbiased comparison of Q fever prevalence/incidence in animals
between MS.
Based on available data, there does not appear to be an upward trend in Q fever
prevalence/incidence in EU MS. However, comparison over time and between countries (or
regions) is associated with considerable uncertainty.
If an unbiased comparison of Q fever occurrence in animals between EU MS and over time
is needed, then monitoring/surveillance would need to be conducted in a harmonised
manner.

2.2.

Magnitude and distribution of Q fever in humans
2.2.1.

Q fever diagnosis in humans

Q fever clinical symptoms in humans are usually non-specific and often relatively mild; hence,
classical differential diagnosis must be supported by laboratory tests for accurate diagnosis of clinical
disease.
Serological testing
The classical method for Q fever diagnosis is serological analysis to detect the presence of antibodies
to C. burnetii antigens. Typically, this relies on ELISA, Complement Fixation or Immunofluroescense
Assay platforms using commercially available or in-house testing kits (Scola, 2002; Fournier et al.,
1998; Schimmer et al., 2009). Serology has an advantage because it can theoretically differentiate
between acute and chronic infection of C. burnetii. This is because there are two antigenic phases
called phase I and phase II that vary depending on the clinical progression of infection. Each phase has
a different antigen profile; in acute Q fever, the immune response is primarily driven by IgM and IgG
antibodies directed against the avirulent form of C. burnetii (Phase II). In the chronic form, IgG and
IgA antibodies predominate and are directed against both the virulent and avirulent forms of bacteria
(Phase I). Acute infection is therefore characterised by elevated phase II antibody levels, and generally
is first detectable after the second week of illness. In chronic Q fever, typically the opposite is true: i.e.
phase I antigens significantly predominate over Phase II (Maurin and Raoult, 1999). This is because
antibodies to phase I antigens of C. burnetii generally require longer to appear and indicate continued
exposure to the bacteria. Thus, high levels of antibody to phase I in later specimens, in combination
with constant or falling levels of phase II antibodies and other signs of inflammatory disease, suggest
chronic Q fever. Antibodies to phase I and II antigens have been known to persist for months or years
after initial infection (CDC, Fact sheet- Q fever4).
Broadly the same diagnostic methods are also used for seroprevalence studies to estimate the extent to
which a given population has been infected by C. burnetii following possible exposure. However this
type of study is not designed to determine the incidence of clinical disease; it is only through the

4

CDC fact sheet; Q fever: www.cdc.gov.ncidod/dvrd/qfever/index.htm (accessed 15/3/10)

EFSA Journal 2010; 8 (5):1595

25

Q fever

combination of clinical symptoms and confirmatory laboratory diagnostics that clinical disease can be
determined.
Direct identification of the agent
In addition to serology, DNA detection methods are becoming increasingly common and widely used.
They have the obviously advantage that they are able to detect the presence of the etiological agent
before the occurrence of seroconversion events that is prerequisite for diagnosis using serological
methods. For example, Real-Time PCR tests have recently been developed in the Netherlands.
Typically they are able to detect the presence of C. burnetii within 10 days of symptom onset.
(Schneeberger et al., 2009).
2.2.2.

Q fever monitoring and surveillance in humans

Within the EU legal framework on communicable disease surveillance and notification, Q fever is one
of the 47 communicable diseases for which surveillance is mandatory in the EU and three EEA/EFTA
countries (Commission Decision 2000/96/EC5). This legal framework requires EU MS to report
surveillance data to ECDC. This underlying legislative requirement is supported by harmonised case
definition of human Q fever under EU legislation (CD 2008/426/EC6) (Table 6):
Table 6: EU harmonised Q fever case definition (adapted from CD 2008/426/EC)

Q Fever (Coxiella burnetii)
Clinical criteria
Any person with at least one of the following three symptoms:
— Fever
— Pneumonia
— Hepatitis
Laboratory criteria
At least one of the following three:
— Isolation of Coxiella burnetii from a clinical specimen
— Detection of Coxiella burnetii nucleic acid in a clinical specimen
— Coxiella burnetii specific antibody response (IgG or IgM phase II)
Epidemiological criteria
At least one of the following two epidemiological links:
— Exposure to a common source
— Animal to human transmission
Case classification
A. Possible case
NA
B. Probable case
Any person meeting the clinical criteria and with an epidemiological link
C. Confirmed case
Any person meeting the clinical and the laboratory criteria

5

Commission Decision 2000/96/EC of 22 December 1999 on the communicable diseases to be progressively covered by the
Community network under Decision No 2119/98/EC of the European Parliament and of the Council
6
Commission Decision 2008/426/EC laying down case definitions for reporting communicable diseases to the Community
network under Decision No 2119/98/EC of the European Parliament and of the Council

EFSA Journal 2010; 8 (5):1595

26

Q fever

However, the range and type of surveillance systems for Q fever throughout the EU varies
significantly and although each system may be adapted to local circumstances in order to maximise
detection of cases (Table 7), there is likely to be significant variability in the case ascertainment
between and within EU MS; it is certainly recognised that case notification rates are dependent on the
level of local medical and scientific interest in Q fever (Raoult, 1996).
Table 7: Q fever - EU surveillance systems overview in humans (from ECDC Annual
Epidemiological Report 2009)
Data reported by
Country

Data Source
Description

Compulsory
(Cp)/Volunta
ry (V)

Comprehensi
ve
(Co)/Sentinel
(Se)

Active (A)
/Passive (P)

Case-Based
(C)/Aggregat
ed (A)

Laboratories

Physicians

Hospitals

Others

National
coverage

Belgium

Reference
Laboratories
National Surveillance
System
System for Mandatory
Notified Diseases
EPIDAT

V

Co

P

C

Y

N

N

N

Y

Cp

Co

P

A

Y

Y

Y

Y

Y

Cp

Co

P

C

N

Y

N

N

Y

Cp

Co

A

C

-

Y

Y

N

Y

Obligatory,
countrywide, based on
a double system of
reporting Hemorrhagic
fevers
National Infectious
Disease Register
(NIDR)
National reference
Centres
SurvNet@RKI IfSG
7.1
Notifiable Diseases
System
Notification System
for Infectious Diseases
CIDR
National Reporting
System

Cp

Co

P

C

Y

Y

Y

Y

Y

Cp

Co

P

C

Y

N

N

N

Y

V

Co

P

C

Y

N

N

N

Y

Cp

Co

P

C

Y

Y

Y

Y

Y

Cp

Co

P

C

Y

Y

Y

N

Y

Cp

Co

P

C

N

Y

Y

N

Y

Cp
Cp

Co
Se

P
P

C
-

Y
N

Y
Y

Y
Y

N
-

Y
Y

Visums

Cp
Cp

Co
Co

P
P

C
C

N
Y

Y
Y

Y
N

N
N

Y
Y

Cp

Co

P

C

N

Y

N

N

Y

Cp

Co

P

C

Y

Y

Y

Y

Y

Cp
Cp

Co
Co

P
P

C
C

Y
Y

Y
Y

N
Y

Y
N

Y
Y

Cp

Co

P

C

Y

Y

N

N

Y

Cp

Co

P

C

N

Y

N

N

Y

Cp

Co

P

A

N

N

Y

N

Y

Bulgaria
Cyprus
Czech
Republic
Estonia

Finland

France
Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania

Luxembourg
Malta

Netherlands
Norway
Poland

Portugal
Romania

National
Communicable
diseases surveillance
System
System 1 mandatory
notification system
Infectious Disease
Prevention and
Control Unit
Osiris
MSIS (group A
diseases)
National Surveillance
System of Infectious
Diseases
Q- fever Surveillance
System
Romanian National

EFSA Journal 2010; 8 (5):1595

27

Q fever

Slovakia

Slovenia
Spain
Sweden
United
Kingdom

Surveillance System
EPIS Epidemiological
Information System
SURVIVAL
Microbiological
Information System
SmiNet
Q fever Surveillance
System

2.2.3.

Cp

Co

A

C

Y

Y

Y

Y

Y

Cp
V

Co
Se

P
P

C
C

Y
Y

Y
N

N
N

N
N

N
N

Cp
V

Co
Co

P
P

C
C

Y
Y

Y
N

Y
Y

N
Y

Y
Y

Infection and disease information in humans

Clinical disease
Harmonised data on Q fever notifications throughout the EU are collected under the European
Surveillance System. This is a single repository under which EU MS upload data collected at national
level on diseases for which surveillance is mandatory in the EU. The most recent information is
presented in two separate outputs: 2007 data is presented in the 2009 Annual Epidemiology report
from ECDC (Annual epidemiologic report on Commuinicable diseases in Europe 2009), and data form
2008 is presented in the Community Summary Report on Trends and Sources of Zoonoses, Zoonotic
Agents and Food-borne outbreaks in the European Union (EFSA, 2008).
In 2007, the broad epidemiological situation from reported data was that 22 EU and EEA/EFTA
countries reported a total of 669 cases of Q fever in 2007 (8 countries reported zero cases), 637 of
which were confirmed. Outbreaks of human infection were reported in two countries (Netherlands
(168 cases) and Slovenia (93 cases) and both these EU MS obtained notification rates above one per
100,000. The majority of other cases were reporting in Bulgaria (36), Germany (83), Spain (159) and
the UK (62). In 2008, 24 EU/EFTA countries reported 1,599 Q fever cases (1,594 confirmed),
representing an increase of over 170% from the previous year. The increase was mainly attributed to
the increase in the Netherlands and in Germany, while 13 EU/EFTA countries reported zero cases
(Table 8). In 2008, the increasingly widespread epidemic in the Netherlands resulted in over 1,000
human cases being notified.
Table 8: Reported confirmed Q fever cases in humans reported to the ECDC, 2007-2008

Country
Austria
Belgium
Bulgaria
Cyprus
Czech
Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania

Report
Type1
–2
A
A
C
–

Total
cases
–
0
17
0
–

–
0
17
0
–

–
0
0.2
0
–

14
36
8
-

2007 3
Confirmed
Cases
–
0
33
8
–

–2
C
C
–
C
C
C
C
–
C
A

–
0
2
–
370
3
0
13
–
0
0

–
0
2
–
370
3
0
10
–
0
0

–
0
<0.1
–
0.5
<0.1
0
0.2
–
0
0

0
2
83
0
7
4
0
0

–
0
2
–
83
0
7
4
–
0
0

EFSA Journal 2010; 8 (5):1595

2008 4
Confirmed
Cases

Cases/
100,000

Total
cases

Cases/
100,000
–
0
0.43
0
–
–
0
<0.1
–
0.1
0
<0.1
<0.1
–
0
0

28

Q fever
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
United
Kingdom
EU Total
Iceland
Liechtenstein
Norway
Total

–2
C
C
C
C
A
C
C
C
C
A

–
0
1,013
0
12
3
0
0
119
7
40

–
0
1,011
0
12
3
0
0
119
7
40

–
–
6.2
0
0.1
<0.1
0
0
0.3
0.1
<0.1

0
168
0
10
6
1
93
159
3
62

–
0
168
0
8
6
1
93
159
3
62

–
0
1.03
0
<0.1
<0.1
<0.1
4.6
<0.1
0.1

C
C
C

1,599
0
0
0
1,599

1,594
0
0
0
1,594

0.5
0
0
0
–

669
0
669

637
0
637

0.16(a)
0
0.16(a)

1. A: aggregated data report; C: case-based report; –-: no report;
2. No surveillance system exists
3. Data from ECDC 2009 Annual epidemiological report
4. Data from Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and food-borne outbreaks
in the European Union in 2008
(a) overall rate excludes data from Spain

Descriptive epidemiology on the age, gender and seasonal distribution on Q fever notifications in 2007
is presented in the ECDC Annual epidemiological Report for 2009, and is reproduced below:
Age and gender distribution: The highest rates were seen in the age groups of 15–24 year-olds
and 45–64 year-olds, with notification rates of 0.24 and 0.23 per 100 000 population,
respectively. Only seven of the 501 cases for which such information was available were
reported among children under the age of 15. The overall rate was higher in men than in
women (0.23 and 0.13 per 100 000, respectively), with a male-to female ratio of 1.78:1.
Seasonality: The information on seasonality was available for the 585 confirmed cases during
2007. The months with the highest number of reported cases were July and August (84 and 69
cases, respectively). In 2006 the majority of cases occurred during June and July which was
linked to spring lambing season in many European countries. The distribution by date of
notification of cases is not very useful as day of onset of illness can be earlier than day of
notification for such an insidious disease.
Seroprevalence
The date collected under EU surveillance capture notified clinical cases of Q fever but there is no EU
harmonised surveillance system to assess the levels of exposure or infection to C. burnetii. However,
many serological studies have been performed to determine the extent to which defined population
groups may have been infected with C. burnetii (see Table 9). Generally this work has been done to
assess levels of seroconversion in the general population and risk groups associated with known
outbreaks, or comparative studies to assess seroconversion in occupational groups. The design, focus
and scale of these studies vary significantly including different diagnostic tests cut off values and,
population groups. This makes direct comparison impossible. However, it can broadly summarised
that, like the clinical case data, there is significant variation in the levels of seroconversion throughout
the EU, but that at the general population level, there are typically a small percentage of individuals
(often between 2-10%) that have evidence of having been infected with C. burnetii. This figure
inevitably rises in areas with ongoing community-based outbreaks of human Q fever, or where
outbreaks are commonly reported and there is some endemicity of C. burnetii. Comparatively high
seroprevalence are also commonly seen in occupational and other groups that have extended exposure
EFSA Journal 2010; 8 (5):1595

29

Q fever

to animal hosts for C. burnetii (farmers, veterinarians, slaughterhouse workers, laboratory workers etc)
(Table 10).
Table 9: Prevalence for C burnetii in human populations in Europe and neighbouring countries
Country

Year of study

% positive

Test

Reference

NA
NA
NA
NA

Number
of tested
141**
131**
121**
63**

Cyprus
Cyprus
Cyprus
Cyprus

57.4
44.3
43.0
52.4

IFA
IFA
IFA
IFA

Psaroulaki et al., 2006a
Psaroulaki et al., 2006a
Psaroulaki et al., 2006a
Psaroulaki et al., 2006a

Cyprus
France
Netherlands
Netherlands
UK (NI)
Greece
Italy
Greece
France
Spain
Spain
Spain
Bulgaria

NA
1982-1990
1982
1983
1986-1987
1987
NA (1987?)
1987
1988
1989
1990
1993
1993-2000

127**
22,496**
222**
359*
2 394
231**
NA
238**
924**
NA
NA
400
1,4353**

64.6
23
83.8
24
12.8
13.8 to 38.1
6.1
42.0
4.03
12.7
50.2
38.4
15

IFA

Spain
France

1994
1995

NA
790*

40.6
1

ELISA
IFA
IFA
IFA
IFA
IFA
IFA
IFA
CFT+
MIFT
IFA
IFA

Psaroulaki et al., 2006a
In Maurin et Raoult, 1999
In Van den Brom and Vellema, 2009
In Van den Brom and Vellema, 2009
McCaughey et al 2008
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
Martinov 2007a

France

1995-1996

785

5

IFA

Spain

1996-1997

1,654

5

IFA

France

1996

620*

3

IFA

France

1996

12,716

0.2

IFA

France
Turkey

1996
1998

208**
102

71
8

IFA
IFA

Spain
Spain
Bulgaria

1998
1999
2001-2004

595
1 654
5 207**

48.1
5.1
18

France
France
France
Bosnia
Herzegovina
Poland

2002
2002
2002
2002

376***
91***
578***
76***

2.9
5.5
14.7
34.2

IFA
IFA
CFT+
MIFT
IFA
IFA
IFA
IFA

2003

90

18

IFA

Canary
Island
Bulgaria
Croatia
Turkey
Turkey
Greece

2003

662

21.5

IFA

2004
2004
2004?
2004
2007

104***
56***
92
339
1007

7.7
14
19.6
1.8 to 13.2
7.5

Greece

2007

850**

6.7

IFA
CF
ELISA
IFA
IFA +
ELISA
IFA +

EFSA Journal 2010; 8 (5):1595

In Psaroulakis et al., 2006a
In Arricau-Bouvery and Rodolakis
2005
In Arricau-Bouvery and Rodolakis
2005
In Arricau-Bouvery and Rodolakis
2005
In Arricau-Bouvery and Rodolakis
2005
In Arricau-Bouvery and Rodolakis
2005
In Psaroulakis et al., 2006a
In Arricau-Bouvery and Rodolakis
2005
In Psaroulakis et al., 2006a
In Psaroulakis et al., 2006a
Martinov, 2007a
Tissot-Dupont et al., 2007
Tissot-Dupont et al., 2007
Tissot-Dupont et al., 2007
Sukrija et al., 2006
In Arricau-Bouvery and Rodolakis
2005
In Psaroulakis et al., 2006a
Panaiotov et al., 2009
Medic et al., 2005
Seyitoglu et al., 2005
In Psaroulakis et al., 2006a
Pape et al., 2009b
Pape et al., 2009c

30

Q fever

Netherlands

2006-2007

5,654

1.5

ELISA
ELISA

Duynhoven et al. 2010

*Blood donors
** Risk group
***humans in the outbreak area

2.2.4.

Interpretation/evaluation of the surveillance data

Overall, it can broadly be concluded from the EU surveillance data that human Q fever persists as a
relatively infrequent clinical disease, but one that occurs throughout the EU/EFTA. Typically human
cases are reported either as single sporadic cases or discrete cluster of cases from a specific source
with no obvious association to an increased general disease risk (Wilson et al., 2009, Orr et al., 2006),
or as part of clusters of infections associated with a known community-based outbreak. The
underlying basic EU/EFTA case numbers have some variance, but the annual notification rates have
the same order of magnitude over time; typically between 500-2000 cases per annum, of which a
significant proportion are associated with outbreaks related with animals. The number of outbreaks in
the EU/EFTA also varies each year, but generally is relatively infrequent: typically between 1-3
outbreak clusters of human infections are reported annually in the EU/EFTA. These are commonly
isolated to a discreet geographical area within a EU MS, although there may be separate clusters and
multiple sources within each outbreak. Typically a relatively small number of infected individuals are
identified in each outbreak (between 10-500), and at least in the last 10 years, they do not usually
persist over consecutive years (Table 11).
Although the underlying epidemiology remains broadly consistent in the EU, it is likely that most
human cases of Q fever are not diagnosed and therefore not reported. This is because prior infection in
animal hosts is often undetected or not notified, which means that public health authorities may not
receive early warning of the presence of the known zoonotic agent in animal populations. In addition,
most infected humans are either asymptomatic, or present with non-specific respiratory symptoms and
mild self-limited infection. Hence the number of cases both at national and EU level are likely to be
significantly underestimated, and therefore it is difficult to assess the real number of C. burnetii
infections in the EU (ECDC, 2009).
Although it is clear that surveillance systems are unlikely to pick up all the clinical cases of Q fever,
increasing levels of general respiratory illness, particularly atypical pneumonia have alerted medical
practitioners to emergent outbreaks in several EU MS (see Table 11). However given the variance in
routine and active surveillance in the EU, it remains uncertain if all such outbreaks within the EU are
identified. It certainly can not be discounted that clusters of human cases that may represent a potential
outbreak event may be missed given the relatively mild unspecific symptomology of most acute
human cases of Q fever, together with the mild and non-discriminatory clinical manifestation of
infection in animals and the fact that the infection in animals is non-notifiable in many EU countries.
Indeed, it is likely that humans act as sentinels for infection; human disease may be the first indication
that C. burnetii is present in a locality. Even in this case, many factors must align before infection is
recognised; alert medical practitioners testing on the basis of clinical symptoms; accurate sample
collection and submission; diagnostic laboratory capacity and capability and result feedback. A recent
study in the Netherlands retrospectively examining hospitalisations for lower respiratory tract
infections has suggested that some local Q fever clusters may have passed unnoticed; six clusters of
excess hospitalisations in adults in areas with Q fever in small ruminants were detected between 2005
and 2007, next to the first recognised human outbreak in 2007 (Schimmer et al., 2007) However, there
is no suggestion that proactive syndromic surveillance would have identified these cases at the time.
The Q fever epidemic in the Netherlands that was first reported in 2007 has shown some divergence
from the general epidemiology of Q fever seen in the EU as a whole. In this case, the infection appears
to be persisting over consecutive years, and disease is becoming both more prevalent and more
widespread in humans following initial notification of an outbreak cluster. Although the outbreaks
were initially confined to a small region within the province of Noord-Brabant in the Netherlands in

EFSA Journal 2010; 8 (5):1595

31

Q fever

2007, the foci of animal infection and associated human disease has expanded to include other
neighbouring provinces over subsequent years.

Human Q fever cases must be notified under EU law. Typically, between 600-1500
cases are notified annually throughout the EU, of which the majority is associated with
specific Q fever outbreaks in animals. Most MS commonly report cases indicating the
widespread distribution of the C. burnetii throughout the EU.
Human cases are likely to be underreported; Q fever symptoms are commonly mild and
non-specific and hence the infection is not commonly considered in differential
diagnosis unless in the locality of known outbreaks.
Humans may act as sentinels for C. burnetii infection; human disease may be the first
indication that C. burnetii is present in a locality.
The challenges of case ascertainment, and the associated underreporting of clinical
infection in the EU, means that it is difficult to draw conclusions on the underlying trend
in C.burnetii infections in the EU. However, the epidemiological pattern commonly seen
in EU outbreaks are localised events of limited duration with numbers of clincial cases
in the order to magtude of 10-500.
The Q fever epidemic in the Netherlands that was first reported in 2007 has shown some
divergence from the outbreak epidemiology of Q fever seen in the EU; the infection
appears to be persisting over consecutive years, and has become more prevalent and
more widespread in humans following initial notification of a outbreak cluster.

2.3.

Significance and impact of Q fever
2.3.1.

Significance and impact on public health

Clinical manifestation and treatment
C. burnetii in humans demonstrates a wide variability in clinical presentation, but broadly can be
classified into acute and chronic infection. Acute and chronic infection can be distinguished on the
basis of clinical expression, temporal course and serological profiles.
Acute Q fever
It is commonly reported that approximately 60% of infections are asymptomatic
seroconversions (Arricau-Bouvery and Rodolakis, 2005). Patients with clinical disease present
a range of non-specific symptoms, the most common of which are flu-like symptoms that is
typically characterised by high fever, headache and cough, atypical pneumonia or hepatitis.
Other rare clinical manifestations have also been described inducing skin rash, nausea
myocarditis, pericarditis, meningoencephalitis, pancreatitis and abortion.
Most symptomatic cases suffer a relatively mild self-limiting infection, but some may need
medical attention (20%), and approximately 1-5% requires hospital treatment that in some
cases requires ventilation support and intensive care.
Patients presenting with acute illness can be effectively treated (Delsing et al., 2009).
Chronic Q fever
The prevalence of chronic Q fever is uncertain, and there are relatively wide ranging estimates
in the literature; Tissot-Dupont et al. report that 0.5 % of patients having had the acute disease
become chronic. Other authors report that approximately 1 % of acutely ill patients become
chronic, while others have proposed up to 5% (Tissot-Dupont et al., 2007; Arricau-Bouvery
and Rodolakis, 2005).
The clinical manifestation of chronic Q fever can be broad, but the most common symptoms
relate to heart and circulatory impairment, of which endocarditits is the most common and
EFSA Journal 2010; 8 (5):1595

32

Q fever

reported in about 60-70% of all chronic cases. Other conditions associated with chronic
Q fever include osteoarticular infections, and chronic pulmonary infections.
In addition to circulatory effects, chronic hepatitis is another common feature as is chronic
fatigue syndrome (Wildman 2002) and fever of unknown origin. Rare manifestations are
osteomyelitis, pericarditis, meningitis, Guillain-Barré syndrome, vertebral infections (Landais
et al., 2007) skin rash and chronic itch (Rustscheff, 2005).
Available antibiotic treatment is effective and well tolerated (Tissot Dupont et al., 2007).
Pregnant women and other risk groups
There are some population groups that have some enhanced risk of developing more severe
clinical outcomes in comparison to the general population.
o There is some evidence that Q fever has increased significance in pregnancy. Acute
infection during pregnancy, whether symptomatic or asymptomatic, may result in
abortion and adverse pregnancy outcomes such as premature birth and low birth rate,
the risk being greater in the first trimester. Furthermore, the risks of developing
chronic Q fever may be increased in pregnant women and if chronic infection is
established, C. burnetii may undergo reactivation during pregnancy (even years after
primary infection) which in turn has been associated with higher rates of abortion,
prematurity, and low birth weight (Stein and Raoult, 1998).
o Because the clinical manifestation of chronic Q fever commonly impacts on heart and
circulation, individuals with pre-existing heart conditions, and particularly those with
heart valve defects, heart valve prosthesis or an arterial grafts have some enhanced
risk of developing chronic disease.
o Disease is more likely to develop in immunocompromised individuals and in patients
with renal failure.
Overview of human outbreaks and associated public health impact
Although annual notification rates of clinical disease remains relatively low in the EU, serological data
indicate that infection is more common than disease notification data indicates. Seroprevalence data
varies significantly in EU (Table 9). Crude extrapolations from basic serological data, could quickly
generate figures that suggest that several million EU citizens may have been infected with C burnetii
during their lifetime. However, there are many differences in sampling and diagnostic methodology
that prevent generalised assessment of this data, and the clinical significance of positive serology
remains uncertain in general populations. Hence, the underlying public health impact from such
infection is also impossible to assess. Overall, it seems likely that even taking well acknowledged
underreporting of Q fever into account, the assumption of Q fever as a disease with relative minimal
general impact in the EU is justifiable.
Notwithstanding the generally low public health impact of Q fever, there are circumstances in which
the risk to public health and the public health impact is significantly elevated. Broadly, this is either
because of:
direct exposure to C.burnetii infection from close contact to susceptible animals that may be
infected; typically occupational or similar exposure (direct contact); or
general community-wide exposure where levels of C. burnetii is elevated in the wider
environment because of significant bacterial shedding from infected animals (indirect
contact).
Direct contact
In most parts of the world, Q fever is primarily seen as an occupational disease. Certainly
seroprevalence studies in occupational groups consistently show higher levels of seroconversion,
indicating that such groups are more likely to have been infected with C. burnetii (Table 9 and 10).
Case control studies have also indicated an association between Q fever and occupational exposure to

EFSA Journal 2010; 8 (5):1595

33

Q fever

animals or animal products (Orr et al., 2006). However there is generally limited evidence in the
literature to indicate that such groups have higher incidence of clinical disease in either acute or
chronic forms than general populations. Hence the clinical significance of the serology studies is
difficult to interpret, but it has been presumed that many cases in occupational groups are not
identified at the time of illness (Orr et al., 2006). This may be a case ascertainment artefact because
sporadic Q fever caused by direct exposure is less likely to be diagnosed than in an outbreak setting, or
occupationally at risk groups may be more resistant to clinical disease following infection. Additional
consideration of routes of exposure via direct contact can be found in Chapter 3.2.2.
Table 10: Seroprevalence of C burnetii in occupational groups and the general populations
Netherlands

Farmers
68% (94)

Veterinarians
84% (221)

General population
2,4% (5654)

Poland
France

17,8% (90)
37% (168

25%(12)

7,8% (22496)

Italy
Spain

73,4% (128)

100%(12)
11%(472)

13,6%(280)
48,6%(595)
23,1%(863)

Sweden
Denmark

28% (147)
3%(163)

13%
36% (87)

References
Richardus et al., 1987
RIVM 2009
Cisak et al., 2003
Thibon et al., 1996,
Tissot Dupont et al., 1992
Monno et al., 2009
Bartolome et al., 2007
Pascual et al., 1998
Macellaro et al., 1993
Bosnjak et al., 2009

Indirect contact
The dispersal of C. burnetii and the associated indirect exposure to the pathogen in community
settings has greater public health significance because it can lead to multiple infections and clusters of
cases. An overview of human outbreaks of Q fever in EU MS and neighbouring counties, based on
literature published since 1999, is presented in Table 10. In the largest outbreaks, in Bulgaria (in
Panagyurische 1993) and the Netherlands (2008), at least 1,000 human cases were recorded. Another
outbreak in Bulgaria (2004) resulted in 220 hospitalisations alone (Kamenov and Tiholova, 2004).
Although no information is published on the level of Q fever associated symptoms in the general
population, one can quickly extrapolate for the hospitalisation data that several hundreds of people are
likely to have suffered some immediate public health impact due to acute infection. Of those, some
will have developed chronic infection with associated negative long term health impact. In the
Netherlands, at least 20% of approximately 3,500 cases reported between2007-2009 were hospitalized,
and 7 fatalities have been associated with acute infection. Furthermore, clinical follow-up
demonstrates that even acute Q fever is not always a mild disease with short duration. Patients
diagnosed with acute infection may suffer from persisting fatigue for several months after disease
onset (Schimmer et al., 2007). In addition, some patients, particularly those with known risk factors,
will develop chronic infection and associated clinical symtomology such as endocarditis. Previous
studies suggest that between 1-5% of those that contract acute infection will go on to develop chronic
Q fever. Crude extrapolation from the Q fever notification rates in the Netherlands would suggest that
of the 3,500 acute clinical cases reported since 2007, between 35- 175 could develop chronic infection.
The impact on such individuals is particularly significant, and will lead to premature death and lower
quality of life in many cases, even if treatment is administered.
An update of the literature review for human outbreaks in European countries made by ArricauBouvery and Rodolakis (2005) was done for this opinion; the results are presented in Table 11.
Comparisons between outbreaks are difficult since outbreak investigations vary on case definition
laboratory tests used.

EFSA Journal 2010; 8 (5):1595

34

Q fever

Table 11: Human outbreaks of Q fever in European countries
Year
Start

1982

End

1983

1984

Most-likely
Source

No. of
cases

Laboratory
diagnosis

Germany

Ruminants

156

CFT

Bulgaria

Ruminants

725

CFT

Country

1985
1987

1988

Bulgaria
Italy

Ruminants
Sheep

544
235

CFT
NA

1990

1995

France

Sheep

289

IFA

1992

Germany

Sheep

80

CFT

1993
1994
1996
1996

Bulgaria
Germany
Bulgaria
France

livestock
Sheep
livestock
Sheep

>1000
>18
NA
29

CFT
CFT
CFT
IFA

1996

Germany

Sheep

56

ELISA

1997

Bosnia

Sheep

26

serology

1999

Germany

82

NA

2000

France

Sheep
manure
Goat manure

10

NA

2000

France

Sheep
manure
Sheep
Sheep
livestock
Sheep

5

IFA

75
3
121
88

NA
NA
CFT
IFA

2000

2000
2001
2002
2002

2001

Germany
Germany
Bulgaria
France

2002

Jul-Sep

United
Kingdom
Germany
Germany
Italy

Straw board

95

CFT

Sheep
Cattle
Sheep

299
8
133

ELISA

Sheep and
goats
NA
Sheep and
goats
Sheep
Sheep and
goats
Sheep
Sheep

133

IFA

60
220

IFA
IFA, CFT

14
22

CFT
IFA

331
110

ELISA
IFA

Goats

182

IFA

Sheep
Sheep

35
18

IFA

2003
2003
2003
2003

Jan-Feb

Italy

2003
2004

Jan-Feb

Spain
Bulgaria

2004
2004

Croatia
Spain

2005
2006

Germany
United
Kingdom
Netherlands

2007
2007
2007

7

Apr
Apr-

Slovenia
France

IFA

Reference(s)

Stelzner et al., 1986
Kramer 1990
In Martinov 2007a
In Martinov 2007a
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
Schneider et al., 1993,
Molle et al., 1995
In Martinov 2007a
Schulze et al., 1996
In Martinov, S. 2007
In Arricau-Bouvery and
Rodolakis 2005
Lyytikainen et al., 1997,
1998
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
In Arricau-Bouvery and
Rodolakis 2005
RKI 2001
RKI 2001
Martinov, S. (2007)
In Arricau-Bouvery and
Rodolakis 2005
VanWoerden et al., 2004
Porten et al., 2006
RKI 2004
In Arricau-Bouvery and
Rodolakis 2005
Starnini et al., 2005
Garcia-Clemente et al., 2007
Panaiotov et al. 2009
Martinov, 2007
Medic et al., 2005
De los Rios Martin et al.,
2006
Gilsdorf et al., 2008
Wilson et al., 2009
Van den Brom and Vellema,
2009
Grilc et al. 2007
INVS 20097

http://www.invs.sante.fr/publications/2009/fievreq_ florac2007/RAPP_FIEVRE_Q_Florac_2007.pdf

EFSA Journal 2010; 8 (5):1595

35

Q fever
May
2008

2008
2008
2009
2009
2009
2010

Jan-Mar

JanMay

Netherlands

Goats

1000

Germany

sheep

>46

Germany
Germany
Netherlands

sheep
sheep

>56
5
345

Netherlands
Germany

Goats

2357
235

IFA

IFA
IFA

Schimmer et al. 2009, Van
den Brom and Vellema,
2009
RKI, 2008, Hamann et al.,
2009
RKI, 2008
Henning et al., 2009
Schimmer et al., 2009
Van der Hoek et al 2010
Brockmann et al., in press

Indirect Immunofluorescence Assay (IFA); Enzyme Linked Immunosorbent assay (ELISA); Polymerase Chain Reaction
(PCR); Complement fixation test (CFT)

In addition to the general elevation of risk to populations exposed to C. burnetii through either direct
or indirect contact with known infection sources, there is also significant variation within populations
in both susceptibility to clinical infection and resultant clinical manifestations. Risk groups such as
pregnant women, the immunocompromised and those with pre-existing heart conditions have an
enhanced risk of serious clinical manifestation to acute infection, and also to developing chronic
disease with associated long term health impairment.
Broader implications of the current Q fever outbreak in the Netherlands
It is difficult to determine whether the expanded epidemic in the Netherlands equates to a more
general elevation of risk for human populations in the EU as a whole. Certain epidemiological factors
associated with the Netherlands outbreak are relatively unique, such as the high density of intensively
farmed goat herds, and their proximity to large urban areas and human populations. It may be that
as-yet poorly defined factors may also play an important role in creating the Dutch situtation. Many
such contributory factors could be proposed including agent factors (such as increased virulence or
transmissibility of circulating strains; this remains poorly defined), unique environmental factors
(associated with climate, wind and temperature), ‗public health‘ factors (including improved
diagnostics and local awareness contributing to high case asecertainment), and host factors (such as
waning immunity in the local Dutch population due to specific population demographics and
urbanisation). However, while the convergent of many risk factors are clearly specific to the Dutch
situtation, there are much in the epidemiological background that is not unique to the Netherlands: the
general mechanisms of C. burnetii maintenance in animals populations, its environmental persistence,
its widespread prevalence, and the presence of domestic ruminants and farming systems that could
lead to amplification of the pathogen in animals are all relatively common in the EU. Hence it is likely
that pathogen spillover from animal hosts will continue to occur, including particularly following
abortion episodes when the bacterial load is greatly elevated. This means that humans will continue to
be exposed to the C. burnetii in the EU both through occupational exposure and direct contact with
infected animals, and through the aerosolisation and dissemination of the pathogen into the wider
environment. It is noteworthy that a study of the evolving epidemiology of Q fever in Germany also
revealed an increase in human disease in recent years (Hellenbrand et al 2001). Increased urbanisation
in rural areas is hypothesised as a contributing factor. If this pattern is mirrored in other EU MS, it is
likely that more people may be exposed to the pathogen in the EU, which in turn is likely to result in
an increase in clincial cases. This is particularly the case if exposed urban populations are more
immunologically naïve to C. burnetii that established rural communities.
Taken together, it is clear that while the impact of Q fever on public health is negligible in most
circumstances, there are clearly specific circumstances and certain population groups where this
underlying assessment of negligible risk is no longer valid. Direct exposure to domestic ruminant
livestock or associated animal products that are the primary reservoir of C. burnetii clearly poses an
enhanced risk of C.burnetii infection in comparison to the general population. However, the greatest
public health risk, and the most significant public health burden arise from Q fever is associated with
EFSA Journal 2010; 8 (5):1595

36

Q fever

community-acquired infection due to spillover from animal reservoirs to humans. As discussed above,
and considered in more detail in Chapter 3, the cause of spillover is multifactoral and complex, but the
resultant impact on public health can be very significant.
In the final analysis, although many uncertainties remain concerning the emergence of Q fever in
humans, strengthening general routine surveillance and reporting in both animal and human
populations will increase the probability that these episodes will be identified early. More specifically,
a risk-based surviellance approach could be helpful in supporting public health action; at base level
some active monitoring to determine the early local presence of C. burnetii in domestic ruminants
would support early awareness of the presence of the pathogen. Where C. burnetii is identified in a
locality, enhanced surveillance, including particularly following abortions in domestic ruminants,
would give early indication of possible amplification and an elavation of public health risk. In
addition, rapid notification of abortion and associated diagnostic testing, irrespective of the presumed
status of C burnetii, would be valuable to ascertain cause and thereby support both animal health and,
if necessary public health action such systems must be complemented by strong and well-defined
communication channels between veterinarians and public health counterparts, to ensure mutual
information exchange on potential Q fever events in both animals and humans. The ‗one health‘
approach to reporting and communication of potential Q fever outbreaks is vital to ensure that early
action is taken to reduce public health risks.

Overall, it is justifiable to consider Q fever as a disease with minimal general public
health impact in the EU; even taking underreporting into account, notified case numbers
are low and human to human transmission is so rare as to be epidemiologically
insignificant.
There are circumstances in which the risk to public health and the impact on public
health is significantly elevated; primarily from either direct (occupational) exposure to
Q fever infected animals, or community based exposure caused by an elevation of
C. burnetii in the wider environment following release and dissemination from infected
animal hosts. The latter has greater public health concern.
There is some consistency in the incidence of acute and chronic disease in EU
outbreaks; typically 50% of those with acute infection report symptoms of which self
limiting flu-like febrile illness is the most commonly described. Of those, approximately
1% will develop chronic infection with more severe long term sequelae.
There is huge variability in clinical manifestation within exposed populations and the
basis for this is poorly understood. However, there are some specific at-risk groups
where likelihood and clinical manifestation may be more severe in comparison to the
general population: those with underlying heart valve disorders, the
immunocompromised and pregnant women. In some circumstances, specific targeted
measures to minimise exposure and monitor infection status may be justified for such
groups.
Treatment with appropriate antibiotics is effective and indicated for the management of
both acute and chronic Q fever.

2.3.2.

Significance and impact on animal health

In ruminants, C. burnetii may induce reproductive disorders including abortion, stillbirth, and the
delivery of weak and non-viable neonates. Signs such as placentitis, endometritis, abortion, stillbirth,
infertility, and weak offspring (Davis et al., 2007) should trigger an investigation, considering Q fever
among the differential diagnoses. C. burnetii localises in the uterus and mammary glands of infected
animals (Babudieri, 1959; Martinov 2007b). Cattle may present with metritis and infertility, and
mastitis has been described (Moffa et al., 1970). Data from Germany indicate that a majority of the
reported cases involved cattle (see section 5.2.1). Experimentally induced Q fever with respiratory
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Q fever

manifestations in lambs and a sheep has been described by Martinov (2007a). Note, however, that
infection in ruminants is frequently subclinical, and Q fever incidence in domestic ruminants remains
unclear because abortion rates – other than in some herds of goats – are frequently low (Rodolakis,
2009) and probably not investigated. Ewes with naturally acquired C. burnetii infection can show no
clinical signs and lamb normally (Berri et al., 2005a). Studies on the impact of Q fever in milk
production are, to our knowledge, not available. In goats, where the lactation period can be extended,
milk production is unlikely to be significantly affected. The impact of C. burnetii infection on the
incidence of mastitis and metritis is uncertain
Based on the data available the impact of Q fever on animal health in Europe is unlikely to be very
high. Although infection with C. burnetii in domestic ruminants is common, clinical disease is rare. In
small ruminants, clinical cases are generally sporadic, and abortion episodes are relatively rare. In the
current Dutch outbreak, however, abortion episodes affecting up to 60% of at-risk goats have been
observed, particularly during the first Q fever outbreak on affected farms. Nonetheless, Q fever has a
much lesser impact than conditions such as ovine brucellosis and enzootic abortion (caused by
infection with Chlamydophila spp.) as a cause of late abortion and associated reproductive disorders in
small ruminants.
Based on the available information, there is limited impact of Q fever on the health of
domestic ruminants (cattle, sheep, goats) in Europe
o In small ruminants, clinical cases are generally sporadic, and abortion episodes relatively
rare. In general, Q fever has a much lesser impact on small ruminants than conditions
such as ovine brucellosis and enzootic abortion (caused by infection with Chlamydophila
spp.). However, the impact on individual goat farms during an abortion episode can be
significant.
3.

Risk factors for C. burnetii maintenance and spillover
3.1.

Transmission routes

A broad range of species has been identified as reservoirs for C. burnetii, including mammals, birds,
and arthropods (ticks). Sheep and goats are the most frequently implicated as the source of human
infection (Rodolakis, 2006). C. burnetii infection occurs mainly after inhalation of aerosols (aerial
transmission) generated from excreta from infected animals (abortion and birth material, faeces, urine,
milk) (Angelakis and Raoult, 2010). Direct transmission (close contact) or indirect (long distance)
through aerosols may occur. (Schimmer et al., 2010). A simplified diagram of the transmission routes
is presented in Figure 3.
Source

transmission

host

indirect transmission
environment
aerosol
abortion material
birth material
faeces/manure
urine
milk

Risk factors

human or
animal

direct transmission

Figure 3: Transmission routes for Coxiella burnetii infection in humans and animals (adapted
from Roest 2010)

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Q fever

The WG developed a simple conceptual model, separately highlighting:
the maintenance of infection in animal populations (focusing on domestic ruminants), and
the spillover of infection from animal populations to humans through a process of
amplification, transmission and exposure (Figure 4).

Figure 4: A conceptual model for maintenance of C. burnetii infection in domestic ruminant
populations, and spillover from animals to humans (A, animal, H, human)
Farmed ruminants, and particularly sheep and goats, are implicated as the main source of
human infection
C. burnetii infection occurs mainly after inhalation of aerosols (aerial trtansmission)
generated from infected animal excreta (abortion and birth material, faeces, urine, milk).

3.2.

A review of published literature
3.2.1.

Factors affecting the maintenance of C. burnetii infection in domestic
ruminants

Factors affecting the maintenance of C. burnetii infection in animal populations can be grouped
according to:
a) Agent factors, relating to the characteristics of C. burnetii, and in particular infectivity,
virulence and resistance to environmental conditions;
b) Host factors, including animal species, susceptibility, infectiousness, age and sex; and
c) Environment factors , related to animal management, as well as manure management and farm
characteristics.
Agent factors
Q fever was described as a febrile illness, which had started to occur in 1933 in abattoir workers in
Brisbane, Queensland, Australia (Derrick, 1937). It was originally identified as a species of Rickettsia
and also isolated from ticks (Davis and Cox, 1938). Based on philogenetic investigations, however,
C burnetii is no longer regarded as closely related to Rickettsiae (Labrenz and Hirsch, 2003) and had
been placed in the Coxiellaceae family in the order Legionalles of the gamma subdivision of
Proteobacteria. It is a gram negative obligate intracellular bacterium, a small pleomorphic rod (0.2–0.4
mm wide, 0.4–1.0mm long) adapted to resist and thrive within the phagolysosome of the phagocytic
cells. The organism may occur as a large cell variant (LCV), small-cell variant (SCV) or small dense
cell (SDC). The LCV of C. burnetii is intracellular and metabolically active, undergoing sporogenic
differentiation to produce resistant, spore-like forms. The SDC and SCV forms are able to survive
extracellularly as infectious particles (OIE, 2009). C. burnetii can survive for up to 42 months at 4-6°C
in milk, 12 to 16 months in wool, 120 days in dust, 49 days in dried urine, 30 days in dried sputum
(NABC, 2010). C. burnetii has a number of important physical characteristics including stability
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Q fever

against acids (up to pH 4.5), temperature (62 C for 30 minutes), UV light and pressure (up to 300.000
kPa). Further, the organism can survive for more than 6 months in 10% saline. C. burnetii is killed
following exposure to 5% chloroform or formaldehyde gas (in an 80% humidified environment) (with
less than 30 minutes exposure), to 5% H2O2, 0.5% hypochlorite and 70% ethanol (all with 30 minute
exposure), and following pasteurization (at least 72°C for 40 seconds) (Frangoulidis, 2010).
C. burnetii is extremely infectious (Byrne, 1997; Kim et al., 2005; Nochimson, 2004). Under
experimental conditions, the inhalation of a single Coxiella cell can produce infection and clinical
disease in humans (Tigertt, 1961); similar studies have not been done in animals. It is likely that the
dose of inoculum is relevant to the course of the infection. Mice inoculated with 105 C. burnetii CbC1
developed an efficient immune response with a weak level of IL10 and a high level of IFN- that
reached a peak after 2 weeks. In contrast, mice inoculated with 107 C. burnetii CbC1 produced a low
level of IFN- and a very high level of IL-10, with possible evolution to chronic disease. The level and
kinetics of IFN- production varied according to the strain isolated (Rodolakis A. unpublished data).
Pulsed field gel electrophoresis (PFGE) and RFLP patterns of 80 C. burnetii isolates derived from
animals and humans in Europe, USA, Africa and Asia allow the distinction of twenty different groups
corresponding to geographical origin of the isolate. However, no correlation between restriction group
and virulence of isolates was detected (Jager et al., 1998). The importance of strain as a risk factor for
both maintenance of infection and disease progression is unknown. Knowledge of the virulence
determinants of C. burnetii has been hampered by a lack of methods for genetic manipulation. Further,
accurate methods are not available to assess strain virulence. Strains isolated from cattle and goats
have been observed as more virulent that those isolated from aborted ewes in mouse models as well as
presenting lower growth in embryonated eggs (A. Rodolakis, unpublished) but this work is still
ongoing.
Using MLVA and MST genotyping methods, it has been possible to identify up to 36 distinct
genotypes of C. burnetii. As yet, there is no evidence of species specificity.

C. burnetii is highly resistant to environmental conditions, surviving for many months
under a range of conditions.
The organism is extremely infectious (in humans, infection could occur following
inhalation of a few organisms). The initial dose is likely to affect the subsequent course
of infection.
The relationship between genotype/isolates and virulence is at the moment unclear.
There is no clear evidence of species specificity.
The importance of bacterial genotype/isolates on maintenance of infection and disease
progression is uncertain.

Host factors
Host factors play a key role in the natural history of C. burnetii infection in human; similar
information for ruminants is lacking. Nonetheless, seroprevalence varies between species of domestic
ruminants in the same geographical area. Further, the evolution of disease, including clinical signs, is
not the same in cattle, sheep or goats.
During chronic infection, C. burnetii is mainly found in the uterus and mammary glands (Babudieri,
1959). Shedding of C. burnetii into the environment mainly occurs during parturition; over 109
bacteria are released at the time of delivery (Babudieri, 1959). Goats and cows mostly shed C. burnetii
in milk and vaginal mucus (Rodolakis et al., 2007; Guatteo et al., 2006a) whereas ovines shed mostly
in faeces (Rodolakis et al., 2007; unpublished GDS data). Goats and cows shed C. burnetii in milk for
several months or years. The udder (Behymer et al., 1977; Bell et al., 1949; Moretti, 1984) and
retromammary lymph nodes (Plommet et al., 1973) can remain infected for more than 20 months.
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Q fever

Goats can be chronically infected and may shed C. burnetii for up to two pregnancies after being
infected (Hachette et al., 2003). In addition, goats can abort twice following infection (Berri et al.,
2007; unpublished ANICAP data) and shed C. burnetii in placenta and vaginal mucus during two
subsequent kiddings (unpublished ANICAP data). In contrast, ewes aborted only once (Berri et al.,
2002; unpublished GDS data) and did not shed in vaginal mucus at subsequent lambings. The duration
of excretion (Table 12) of the agent, husbandry conditions and other factors may each play an
important factor in the differences observed in animal seroprevalence and the persistence of infection.
Table 12: Longest observed duration of excretion during the follow up of naturally or
experimentally infected animals (from Arricau-Bouvery, 2005)

Cow
Goat
Ewe

Vaginal mucus
Not determined
14 days
71 days

Duration of shedding
Feces
14 days
20 days
8 days after lambing

Milk
13 months
52 days
8 days

There is a significant relationship between age and seroprevalence in sheep (Kennerman et al., 2010),
most likely as a consequence of opportunity for exposure. In infected flocks, seroprevalence is very
high among adults, noting that replacement ewes (<10 months) are not exposed to the bacteria until
the lambing season (Garcia-Peres et al., 2008). At their first kidding, young goats shed more
C. burnetii than adults (6.2 versus 2.8 log for previously infected adults; unpublished ANICAP data).
A similar pattern is observed in cattle herds (Guatteo et al. 2008). The role of males in the persistence
of infection is not well studied, although C. burnetii has been isolated from bull semen (Kruszewska
et al., 1997).
Other animals may also play a role in the maintenance of the infection in domestic ruminants. The
reservoirs for C. burnetii are extensive, but only partially known, including mammals, birds and
arthropods (mainly ticks). Cats and dogs, but perhaps also foxes, may play a role in the persistence of
the disease on a farm. Over 40 ticks species can be naturally infected (Maurin and Raoult, 1999). They
are likely to play a significant role in transmission among wild vertebrates, but are not considered to
be essential in the cycle of C. burnetii infection in livestock (Babudieri, 1959). Nonetheless, a strong
correlation has been reported between seropositivity and ticks infestation in animals (Psaroulakis
et al., 2006). Wild rats may constitute a reservoir of C. burnetii and play a role in the maintenance of
infection (Webster et al., 1995)

The evolution of infection (including duration and routes of excretion, clinical
presentation) varies between different farmed animal species, which may influence
animal seroprevalence and persistence of infection.
Shedding of C. burnetii mainly occurs around parturition. Abortion products are where
largest bacterial concentrations are found but birth products, vaginal mucus, milk
urineand faeces are also sources.
In general, seroprevalence increases with age, most likely as a consequence of
opportunity for exposure.
The role of males and of transplacental transmission in the persistence of infection is
uncertain.
A range of animal species may play a role in the maintenance of infection in domestic
ruminants, including cats, dogs and possibly foxes and rats.
Ticks can be naturally infected with C. burnetii, but seem not to be important in the
maintenance of infection in domestic ruminants.

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Q fever

Environment factors
As in humans, it is likely that infection of livestock occurs mainly by inhalation of contaminated
aerosols. Consequently, pathogen pressure is likely to be increased with factors that increase the
concentration of C burnetii in the environment (including herd size, synchronization of
lambing/kidding, regrouping of animals from different flocks). Animal density and husbandry
practices have been investigated as potential risk factors for increased seroprevalence of Q fever in
animals (Martinov et al., 2007). In sheep, a significant association was found between seroprevalence,
but not PCR status, and size of flock (Kennerman et al., 2010; Garcia-Perez et al., 2008). In Danish
dairy herds, there was no significant association between the regional density of dairy farms and the
prevalence of antibody-positive farms (Agger et al., 2010). Abortions have also been identified as an
important risk factor for herd status. Abortions in goat herds were linked to exposure, at a state fair, to
another herd where goats had kidded prematurely (Sanford et al., 1994). Similarly, a link has been
identified between cattle abortion and the serological status of the herd to Q fever (Cabassi et al.,
2006). Consequently, husbandry practices that control the exposure of animals to infectious doses of
C. burnetii, such as segregation of areas for lambing and kidding as well as removal of placenta and
abortion materials, will be of use in reducing bacterial exposure.
The role of manure in transmission of Q fever between ruminants and human is well documented
(Berri et al., 2003; Reintjes et al., 2002). Using PCR methods, transplacental infection has been
demonstrated in the aborted foetus of experimentally infected goats, however, neither lesions nor
C. burnetii antigens were detected in foetuses from goats killed during gestation (Sanchez et al.,
2006). A recent study implicated macrophages in the pathogenesis of C. burnetii infection, suggesting
that they transport the organism to the foetus (Bildfell et al., 2000).

A range of environment factors have been sugested to influence the maintenance of
infection in farmed animal populations, including increased herd/flock size, animal density,
and herd/flock density. Pathogen pressure is likely to increase in association with farm
factors that increase the concentration of C. burnetii in the environment.
C. burnetii contaminated manure has been identified as a source for Q fever in human
outbreaks. It is likely that it also plays a role on the maintenance of infection in animal
populations.

3.2.2.

Factors affecting the spillover of C. burnetii from domestic ruminants to
humans

The mechanisms for spillover of infection from farmed livestock to human populations may be best
understood if considered as three related stages stages:
i.
ii.
iii.

Amplification, in the domestic ruminants population;
Transmission, either directly or indirectly; and
Exposure of humans.

Amplification
A number of factors are associated with the maintenance of infection, as discussed in section 3.1.2. In
several human outbreaks, human disease as linked with parturition, and particularly abortion, in
domestic ruminants. Several authors have described a seasonal variation in the incidence of human
disease in the spring and summer, which has been attributed to spring lambing (Maurin and Raoult
1999; Hellenbrandt et al., 2001) or kidding (Schimmer et al., 2010). An infected dairy goat farm with
abortion problems has been identified as the most likely source of a cluster of human cases in the
Netherlands in the 2008 outbreak (Schimmer et al., 2010). In a study in France, human cases have

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Q fever

been associated with reported abortions in goats, but not cattle (Chaillon et al., 2008). Parturition, and
particularly abortion, is associated with increased concentrations of bacteria in the environment.
Parturition in animals, and particularly abortion, is associated with increased concentrations
of bacteria in the environment.
Transmission and exposure
A range of factors are associated with transmission and exposure, as follows:
From experimental and epidemiological evidence, there is no doubt that contaminated aerosols
are the major mechanism whereby C. burnetii is transmitted to humans (Benenson and Tigertt,
1956; Tigertt et al., 1961; Gonder et al., 1979; Marrie et al., 1989).
Persons in contact with domestic ruminants can be infected by inhalation of contaminated
aerosols from amniotic fluid or placenta. Some studies have identified a higher human
seroprevalence in healthy populations living in rural instead of urban areas and also in humans
with occupations involving contact with livestock (Cyprus, Psaroulaki, 2006a; Greece, Pape,
2009b), whereas others have not (Spain, Cardenosa, 2006; Turkey, Kilic et al., 2008). Several
studies have identified a higher seroprevalence to Q fever among farmers, abattoir workers
and veterinarians, compared to the general population (Moffa et al., 1970; Bosnjak et al.,
2009; Whitney et al., 2009). In 2009, in its assessment of meat-associated microbiological
hazards, the Australian Food Standards8 suggested that „Cattle [sheep and goats] may carry
pathogens normally associated with handling, which could potentially be transmitted via meat
consumption. Notes: Examples include Anthrax (Bacillus anthracis), Melioidosis (Burkolderia
pseudomallei), Q fever (Coxiella burnetii)‟. In California, 29% of workers at a local
meatpacking plant were seropositive to Q fever, with the majority having recently experienced
a clinical illness compatible with Q fever (Anonymous, 1986). A Q fever outbreak in a meat
processing plant in Scotland has been reported (HPS, 2006; Donaghy et al., 2006).
Many cases of Q fever in humans are unrelated to occupation. In several Q fever outbreaks,
including the current outbreak in the Netherlands, cases have occurred in both rural and urban
areas (Hawker et al., 1998; Schimmer et al., 2008; Schimmer et al., 2009).
Several recent outbreaks have been associated with visits to school/hobby farms (de los Rios
Martin et al., 2006, Porten et al., 2006, Tissot-Dupont et al., 2005). Laboratory personnel who
work with infected animals are also at risk (Johnson and Kadull, 1966; Marrie 1990a, 1990b,
1990c).
Humans may also be infected by handling contaminated wool (Abinanti et al., 1955).
In intensive farming premises, the handling of manure (which can be heavily contaminated
with C. burnetii from faeces, urine, reproductive fluids and tissues such as placenta etc) can
generate infective aerosols (Hatchette et al., 2001). Use of manure in gardens has been
identified as a risk factor for human infection (Psaroulaki, 2006a). In the Dutch outbreak, a
seasonal variation was observed during 2007 and 2008, with peak incidence from December
to May correlating with the spread of manure from goat stables (Delsing and Kulberg, 2008).
In the Netherlands, substantial amounts of manure are transported from goat farms (generally
in the south of the country) to other locations. There has been no evidence of a rise in human
cases at locations where this manure has been spread (Vellema et al., 2010, Berri et al., 2003).
There is significant variation in Q fever notificaiton rates between women and men: men are
almost twice as likely to develop clinical disease. These differences have been proposed to be
due to protective effects of female hormones (Leone et al., 2004). There is also a significant

8

Australian Food Standards (2009). Assessment of Microbiological Hazards associated with the Four Main Meat Species.

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Q fever

age-related bias in clincial notification, with adults 5 times more likely to present clinical
disease in comparison to those under 15 years of age.(Rault et al 2005)
There are also instances in the global literature of human Q fever cases being associated with
direct exposure to other animal hosts of C. burnetii , including wild animals (rabbits and rats)
(Marrie et al., 1996, Webster 1995) and pet animals (cats and dogs) (Werth 1989). In North
America, outbreaks of Q fever have resulted from direct and indirect contact with parturient
cats (Marrie et al., 1988a; Marrie and Raoult, 2002). However, such cases appear rare and
where they have occurred they have usually been associated with exposure to animals that
have either recently aborted or given birth.
Environmental factors such as wind and precipitation have been linked with human outbreaks
(Karagiannis et al., 2009; Porten et al., 2006; Gilsdorf et al., 2007). A recent Dutch study
investigated the relationship between environmental factors (vegetation index, land cover, soil
characteristics, soil humidity, past weather conditions) and transmission to humans from
infected farms. Key risk factors of importance included farms with a low vegetation density,
and areas with drier soils (Hunink et al., 2010), highlighting the importance of wind in Q fever
spread. A relationship between farm topography and human cases was found in several
outbreaks in Bulgaria and France.
It is likely that windborne transmission plays an important role in the dissemination of
C. burnetii (Tissot Dupont et al., 2004). In the current Dutch outbreak, humans living within 2
km of an large infected dairy goat farm had a much higher infection risk than those living
more than 5 km away (Schimmer et al., 2010). In an earlier study, humans within 50m of a
presumed infection source (a sheep meadow) at 8.7 times greater risk that those 400m away
(Gilsdorf et al., 2007). The influence of distance on risk is likely to vary depending on wind
and other weather conditions. Other human cases have been linked to transmission in
association with helicopters (Carrieri et al., 2002), and dust storms (Panaiotov et al., 2009).
Ticks are known hosts of C. burnetii. Over 40 tick species (including Dermacentor
marginatus, Ixodes ricinus, and Rhipicephalus sanguineus) can be naturally infected with
C. burnetii, but they do not appear to be important in the maintenance of infections in
livestock or humans (Maurin and Raoult, 1999). The organism does, however, multiply in the
gut cells of ticks, and large numbers of C. burnetii are shed in tick faeces. Ticks may be more
relevant for the transmission of C. burnetii to domestic mammals than to humans (Kazar,
1996).and is thought to play a role in maintenance of the pathogen in wildlife reservoirs. Ticks
have been implicated in human infections on rare occasions, including via inhalation of
contaminated tick faeces in wool (Hellenbrand et al., 2001).
.
Major outbreaks in humans may occur both in rural and urban areas and many cases of
Q fever in humans are unrelated to occupation.
Persons can be infected by inhalation of contaminated aerosols. This probability increases
with proximity with farm animals.
The handling of manure (which can be heavily contaminated with C. burnetii from faeces,
urine, reproductive fluids and tissues such as placenta etc) can generate infective aerosols.
A range of environmental factors (wind, farms with a low vegetation index, drier soils,
farm topography) have been associated with human outbreaks. Wind dispersion is likely to
play an important role in the dissemination of C. burnetii.

3.3.

Country case studies
3.3.1.

Bulgaria

a. Overview
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Q fever

Bulgaria has a long history of Q fever, and Q fever awareness. Human cases were first reported in the
Balkan region (including Bulgaria) in 1940, among visiting soldiers (Imhauser, 1949; Bieling, 1950;
Robbins et al., 1946; Serbezov et al., 1999, Teoharova et al., 2002, Martinov 2006). The first case in a
Bulgarian resident was diagnosed in 1949 (Mitov, 1949). Pioner of the studies in animals in Bulgaria
is S. Angelov (BAN 1951). Subsequently, there have been both sporadic cases and outbreaks. In
Bulgaria, the disease is notifiable both in humans and animals, and diagnostic facilities are available
(see section 3.1.).
b. Magnitude and distribution
In the last 25 years, there have been 12 outbreaks in humans, leading to between 121 and more than
1,000 serological confirmed cases per outbreak (Martinov, 2007a). Outbreaks have occurred in several
areas and years (e.g. Kneyzha, 1984; Pavvlikeni, 1985; Etropole, 2002; Botevgrad, 2004), sometimes
in the same place on more than one occasion (e.g. in Panagyurische, 1992-1993, 1995) (Serbezov
et al., 1999).
Prevalence estimates are available for humans, animals and ticks, based on a large number of samples
(19,560 patients with atypical pneumonia; 319,993 sera from domestic and wild animals collected
over the last 50 years; 1,769 collected ticks from animals):
Seroprevalence among patients with symptoms of Q fever was 15.0% (of 14,353 patients)
during 1993-2000, and 18.0% (of 5,207 patients) during 2001-2004 (Martinov, 2007a; using
MIFT and CFT). During a general community survey in the 90s (most probably 1995-97)
from 9 Bulgarian regions (a random sample of 224 sera from the human serum bank), a
seroprevalence of 38% was measured and 167 out of 252 patients (66%) with
bronchopneumonia and acute flulike symptoms had antibodies to phase II C. burnetii detected
by CFT or microagglutination test (MA) in 6 regions of the country (Serbezov et al., 1999).
In animal populations, prevalence estimates vary by species, area and time. Four-fold
differences were observed among domestic ruminants in different areas of Bulgaria (Serbezov,
1973). Seroprevalence estimates were obtained between 1950-2006, from goats, sheep and
cattle presented in Martinov (2007a), respectively:
o 1950-1976: Goats (20.5 %), sheep (15.3%), cattle (19.8 %)
o 1977-1988: Goats (10.8 %), sheep (18.2%), cattle (11.8%)
o 1989-2006: Goats (7.6 %), sheep (4.8 %), cattle (5.4 %)
In ixodic ticks, 16.8% (of 1,769 tested) were infected with C. burnetii (Martinov, 2007a; using
the immunofluorescent haemocytic test). In a detailed investigation, 22-26% ticks were
infected (Georgieva, 1984).
c. Risk factors
In Bulgaria, a range of risk factors have been described for the maintenance of C. burnetii in animal
populations and spillover to humans:
Strain. Different pathogenic effects have been observed in guinea pigs and mice when
infected with different isolates from domestic ruminants (Martinov, 2007a, 2007b). These
results may partly explain the observed differences in the clinical presentation of Q fever in
humans in different areas in Bulgaria. However, further work is needed, including the genetic
characterisation of isolated strains, and the investigation of their pathogenic effect in well
recognised model(s).
Host maintenance species. C. burnetii infection (based on antibody response and/or strain
isolation) has been observed in a wide variety of animals, including several species of
domestic livestock, domestic pets, a wide range of wild mammals, birds and ticks (Martinov,
2007a). Two cycles for persistence were proposed, including:

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Q fever

o

[a] natural foci (ticks, wild mammals, birds, with spillover to domestic animals),
resulting in ongoing maintenance of C. burnetii in the environment, and cyclic
recurrence of the disease in both wild and domestic animals, and

o

[an] agricultural foci (cattle, sheep and goats, with spillover to humans), which
presents the main source for infection to humans.

Host spillover species. Goats were considered the most-likely infection source for humans
during the Panagyurische outbreaks in 1992, 1993 and 1995, as these were the only domestic
livestock species in the proximity during the outbreak (Serbezov et al., 1999). In other cases,
a sharp increase in seroprevalence in goats, sheep and cattle was observed in association with
human outbreaks (Martinov, 2007a; Panaiotov et al., 2009). During the Etropole (2002)
ourbreak, 60.5 % of small ruminants (sheep and goat) were seropositive. In the Etropole
(2002) and Botevgrade (2004) outbreaks, there were no reports of abortion episodes in
domestic ruminants, (Ivan Yordanov, Animal Health Department, RVS Sofia district, 30
March, 2010, pers. communication).
Animal husbandry systems. In Bulgaria, there have been substantial changes in animal
husbandry systems over time: extensive animal housing systems were in place during 19501976, centralised, industrial-type housing was introduced during 1977-1988, and numerous
small private farms have been operating since 1989 (Martinov, 2006). These changes may
have contributed to the observed drop in C. burnetii seroprevalence in domestic livestock
during this period. Outbreaks in humans have continued despite this observed fall in
seroprevalence (Kneyzha, 1984; with 725 human cases; Pavlikeni, 1985; with 544 human
cases Panagyurishe, 1992, 1993, 1995; Sopot, Troyan, Blagoevgrad, Pleven, 1996-2000;
Etropole, 2002; Botevgrad, 2004).
Herd size and structure. There has been a fundamental change in herd size since the late
1980s, following the collapse of large state premises and cooperative farms. This has resulted
in a substantial reduction in sheep numbers (8 million in 1990, 3 million in 1997) and an
increase in the number of goats (430 000 in 1990, 1 million in 1997) (Serbezov et al., 1999).
Cattle herds and sheep flocks tend to be large, but managed separately from the human
population, whereas goats are kept in a large number of small herds, including some that are
held in towns and close to human settlements.
Seroprevalence in animals. Human outbreaks have often occurred in areas where
seroprevalence in domestic ruminants was high. In the Etropole (2002) and Botevgrad (2004)
outbreaks, the following serological results were recorded in livestock close to the outbreak:
o

In cattle: 11.6-33%, compared with 7.1-13.1% in the population more broadly,

o

In sheep: 46.7-59.5%, compared with 8.3-14.1% in the population more broadly, and

o

In goats: 63.3 to almost 100%, compared with 7.4-21.7% in the population more
broadly (Martinov et al., 2007a).

Animal proximity. The gathering and movement of domestic ruminants through towns is
believed to be a risk factor of a number of epidemics, including the outbreaks in Botevgrad in
2004 and in Panagyurische in 1992, 1993 and 1995. In Botevgrad, sheep and goats were
gathered around the town by shepherds then subsequently moved to grazing areas (Panaiotov
et al., 2009). Similar practices were observed in association with large human outbreaks
(more than 500 cases) in Kneyzha in 1984 and Pavlikeni in 1985 (Serbezov et al., 1999).
Most of the human cases were not employed in agriculture or the processing of animal
products (Serbezov et al., 1999); further, in Botevgrad outbreak, most human cases were not

EFSA Journal 2010; 8 (5):1595

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owners of goats, sheep or cattle (Ivan Yordanov, Animal Health Department, RVS Sofia
district, 30 March, 2010, pers. communication).
Timing/concentration of lambing/kidding. There has been a shift in the seasonal presentation
of human cases in Bulgaria since the 1990s (from Jan-Apr to Apr-Jul; in Serbezov et al.,
1999), coincident with a change in the timing of lambing and kidding. Following the collapse
of collective farming, the practice of artificial insemination of ewes was stopped. Until 1990,
artificial insemination of ewes was conducted over a defined insemination period in early
autumn; in the 1990s, this practice was abandoned and the delivery period was extended. This
change in practice, in association with an increase of goat numbers, has lead to an increase of
goat deliveries over a more-extended kidding period. Sheep deliver in January-February,
whereas goats deliver in March-April.
Geography. Most of the most-recent 25 outbreaks have occurred in small towns located in
valleys close to mountains or semi-mountains areas (Panagyurische, Sopot, Troyan,
Etropole), or in regions with specific climatic conditions with strong winds (Kneyzha). In the
most recent outbreak in Botevgrad (2004), cases were observed in a town of approximately
20,000 individuals in a valley close to the St. Planina mountain (Panaiotov et al., 2009).
Weather conditions. During the Botevgrad outbreak in May-June 2004, the weather
conditions including a dust storm (at the beginning of May, as reported by residents of the
town), a thunderstorm without rain precipitation (on 2 May), heavy rain (3 May), and strong
wind (greater than 5m/s), without further rain (during 4-6 May) (Panaiotov et al., 2009).
d. Control options
The following control options were undertaken during the Botevgrad outbreak in 2004:
Humans: All patients were hospitalised. Schools were closed for a month during the outbreak,
coincident with the summer holiday. Relevant authorities undertook a campaign of public
awareness.
Animals: All animals were kept in controlled yards outside the town. Those passing through
the town had to follow certain roads, which were disinfected (aerosol disinfection with
chlorenol) every day. Sheep and goats were treated by washing, whereas cows were
disinfected by spraying acaricides (ectomine 3%). Acaricides were also sprayed on public
parks and roads. Protective facial masks were used by people when applying these measures.
Farmers were required to remove animal excrement and disinfect farm places. Potentially
contaminated material were transported outside the town, and disinfected or burned. Milk
collection was stopped. Also, meetings were organised between the local authorities,
veterinary and public health government bodies (Ivan Yordanov, Animal Health Department,
RVS Sofia district, 30 March, 2010, pers. communication).
e. Implications/lessons learned
Two different maintenance cycles for C. burnetii are suggested ([a] natural foci, [an]
agricultural foci). Domestic ruminants (cattle, sheep, goats) are considered the common link
between these two foci.
Risk factors have mainly been identified based on epidemiological observation and
association.
Key risk factors are believed to include:
o
o

An increase in goat numbers, and a change in goat husbandry,
Proximity with goats and sheep of naïve population, and

EFSA Journal 2010; 8 (5):1595

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Q fever

o
o

Dry, windy weather conditions.
Massive reservoir of the infection into the natural foci

Change of the seasonal pattern of human cases appears to be associated with changes in
livestock husbandry systems, insemination practices, population and proximity.
Human outbreaks have continued despite an observed decrease in seroprevalence among
domestic ruminants, particularly goats.
Reporting of Q fever in a given territory depends on the attention of public health authorities,
and the availability of diagnostic methods.
The efficacy of control options has not been formally assessed. Nonetheless, the rapid fall in human
cases during the outbreak in Botevgrad (2004) could be attributed to measures leading to a rapid
segregation of the animal and human population, the removal of farms, and the disinfection of the
environment on farms and paths. There was also an associated increase in public health awareness
following the outbreak.

There is a long history of Q fever, and of Q fever awareness, in Bulgaria.
In the last 25 years, there have been a number of large human outbreaks.
Infection with C. burnetii is prevalent in humans, domestic ruminants and ticks, varying
by area and time.
A number of risk factors for maintenance of C. burnetii (in domestic ruminants) have
been identified including bacterial strain, the presence of wildlife, the type of domestic
ruminant and husbandry system. Additional risk factors for spillover of C. burnetii (to
humans) include herd size and structure, seroprevalence in animals, animal proximity,
the time and concentration of lambing/kidding, geography and weather conditions.
Outbreaks appear to be linked to an increase in goat numbers, a change in goat
husbandry, proximity to goats and sheep, and dry, windy weather conditions. Evidence
in support of these risk factors is mainly based on epidemiological associations.
Human outbreaks have continued, despite an observed decrease in seroprevalence among
farmed ruminants, particularly goats.
No formal assessment of control options has been conducted. Nonetheless, control
effectiveness has been attributed to :
o rapid segregation of the animal and human population;
o Increased attention of public health authorities (earlier diagnosis and proper antibiotic
treatment of humans), and
o Measures applied to reduce environmental contamination

3.3.2.

France

a. Overview
Q fever is a well-recognised disease in France. However, the disease is not notifiable, either in human
or animals and informationabout prevalence and incidence are not centralized at a national level. In
recent years, Q fever has been a public health concern on several occasions. A comprehensive report
was published in 2004 by the French Food Safety Agency (AFSSA, 2004). In addition, some
recommendations for a better control of Q fever in clinically affected herds or flocks were produced in
2007 by a group of experts under the auspice of the ACERSA (the French organisation in charge of
animal health certification) (De Crémoux et al., 2007).

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b. Magnitude and distribution
In humans
Several studies have been published, mainly by the NRL (Prof D. Raoult, University of Marseilles)
The seroprevalence of Q fever in blood donors in the Marseilles area was estimated to be about 4 %
(Tissot Dupont, 1992), consistent with other data from the south of France (5 %) and Burgundy (4.4%)
(AFSSA, 2004). In the southern part of the country (Provence Alpes Cote d‘Azur region), a
seroprevalence study conducted in pregnant woman indicated that between 0.8 and 1.3 women per
1,000 had antibodies levels which could be attributed to recent infections (less than one year) (Rey
et al., 2000). When these data were extrapolated to the whole country, it was suggested that the annual
incidence in France would be in the range of 0.1-1 per 1,000 (Maurin and Raoult, 1999; Tissot-Dupont
et al., 1992). The Chamonix Valley outbreak in 2002 is the most recent episode of major public health
concern, with 89 confirmed human cases including 71 with clinical signs. Nine people, in high risk
groups, received long term therapy. In May 2007, 5 patients with Q fever-like symptoms were
reported in the rural southern French town of Florac with 18 cases confirmed after an epidemiological
survey
In animals
There is no official epidemiological database for Q fever in animals in France. A national reference
laboratory was recently nominated by the French Ministry of Agriculture (Laboratory for Ruminant
and Bee Pathology Studies, AFSSA Sophia Antipolis, France). However, data are available mainly
from local studies conducted with the aim to estimate the C burnetii infection situation in a
geographical area or during a limited period of time.
Q fever diagnostics is not mandatory in France when abortion occurs in herds or flocks, and therefore
Q fever incidence is probably underestimated. During a 5 year period in the district of Deux-Sevres, 5
out of 21 flocks of goats experienced abortion due to Q fever (Chartier et al., 1997). Surveys
conducted between 1993 and 1996 in bovine herds from several administrative districts indicated that
Q fever was the cause of abortion in between 0.5 and 3.8 % of the cases (Berger, 1999). In the past,
the prevalence of the infection has mainly been estimated using seroepidemiological studies, even
though data are not directly comparable due to the lack of harmonization of the techniques. There is a
huge variability of the rate of seropositive domestic ruminants in France (AFSSA, 2004). Despite
these limitations, animal-level prevalence based on various local studies done in France was estimated
by AFSSA (2004) as :
o 1 to 15% for cattle,
o 0 to 20% for sheep, and
o 2 to 12 % for goats.
At the herd or flock level, the estimated prevalence is:
o 39 to 73% (cattle),
o 0 to 89% (sheep), and
o 10 to 40% (goats).
No national survey has been conducted to estimate the prevalence of Q fever in domestic ruminants.
Local and regional data are available, but comparison is problematic. Nevertheless it appears that
C burnetii infection is common in ovine and goat flocks, and is probably more widespread in the south
compared to the north of France. Data regarding cattle are lacking since abortion is less frequently
reported .
c. Risk factors
The wind is considered an important risk factor in France. In the La Crau area where sheep farming is
important and where there is a tradition of outside lambing, the incidence of acute Q fever is 5.4 times
higher than in the city of Marseilles. There is a seasonal pattern of human cases, being highest in
spring in association with lambing, and a dry and windy environment. Further, human cases mainly
located downwind from lambing (Tissot-Dupont et al., 1999, 2004). In 1996, 120 cases were reported

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Q fever

in the town of Briançon, and were attributed to aerosols dispersed by intense helicopter activity in the
vicinity of an old slaughtering house (Carrieri et al., 2002).
A case-control study was performed following the Chamonix valley outbreak in summer 2002. In this
study, cases were more likely to have been in close contact with sheep, or to have attended or
otherwise watched the migration of sheep to their summer location. It is likely that aerosol
contamination could explain most cases (INVS, 20059). Aerosol contamination consecutive to the
cleaning of contaminated pigeon faeces was also reported to be the cause of acute Q fever case in five
members from the same family (Stein and Raoult, 1999). Professional exposure was investigated in a
cohort of 323 human cases (Tissot-Dupont et al., 1992), but was found not to be significant. Of 477
patients affected by Q fever, 8% were agriculture workers or veterinarians, 38% were people living in
rural areas, and 35% had had contact with new born or pregnant animals (Raoult et al., 2000). Of 80
French patients with pneumopathy due to C. burnetii, 32 had contact with animals (59% with sheep,
15.6% with cattle, 28.1% with goat and14.6% with cats) (Caron et al., 1998). A case-control study was
carried-out in a hyperendemic area (Etang de Berre, south of France) from 1996 to 1999. Besides the
role of wind, this study identified exposure to a teaching farm as a key risk factor (Tissot-Dupont
et al., 2005).
The risk factor analysis conducted during the human outbreak in Florac (2007) revealed a significant
association between acute infection and living or working near an area where manure had been spread,
outdoor sport activities, attending the training center‘s canteen for eating, working or social activities.
No link between any particular dairy food item and the occurrence of acute infection was observed
(INVS, 200910, King et al., submitted). Of all (26 tested) goat, sheep and cattle herds/flocks located
within a five kilometre radius of Florac, 11 were ELISA-positive to C. burnetii infection. Nine
herds/flocks were positive by quantitative PCR, including 3 flocks of sheep and 1 flock of goats with
low shedding levels, 2 flocks of sheep and 1 flock of goats with medium shedding levels and 2 sheep
flocks with high shedding levels. It was concluded that the observed excess of cases of Q fever in
Florac, an area endemic for this infection, in spring 2007 could be explained by airborne transmission
from infectious ovine flocks situated close to the town.
d. Control options
During the last two outbreaks in France (Chamonix, 2002; Florac, 2007), control options were taken in
order to limit the outcome of the disease in affected humans and to prevent further infections in
humans. Measures may depend on the local situations. Some examples are given:
Local surgeons were informed about the situation and received recommendations to screen
humans at risk using serology. Pregnant woman were treated and received medical care until
giving birth. Humans with symptoms had a cardiac echography and received a preventive
treatment, on evidence of a valvulopathy, to avoid the risk of chronic Q fever. A national press
bulletin was released recommending medical care (serology and preventive treatment, if
positive) for people who had stayed temporarily in the affected areas during the epidemic.
Blood donation was forbidden from people who stayed in the affected areas during the
outbreaks, and blood products collected during this time were discarded.
Regarding domestic ruminants, several sanitary measures regarding animal movements were
taken (control of animal gathering, no participation in exhibitions, allowing transportation
only by trucks). Recommendations for good-practice, in particular for manure spreading and
dealing with animal birth and abortion products, were implemented. The vaccination of
non-infected animals using a phase I vaccine on seropositive farms was recommended.
Declaration of abortions among herds and the burying of biological materials, such as

9

http://www.invs.sante.fr/publications/2005/fievre_q_chamonix/rapport_fievre_q.pdf
http://www.invs.sante.fr/publications/2009/fievreq_florac2007/index.html

10

EFSA Journal 2010; 8 (5):1595

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Q fever

placentas and birth products, was recommended. Farmers were advised to carry out the
removal of carcasses by quartering, to store manure a minimum distance from human
dwellings, to spread it onto fields with the least exposure to wind, and to plough it in
immediately after spreading.
During the Florac outbreak, dairy production from herds around Florac was pasteurized before
distribution in accordance with recommendations of the French Agency for Food Safety
(AFSSA, 2004). However, since no clinical human case has been associated with consumption
of crude milk products, either in this or other recent Q fever outbreaks in France, systematic
pasteurization of milk is no longer required.
e. Implications/lessons learned
Q fever is endemic in France in domestic ruminants but regional and species differences are
noticeable. The impact of Q fever on domestic ruminant health does not appear high, but improved
surveillance is needed, especially for abortion. Q fever is periodically a public health issue and
outbreaks have been reported in recent years. However, there is no apparent trend towards an increase
of human case throughout the country. All recent human outbreaks were linked to an animal source
and contaminated dust or aerosols. Therefore, control options in affected farms should focus on
sanitary measures to avoid spreading of contaminated materials and to limit the extent of excretion of
C. burnetii by infected flocks or herds. Vaccination of ruminants with a phase I vaccine may be the
most-effective method to decrease C. burnetii excretion into the environment, but is more effective if
given to seronegative animals. Because C. burnetii is highly resistant in the environment, vaccination
is likely to have an impact only in the longer term. Finally, further work is needed to evaluate the
efficacy of the various control options that can be implemented.

Q fever is well-recognised in France. The disease is not notifiable in either humans or
animals, and there is currently no centralized reporting system.
There have been several recent outbreaks of Q fever in humans: in Chamonix in 2002
(89 confirmed cases) and Florac in 2007 (19 confirmed cases).
No national survey has been conducted to estimate the prevalence of C burnetii infection
in domestic ruminants. Local and regional data are available, but comparison is
problematic. Nevertheless it appears that C burnetii infection is common in ovine and
goat flocks, and is probably more widespread in the south compared to the north of
France.
Human cases have been linked to environmental conditions (dry, windy weather) and
proximity to domestic ruminants (contact with animals particularly during parturition,
observing sheep movement, in the locality of manure spreading, a seasonal pattern in
humans that is coincident with time of lambing).
A broad range of control options were applied during the recent human outbreaks in
Chamonix and Florac. On infected farms, control options should focus on sanitary
measures to avoid spreading of contaminated materials and to limit the extent of
excretion of C. burnetii.
Vaccination of ruminants with a phase I vaccine may be the most-effective method to
decrease C. burnetii excretion into the environment, but is more effective if given to
seronegative animals. Because C. burnetii is highly resistant in the environment,
vaccination is likely to have an impact only in the longer term.

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3.3.3.

Germany

a. Overview
It is now commonly accepted that Q fever was introduced into Germany shortly after WWII. Infection
was first observed in the southern parts of Western Germany (Württemberg, Baden and Bavaria). Prior
to 1950, a total of 3,000 patients and 20 deaths were registered, with attack rates of 20% to 46% in
small villages. Contact with domestic ruminants was identified as the main source of infection,
although outbreaks in slaughterhouses were also reported. A large outbreak with more than 500 cases
and 3 deaths has been reported at a dairy fair in Krefeld, Nordrhine-Westphalia in 1958 (Schaaf,
1969). Subsequently, Q fever has spread throughout the two former German states, and is now
considered endemic in Germany.
b. Magnitude and distribution
Q fever has been notifiable in Western Germany since 1962, and in Eastern Germany since 1979
(Hellenbrand et al., 2001). Hellenbrand et al. (2001) present a synopsis of Q fever between 1947 and
1999. They calculated the average annual incidence of Q fever of 1.1 per million population (19791999), with Baden-Württemberg (4.1 per million), Hesse (2.8 per million), Rhineland-Palatinate
(0.9 per million) and Bavaria (0.8 per million) being most affected. In a recent publication, Conraths
et al. (in press) stated that roughly 200 to 400 human cases were registered each year from 2007 to
2009, again most frequently in Baden-Württemberg, Hesse and Bavaria. No significant increase in
cases was seen in Northrhine-Westphalia or Lower Saxony. During a SurvStat@RKI survey
conducted during the years 2004 to 2009, it was clear that many regions notify sporadic cases or
outbreaks regularly, or even every year, e.g. Jena (Thuringia), Göppingen (Baden Württemberg),
Lahn-Dill Kreis (Hesse), Aschaffenburg (Bavaria) etc. These findings demonstrate that Q fever, once
it has become endemic, will remain within local reservoirs for years or even decades. Consequently,
greater outbreaks in humans are registered periodically in these regions. In an update of their work,
Hellenbrand et al. (2005) published some further larger outbreaks during the time period 1999 to 2003;
i.e. outbreaks in Miltenberg, Bavaria (1999; n>100, due to sheep shearing), Ebersberg, Bavaria (1999,
n=19, due to occupational contact to sheep), Rottweil-Göllersdorf, Baden-Württemberg (1999; n=118,
due to exposure to sheep and shearing), Stetten, Baden-Württemberg (1999; n=39, due to a sheep fair
with a shearing show) and Tübingen, Baden-Württemberg (1999; n=13, due to sheep farm). In Table
18 Appendix C, selected outbreaks from 1990 to 2009 are listed. Each has been published in local or
international journal, with exception of an outbreak due to deer in 1997. All outbreaks involving more
than two cases have to be investigated by local authorities; a final report has been prepared, but often
not published. Reports in the local daily press are not included.
Seroprevalence studies in humans have been conducted only sporadically, mostly triggered by human
outbreaks. In a Germany-wide survey amongst blood donors (n=1,611 during 1983-1986), 22% of
samples were positive (Schmeer et al., 1987). Further, 22% of blood donors from the German army
(n=1,651) had anti-Coxiella antibodies (Werth et al., 1991). These sera were collected during 1985 to
1987. Both studies used phase I/II antigen ELISAs. 15.5% of sera from Hesse (n=207, healthy blood
donors) were positive. In 1993, Frost and Hengst found 2.4% to 19.8%, and 16.2% to 56.6%, of sera
(n=1.208) positive when using CFT and ELISA, respectively. The survey was done on the population
of Wiesbaden, Darmstadt, Frankfurt and Giessen (south and middle Hesse). However, in groups of
diseased patients, 30.9% to 60.0% of sera were positive. In 2002, Sting et al. found 56 of 255 farmers
whose dairy cows had abortion problems seropositive for anti-Coxiella antibodies. Abortion and
seroprevalence of cows >20% was correlated with a higher seroprevalence rate in their owners.
Homuth et al. (2006) investigated the sera of 145 farmers, 26 vets and 40 visitors at the agricultural
fair ‗Eurotier‘, Hannover during 2004, and found 1.8%, 0.0%, 0.0% to be truly seropositive,
respectively. Brockmann et al. (in press) report a seroprevalence among inhabitants (n=1,036) from
rural and urban municipalities in Baden-Württemberg of 0 to 18%. In the former German Democratic
Republic, the first cases of Q fever were reported in the beginning of the 1980s. Klug and Maeincke
report on a survey in personnel of a dairy farm: of 556 serum samples tested, 38 (6.8%) were positive
(Klug and Maenicke, 1985). From 1979 to 1990, a total of 209 human cases, but no deaths, were
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reported (Kramer, 1991). A large outbreak, involving 156 patients, in Meinungen, Thuringia was
observed in 1982/83. Kramer (1991) also reports on single cases in the northern districts. Lange and
Hunstock (1993) report on surveys conducted in a veterinary diagnostic institute, and on farms, during
1983 to 1990. Of 767 serum samples, 7.8% were positive. Seroprevalence was higher among milkers
(19.1%), plant farmers (16.4%) and veterinarians (14.3%), in comparison with shepherds (7.4%). In a
veterinary institute, seroprevalence among stockmen was 14.3%, in comparison to drivers (6.3%), vets
(4.3%) and technicians (9.1%), which suggests that time of exposure, direct contact and the type of
occupation were associated with a higher risk for serological conversion. The high seroprevalence
among tractor drivers was attributed to the high risk of inhaling contaminated aerosols whilst
spreading manure and slurry onto the fields. The high seroprevalence connected to ‗calf production‘ is
probably related to milk preparation. The positive titers in the institute personnel were caused either by
using laboratory animals as ‗diagnostic tools‘, working in the autopsy area or transporting samples
(=drivers). However, clinical presentations in all groups were rarely seen.
Q fever in animals in Germany is „meldepflichtig‟; i.e. owners of infected animals, vets and diagnostic
facilities have to inform the local authorities on the occurrence of Q fever (including serological
positive results). State veterinarians then report cases to the federal authorities who are in charge for
gathering these notifications. Hellenbrand et al. (2009) note reports of approximately 300 herds
affected annually with Q fever during the period between 1980 and 1998. In the last decade, Conraths
et al. (in press) found that approximately 130 herds have been notified annually. Germany-wide testing
is not mandatory. Data are generated mainly during veterinary practice (increased abortion rate), from
dairy animals, whose milk is sold without pasteurisation and from human outbreak surveys
(Hellenbrand et al., 2009). In herds/flocks with clinical symptoms, 75% of animals may test positive.
These authors also stated that in 1998, 7.8% of cattle (n=21,191), 1.3% of sheep (n=1,346) and 2.5%
of goats (n=278) were Q fever positive using various tests. Thirteen of 16 German states contributed to
this data survey. In the 1980s, approximately 5 to 10% of cattle herds without, and up to 69% with,
fertility problems were positive for C. burnetii infection, respectively (Hellenbrand et al., 2005). The
seroprevalence in cattle was high in Bavaria, Hesse, Sotuthern Westphalia, Baden-Würtemberg
(Woernle and Müller, 1986; Krauss et al., 1987; Hellenbrand et al., 2001). In a recent study from
Baden-Württemberg, Wagner-Wiening and Brockmann (2009) found that 85% of the reported cases
involved cattle. During 2001 to 2008, a total of 55,373 serological (ELISA and CFT) and 3,491 direct
(PCR and STAMP) tests were conducted: 10.5% (cattle: 8.7%; sheep: 26.4%; goat: 20.1%) and 8% of
these samples were positive, respectively. Most reports concern Q fever in cattle (see Table 19
Appendix C). Interestingly, high seroprevalence was also found in dogs and cats from Germany: 13%
(n=1.127) and cats 26% (n=108) using ELISA, respectively (Werth et al., 1987). Very rarely, culture
was attempted: Heil-Franke et al. (1993) found that 2.0% of aborted calves were positive for
C. burnetii.
In the former German Democratic Republic (GDR), C. burnetii infection was found by means of
serological investigation: during the years 1980 to 1989, 8.3% of cattle, 0.7% of sheep, and 2.8% of
dogs were seropositive, whereas goats, pigs and pheasants tested negative for Q fever (Kramer, 1991).
Regional differences were noted: e.g. in the district of Neubrandenburg, 20% of sheep flocks were
positive and 12.6% of dogs were positive in the district of Rostock. In 11 of 13 districts, positive cows
were present (1.7-23.3%). Kramer (1991) subsequently stated that Q fever was endemic in cattle herds
in the GDR. In some natural foci, Q fever was found in roe deer (Capreolus capreolus) and red deer
(Cervus elaphus). In middle Thuringia, 100% of tested dairy farms and 47% of tested sheep farms
(n=17) were positive for Q fever (Lange and Klaus, 1992). A total of 4.337 ovine serum samples were
investigated during 1983-1986 using CFT: 0.6 to 4.3% of animals in each herd were positive. A
correlation between the number of animals in a herd and the level of management (specifically, poor
management) was noted. A good overview of Q fever in the GDR is available (Kramer, 1990).
Infection with C. burnetii is ubiquitous in sheep and cattle, and probably also in goats, throughout
Germany. Regional differences in distribution are found. Natural reservoirs of infection are present,
which make eradication unlikely. Currently, there is no vaccine licensed for use in cattle, sheep or

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goats. The role of dogs and cats in the infective cycle is unknown. The prevalence in ruminant herds is
high, and appears to have remained unchanged during the last three decades.
c. Risk factors
Of 40 outbreaks investigated during the period, 1979 to 1999, 24 were associated with sheep.Sources
of infection included products of conception, contaminated manure and dust from shearing. In most
cases, either migrating sheep or neighbouring sheep farms could be identified as possible sources. Dry
weather and/or wind were also identified as risk factors. In 6 cases, cattle were identified as the source
of infection (as a result of contact with aborted material, contaminated milk or with cows at abattoirs).
These authors noted a shift from winter to summer outbreaks, possibly due to changes in the sheep
production system; nowadays lambing occurs throughout the year with the introduction of at least two
mating periods per year. Recent outbreaks are also been more frequently associated with urban areas.
In a recent study from Baden-Württemberg, Wagner-Wiening and Brockmann (2009) correlated
available data from human cases and sheep density per km2. They found that human Q fever risk was
higher in areas of higher sheep density (a relative risk of 2.8 if 1 sheep/km2; 19.16 if 10 sheep/km2;
182.55 if 100 sheep/km2, compared to areas without sheep). In municipalities without any notified
case, 7.4% of human residents were seropositive for Q fever compared with 20% in endemic
municipalities. Interestingly, the presence of cattle in municipalities was considered protective. They
found no correlation for ‗dry climate‘. In Baden-Württemberg 191 of 1,109 municipalities reported Q
fever cases.
No significant and recurrent risk factors for Q fever have been identified, apart from direct or indirect
contacts (e.g. dust, aerosols, manure) with infected animals and their contaminated products (birth
products, faeces) (see also Table 18 Appendix C). Diseased animals may pose a higher risk to those
who are taking care for them. Obstetric procedure conducted on animals without clinical signs may
lead to human disease. The role of cats and dogs has not been clarified. The role of natural reservoirs
e.g. wild animals, arthropods or the environment to maintain the infectious cycle within farm animals
i.e. ruminants or cervids is unclear. The quality of farm management is important for clinical disease
in farm animals.
d. Control options
The following options have been applied in herds, to reduce losses for farmers:
antibiotics
antibiotics with vaccination (phase 1 and phase 2)
antibiotics (shortly before parturition to reduce the number of shed bacteria) and vaccination
and culling of seropositive animals
exclusion of seropositive males from breeding
single boxes for birth
regular disinfection with effective disinfectant
use of acaricides (before grazing period, sheep)
disinfection of the fleece (bathing, sheep)
introducing only of Coxiella-negative new animals; quarantine
removing aborted offspring and placenta material (sheep!) immediately
composting of manure for 6 months under plastic foil / earth with non-hydrated lime;
spreading only of manure only without wind and when the weather is dry; manure should be
ploughed under immediately
separation of gravid ewes
reimbursement for all countermeasures for the animals owners
good management practise: feed, water, etc
sentinel animals
no ‗sharing‘ of male animals

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The following options have been used to reduce the potential for transmission of C. burnetii to
humans:
keeping distance to human settlements
no exhibition of gravid domestic ruminants in the last trimester or tick infested animals, no
birth in the public
serological surveys in domestic ruminants and reservoir animals
reduction of stock drive; using tracks far away from human settlements
control of pet sheep in zoos, schools, nursing homes and culling of positive animals
using only Coxiella negative animals in animal experiments e.g. sheep
control of fences (sheep)
restriction of entry for farm visitors etc.
changing of clothes before leaving the farm
special movable equipment
pasteurisation of milk; no selling of raw milk
The following options have been applied during outbreak management:
interchange of information between veterinary public health – public health
serological control of all contact persons, identification of persons with special risk e.g.
immunosuppressed persons
e. Implications/lessons learned
Q fever is endemic in Germany. A constant but underreported number of sporadic cases and outbreaks
in man and domestic ruminants are notified every year. The disease is most often seen in humans but
has no significant impact on animal health. Therefore, new strategies combining the interests of public
health and veterinary public health have to be developed to control Q fever in the future.
Infection with C. burnetii is ubiquitous in sheep and cattle, and probably also in goats, throughout
Germany. Regional differences in distribution are found. There exist natural reservoirs which make
eradication unlikely. Currently, there is no vaccine licensed for use in cattle, sheep or goats. The role
of dogs and cats in the infective cycle is unknown. The prevalence in ruminant herds was always high
and appears to have remained unchanged during the last three decades.

There is a long history of Q fever and infection in Germany. In humans, both sporadic
cases and outbreaks are reported each year. Sheep are the most-frequently implicated
source for human outbreaks. Human seroprevalence is variable, and highest among those
with close contact with livestock.
C. burnetii is endemic among domestic ruminants (sheep, cattle, and probably goats) in
Germany. Seroprevalence is high, with no evidence of change over the last 3 decades.
Q fever is notifiable in Germany, and Q fever cases (clinical signs and/or serological
evidence) are relatively common.
Currently, there is no vaccine licensed for use in domestic ruminants.
Human Q fever risk is strongly associated with direct and/or indirect contact with infected
animals, including those without clinical signs. In one study human cases have been
associated with sheep density per km2.

3.3.4.

The Netherlands

a. Overview
Q fever was first diagnosed in the Netherlands in 1956 (Westra et al., 1958). There was no evidence of
infection in the several years prior to this (Wolff and Kouwenaar, 1954). No antibodies against Q fever
were found in 6,000 samples collected between 1954 and 1956 from humans with an atypical
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pneumonia (Dekking and Zanen, 1958). In a seroepidemiological study performed between 1968 and
1983, an average seroprevalence of 76% was found in high-risk groups, including veterinarians,
taxidermists and female wool spinners. In 1982, 186 of 222 (84%) farm animal veterinary practitioners
were seropositive to Q fever, compared to 86 of 359 (24%) blood donors sampled in 1983. The
seropositive results of the veterinarians were equally distributed over all age groups, suggesting most
infections had occurred in early childhood. Males were more often infected than females (Richardus
et al., 1984; Houwers and Richardus, 1987; Richardus et al., 1987).
In 1978, Q fever became a notifiable disease in humans. The number of notifications between 1978
and 2006, ranged between 1 and 32 cases annually, with an average of 17 cases per year. These cases
predominantly involved patients with occupational risk. The total number of hospitalized persons in
the period 1994–2001 was 49 (Delsing and Kullberg, 2008; Schimmer et al., 2009).
Since May 2007, the Netherlands is facing an increasing human Q fever problem.
b. Magnitude and distribution
In humans:
In May 2007, several cases of atypical pneumonia were reported in the province of NoordBrabant (Steenbergen et al., 2007). Retrospective investigation identified C. burnetii was the
causal agent. In 2007, a total of 168 confirmed human cases were reported. The majority of
cases presented between weeks 18 and 24 (May- June). The cases ranged from 7 to 87 years,
the female to male ratio was 1:1.7, and the hospitalization rate was 50.0% (Schimmer et al.,
2008; van der Hoek et al., 2010). Many patients suffered from persisting fatigue for several
months after the onset of the disease (Nabuurs-Franssen et al., 2009).
In 2008, Q fever returned and at the end of the year 1,000 human cases had been registered,
making it the largest community outbreak of Q fever ever recorded in the world. The main
symptoms were fever, fatigue, night sweating, severe headache and general malaise. In 65%
of the cases, pneumonia was reported (Delsing and Kullberg, 2008; Schimmer et al., 2008;
Schimmer et al., 2009), with a hospitalization rate of 20.9% (van der Hoek et al., 2010).
In 2009, a total of 2,357 new Q fever patients were registered on the national infectious
disease notification database. As clinical signs and symptoms of Q fever are aspecific, this
high number is probably influenced by increasing awareness among patients and doctors.
Nonetheless, the hospitalization rate was 19.7%, comparable to the situation in 2008 (van der
Hoek et al., 2010).
In the first ten weeks of 2010, 237 cases were notified, which was not expected, given
experiences from the preceding 2 years. Further, the epidemic is expanding geographically,
although most notifications are still from the province of Noord-Brabant.
The seroprevalence of C. burnetii was investigated in 5,654 nationally representative samples
taken prior to the human outbreaks (February 2006-June 2007) (van Duynhoven et al., 2010).
Overall, the seroprevalence (past infections) was 2.4%. Ongoing studies in the high incidence
areas show higher seroprevalence and among specific risk groups more than 80% have
antibodies, suggesting old infection.
In animals:
In 2005, Q fever was diagnosed for the first time in the Netherlands, as a cause of abortion on
a dairy goat farm. Diagnosis was confirmed by using immunohistochemistry on sections of
placenta (Wouda and Dercksen, 2007). A second case was diagnosed later in 2005. In 2006,
2007, 2008, and 2009, six, seven, seven, and six new cases, respectively, were confirmed on
dairy goat farms, mainly in the southern part of the country. In the same period, two cases of
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abortion caused by C. burnetii were found on dairy sheep farms, one in the southern and one
in the northern part of the country. The average number of goats per infected farm was 900, of
which 20% of the pregnant goats on average (10% to 60%) had aborted. The average number
of sheep for the two infected sheep farms was 400 and the abortion rate was 5% (van de Brom
and Vellema, 2009).
In 2008, all 15,772 blood samples from small ruminants to be tested for Brucella melitensis
monitoring, were also tested for Q fever using an ELISA (Ruminants Serum Q fever LSI Kit,
LSI, Lissieu, France). From those samples, 12,363 were of ovine and 3,409 of caprine origin.
Based on these blood samples, seroprevalence for sheep in the Netherlands was 2.4% (95%
confidence interval [CI]: 2.1–2.7) and for goats 7.8% (95% CI: 6.9–8.7) (van den Brom and
Vellema, 2009).
Dairy sheep and dairy goat farmers were also given the opportunity to test bulk milk samples
using a PCR (TaqvetTM Coxiella burnetii, TaqMan Quantitative PCR, LSI, Lissieu, France).
In total, 306 bulk milk samples were tested and 79 (26%) were positive (van den Brom and
Vellema, 2009).
By 18 February 2010, 73 dairy goat farms and 2 dairy sheep farms, out of the total of 360
dairy goat farms and 40 dairy sheep farms with more than 50 animals in the Netherlands, had
been declared infected based on PCR-positive bulk milk testing.
c. Risk factors
The sheep and goat industry in the Netherlands is relatively small with less than one million breeding
ewes and a quarter of a million breeding goats (I&R-database, 2009). The total number of registered
small ruminant farms is slightly more than 50,000, of which 360 are professional dairy goat farms with
over 200 adult goats and 40 are professional dairy sheep farms. All dairy goats are housed throughout
the year, except approximately 17,000 goats kept on organic farms. The dairy goat industry started
following the introduction of the milk quota system in the dairy cattle industry in 1984. In the ensuing
25 years, total goat milk production has grown from almost zero to over 150 000 tonnes annually (van
den Brom and Vellema, 2009).
In retrospect, a large human cluster in an urban area in 2008 could clearly be linked to a dairy goat
farm with more than 400 animals with a Q fever related abortion episode a few weeks before the first
human cases presented. Persons living within 2 kilometres of the farm had a much higher risk for
Q fever than those living more than 5 kilometres away (relative risk 31.1 [95% CI 16.459.1])(Schimmer et al., 2010).
There is consensus among public health and veterinary professionals that most of the human Q fever
cases are linked to abortion on large dairy goat farms, and to a much lesser extent on dairy sheep farms
(van der Hoek et al., 2010). Additional factors such as the role of manure or strain virulence possibly
influencing transmission are currently under investigation.
C. burnetii can be typed using by MLVA (Arricau-Bouvery et al., 2006; Svraka et al., 2006). In the
Netherlands, in total 14 different MLVA types have been found in 253 clinical samples from dairy
goats, and two from dairy cattle. One MLVA type is predominantly present on dairy goat farms with
abortion problems due to Q fever and on all goat farms in Noord-Brabant. One goat farm outside
Noord-Brabant showed a different MLVA type. The two cattle MLVA types of C. burnetii could
clearly be distinguished from all goat MLVA types (Roest, 2010).
A large multidisciplinary research programme is being conducted, to generate an improved
understanding of Q fever, including C. burnetii transmission, to inform improved control options.

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d. Control options
Before June 2008, abortion outbreaks were reported on a voluntary basis to the Animal Health Service
(GD) and confirmed by immunohistochemistry (Wouda and Dercksen, 1997). Since June 2008,
Q fever in small ruminants is notifiable in the Netherlands. Notification criterion for farms with over
100 breeding animals is an abortion wave, defined as an abortion percentage over 5% of all pregnant
small ruminants. For smaller holdings, three or more abortions in a 30-day period is used as the basis
for notification of authorities.
Because of the consensus between public health and veterinary professionals that most of the human
Q fever cases are linked to abortion waves on large dairy goat farms, and to a much lesser extent on
dairy sheep farms, interventions have focused on these types of farms. Veterinarians, physicians and
the public were informed through targeted mailings, publications and the media.
Since November 2008, all owners of non-pregnant sheep and goats in the area where most of the
human cases had occurred in 2008 were given the opportunity to vaccinate their animals on a
voluntary basis with a Phase I vaccine containing inactivated C. burnetii. The aim of the vaccination
was to reduce shedding of C. burnetii and thus, environmental contamination, to reduce human
exposure. In spring 2009, the Dutch government implemented a compulsory vaccination campaign in
the infected area, the province of Noord-Brabant and parts of the provinces of Gelderland, Utrecht and
Limburg. This vaccination campaign is compulsory for dairy sheep and dairy goat farms with over 50
animals and for farms with intensive animal–human-contact. Between April and November 2009,
approximately 250,000 small ruminants were vaccinated.
In 2010, compulsory vaccination will be applied on a larger scale, and more than 1.5 million doses
will be available.
Since February 2009, a stringent hygiene protocol became mandatory for all professional dairy goat
and dairy sheep farms in the Netherlands, independent of their Q fever status. The protocol includes
some mandatory and some voluntary measures, aiming to preventing environmental contamination.
Farmers are obliged to fight against other animal reservoirs, are not allowed to take out manure from
their stables for at least one month after the lambing season, are obliged to cover manure during
storage and transport and will have to plough it under immediately or after composting it for at least
three months. Aborted foetuses and placentas have to be rendered and records of all measures taken
have to be kept for at least one year. Farmers are advised to take some voluntary measures to improve
general hygiene. They are stimulated to bring in fresh straw every day during the lambing period and
to submit aborted foetuses for pathological examination. Farmers are also encouraged not to admit
pregnant women, children and elderly people into their stables (van den Brom and Vellema, 2009).
On 1 October 2009, bulk milk monitoring became mandatory on farms with more than 50 dairy goats
or dairy sheep, and PCR positive bulk milk has since been used as an additional criterion for
veterinary notification of Q fever. The initial frequency of testing each farm every other month was
increased to once every two weeks from 14 December 2009 onwards.
In 2010, the number of positive farms is expected to increase towards the peak of the lambing season
(March-April). To reverse the trend of the last three years, drastic measures were implemented,
including the large-scale culling of pregnant goats on infected farms, which started at the end of
December 2009. Table 13 represents an overview of all recent measures taken by the Dutch
authorities.

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Table 13 : Overview of legislation concerning Q-fever in the Netherlands
Date of
implementation

Document
code

Measure

Reason

12Jun08

TRCJZ/20
08/1622

Q fever notifiable in dairy goat and dairy
sheep; Notification when over 5% of abortion
within 30 days at farms with more than 100
animals and when over 3 abortions within 30
days at farms smaller than 100 animals

Identification of Q fever
positive farms

12Jun08

TRCJZ/20
08/1645

Prohibition to take manure out of the stable
for 90 days after notification
Visitors ban for 90 days after notification

16Oct08

TRCJZ/20
08/2817

Special dispensation of Coxevac (CEVA)
Q fever vaccine to be used in the Netherlands
Voluntary vaccination in dairy sheep and
dairy goats at farms with more than 50 goats
or sheep, pet zoos and nursing farms in the
restricted 45 km zone (Figure 3)

02Feb09

TRCJZ/20
09/244

20Apr09

TRCJZ/20
09/1142

01Oct09

Regulation
40823

Prohibition to farm more than 50 dairy goats
and dairy sheep if not certain hygienic
measures are implemented such as, other
animal reservoirs control, manure measures,
rendering foetuses and placenta's (see text)
Mandatory vaccination of dairy sheep and
dairy goats on farms with more than 50
animals, on care farms, pet zoos and zoos in
the extended area (Figure 4) before 1 January
2010
Mandatory bulk tank milk monitoring on
Q fever every two months
Prohibition to transport dairy sheep and dairy
goats from a positive farm. Vaccinated
animals may be transported to positive farms
Visitors ban at positive farms

09Dec09

Regulation
96744

Ban on increase of the numbers of dairy goats
and dairy sheep on a farm
Ban on reproduction of goats

14Dec09

Regulation
98748

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Mandatory bulk tank milk monitoring for
Q fever every two weeks

Avoidance of the spread
of Q fever via manure
and killing of C. burnetii
in the manure
Avoidance of direct
contact with humans
To start vaccination with
a phase I vaccine against
Q fever
To prevent abortion and
shedding of the
bacterium, because of
shortage of the vaccine
only a small area can be
vaccinated
To further prevent the
spread of C. burnetii
from the farm toward
humans
Extended prevention of
abortion and shedding of
C. burnetii by dairy goats
and dairy sheep
An improved system to
detect farms where
C. burnetii is present
Prevention of the spread
of Q fever by direct
transport of animals to
negative farms
Prevention of direct
contact with positive
animals
To avoid the risk of
spread of Q fever from a
farm
To avoid the risk of
spread of Q fever from a
farm
To enable a more
detailed follow up of
farms that become
positive, thereby
allowing measures to be
taken as early as possible
to reduce the risk of
spread of Q fever to
humans

59

Q fever

16Dec09

Regulation
99604

Prohibition to take the manure out of the
stable within 30 days after the ending of the
lambing season

If manure has to be taken out of the stable, the
manure should be stored on the farm for 90
days

16Dec09

Letter to
the
parliament;
VDC
09.2695/C
PM

Culling of all pregnant goats and sheep on
Q fever positive dairy goat and dairy sheep
farms

18Dec09

Regulation
101785

Prohibition to add sheep or goats to a farm

Regulation
72246

Mandatory vaccination of dairy sheep and
dairy goats, on care farms, pet zoos, zoos, on
farms with lambs exhibitions, wandering
shepherds and in natural reserves nationwide
before 2011

01Jan10

To avoid the possible
spread of Q fever from
the manure
To avoid the possible
spread of Q fever from
the manure and to
stimulate composting on
the farm to reduce the
load of viable Q fever
bacteria
To reduce the risk of
human Q fever in the
spring of 2010. No
differentiation between
infected and non infected
positive pregnant
animals could be made
on the basis of one
individual test
To avoid enlargement of
farms
To avoid the risk of
spread of Q fever from a
farm nation wide

e. Implications/lessons learned
Q fever was present in the Netherlands prior to 2005, but few clinical problems were seen.
Approximately 20 human cases were seen each year. The reasons for the emergence of clinical
problems in the animal population in 2005, and in the human population in 2007, are still unclear.
Several hypotheses are suggested, including:
A steady increase of the dairy goat population since 1984. Goats were kept on large farms
with on average more than 600 goats. Q fever animal outbreaks are observed on the larger
farms. Population dynamics of infectious diseases can change depending on the size of the
farm;
Intensive goat husbandry in a highly populated area;
Dry weather conditions and strong winds during and after the lambing season; and
A change in the virulence of C. burnetii.
Research has been initiated to investigate each of these hypotheses.
Evaluation of the effectiveness of individual control options has proved problematic, for a number of
reasons:
It has been hampered by the large number of outbreaks in a relatively small area, and the
number of potential sources of infection,
There has been no observed decline in human cases, despite widespread implementation of
draconian measures, including vaccination, strict hygienic measures and the killing of all
pregnant goats on bulk milk PCR positive farms, and
The relationship between animal excretion and human exposure is not always clear.
Consequently, there is a need to evaluate options taken in the animal reservoir through
changes in the abortion rate or excretion of C. burnetii.
The importance of environmental contamination on human exposure is unclear, and may have
been underestimated so far.

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Q fever was first diagnosed in the Netherlands in 1956, and became a notifiable
disease in humans in 1978. Between 1978 and 2006, there were an average 17 human
cases each year.
The current Q fever outbreak first emerged in May 2007 and is now the largest
community outbreak of Q fever ever recorded. In total, 168 human cases were
confirmed in 2007, 1,000 in 2008, 2,357 in 2009, and 237 in the first 10 weeks of
2010. The hospitalization rate was 50% in 2007, 20.9% in 2008 and 19.7% in 2009.
Since 1984, there has been a very large expansion in dairy goat production, to over
150,000 tonnes of milk annually.
Q fever was first diagnosed as a cause of abortion on a dairy goat farm in 2005.
There is consensus among public health and veterinary professionals that most of the
human Q fever cases are linked to abortion waves on large dairy goat farms, and to a
much lesser extent on dairy sheep farms.
A large multidisciplinary research programme has commenced, to generate an
improved understanding of C. burnetii infection and Q fever, and to inform improved
control options.
A broad range of control options have been implemented, including compulsory
notification of abortion episodes in small ruminants, blood and bulk milk testing,
vaccination, stringent hygiene measures (other animal reservoirs control; manure
handling, storage and transport; risk material handling), large-scale culling of
pregnant goats. As yet, these measures have not lead to any observed decline in
human cases.
Reasons for the emergence of the current outbreak are unclear, but may be related to
the increase in the number of goats and goat farms, changes to the intensity of goat
production in highly populated areas, to dry weather conditions and strong winds
during and after the lambing/kidding season and to changes in the virulence of
C. burnetii. Research has been initiated to investigate each of these hypotheses.
Evaluation of the effectiveness of individual control options has proved problematic.

4.

Food safety aspects
4.1.

Introduction

The bacterium Coxiella burnetii, is the causal agent of Q fever, an acute (on occasion chronic) febrile
illness that occurs in humans worldwide. Human clinical Q fever is most commonly seen in isolated or
sporadic cases, while mild Q fever cases can often go undiagnosed and therefore unreported.
The disease is usually associated with livestock rearing, dairy farming or employment in abattoirs. In
recently described major outbreaks, infected persons were living within a few kilometres of dairy goat
farms where an upsurge of abortions was detected (Schimmer et al., 2010). Outbreaks of human Q
fever may occur both in rural and urban areas (Schimmer et al., 2008 and 2009; Hawker et al., 1998).
Aerosol spread of C. burnetii from the affected herds/flocks of domestic animal and their excreta and
bedding are considered to be the main route of infection for human cases in such outbreaks. The main
factor related to human outbreaks has been the proximity of patients to small ruminants with clinical
Q fever, notably abortion, sometimes near densely populated areas. There are correlations, firstly
between the density of farming and animal populations (Hatchette et al., 2001) and, secondly, the
proximity to residential areas of the affected farming enterprises (Panaiotov et al., 2009). Source
attribution of sporadic cases, independent of outbreaks, is less clear.

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Most cases of C. burnetii infection in animals are asymptomatic. Diagnosis of C. burnetii infection in
food-production animal populations has often arisen as a sequel to the diagnosis of Q fever in humans.
For example, Ganter et al. (2010) reported that when family doctors in Germany identify an outbreak,
veterinary officials are informed and steps were then taken to identify the source. In human outbreaks,
a causal association between patients and their exposure either direct or indirect, to herds or flocks
undergoing abortions and related conditions attributed to C. burnetii infection, is often established.
It is acknowledged that occupational and airborne exposures are considered to be the main
transmission pathways for C. burnetii infection. Transmission by the oral route is documented and has
been described as a secondary route of infection (reviews by Cerf and Condron (2006) and Angelakis
and Raoult, (2010). This chapter addresses the extent to which food may act as a vehicle for the
transmission to humans of the aetiological agent of Q fever, Coxiella burnetii and the means of
limiting or eliminating exposure to humans by this route.
4.2.

Risk factors for foodborne C. burnetii infection

Factors to be taken into account when considering food-borne transmission of C. burnetii to humans
include the characteristics of the bacterium (including dose-response), its occurrence in food and
identification of the food types most at risk of exposure, the means of its control along the food chain
and, lastly, the susceptibility of the consumer. Also to be considered is the outcome for the exposed
host, i.e., whether exposed but not infected, infected but not diseased or exhibiting clinical signs of
disease.
Characteristics of the bacterium, Coxiella burnetti, that are of relevance to food-borne risk are related
to exposure to the small cell variant (SCV or endospore), which is environmentally stable and is the
form phagocytosed by macrophages during early infection. The endospore displays a tropism for
reproductive organs including the mammary gland, is secreted in the milk of infected animals, both
from clinical cases and asymptomatic carriers and is excreted in the detritus of normal births and
abortions as well as in the urine and faeces of infected animals. Endospores are extremely resistant to
heat, pressure, desiccation and can remain viable for several months in dairy products, meat and meat
products, water, aborted foetuses, manure, wool, hay, equipment, and clothing during conditions of
high humidity, low temperatures, and no sunlight. Endospores are metabolically inactive and thus
remain stable in soil and dust over many years (Frangoulidis, 2010) and can be spread in dust or
windborne aerosols for up to 11 miles (18 Km) (Hawker et al., 1998). For example, C. burnetii can
survive at 4-6°C for 42 months in milk, 12 to 16 months in wool, 120 days in dust, 49 days in dried
urine and 30 days in dried sputum (NABC, 2010). C. burnetii shows some important physicochemical
characteristics including: stability against acids (down to pH 4.5); UV light, pressure (up to 300 MPa);
and can survive in 10 % saline for more than six months. C. burnetii is killed by exposure (30
minutes) to 5 % H2O2, 0.5% hypochlorite, 70% ethanol, and in less than 30 minutes by 5% chloroform
or formaldehyde gas (in a 80% humidified environment) or pasteurization, at least 72 C for 40
seconds (Frangoulidis, 2010; Waag, 2007) or 161 F/71.7 C for 15 seconds (Enright et al. (1957a).
Studies in France demonstrated that duration of sheding of C. burnetii in sheep, is longer in vaginal
mucus, whereas in goats is in milk and in the case of cattle, in milk (Rodolakis et al., 2007). These
authors suggested that this could explain why human outbreaks of Q fever are more often related to
ovine flocks than to bovine herds. Regarding the recent outbreak in the Netherlands it was concluded
to be mainly associated with clinical Q fever in nearby dairy goat flocks and, to a lesser extent, in
dairy sheep flocks. In this respect, some 2.4% of the sheep and 7.8% of the goats in the Netherlands
were sero-positive by ELISA (Schimmer et al, 2008, 2009; Vellema et al., 2010; Roest et al., 2010). In
the area of this recent outbreak and in the rest of the country bulk milk tank (BMT) samples from goat
and sheep dairy farms were tested. The normal procedure includes an initial test carried out by the
Animal Health Service (AHS, GD) using real-time PCR. If positive this sample is again tested by the
Central Veterinary Institute (CVI). If confirmed positive, then a further sample is taken by the Food
and Consumer Product Safety Authority (VWA) and if that sample is confirmed as positive the
flock/herd is then designated as officially positive for Q fever (Roest et al., 2010). Testing of BMT
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samples by PCR from dairy goat and dairy sheep farms in the Netherlands in 2008, showed 30% of the
samples positive.
The BMT screening by PCR is undertaken to identify infected flocks of animals; however a positive
result is not necessarily an indication that the milk contains infective C. burnetii (Vellema et al.,
2010). BMT testing of samples is not used for the diagnosis of abortion due to C. burnetii, as infected
goats and cows without clinical signs can shed C. burnetii in their milk (Rodolakis, 2010). Studies in
Germany highlighted that 30 out of 50 human Q fever outbreaks were causally linked to sheep farming
in the same area (Ganter et al., 2010). The same authors also linked outbreaks in 2003 and 2005 to
shedding of C. burnetii by one infected sheep in the first outbreak and to a few sheep in the second.
During the period 2001 and 2009 Q fever was diagnosed in 1,213 herds with 52% of these occurring
in Bavaria and 87% of the cases occurred in cattle. Positive sheep were 7% and 1% in goats.
Because the infective stage of C. burnetii is present in aerosols from contaminated premises and in
animal manures and excreta especially around the time of birth or abortion, contamination of on-farm
milk, of exposed waterways and of fresh produce, particularly those products produced on land with
spread contaminated manure and slurries, is unavoidable. Accordingly there is a risk of human
exposure to C. burnetii from contaminated animal products, water and fresh produce.
There is limited information on the dose response of C. burnetii for humans. Generally, it is
considered, but not proven, that exposure to aerosols with as low as one bacterium may lead to
infection (Harrison et al., 1990; Bayer, 1982; Johnson and Kadull, 1966), a conclusion that supports an
earlier estimate of 10 microorganisms or fewer (Tigertt et al., 1961). The exposure dose has been
shown to vary inversely with the length of the incubation period (Benson and Tigertt, 1956).
Studies carried out by Enright et al. (1957a) demonstrated that C burnetii survived prolonged time in
the udder (up to 405 days post-infection), while Moffai et al. (1970) reported that C. burnetii can
multiply in the udder of cows for at least three years. In a study in Switzerland, screening for the
presence of C. burnetii in BMT samples from cows, sheep and goats revealed that 17 of 359 (4.7%) of
bovine milk samples examined tested positive for C. burnetii. In contrast, all 81 ovine and 39 caprine
BMT samples tested negative for C. burnetii (Fretz et al., 2007). Another study reported shedding of
C. burnetii in goat milk during the first lactation and of 21 goat kids fed bulk milk from the infected
dams during their first lactation period, only three kids were serologically positive (Berri et al.,
2005b). The same authors (Berri et al., 2007) also showed excretion in milk and vaginal swabs in the
2nd lambing season (13% and 23% PCR-positive milk samples one and two weeks post parturition
respectively). Overall, 17 and 14 females (out of 39) excreted the bacteria into milk at the first and the
second kidding season, respectively. Twelve of them shed the bacteria at both kidding seasons.
Both clinical cases and asymptomatic bovine, ovine and caprine carriers excrete the bacterium
intermittently throughout lactation in variable numbers, based on studies using PCR.
Along with others, Enright et al. (1957a and b) considered that consumption of contaminated milk
may constitute a means of transmission of C. burnetii to humans. These latter authors also reported on
the numbers of C. burnetii in cow‘s milk and related these to infective doses as measured by
intraperitoneal injection of 2 ml. milk in guinea pigs. Eight out of 109 raw milk samples contained
viable burnetii, and of a further 376 retail milk samples (each sample was from a different creamery
and was a composite from different producers supplying the creamery) 14 raw and one pasteurized
sample contained C. burnetii. The maximum number of bacteria demonstrated in these samples was
1,000 infective guinea pig doses11. Milk samples from 137 individual cows in a dairy herd were also
examined and 18 samples were found to contain viable C. burnetii at different levels. Experimental
studies showed that the maximum infective titre in the milk was 10,000 infective guinea pigs doses.
As the infective dose was determined after intraperitoneal injection, this should not to be regarded as

11

An infective guinea pig dose may be defined as the minimum number of C. burnetii required to infect a guinea pig by
intraperitoneal inoculation. In this study these organisms were always contained in 2 ml of inoculum.

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the dose necessary for oral infection. Later studies questioned the origin of the C. burnetii strains used,
whether they were from one or more animals and whether a single strain or a mixture of strains was
used. Other authors report on the dose response for the oral route and stated that moderate doses would
not result in clinical disease (Madariaga et al., 2003).
The risk of acquiring meat-borne infection by ingestion of meat carrying C. burnetii as a result either
of a bacteraemia or contamination at slaughter, is undetermined. In cases involving abattoir workers, it
is most likely that infection is via occupational exposure. Moffai et al. (1970) cited reports from
different sources that abattoir workers and veterinary practitioners have the highest seroprevalence
(between 24-33 %) for C. burnetii. The Australian Food Standards, in its Assessment of
Microbiological Hazards associated with the Four Main Meat Species (2009), listed Q fever as a
hazard as follows: “Cattle [sheep and goats] may carry pathogens normally associated with handling,
which could potentially be transmitted via meat consumption. Notes: Examples include Anthrax
(Bacillus anthracis), Melioidosis (Burkolderia pseudomallei) and Q fever (Coxiella burnetii)”.
The Australasian Meat Industry Employees Union raised concern over the approximately 600 cases of
Q fever reported nationally each year, with 90% of cases being reported in Queensland, leading to 200
people being hospitalised and three deaths occurring as a result of the disease and the related costs due
to disease. There have been no scientific reports that identified the consumption of meat as a source of
infection for these workers (AMIEU, 2010). In California, workers at a local meatpacking plant that
processed mutton were surveyed and 29% reacted positive to Q fever, with the majority having
recently experienced a clinical illness compatible with Q fever (Anonymous, 1986). In a Q fever
outbreak in a meat processing plant in Scotland, blood tests confirmed Q fever in 24 patients (HPS,
2006; Donaghy et al., 2006). Other indications that Q fever can arise as an occupational disease were
reports that the risk of infection was associated with an occupation in the dairy cow sector: 39 of 359
such persons studied (11%) were seropositive for C. burnetii while veterinarians had the highest
seropositive rate (36%) (Bosnjak et al., 2009). A similar study among veterinarians in the US found
antibodies against C. burnetii in 113 (22.2%) of 508 samples tested (Whitney et al., 2009).
C.burnetii was also studied for its potential as a biological weapon in aerosolised form or as a
contaminant of food, water, or possibly even postal mail (Madariaga et al., 2003). In that study it was
stated that ingestion of ―moderate doses‖ of C. burnetii would be unlikely to produce clinical
symptoms.
4.3.

Milk and dairy products as a source of C. burnetii for the consumer

Milk containing C. burnetii is documented by several authors as possible source of oral infection
(Marmion et al., 1956; Christie, 1980; Fishbein and Raoult, 1992), and was also documented by EFSA
in an earlier opinion (EFSA, 2006). The significance of infection acquired via the oral route remains a
subject of discussion (Lorenz et al., 1998) and the role of drinking unpasteurized milk in C. burnetii
infection remains controversial. Epidemiologic studies suggest that the consumption of contaminated
unpasteurized milk has been a mode of exposure to C burnetii for humans (Christie, 1980; Fishbein
and Raoult, 1992; Benson et al., 1963; Brown et al., 1968; Connolly et al. 1990; Hatchette et al, 2001).
Benson et al., (1963) reported that 42 of 120 persons who were routinely drinking unpasteurized milk
tested positive for C. burnetii in at least one immunological test during the reference period. While
none of the positives showed any sign of clinical disease, the presence of Complement Fixation (CF)
antibodies was considered to indicate that exposure to C. burnetii had occurred. Similar findings on a
seroconversion without infection or clinical signs were also reported by Fishbein and Raoult, (1992).
In contrast to the findings of Benson et al. (1963), there are also reports on the absence of any
immunological response in 34 people drinking unpasteurized milk naturally infected with C. burnetii
in an area where Q fever was endemic in cattle (Krumbiegel and Wisniewski, 1970). The latter authors
suggested that failure to produce response was likely due to a different dosage or to the nature of the
Coxiella strains present. This difference in strain was also suggested in the recent Q fever outbreak in
the Netherlands where typing of the C. burnetii bacterium involved in the outbreak revealed that the
same strain was isolated from 92% of the samples from the goat farms in the outbreak area. Samples
taken from a few cattle were clearly distinguished from the samples taken from the goats. It was
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questioned if this strain was more virulent than others. This virulence will now be tested using the
Dutch strains and some strains isolated in France (Roest et al., 2010). The above supports the
likelihood that infection in occupationally exposed people is due to inhalation of contaminated
aerosols rather than consumption of contaminated dairy products. Meanwhile, as stated above, a PCR
positive BMT test result is also not in itself conclusive evidence that the said milk contains viable
(infective) C. burnetii (Vellema et al., 2010).
From the above it is recognised that drinking milk containing C. burnetii can result in sero-conversion
although it remains unclear as to whether, and if so, to what extent, clinical disease can result from the
consumption of milk or dairy products, or of other foods containing C. burnetii.
4.4.

Heat treatment as a means of controlling C. burnetii in milk and dairy products.

Pasteurization is the main method used to eliminate C. burnetii from milk, if present. The Codex
Committee on Food Hygiene in 2004 defined pasteurization as follows: ―Pasteurization is a
microbiocidal heat treatment aimed at reducing the number of any pathogenic microorganisms in milk
and liquid milk products, if present, to a level at which they do not constitute a significant health
hazard. Pasteurization conditions are designed to effectively destroy the organisms Mycobacterium
tuberculosis and Coxiella burnetii” (Anon, 2004). It also describes the current methods in use for
pasteurization12.
Enright et al. (1957) reported that the pasteurisation method then used for cow‘s milk (i.e. 143
F/61.66 C for 30 minutes) did not eliminate C. burnetii but that heating milk at 145 F/62.77 C for
30 minutes inactivated C. burnetii in concentrations of 100,000 infective guinea pig doses per 2 ml.
Further results of these studies demonstrated that an alternative minimum standard temperature/timing
for the pasteurization of milk, namely, 161 F/71.66 C for 15 seconds, could be recommended. The
latter time/temperature combination is now the current standard for pasteurization. It should be noted
that Enright et al. (1957) did not provide details on the origin of the C. burnetii strains used in the
above study, or whether or not the strains used were from one or more animals or whether a single or
mixture of strains was used.
The effect of some variables such as fat content or total solids in milk on the effectiveness of
pasteurisation regarding the inactivation of C. burnetii in milk of different animal species is lacking.
Studies on the inactivation of C. burnetii in liquid milk products containing more fat or added sugar or
flavouring were reported by Enright (Enright, 1961, cited by Juff and Deeth, 2007). Heat resistance of
C. burnetii in these products was determined using a laboratory scale heat exchanger and an inoculum
of 10,000 infectious guinea pig doses of a strain of C. burnetii per ml of product, i.e. an inoculation
rate stated as realistic in terms of the levels that can occur in raw milk delivered to a processor.
Pasteurisation of cream (up to 40 per cent butter fat) and chocolate milk (4% butterfat and 22.5% total
solids) at the recommended standards for milk, i.e. 161 F/71.66 C for 15 seconds, was shown to be
inadequate to eliminate C. burnetii from these products. Increasing the temperature to 166 F/74.4 C
for 15 seconds was effective in eliminating C. burnetii. Likewise, pasteurisation of ice cream mix at
175 F/79.4 C for 15 seconds was also effective in eliminating C. burnetii. Finally, Stumbo (1973,
cited by Juff and Deeth, 2007) reported generalised data of D65.6 C = 0.50-0.6 minutes and z values of
4.4-5.5oC for C. burnetii.
Data on the effectiveness of heat treatment, as a component of cheese making, in inactivating C.
burnetii are lacking.

12

Currently there are two types of pasteurization used: high temperature/short time (HTST) and ultra-high temperature
(UHT). There are basically two methods for the HTST type of pasteurization in use- batch and continuous flow. HTST
pasteurization processes must be designed so that the milk is heated evenly, and no part of the milk is subject to a shorter
time or a lower temperature. To ensure destruction of all pathogenic microorganisms, time and temperature combinations
of the process have to be respected. For milk these are 63° C for not less than 30 min. or 72° C for not less than 16 sec.

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5.

Control options in domestic ruminant populations
5.1.

Infectious disease epidemiology (concepts and applications)

A frequently used model to describe the transmission of infectious diseases is the so-called SIR model
that assumes that a population consists of susceptible (S), infectious (I) and recovered (R) individuals.
The rate at which a susceptible individual (S) becomes infected is determined by the transmission rate
parameter β (average number of new infections caused by one infectious individual per unit of time)
and the number of infectious individuals present. An infectious individual is considered to have
recovered when no longer infectious. It is assumed that recovery occurs at a rate α, which has an
expected value equal to the inverse of the duration of the infectious period. From these two events, it
follows that the average number of new infections caused by one infectious individual in a totally
susceptible population (R0) equals β/α (Diekmann and Heesterbeek, 2000). R0 is unambiguously the
key parameter of the epidemiological models, because it tells us whether infections can (R 0>1) or
cannot (R0<1) spread in a fully susceptible population, and thus whether control options such as
vaccination are effective in eradicating the pathogen from a population. The equivalent of R 0 in a
population housing both Susceptible and Recovered individuals is Re, which is also determined by the
proportion of Recovered individuals in the population.
Applied to Q fever, this means that the transmission of C. burnetii infections depends on:
The proportion of the population susceptible to infection and the degree of susceptibility of the
animals, which is linked to a range of host factors, including past exposure to the agent, the
duration of active and maternally-derived immunity, and population dynamics (recruitment
rate into the population, death rate due to infection) (van Dijk, 1994);
The proportion of the population infectious and the degree of infectivity, which is also linked
to a range of host factors, including abortion/giving birth, length of the infectious period,
active and passive maternally-derived immunity (van Dijk, 1994); and
The adequacy of contact between individuals in a population, which is a composite of three
key aspects of infectious disease epidemiology, specifically the number of contacts per unit
time, the transmission potential per contact and contact structure within the flock (whom has
contact with whom) (Halloran, 1998). Both host and agent factors are important. Host factors
include population density, population social structure, management methods (including
husbandry and housing), and heterogeneity in transmission arising from factors relating to age,
genetics, spatial distribution and behaviour, whereas agent factors include the intrinsic
contagiousness of the agent and the mode of transmission. Depending on the infectious agent,
vector factors may also be relevant, including, competence or efficiency and mean bites per
unit time (van Dijk, 1994).
This theoretical understanding of infectious disease epidemiology can be directly translated to
measures to prevent and/or control infection by reducing transmission (within defined populations,
such as herds) and spread (between populations). The latter can be regarded as animals of different
populations having contact. Consequently, population size plays a role in the latter.
Specifically, there are two broad measures to limit transmission and spread of directly transmissible
infections in populations:
Reducing the proportion of the population susceptible and decreasing the infectivity of
infected individuals, generally through vaccination. Mass vaccination programmes, which
effectively lower Re, are reliant on both ‗vaccine efficacy under field conditions‘ (degree of
reduction of susceptibility and infectivity (both level and duration)) and ‗overall coverage
rate‘ (the overall proportion of susceptible animals that are vaccinated). Besides vaccination, a
range of measures are routinely used to limit the duration of infectiousness, including
(prophylactic and therapeutic) antimicrobial treatment, test and slaughter, etc.

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Reducing the adequacy of contact between individuals (animal-animal, animal-human,
human-human) through measures to:
o

Reduce the number of contacts per unit time. A broad range of measures are
commonly applied to limit contact during animal disease control, including
quarantine, test and slaughter, livestock movement control, changes to farm
management etc

o

Reduce the transmission potential per contact. As a feature of the infectious agent, the
transmission potential is generally difficult to influence within populations. However,
these measures can be very important for reducing the transmission potential per
indirect contact between different flocks (hygienic measures).

o

Reduce the number of different farms in contact. By limiting the numbers of different
farms in contact with each other (trade restrictions), transmission can be reduced.

The above discussion is generic, but provides a robust framework for consideration and assessment of
control options for Q fever in animal populations, as outlined in section 5.2.3.

As with other contagious diseases, the transmission of C. burnetii in animal populations
depends on:
o The proportion of the population susceptible to infection, and the degree of
susceptibility of the animals,
o The proportion of the population infectious, and the degree of infectivity, and
o The adequacy of contact between individuals in a population.
There are two broad measures to limit transmission and spread of directly transmissible
infections in populations, including:
o Reducing the proportion of the population susceptible and decreasing the infectivity of
infected individuals, and
o Reducing the adequacy of contact between individuals through measures that reduce
the number of contacts per unit time, the transmission potential per contact and the
number of different farms in contact.
These concepts in infectious disease epidemiology provide a generic framework to provide
a qualitative assessment of available control options for Q fever.

5.2.

Available control strategies
5.2.1.

The importance of surveillance/monitoring and case ascertainment

Control measures for C. burnetii can only be effectively implemented if cases are detected and
confirmed. This requires systematic and reliable classification of units/farms as cases. The basis for
such a classification is an agreed case definition. Case detection can be based on suspect case
reporting (passive surveillance) or screening (active surveillance).
In order to be able to assess the effectiveness and efficiency of an intervention as part of a control
effort, surveillance after the implementation of control needs to be implemented. Effective
surveillance activities during control programmes typically include case detection, reporting of suspect
cases, follow-up investigations and diagnostic confirmation of cases. Surveillance should therefore be
an integral part of any control programme. In return, the detected cases will then be subject to control
options. Legal basis is required for compulsory control options.

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Control measures for C. burnetii can only be effectively implemented if cases are detected
and confirmed.
Effective surveillance activities as part of control programmes typically include case
detection, the reporting of suspect cases, follow-up investigations and diagnostic
confirmation of cases.

5.2.2.

General considerations

The choice of a Q fever control strategy will depend on the overall objective of the control effort. This
could, for example, be limited to avoiding severe cases or a focus on ―problem‖ farms or – at the other
end of the spectrum – attempt complete eradication of C. burnetii infection in the entire population. In
order to determine the objective of control at Community level, the appropriate level of protection for
other EU MS needs to be discussed. Although the effectiveness of interventions is an important aspect
in this, it essentially remains a risk management decision because other factors such as economics also
need to be considered.
The objective at regional level will be strongly influenced by the current prevalence of the
pathogen/disease. For example, if C. burnetii is widely occurring and the majority of farms are
affected, an eradication objective is likely to be unrealistic. Whether control will be compulsory or
voluntary will also have to be considered. For voluntary control, the issue of herd/animal status
certification and implications on movement of animals needs to be discussed.
A prerequisite for any control programme is the ability to classify farms or animals into infected/notinfected or diseased/not-diseased. This will require an agreed case definition which can generally be
based on clinical, pathological or laboratory criteria or a combination. The case definition should be of
sufficient sensitivity and specificity such that the control objectives can be achieved with the available
resources.
Based on the biology and epidemiology of an agent, individual control options may be more or less
effective. For example, if alternative transmission pathways exist as is the case for C. burnetii, control
of only one pathway (e.g. animal trade) may be of reduced effectiveness and may not achieve the
desired objective if other pathways such as aerosol transmission persist. While some control strategies
may be effective in reducing transmission between farms, they may have severe negative
consequences. For example, movement restriction may be a useful approach, but will impact on trade
and possibly on animal welfare. The choice of control strategy is limited if wildlife reservoirs are
present, which is the case with C. burnetii.
Some interventions may be costly or logistically difficult to implement as part of a general control
programme. However, there may be special circumstances, such as a large outbreak, that may still
justify their implementation. It should therefore be agreed, which events should trigger interventions.
Certain interventions – particularly movement restrictions – may also be considered as short-term
measures when there are new features of a disease indicating a change in pathogenicity. Such
precautionary measures will then allow gaining time to investigate the emerging strain and to adjust
the control strategy as required.
The optimal control strategy may not consist of a single approach but may require a combination of
several control interventions. A risk-benefit analysis could be conducted in order to assess the
justification of control options at Community level.

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The choice of Q fever control strategy will depend on the objective of the overall control
effort. This is essentially a risk management decision, based on an understanding of
control effectiveness and other factors, including economics.
At a regional level, the control objective will be strongly influenced by the current
prevalence of the pathogen/agent.
An agreed case definition is a prerequisite of any regional control programme, given the
need to classify farms or animal into infected/not-infected or diseased/not diseased,
The effectiveness of individual control options will be influenced by the biology and
epidemiology of the agent. Alternative transmission pathways need to be considered. The
choice of control strategy is limited, as with C. burnetii, if wildlife reservoirs are present.
Although some interventions may be costly or logistically difficult, their use may be
justified under special circumstances (for example, large outbreaks).
The optimal control strategy may require a combination of several control interventions. A
risk-benefit analysis could be conducted at Community level.

5.2.3.

Specific control options

A list of possible control options was elaborated. Some of these control options focus specifically on
small ruminants (goats, sheep) as opposed to cattle, given that cattle appears to have a minor role in
the spillover of C. burnetii infection from domestic ruminants to humans. A brief descriptionof the
control optionsis provided in this section. Limitations and an assessment of effectiveness and
sustainability of these options are presented in Table 14.
a. Vaccination
Current vaccines used in humans and animals include formalin-killed, whole-cell vaccine preparations
(WCV) (Marmion et al., 1990) and chloroform methanol-extracted bacterial residue (CMR) (Williams
et al., 1986, 1992; Fries et al., 1993; Waag et al., 1997). The two types of vaccines (WCV and CMR)
protect monkeys (Macaca fascicularis) against fever and bacteriemia after challenge with an aerosol
(Waag et al., 2002). They also induce protection on mice and guinea pigs challenged with virulent
phase I C. burnetii by aerosol (Waag et al., 1997) or intra-peritoneal injection (Kazar et al., 1995;
Zhang et al., 2004, 2007).
In animals, the most effective vaccines are those composed of inactivated whole phase I bacteria.
Bacterial shedding in placental tissue and milk was strongly reduced in experimental infection or in
natural C.burnetii infection of ewes and cows vaccinated by phase I vaccines (Brooks et al., 1986;
Sadecky et al., 1975, Sadecky and Brezina, 1977). However, several studies report that, phase I
vaccines failed to prevent shedding in milk in naturally infected cows prior to vaccination (Biberstein
et al., 1977; Schmeer et al., 1987), highlighting the role of the vaccine in protecting uninfected but not
in treating infected animals. Vaccination efficacy will depend on whether immunisation precedes
infection (preventive vaccination) or not (outbreak vaccination). The efficacy of two commercial
vaccines compound of inactivated C. burnetii reference strain Nine Mile —a phase I and a phase II
vaccine —was compared in pregnant goats experimentally infected with a dose of C. burnetii
sufficient to cause abortion or premature birth in 85% of the goats in the control group (ArricauBouvery et al., 2005). The phase I vaccine prevented abortion, and dramatically reduced the shedding
of C. burnetii in milk, vaginal mucus, and faeces, thereby reducing both environmental contamination
and the risk of transmission to humans. In contrast, the phase II vaccine did not show any difference
compared to the control group.
The efficacy of the phase I vaccine was also studied in naturally infected cows (Guatteo et al., 2008). .
When vaccinated while not pregnant, an initially non infected animal had a five times lower
probability of becoming a shedder than an animal receiving a placebo. An animal which was
vaccinated when pregnant had a similar likelihoodlity of becoming shedder as an animal receiving the
placebo. The authors hypothesize that pregnancy had an adverse effect on the immune response.

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A similar study was carried out in 3 caprine herds on 1701 goats (1081 adults and 620 young animals)
(David and de Cremoux ANICAP, 200913). More than 73% of the adults shed C burnetii in the vaginal
mucus before vaccination while 67.7% of the young did not. 202 young goats and only 2 adults were
uninfected before vaccination. As in cows, vaccination of young non-infected goats with phase I
vaccine reduced significantly the shedding of C burnetii (around 2 logs) in vaginal mucus after
parturition.
A bovine herd in which abortions due to Q fever were diagnosed in 2001 was vaccinated with a Phase
I vaccine in 2004-2005. Each cow received the vaccine twice at 3 weeks of interval and a yearly
booster vaccination between 2 and 5 weeks after calving. The efficacy of the vaccine was assessed by
following the shedding of C. burnetii in vaginal mucus and milk. For this purpose, qPCR was
performed on vaginal mucus and milk the day of calving and 3 days after. The shedding was also
assessed 1, 3 and 7 weeks after calving in individual milk samples as well as in bulk milk samples.
Four years were needed to stop the shedding, indeed the first year, 40% of the cows shed C. burnetii at
least by one route, the second year 18% were still shedding and 10% the third (Camuset and Remmy,
Word Buiatric Congress Budapest, 2008).
Field and experimental data is lacking on the epidemiology of infection in, and between, infected
flocks. For example, Re and Rh for Q fever in vaccinated flocks are not known. Further, based on
current diagnostic tests, it is not possible to serologically distinguish vaccinated and naturally-infected
animals.

In animals, phase I vaccines are much more effective than Phase II vaccines.
Preventive vaccination (immunisation preceding infection) is much more effective than
outbreak vaccination (infection preceding immunisation).
Preventive vaccination in goats, using a phase I vaccine, prevents abortion and
dramatically reduces the shedding of C. burnetii in milk, vaginal mucus and faeces,
thereby reducing both environmental contamination and the risk of transmission to
humans. In cattle, phase I preventive vaccination substantially reduced shedding.
Vaccination is a long-term control strategy, particularly in heavily infected herds.
Field and experimental data is lacking, on the epidemiology of infection in, and between,
infected flocks. For example, Re and Rh for C. burnetii infection in vaccinated flocks is not
known.
Based on current diagnostic tests, it is not possible to serologically distinguish vaccinated
and naturally-infected animals.

b. Antibiotic treatment
Antibiotic treatment is used effectively in humans to reduce clinical symptoms associated with
Q fever. Antibiotic treatment was not demonstrated to be effective in preventing the shedding of
bacteria or limiting the duration of bacterial excretion, either in sheep (Astobiza et al., 2009) or goats
(Blain, 2007).Consequently, antibiotic treatment is not effective in influencing the epidemiology of
infection in animal populations, and cannot be recommended (Berri et al.,2005a). Widespread
antibiotic usage should also be avoided to limit the development of antibiotic resistance (WHO, 2001).
Antibiotic treatment in animals is not effective in substantially reducing either the level or
duration of bacterial shedding in domestic ruminant populations.
c. Removal of risk material (placentas, aborted foetuses)

13

In Rodolakis 2010. Q fever in France. Q fever conference, Breda, The Nederlands, 25-26 February.

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This strategy concerns the collection and removal of risk material (placentas, aborted foetuses) to
specific rendering plants or by other methods of safe disposal. The rationale for this approach is that,
in infected flocks, risk material can contain very large numbers (109-1012) of C. burnetii (Babudieri,
1959). In many farming systems, it may not be possible to retrieve all risk material.
The removal of risk material, such as placentas and aborted fetuses, has been suggested, noting
that these materials have the potential to contain very high numbers of C. burnetii.
d. Manure management
Animal husbandry systems vary considerably between EU MS. Consequently, there are also
considerable differences in methods of manure management, for example: in terms of storage location
(on-farm, at a remote site), method of covering (if at all), the addition of lime (or not), industrialized
composting, steem treatment of manure. The following systems were assessed for effectiveness:
Deep litter systems, where goats are kept indoors on straw litters, straw is added regularly and
removed only 3-4 times a year. The manure is usually moved to another location in or out of
the farm.
Slurry treated with cyanamide calcium
Manure composting for a period of time with or without covering
Untreated slurry is removed and spread onto fields
The goal of manure treatment is to reduce the viable bacterial load of the manure after the production
of the manure, either through chemical (Arricau-Bouvery et al., 2001) or heat treatment.
Composting is a manure fermentation process that kills bacteria as temperatures rise. Traditional
composting consists in piling manure, between concrete walls and fermentation for 3 months. The
inside temp is estimated to be a minimum of 50 C and this process will lead to a minimum of 4.3*10-7
reduction of Coxiella (based on data extrapolated from experiments in milk pasteurization). Industrial
composting consisting of treatment for 1 month for min 50°C and is estimated to lead to a minimum
1.7*10-7 reduction of Coxiella. Pasteurizing industrial compost at 70°C for 20 min will lead to higher
reduction of Coxiella but the degree of reduction is unknown at the moment. A comparison between
traditional and industrial composting processes shows that their effectiveness is basically similar
(VWA, 2009).
Exact levels of Coxiella in the manure and how effectively they are killed in the standard fermentation
process cannot be determined to date but research in the topic is currently ongoing.
The level and duration of heat achieved is affected by a range of factors including the level of
moisture, the duration of composting and the presence of aerobic conditions (Vellema et al., 2010).
There is a limited understanding of the role of manure in the spillover of infection to humans. In the
Netherlands, where manure is often transported off-farm to a remote site, there have been no known
human Q fever cases linked to manure transport or remote storage.
There are differences in systems of manure management between EU MS.
Often either chemical or heat treatment is used to reduce the load of viable bacteria. A range
of factors affect the level and duration of heat achieved, including the level of moisture, the
duration of composting and the presence of aerobic conditions.
e. Culling of pregnant animals
The culling of pregnant goats/sheep was recently used as a short term control measure spanning the
pregnancy/lambing period on dairy goat and sheep farms in the Netherlands. This decision was taken
in the face of a rising number of human Q fever cases and of Q fever outbreaks (with abortion) on a
number of farms. The rationale for this approach is that infected animals shed bacteria in largest
numbers at and shortly following parturition (Arricau-Bouvery et Rordolakis 2005).

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The culling of pregnant females would lead to a reduction in bacterial shedding, noting that
shedding is greatest from infected animals at or shortly following parturition or abortion.
f. Identifying and culling of shedders
The culling of shedders has been suggested as one possible strategy to control Q fever in animal
populations. This strategy relies on a „test and cull‟ approach, to facilitate the identification and
culling of infected animals that are excreting C. burnetii, thereby reducing the overall prevalence of
infection in a herd.
The culling of shedders relies on a ‗test and cull‘ approach.

g. Temporary breeding ban
A temporary breeding ban has been considered on the same premise as that suggested for the culling
of pregnant animals. With a temporary breeding ban, the opportunity for bacterial shedding is greatly
reduced. As part of the broader control strategy in the Netherlands, the temporary breeding ban is
expected to precede subsequent repopulation with vaccinated animals.
A temporary breeding ban would substantially reduce the opportunity for bacterial shedding.
This strategy would be expected to precede subsequent repopulation with vaccinated animals.
h. Control of animal movement between farms of differing infection status
The control of animal movement is used as a strategy to prevent and/or control a number of animal
diseases. In the context of Q fever, the introduction of infected animals into naïve herds could be
avoided if there were control of movement of animals of defined status between herds of defined
status. However, this strategy is reliant on the reliable classification of animals and herds (for example,
a farm-level certification system including testing scheme, cut offs, status definition etc). Given the
diagnostic quality of currently available diagnostic tests, however, considerable uncertainty is likely to
remain as to the true status of an animal or herd. Further, alternative transmission pathways may
persist, and reduce the effectiveness of this intervention.
The control of animal movement between farms of differing infection status might be
considered as a method to prevent the introduction of infected animals into naïve herds, but
only if there were a reliable means to classify animals and herds.

i. Stand still measures
This is a temporary movement restriction applied at a regional level or in a zone that is defined for
disease control purposes. It is typically applied during a major disease outbreak with the objective to
eliminate transmission related to trade, and to gain time. A stand still is normally combined with other
interventions such as outbreak investigation, tracing, stamping-out, testing, outbreak vaccination and
cleaning and disinfection. Note that the status of herds inside and outside the zones would need to be
defined, for example through systematic investigations, including testing. It is assumed that all units
outside the zone are negative. The presence of positive wildlife is a challenge for defining zones, but
examples exist how to deal with this, for example, from classical swine fever.
Stand still measures are typically applied during an outbreak, with the objective to eliminate
transmission related to trade, and to gain time.

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Q fever

j. Changes to farm characteristics (number of animals/farm size, farm location)
This control option concerns a number of potential changes to farm characteristics, including the
number of animals per farm/farm size, and farm location:
Number of animals/farm size: According to the mass action principle, given all things being
equal (such as density of animals within the flock), the transmission within a population is
independent of the number of animals in the population (R0 does not increase as population
size increases; Bouma et al., 1995). However, as farm size increases, the probability of
introduction of a pathogen increases. The reason is that more contacts from outside the farm
take place (for example, more replacement stock and more feed is introduced into a farm). In
addition, as farm size increases, more animals can become infected, and consequently the
infectious load produced in a large farm exceeds that of a smaller farm. In addition, large
farms will also have more outbound contacts than smaller farms (for example, more animals
will leave the farm, more milk is delivered). The above reasoning assumes that all other things
are equal between large and small farms (such as bio security measures, trading policy, etc.),
which might not be realistic if larger farms were to take more risk-reducing measures than
smaller ones as for example closed stables.
Farm location: Proximity to goat farms has been reported as a significant risk factor for
human infection (Schimmer et al., 2010.). Given that neighbourhood spread is important in
many animal diseases, density-dependent infection is also likely for the spread of C. burnetii
between farms (such as, for example, has also been shown for avian influenza, CSF, FMD,
etc.; Boender et al., 2007a, 2007b, 2008). To date, however, no published information about
Q fever is available. As a consequence, give all things equal, increasing the distance between
farms will decrease transmission and increasing distance to human dwellings will reduce
exposure of humans. Unfortunately, we cannot yet suggest an optimal distance between farms,
or between a farm and a human dwelling. The reason is the lack of quantitative data of
between-flock transmission and its relation with other factors such as flock size and bio
security measures (see above). Such data are of great importance, because of the highly nonlinear nature of the transmission process.

Changes to farm characteristics have been raised as potential methods of
prevention/control of Q fever, including:
o Changes in animal numbers/farm size. All other things being equal, R0 does not
increase with increasing population size. However, introduction probability is likely to
increase with increasing farm size, because there is greater opportunity for contact
outside the farm. Further, the infectious load on large infected farms will be greater
than on small infected farms.
o Changes in farm location. All other things being equal, between-herd spread will
decrease with increasing distance between farms. Similarly, the risk of human exposure
will decrease with increasing distance from human dwellings. However, the optimal
distance between farms, or between farms and humans dwellings, is currently not
known. This could be estimated once quantitative data were available of between-flock
transmission, and its relation with other factors such as flock size and biosecurity
measures.

k. Control of other animal reservoirs of infection
A range of other animal species, apart from cattle, sheep and goats, can become infected with
C. burnetii (Stoker and Marmion, 1955; Webster et al., 1995; Martinov et al., 2007a). However, their
role in the epidemiology of C. burnetii in domestic ruminants is not completely understood. For this
reason, the impact of this control measure is uncertain.

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Q fever

The role of other animal reservoirs of infection in the epidemiology of C. burnetii infection in
domestic ruminants is not completely understood. The impact of this control measure is
uncertain.
l. A segregated lambing/kidding area
A segregated lambing/kidding area has been proposed, as a means to reduce within-herd transmission
of C. burnetii. The rationale for this approach is that infected animals shed bacteria in largest numbers
at and shortly following parturition (Arricau-Bouvery et. al., 2001)
A segregated lambing/kidding area has the potential to reduce within-herd transmission,
noting that shedding is greatest from infected animals at or shortly following parturition.
m. Shearing management
A number of Q fever outbreaks in humans have been associated with shearing of sheep (Hellenbrand
et al., 2001; Hellenbrand et al., 2005).Sheep wool can become heavily contaminated with tick faeces
(1g can contain up to 1012 bacteria) and infected birth products. Dust containing C. burnetii is
produced during shearing, and bacterial DNA can be found in the air of barns where sheep have been
shorn (Schulz et al., 2005). In such situations, shearing personnel should wear protective filter masks
and the fleece should be kept wet or even disinfected. Shearing should be done in closed barns.
A number of Q fever outbreaks in humans have been associated with sheep shearing.
Wool can become heavily contaminated with C. burnetii, through contact with tick faeces and
infected birth products.
n. Tick control
Some authors consider ticks as an important reservoir of infection (Eldridge and Edman, 2000, Stoker
and Marmion, 1955; Martinov, 2007a). Consequently, tick control intervention may play a role in
limiting a potential reservoir.
Ticks may be a reservoir for the infection, and therefore tick control intervention can play a
role .
o. Stamping out
Stamping out (the slaughter of all animals on defined, infected farms) may be warranted in emergency
situations where public health is at risk. This would lead to an immediate reduction in transmission
from highly focal problem herds. By definition, stamping out will prevent further shedding from
infected animals, however, it will not directly address problems of environmental contamination. We
are unaware of any published information about the effectiveness of stamping out to control Q fever
outbreaks.
Stamping out (the slaughter of all animals on defined, infected farms) may be warranted in
emergency situations where public health is at risk.
p. General biosecurity including visitor ban
Biosecurity refers to hygienic measures and protocols that are applied on farms to limit the
introduction and spread of infectious diseases of animals. To be effective, these measures and

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Q fever

protocols are applicable to all people who enter or leave a premise where farm animals are kept.
General guides for good biosecurity practice are available (DEFRA, 200814). These measures will
reduce, but not eliminate, the risk of C. burnetii introduction on to non-infected farms. A visitor ban
will reduce the number of humans in direct contact with infected animals, but may have limited impact
on methods of indirect contact (for example, through wind-borne spread). We are unaware of any
published information about the effectiveness of general biosecurity to control the zoonotic impact of
Q fever outbreaks.
Biosecurity refers to hygienic measures and protocols that are applied on farms to limit the
introduction and spread of infectious diseases of animals.
A visitor ban will reduce the number of humans in direct contact with infected animals, but
may have limited impact on methods of indirect contact (for example, through wind-borne
spread).
5.2.4.

Effectiveness and sustainability of potential control options

An assessment of effectiveness and sustainability of individual control options for C. burnetii infection
in domestic ruminant populations is presented in Table 14, in relation to impact on animal health
(reducing within-herd transmission, limiting spread to other farms) and public health (reducing
spillover to humans). This assessment was conducted using expert opinion, as outlined in
Section 1.2.3.

14

http://www.defra.gov.uk/foodfarm/farmanimal/diseases/documents/biosecurity_guidance.pdf (accessed 12/4/10)

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Q fever

For almost all of the control options, there is a medium to high level of uncertainty
associated with estimates of control effectiveness. Little published information is
available, and estimates of effectiveness are primarily based on expert opinion,
derived from observation rather than rigorous scientific assessment.
The relative importance of specific transmission pathways for C. burnetii is not
known. In the absence of such information, it has not been possible to accurately
estimate the effectiveness of individual control options.
It is likely that control methods would need to be used in combination, given that:
o No control measure is likely to be completely effective in limiting within-herd
transmission, between-herd spread and spillover to humans, and
o Within-herd transmission, between-herd spread and spillover to humans are each
likely to involve more than one transmission pathway.
Based on currently available information and expert opinion, it is likely that there is
considerable variation in the effectiveness of different control options. The most
effective control options include:
o To limit within-herd transmission: preventive vaccination, culling of pregnant
animals, breeding ban
o To limit between-herd spread: preventive vaccination, culling of pregnant
females, breeding ban, manure management [treating slurry with cyanamide
calcium, deep litter composting]
o To limit spillover to humans: preventive vaccination, culling of pregnant
females, breeding ban, manure management [treating slurry with cyanamide
calcium, deep litter composting]
Vaccination is a long-term control option; effectiveness may not be observed in the
short-term.
Many of the control options are consistent with good farming practice and could be of
value in reducing the risk of future outbreaks
Many control options are unlikely to be sustainable in the medium-to-long term, for a
broad range of reasons.Some control options are best suited for use in the face of an
outbreak.
A number of methods could be considered to limit the risk of introduction of
C. burnetii onto uninfected farms, including biosecurity, control of animal movement
and manure management.
Control measures to address proximity between humans and small ruminants,
particularly around the time of lambing/kidding, would be expected to meaningfully
contribute to a reduction in spillover from animal populations to humans.

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Q fever

Table 14: Effectiveness, sustainability of potential control options for C burnetii infection in domestic ruminant populations
Effectiveness/Uncertainty
Relating to public health
(reducing spillover from
farmed animal
populations to humans)

Relating to animal health
Control option
Reducing within-herd
transmissiona
EffectiveUncertnessa
aintyb

Limiting spread to other
farmsa
EffectiveUncertnessa
aintyb

Effectivenessa

Sustainabilityc

Uncertaintyb

Preventive
vaccination
(immunisation
preceding infection)

High

Medium

High

Medium

High

Medium

High

Culling of pregnant
animals

High

High

High

High

High

High

Lowd

Low

High

High

Medium

High

Medium

High

Manure management
[slurry treated with
cyanamide calcium]
Manure management
[deep litter systems,
manure composting
for 3 m]

None

High

High

High

High

High

High

Temporary breeding
ban

High/

High

High

High

High

High

Lowd

Identifying and
culling of shedders

Low

Medium

Low

Medium

Low

Medium

Lowd

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Limitations

In animals, phase I vaccines are much more effective than
Phase II vaccines. Effectiveness will depend of the use of
vaccination in all farms in a region, and the combined use
of other measures. There is a need for a sufficient vaccine
supply. Cost may become a limitation.
Extremely high costs including political, financial (both
for restocking and production loss) and social. Culling of
pregnant healthy animals is a real ethical (and in some
countries legal) problem. Leads to the generation of
biological waste. Impact may not be observed in a short
medium term, as a result of environmental contamination.
Non-pregnant animals can also shed C. burnetii.

Financial costs associated with storage. Potential
opportunity costs (constraints on time to sell or spread).

With goats: Financial costs, particularly reduced
production (noting that goats can milk continually for 22½ years). Costs will increase greatly if temporary
breeding ban is extended.
With sheep: Financial costs are much greater in sheep
than goats (as extended lactation is not possible)
Shedders are difficult to identify, given current diagnostic
methods.

77

Q fever

Control of animal
movement between
farms of differing
infection status

Low

High

Medium

High

Low

High

Lowd

Stand still

Low

High

Medium

High

Low

High

Lowd

Control of other
animal reservoirs of
infection

Low

High

Low

High

Low

High

High

Tick control

Low

Medium

Low

Medium

Low

Medium

High

Changes to farm
characteristics
[number of
animals/farm size,
farm location]

Low

High

Medium

High

Medium

High

High

Wool shearing
management

Low

High

Low

High

Medium

High

High

Outbreak vaccination
(infection preceding
immunisation)

Medium

Medium

Medium

Medium

Medium

Medium

Highd

Removal of risk
material (placentas,
aborted foetuses)

Medium

High

Medium

High

Medium

High

High

A segregated
lambing/ kidding area

Medium

High

Medium

High

Medium

High

High

Stamping out

None

Medium

High

Medium

High

Lowd

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Strategy is only possible if the infection status of each
herd is known, i.e. requires mass testing/screening of all
herds participating in trade. Likely to be more effective in
limiting long distance spread. Requires identification and
certification of animals and herds, and a legal basis if it is
to be compulsory. There may be a substantial financial
cost .
Not well suited to Q fever, noting that C. burnetii
infection is widespread. May be logistically difficult to
implement, but provided the legal basis is available and
the consequences are justifiable, Financial cost (loss of
benefits from trade). Strategy is only possible if the
infection status of regions or zones is known. Requires
certification of animals and a legal basis. Likely to be
more effective in limiting long distance spread.
The specific effectiveness against Q-fever is difficult to
be measured The activities should be part of the routine
prophylactic measures but is difficult to estimate
threshold or acceptable level of the applied measures.
The potential for environmental pollution and tick
resistance, the need for special authorization.
The threshold (number of animals/farm size) is not
known, but will depend on both proximity to humans and
farm infra-structure (eg closed stables may lead to
increased within-herd transmission but reduced potential
for spillover). Very high initial costs.
It is not clear how to decontaminate or dispose of
Coxiella contaminated wool. Effectiveness will be related
to distance between farms.
In animals, phase I vaccines are much more effective than
Phase II vaccines.
Impact may not be observed in a short-medium term as a
result of environmental contamination. Requires
sufficient vaccine supply.
Creates biological waste. Feasibility will depend on the
farming system. It is unlikely that there will be complete
removal in any system.
Depends on the effective of separation. There are cost
implications.
Depends on the level of existing environmental
contamination. The policy for repopulation needs to be
established

78

Q fever
Visitor ban
Manure management
[untreated slurry,
subsequent land
spreading]
Antibiotic treatment

None
Low

None

High

Low

Low
-

None

High
-

Low

Medium
-

None

High
-

Low

High
High

Low

Effectiveness at limiting spread to other farms and
reducing spillover to humans depends on subsequent land
spreading method and possible treatment.
The treatment is not effective in substantially reducing
either the level or duration of bacterial shedding in
domestic ruminant populations, and could induce
antibiotic resistance.

a. Effectiveness was assessed as follows:
High, very effective;
Medium, moderately effective;
Low, very limited effect;
None, no effect.
b. The level of uncertainty was considered:
High: Scarce or no data available; evidence provided in unpublished reports, or few observations and personal communications, and/or authors‘ or experts‘ conclusions vary considerably
Medium: Some or only incomplete data available; evidence provided in small number of references; authors‘ or experts‘ conclusions vary, or limited evidence from field observations, or solid and complete
data available from other species which can be extrapolated to the species being considered
Low: Solid and complete data available; strong evidence in multiple references with most authors coming to the same conclusions, or considerable and consistent experience from field observations.
c. The scale of sustainability included:
High, sustainable in the long-term;
Medium, sustainable only in the short-to-medium term;
Low, sustainable only in the short term.
d. Particularly suited for outbreak response

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CONCLUSIONS AND RECOMMENDATIONS
CONCLUSIONS
TOR 1: To assess the significance of the occurrence of Q fever in the EU Member States for a better
understanding of the scale and distribution of the disease and infection (with the focus on farm
animals and humans):
Based on available evidence,
Coxiella burnetii infection is endemic in domestic ruminants (cattle, sheep, goats) in most, if
not all, EU MS, although there is considerable uncertainty about estimates of prevalence and
incidence.
Although infection in domestic ruminants is common, disease is rare. The overall impact of
C. burnetii infection on the health of domestic ruminants in EU MS is limited. However, the
impact on individual goat farms during an abortion episode can be significant.
C. burnetii infection in humans is present in most, if not all, EU MS, although there is
considerable uncertainty about estimates of prevalence and incidence.
Q fever is a zoonotic disease with limited public health impact within the EU, although in
certain epidemiological circumstances and for particular risk groups the health impact can be
significant. Many cases of Q fever in humans are unrelated to occupational exposure. As yet,
the Q fever burden of disease in humans has not been determined.
TOR 2: To assess the risk factors for Q fever occurrence and persistence in animal husbandry, and the
related risks for humans, taking into account at least the presence and density of susceptible livestock
and the type of husbandry in which they are kept:
Based on available evidence,
C. burnetii infection is endemic in domestic ruminants throughout Europe. Therefore, it seems
likely that infection can be maintained in a wide range of husbandry systems.
There is considerable uncertainty about the relative importance of risk factors for maintenance
of C. burnetii infection in domestic ruminant populations, and for spillover from domestic
ruminants to humans. Further, for most of these risk factors, causality has not been
established. There is also an incomplete understanding of the transmission pathways for either
maintenance or spillover.
Maintenance of C. burnetii infection within a farm might be favoured by persistently infected
domestic ruminants, other animal reservoirs of infection, ticks, husbandry practices that favour
within-herd transmission and/or environmental contamination.
Currently, there is no clear evidence of an association between bacterial genotypes/isolates
and virulence. Further there is no clear evidence of species specificity. The importance of
bacterial genotype/isolate on maintenance of infection and disease progression is uncertain.
Among EU MS, there are some differences in the risk factors associated with spillover of
C. burnetii infection from domestic ruminants to humans. Nonetheless, some risk factors are
common, including:
o

an association between human infection and small ruminants (sheep and goats),

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o

an indication of proximity between animals and human populations, particularly in
association with parturition in animals (and to abortions, in the case of goats), and

o

specific climatic conditions, in particular dry, windy weather.

In humans, the risk of exposure to C. burnetii is increased in several circumstances, either:
o

Following close contact with animals infected with C. burnetii, or

o

Following community-based exposure, caused by an elevation of C. burnetii in the
wider environment following release and dissemination from infected animal hosts.

There is no conclusive evidence in support of a link between an increased density of animals
and/or farms and spillover of C. burnetii from infected farms to humans. However, such a link
would be consistent with the consequences of increased pathogen pressure.
The factors leading to outbreaks of Q fever in the human population are not fully understood.
Risk factors are likely to interact, and the importance of any single risk factor may be difficult
to evaluate.
Related to food safety15
The widespread distribution of C. burnetii in food producing animals and its occurrence in the milk
supply has called into question the role of food as a vehicle for the transmission of this zoonotic
bacterium to humans. The conclusions reached in this Opinion address this concern.
C. burnetii infection in occupationally or otherwise exposed people is mainly due to inhalation
of infected aerosols rather than consumption of contaminated food (e.g. contaminated milk
and dairy products)
C. burnetii is excreted in milk of infected animals (cattle, sheep and goats) for variable periods
during lactation irrespective of whether these are showing clinical signs or not.
In addition, milk can be contaminated with C. burnetii by faecal materials or from sites of
infection in the periparturient and/or lactating animal
Contaminated milk and milk products can be considered as a source of exposure to C. burnetii
for humans; however, no comprehensive data are available on the numbers of C. burnetii
contained in milk.
There are epidemiological indications that consumption of milk and/or milk products
containing C. burnetii has been associated with sero-conversion in humans. However, no data
are available on the dose-response for human infection through food.
There is no conclusive evidence that the consumption of milk and milk products containing
C. burnetii has resulted in clinical Q fever in humans.
No data are available with reference to differences in the pathogenicity for humans of the
different C. burnetii strains acquired through food.
Consumption of raw milk and raw milk products represent a relatively greater risk of human
exposure to C. burnetii than the consumption of both milk and dairy products made with milk
that has undergone appropriate heat treatment.

15

The conclusions related to food safety were adopted by BIOHAZ Panel on 22 April, 2010.

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There are no data available regarding the potential of transmission of C. burnetii infection to
humans through consumption of meat, meat products or fresh produce.
TOR 3: To assess the effectiveness and efficiency of disease control options such as vaccination,
pharmaceutical treatments, establishing animal movement restrictions, the culling of animals,
etcetera.
For almost all of the assessed control options, there is a medium to high level of uncertainty
associated with estimates of control effectiveness. Little published information on control
effectiveness is available, and estimates of effectiveness are primarily based on expert
opinion, derived from field observation and experience, rather than rigorous scientific
assessment.
It is likely that individual control options would need to be used in combination, given that:
o

Within-herd transmission, between-herd spread and spillover to humans are each
likely to involve more than one transmission pathway, and

o

No control measure is likely to be completely effective in limiting within-herd
transmission, between-herd spread and spillover to humans.

There is variation in the sustainability of the assessed control options.
A number of long-term control options were identified, including preventive vaccination,
manure management (based on systems that effectively reduce bacterial load, and therefore
environmental contamination), changes to farm characteristics, wool shearing management,
segregated lambing/kidding area, removal of risk material, visitor ban, control of other animal
reservoirs and tick control. Each of these options, except for the last two, relate specifically to
small ruminants. These options are ranked according to effectiveness, as assessed by expert
opinion, in reducing spillover from domestic ruminants to humans.
Several options were not considered sustainable for long-term control, but may have a role in
the face of an outbreak, including the culling of pregnant animals, a temporary breeding ban,
stamping out, identification and culling of shedders, control of animal movements and stand
still. Each of these measures relate specifically to small ruminants. These options are ranked
according to effectiveness, as assessed by expert opinion, in reducing spillover from domestic
ruminants to humans.
C. burnetii is highly resistant in the environment; consequently, persistent environmental
contamination is a matter of concern.
Vaccination can be used both to reduce the risk of future outbreaks (preventive vaccination)
and in the face of an outbreak (outbreak vaccination), noting that:
o

Preventive vaccination is more effective than outbreak vaccination,

o

Phase I is more effective than phase II vaccination,

o

Vaccination is more effective in non-infected than infected animals,

o

Effectiveness may not be observed in the short-term.

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RECOMMENDATIONS
TOR 1: To assess the significance of the occurrence of Q fever in the EU Member States for a better
understanding of the scale and distribution of the disease and infection (with the focus on farm
animals and humans):
Harmonization of diagnostics and agreed case definitions are needed.
PCR is suitable as a method for the routine diagnosis of C. burnetii infection in domestic
ruminants, keeping in mind its strengths and weaknesses
Improved diagnostics are needed:
o

To substantiate freedom from infection, and

o

In situations when a test-and-cull strategy needs to be implemented.

Further work is needed to better understand the pathogenesis of Q fever in different animal
species to facilitate the development of improved diagnosis to distinguish:
o

Antibodies to phase I and phase II antigens, and

o

Vaccinated and naturally infected animals.

There is a need for harmonized field and laboratory data collection about C. burnetii infection
in animals in EU MS, to allow comparison of prevalence/incidence estimates over time and
between countries.
There is a need to strengthen systems to promote rapid identification and reporting of Q fever
in animals (abortion episodes).
Consideration should be given for support of early information exchange between
veterinarians and public health counterparts regarding potential events with zoonotic potential,
including Q fever.
Further studies on the estimation of Q fever burden of disease in humans are needed.
TOR 2: To assess the risk factors for Q fever occurrence and persistence in animal husbandry, and the
related risks for humans, taking into account at least the presence and density of susceptible livestock
and the type of husbandry in which they are kept:
Prevalence and incidence studies in domestic ruminants should focus on small ruminants,
rather than cattle, to provide a clearer picture of the risk of exposure for humans.
Further investigations and research are needed to:
o

Clarify the relationship between genotype and virulence, the molecular basis for
virulence, and the relationship between mice models and virulence studies in domestic
ruminants,

o

Determine the host specificity of different bacterial isolates,

o

Identify factors influencing the maintenance of infection, including an improved
understanding of transmission pathways,

o

Quantify the number of bacteria excreted under different conditions,

EFSA Journal 2010; 8 (5):1595

83

o

Quantify survival of C. burnetii in the environment,

o

Clarify the role of environmental contamination and climatic factors in the spillover of
infection from animals to humans, and

o

Clarify the trade off between farm density and farm size in the maintenance and
spillover of infection.

TOR 3: To assess the effectiveness and efficiency of disease control options such as vaccination,
pharmaceutical treatments, establishing animal movement restrictions, the culling of animals,
etcetera.
Future investigations are needed to objectively assess the effectiveness of control options for
C. burnetii infection in domestic ruminant populations. Assessment should focus on relevant
epidemiological parameters, including rates of within-herd transmission, between-herd spread
and spillover from animal populations to humans.
Control measures should generally be used in combination, given that:
o

Within-herd transmission, between-herd spread and spillover to humans are each
likely to involve more than one transmission pathway, and

o

No control measure is likely to be completely effective in limiting within-herd
transmission, between-herd spread and spillover to humans.

Longer-term measures to control C. burnetii infection in domestic ruminants should be
considered in those situations where the public health risk is considered unacceptable. Control
measures where effectiveness at reducing spillover was assessed as either high or medium
include preventive vaccination, appropriate manure management, changes to farm
characteristics, wool shearing management, segregated lambing/kidding area, removal of risk
material and visitor ban.
Control measures to address proximity between humans and small ruminants, particularly
around the time of lambing/kidding, would be expected to meaningfully contribute to a
reduction in spillover from animal populations to humans.
There is a need to build awareness among farmers and veterinarians of C. burnetii infection in
farmed ruminants, including risk factors for spillover from domestic ruminant populations to
humans.
Short term measures such as the culling of pregnant animals, a temporary breeding ban,
stamping out, identification and culling of shedders, control of animal movements and stand
still could be used to reduce shedding from infected animals. However, other measures
(including preventive vaccination, manure management, wool shearing management,
segregated lambing/kidding area, removal of risk material) should be considered to reduce
human exposure through environmental contamination.
Vaccination should be considered as a long-term control measure. In order to better assess
vaccine efficacy, it is recommended that field and experimental data are gathered, to improve
our understanding of the epidemiology of C. burnetii infection in, and between, infected
flocks, both prior to and following vaccination.
Antibiotic treatment is not effective in substantially reducing either the level or duration of
bacterial shedding in domestic ruminant populations; therefore the use of antibiotics cannot be
recommended.
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EFSA Journal 2010; 8 (5):1595

97

APPENDICES
APPENDIX A - LITERATURE SEARCH
ISI search
Qualifiers
Disease:
Q fever OR Q fever or Coxiella OR C burnetii OR burnetii OR Query fever OR Nine Mile OR Balkan
grippe
AND
Host:
Cow$ OR Cattle OR Bovine OR Calf$ OR Bull$ OR Heifer$ OR Livestock OR Ruminant$ OR Herd$
OR Sheep OR Ram$ OR Lamb$ Or Flock$ OR Ovis OR Ovine OR Ewe OR Goat OR Capra OR Kid
OR billy goat OR he-goat OR farm animals OR farm Or Domestic or host$
Time frame - Year of publication: 2005 - 2010
409 reports from ISI 4 /2/2010
AND
Location:
Europe OR Europa OR EU OR Austria OR Belgium OR Bulgaria OR Cyprus OR Denmark OR
Germany OR Netherlands Or France OR United Kingdom OR UK OR Ireland OR Spain OR Portugal
OR Luxembourg OR Switzerland OR Italy Or Greece OR Czech republic OR Slovakia OR Slovenia
OR Hungary OR Romania OR Poland OR Sweden OR Finland OR Latvia Or Lithuania Or Estonia Or
Norway OR Iceland Or Switzerland Or Turkey Or Croatia Or Macedonia Or Kosovo Or Albania Or
Bosnia OR Montenegro Or Yugoslavia or Serbia
139 reports from ISI 4/2/2010
PubMed search
Title/abstract
Q fever‖ or Q fever or Coxiella or ―C burnetii‖ or burnetii or ―Query fever‖ or ―Nine Mile‖ or Balkan
grippe) AND (Cow$ OR Cattle OR Bovine OR Calf$ OR Bull$ OR Heifer$ OR Livestock OR
Ruminant$ OR Herd$ OR Sheep OR Ram$ OR Lamb$ Or Flock$ OR Ovis OR Ovine OR Ewe OR
Goat OR Capra OR Kid OR billy goat OR he-goat OR ―farm animals‖ OR farm Or Domestic or host$)
AND (Europe OR Europa OR EU OR Austria OR Belgium OR Bulgaria OR Cyprus OR Denmark OR
Germany OR Netherlands Or France OR United Kingdom OR UK OR Ireland OR Spain OR Portugal
OR Luxembourg OR Switzerland OR Italy Or Greece OR Czech republic OR Slovakia OR Slovenia
OR Hungary OR Romania OR Poland OR Sweden OR Finland OR Latvia Or Lithuania Or Estonia Or
Norway OR Iceland Or Switzerland Or Turkey Or Croatia Or Macedonia Or Kosovo Or Albania Or
Bosnia OR Montenegro Or Yugoslavia or Serbia
Time frame : 2005 - 2010
434 reports from PubMed 4 /2/2010
119 reports from ISI 4 /2/2010
Combine results of ISI and PubMed search 138 + 119 = 257
Automatic removal of the duplicates
220 combined result
Manual removal of the duplicates
183

EFSA Journal 2010; 8 (5):1595

98

Q fever

The search sensitivity was verified by comparison with a set of records provided by the WG of
experts.

Relevance criteria
The title and abstracts were screened independently for relevance by 2 reviewers following the criteria
described below:
Criterion
Language publication

Concerns epidemiological aspects
of C.burnetii infection in humans
and or animals
Concerns
diagnostic
of
C.burnetiiinfection
Concerns control options for
C.burnetii infection in animals
Constitutes a review paper
including epidemiological aspects
of C.burnetii infection in humans
and or animals

included
English abstract and text available
in English, French, Spanish, Dutch,
German

excluded
Abstract not available or text not in
English, French, Spanish, Dutch,
German

yes

no

yes

no

yes

no

yes

no

Disagreements were discussed by the 2 reviewers. When no consensus was possible the record was
included for review of the full text.
Relevant:110
Not relevant : 59

A second relevance screening of titles and abstracts was conducted based on the below criteria leading
to the inclusion of the records in 5 groups.
Groups Criterion
Primary research that provides information on Q fever
1
epidemiological aspects.
Primary research that provides information on diagnostic of
2
C.burnetii infection
Primary research that concerns control options for C.burnetii
3
infection in animals
Constitutes a review paper including epidemiological aspects of
4
C.burnetii infection in humans and or animals
5
Concerns food safety aspects

included

excluded

Results*

yes

no

77

yes

no

23

yes

no

7

yes

no

9

yes

no

4

*Some records were included in more than 1 category
Data extraction
Group 1 records full text were classified also in terms of study design and sampling strategy
Data was extracted from 22 records; results are presented in Table 4 – Animal seroprevalence

EFSA Journal 2010; 8 (5):1595

99

Q fever

APPENDIX B - AD HOC EFSA CONSULTATION (2010)

In order to collect Q fever occurrence data from EU MS and neighbour countries a email and
questionnaire was send by EFSA (see bellow) on the 1/2/2010.The request was distributed to both the
Animal Health and Welfare network and the Zoonosis task force and deadline of 10/2/2010 was
established. Replies were received from 24 of 27 EU MS plus Norway.

“Dear Task Force member and Animal Health network member,
I am contacting you about your latest data on Q fever in animals. This disease is now topical due to the Q fever
outbreak in the Netherlands.
The European Commission has sent EFSA a mandate (see attached) asking for scientific advice about Q fever,
specifically on the significance of the occurrence of Q fever in the EU Member States, the risk factors related to
Q fever infection in animals and possible control options.
EFSA‟s Animal Health and Welfare panel (AHAW) is taking the lead in this mandate and they will prepare a
scientific opinion on the Q fever to address Commission‟s questions. The opinion has a tight time line, it should
be provided by 30 April 2010.
The AHAW working group on Q fever is collecting available information at Member States level to describe the
current Q fever situation in animals within the EU, specifically data is required to address the questions below:
Number of farm-level outbreaks (clinical disease) where Q fever was confirmed
Number of animal-level tests conducted [surveillance, clinical investigation], number of positive
Whether there is a programme of active Q fever surveillance [representative, non-representative
sampling]: % farms seropositive, % animals seropositive
To answer these questions we would like to ask if you could provide data on Q fever in animals in 2009 by
filling in the excel worksheet QFEVER . If you have additional data on testing for Coxiella burnetii could you
report it in the worksheet OtherData. Additionally could you report your cattle, sheep and goat populations for
2009 (and for 2008 and 2007 if you have not previously provided this).
Please note that AHAW working group already has received the data reported on Q fever and animal
populations by the Member States in the framework of the annual zoonoses reporting (Directive 2003/99/EC) for
the years 2005-2008. Thus, there is no need to report this data again.
We would be most grateful if you could send the data to us by the 10th FEBRUARY 2010. The formal reporting
of the Q fever in animals results in the framework of the zoonoses reporting (Directive 2003/99/EC) will take
place later, by end May through the zoonoses reporting web application, as usual.
You can send your information to us by e-mail to qfever@efsa.europa.eu and we would ask you to use the
attached excel file.
This e-mail is sent both to the members of Task Force of Zoonoses Data Collection and of AHAW network
members. We would kindly ask you to coordinate together at the national level regarding this request.
Thank you in advance for your support and collaboration! In case you have any questions, do not hesitate to
contact us (ana.afonso@efsa.europa.eu or milen.georgiev@efsa.europa.eu )
With the best regards”

EFSA Journal 2010; 8 (5):1595

100

Q fever

Total Tested: Please provide the total number of animal-level tests, and the total number of these that were
positive, Coxiella burnetii (Q fever) in Goats, Sheep and Cattle in 2009 in your country
Animals
positive for
Herds positive
Source of
Coxiella
for Coxiella
information
Animals tested
burnetii
Herds tested
burnetii
Animal species
Cattle
Sheep
Goats
Clinical Investigations: Please provide the results of testing for Coxiella burnetii (Q fever) in the context of
clinical investigations. Specifically if data is available report the number of herds tested and the number of
herds testing positive in response to clinical investigations to allow an assessment of the number of outbreaks
occuring in your country in 2009.
Samplin
Test Type
Source of
Animals
Animals
Herds
Herds
Animal
g Stage
information
tested
positive for
tested
positive for
species
Coxiella
Coxiella
burnetii
burnetii
Cattle
Sheep
Goats
Monitoring & Surveillance: Please provide the results of testing for Coxiella burnetii (Q fever) in the context
of surveillance, monitoring and national surveys. Specifically if data is available report the number of animals
tested and the number of animals testing positive to allow an assessment of the prevalence within your country
in 2009.
Sampling Sampling
Test
Source of
Animal
Animals
Herds
Herds
Animal
Stage
Context
Type
information s tested positive for
tested
positive
species
Coxiella
for
burnetii
Coxiella
burnetii
Cattle
Sheep
Goats

EFSA Journal 2010; 8 (5):1595

101

Q fever

APPENDIX C - INFECTION AND DISEASE INFORMATION
Table 15 : Number of laboratory tests conducted in European countries for C. burnetii in
domestic ruminants and number (%) positive, by species, based on data collected in the
EFSA/ECDC zoonoses database about 2006-2008 and collected from ad hoc EFSA consultation
(2010) about data in 2009
CATTLE

Country
Austria
Belgium
Bulgaria
Cyprus
Czech
Republic
Denmark
Estonia
Finland
France
Germany

Animal
2006
population No No
in 2008
test pos %
1 997 209
863 72 8.3
166 4
2.4
2 618 040
.
.
.
584 810
*55 600
1 443 640
1 598 038
236 681
915 345
19 366 182
12 987 543

2007
No
No
test pos
1070 16
220 73
3366 368

236

59

25.0

.

.
.
1139
7
.
510
.
552

.
.
99
8
.
33
.
86

.
.
8.8

.
.
7
0
6936 742

.
6.5
.
15.6

.
536
.
464

Greece
Hungary
Ireland
Italy

768 890
790 036
6 232 527
5 967 760

Latvia
Lithuania
Luxembour
g
Malta
Netherland
s
Poland
Portugal
Romania
Slovakia

380 363
731 250
196 300

.

.

.

.

16 836
3 890 195

.

.

.

51
170

0
0

Slovenia
Spain
Sweden
United
Kingdom
United
Kingdom
(N.I.)
Norway
Switzerland

469 983
5 554 871
1 559 725
10 106 985

6 080 517
1 478 774
*2 683 600
504 797

.

.
40
.
114

No
%
test
1.5 1147
33. 314
2
10. 249
9

2008
No
pos
13
25
27

%
1.1
8.0

No
test
926
1692

2009
No
pos
%
31
3.4
301 17.8

10.8

3353

161

4.8

NA
0

NA
0

NA
0

33
0
0
NA
152

16.1
0
0
NA
NA

.

.

.

.

.
0.0
10.
7
.
7.5
.
24.
6

.
.
11866

.
.
1270

.
.
10.7

205
0
25
NA
NA

.
4
.
1743

.
0
.
320

.
0.0
.
18.4

2
584
283
NR

1
36
23
NR

50
6.2
8.1
NR

NR
NA
0

NR
NA
0

.

.

.

NR
NA
23

1062 1

0.1 1201

5

0.4

NR
NA

NR
NA

NR
NA

0.0
0.0

91
147

2.2 1130
4.1 .

453
.

40.1
.

7334 37
3
.
.
.
.
.
.
.
.

5.1

7587 224

3.0 5786

281

4.9

369
1
NR
NR

20
0
NR
NR

5.4
0
NR
NR

.
.
.
.

.
.
.
.

.
.
.
1

.
.
.
.

1305
.
.
.

59
.
.
2

4.5
.
.
.

415
198
33
1373

17
60
1
2

4.1
30.3
3.0
0.14

.

.

.

.

.

.

5182

323

6.2

NA

NA

NA

.
.

.
.

.
.

.
.

.
.

.
.

.
2660

.
64

.
2.4

68
NR

0
NR

0
NR

%

No
test

2008
No
pos

%

No
test

2009
No
pos

%

.

2
6

.

SHEEP
Country

Animal
population
in 2008

No
test

EFSA Journal 2010; 8 (5):1595

2006
No
pos %

No
test

2007
No
pos

102

Q fever
Austria
Belgium
Bulgaria

389 379
205 624

Cyprus
Czech
Republic
Denmark
Estonia
Finland
France

267 300*

Germany
Greece

2 537 791

Hungary
Ireland
Italy

1 114 681
3 422 900*
7 385 812

Latvia
Lithuania
Luxembour
g
Malta
Netherland
s
Poland
Portugal
Romania
Slovakia
Slovenia

66 801
51 327
8 100*

1 293 909

78
4
.

18
0
.

23.1
0.0
.

9
0
1
0
3410 381

0.0 27
0.0 2
11. 820
2

0
0
41

0.0
0.0
5.0

197 823
173 131
64 087
122 218
7 715 207

5 550 390

12 942
1 212 956
310 689
3 144 600*
8 881 600*
372 039
138 958

Spain
22 439 727
Sweden
508 921
United
33 131 009
Kingdom
United
Kingdom
(N.I.)
Norway
Switzerland

.

.

.

330

133

1425 96
.
.

6.7
.

527
202

31
41

70

3

4.3

27

2

1856 18
2

9.8

903

150

34
1
1709

0
0
116

0
0
6.8

NA
0

NA
0

NA
0

0
0
NA
NA

0
0
NA
NA

.

.

.

61**
0
NA
NA

1880
30

194
8

10.3
26.7

NA
35

40
1

NA
2.9

4

0

0.0

16. 9
6

0

0.0

82
NA
NR

3
NA
NR

3.66
NA
NR

NR
NA
NA

NR
NA
NA

NR
NA
NA

NR
NA

NR
NA

NR
NA

0
0
NR
NR
155

0
0
NR
NR
3.3

12
0
0

44.4
0
0

40.
3
5.9
20.
3
7.4

.

.

.

144

0

0.0 129

13

10.1

.
55

.
1

.
1.8

1
75

.
0

.
.
0.0 727

.
64

.
8.8

3200 19

0.6

3758 3

0.1 1476

0

0.0

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

2

.

0
15
NR
NR
4669*
*
27
0
1709

.

.

.

.

.

.

1022

126

12.3

NA

NA

NA

.
.

.
.

.
.

.
.

.
.

.
.

.
141

.
2

.
1.4

627
NR

0
NR

0
NR

%
0.0
.
.

No
test
109
2
25

2008
No
pos
11
0
3

No
test
90

2009
No
pos
2

%
2.2

774
NA
0

58
NA
0

7.49
NA
0

61**
0
NA
551

0
0
NA
82

0
0
NA
14.9

GOATS
Country

Austria
Belgium
Bulgaria
Cyprus
Czech
Republic
Denmark
Estonia
Finland
France

Animal
population
in 2008
77 655
48 379
238 157
318 400*

No
test
20
2
.

2006
No
pos %
6 30.0
0
0.0
.
.

No
test
5
.
.

2007
No
pos
0
.
.

%
10.1
0.0
12.0

23 459
23 142
2 166
5 918
1 267 198

.

EFSA Journal 2010; 8 (5):1595

.

.

110

33

30.
0

.

.

.

103

Q fever
499

78

15.6

NA

24

NA

.

.

.

5

4

80

0

10.
5
14.
9
0.0

14

0

0.0

141

13

9.2

11

2

62
NA
18.2
NR
NR
NA
NA

1
NA
NR
NR
NA
NA

1.61
NA
NR
NR
NA
NA

.

74

7

9.5

160

51

31.9

.
4

.
57.1

.
24

.
5

.
20.
8

.
5

.
3

.
60.0

0

0.0

227

0

0.0

130

2

1.5

Spain
2 877 611
.
.
.
.
.
Sweden
5 509
.
.
.
.
.
United
96 156
.
.
.
.
3
Kingdom
United
.
.
.
.
.
Kingdom
(N.I.)
Norway
.
.
.
.
.
Switzerland
.
.
.
.
.
NA – information not available
NR – no reply to the consultation in 2010
*Data source - EUROSTAT
** sheep and goats (not specified exact number per species)
*** herd level data

.
.
.

.
.
.

.
.
1

.

54

.
.

.
139

Germany
Greece

190 000*
2 715 177

Hungary
Ireland
Italy
Latvia
Lithuania
Luxembour
g
Malta
Netherland
s
Poland
Portugal

66 000*
7 800*
951 158
12 973
7 386
2 900

Romania
Slovakia
Slovenia

898 300*
7 775
24 228

227

17

7.5

190

20

.

.

.

114

17

50

1

2.0

76

291

15

5.2

.

.

.
7

176

6 402

NR

354 878
37 238
495 900*

1
37

NR NR
58**
*
0
0
0
0
NR
NR
155

NR
NR
3.3

.
.
.

NR
NR
4669*
*
131
3
19

82
0
1

62.6
0
5.3

5

9.3

NA

NA

NA

.
9

.
6.5

31
NR

0
NR

0
NR

Table 16 : Details of tests conducted in European countries during 2009 as part of a clinical
investigation for C. burnetii in domestic ruminants, by species and country, based on data
collected from ad hoc EFSA consultation (2010)
CATTLE
Sampling stage

Test

Country
Austria
Belgium

Bulgaria
Cyprus
Czech Republic
Denmark

Estonia
Finland
France
Germany

at farm-blood
CF
at farm-blood
ELISA
at farm-milk
PCR
at farm-organ/tissue PCR
NA
NA
NA
placenta or fetus FISH technique
material
from
abortions
at farm-blood
NA
NA

EFSA Journal 2010; 8 (5):1595

ELISA

No
test
926
680
16
125

Animals
No
pos
31
58
6
23

.
.
.
.

Herds
No
pos
26
.
.
.

%
3.3
8.5
37.5
18.4

14

1

7.1

.

.

.

0
25

0
0

0
0.0

.

.

.

No
test

%
.
.
.
.

104

Q fever
Greece
Hungary

at farm-blood
at farm-blood
at farm-organ/tissue

Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden

at farm-blood
NR
NR
NA
at farm-organ/tissue
NR
at farm-organ/tissue

United Kingdom
Norway
Switzerland

ELISA
CF
immunohistochemi
cal test
ELISA

2
453
131

1
34
2

50.0
7.5
1.5

1
.
.

1
19
2

100.0
.
.

4

4

100.0

1

1

100.0

PCR

23

0

0.0

8

0

0.0

PCR
CF
PCR

113
1

20
0

17.7
0.0

NA
8
1

0
2
0

0
25.0
0.0

198
0
16

60
0
1

30.3
.
6.3

8
2
2

2
0
1

25.0
0.0
50.0

1

0

0.0

1

0

0.0

1
1373
1

0
2
0

0.0
0.1
0.0

1
874
1

0
2
0

0.0
0.2
0.0

at farm-organ/tissue
NR
NR
NA
at farm-blood
ELISA
at farm-bulk milk
ELISA
at
farm-individual ELISA
blood
at
farm-individual PCR
milk
at farm-organ/tissue PCR
at farm-organ/tissue CF
at farm-blood
NR
SHEEP

Country

Sampling stage

Test

Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary

at farm-blood
at farm-organ/tissue
NA
NA
NA
NA

CF
PCR

Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia

NA
NR
NR
NA
NA
NR
at farm-organ/tissue
NA
at farm-organ/tissue
NR
NR
NA

NA
NA
NA
at farm-blood
at farm-blood
at farm-organ/tissue

EFSA Journal 2010; 8 (5):1595

ELISA
CF
immunohistochemi
cal test

No
test

Animals
Herds
No
%
No
No
%
pos
test
pos
34
0
0.0
.
0
1
0
0.0
.
.

0

0

0

35
40
42

1
0
3

2.9
0.0
7.1

PCR
PCR

15

0

0.0

.
.

4
.
.

1
0
2

25
.
.

NA

0

0

.

0

.

105

Q fever
Spain

at farm-blood

Sweden
United Kingdom
Norway
Switzerland

NA
at farm-organ/tissue
at farm-blood
NR

Indirect
Immunofluorescen
ce assay (IFA)
CF
ELISA

27

12

44.4

2

1

50

1709
25

0
0

0.0
0.0

816
3

0
0

0
0

GOATS
Country

Sampling stage

Test

Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary

at farm-blood
NA
NA
NA
NA
NA

CF

Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain

NA
NR
NR
NA
NA
NR
at farm-organ/tissue

NA
NA
NA
at farm-blood
at farm-blood
at farm-organ/tissue

NR
NR
NA
at farm-blood

ELISA
CF
immunohistochemi
cal test

PCR
CF

Indirect
Immunofluorescen
ce assay (IFA)
ELISA
CF

No
test

Animals
Herds
No
%
No
No
%
pos
test
pos
90
2
2.2
.
2

.

0

0

0

5
60
2

4
0
1

80.0
0.0
50.0

1
.
.

1
0
1

100.0
.
.

1
37

0
0

0.0
0.0

NA
1
.

6
0
0

NA
0.0
.

131

82

62.6

4

3

75.0

Sweden
at autopsy blood
3
0
0.0
1
0
0.0
United Kingdom
at farm-organ/tissue
19
1
5.3
15
1
6.7
Norway
NA
Switzerland
NR
Indirect Immunofluorescence assay (IFA), Enzyme Linked Immunosorbent assay (ELISA), Polymerase Chain Reaction
(PCR), Complement fixation (CF)
* Investigation in relation to clinical symptoms in the population (animals)
NA – information not available; NR – no reply to the consultation in 2010

EFSA Journal 2010; 8 (5):1595

106

Q fever

Table 17 : Details of tests conducted in European countries during 2009 as part of a monitoring
and/or surveillance activities for C. burnetii in domestic ruminants, by species and country,
based on data collected from ad hoc EFSA consultation (2010)
CATTLE
Country

Sampling stage

Austria
Belgium

NA
at farm-bulk milk
at farm-bulk milk
at farm-milk

Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
United Kingdom
Norway
Switzerland

Test

No
test

Animals
No
%
pos

No
test

Herds
No
pos

%

ELISA
PCR
ELISA
CF

.
.
871
3353

.
.
214
161

.
.
24.6
4.8

1043
159
364
168

727
37
270
67

69.7
23.3
74.2
39.9

0

0

0

NA
NA
at farm-bulk milk
NA
NA
NA

ELISA

0
.

0
.

0
.

1871

2

0.2

at farm-blood
NR
NR
NA
NA
NR

ELISA

0
279

0
19

0
6.8

202

19

9.4

CF

256

0

0.0

0
11

0
0

0
0.0

ELISA

415

17

4.1

76

9

11.8

CF

14

0

0.0

.

.

.

ELISA

67

0

0.0

45

0

0.0

NA
NR
NR
at farm-blood
NA
at AI station-blood
NA
at farm-blood
NR

SHEEP
Country

Sampling stage

Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France
Germany
Greece
Hungary

NA
NA

Test

No
test

Animals
No
%
pos

No
test

Herds
No
pos

%

CF

1709

116

6.8

76

40

52.6

0

0

0

0

0

0

0

0

0

NA
NA

NA
NA
NA

EFSA Journal 2010; 8 (5):1595

107

Q fever
Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
United Kingdom
Norway
Switzerland

NA
NR
NR
NA
NA
NR
at farm-milk
NA
NA
NR
NR
NA
NA
NA
at farm-blood
at farm-blood
NR

PCR

ELISA
ELISA

5737
602

53
0

40**

0

0

0.9
0.0

.
121

.
0

.
0.0

GOATS
Country

Sampling stage

Austria
Belgium
Bulgaria
Cyprus
Czech Republic
Denmark
Estonia
Finland
France

NA
NA

Germany
Greece
Hungary
Ireland
Italy
Latvia
Lithuania
Luxembourg
Malta
Netherlands
Poland
Portugal
Romania
Slovakia
Slovenia
Spain
Sweden
United Kingdom
Norway

Test

No
test

Animals
No
%
pos

No
test

Herds
No
pos

%

CF

774

58

7.5

51

26

51

0

0

0

0

0

0

402
149

72
10

17.9
6.7

10
10

8
2

80
20

0

0

0

.

.

.

2

1

50

360

58

16.1

.
1
348

.
0
0

.
0
0

NA
NA

blood
vaginal swab
NA
NA
NA
NR
NR
NA
at farm-milk
NR
at farm-milk
NA
NA
NR
NR
NA
NA
NA
at farm-blood
at farm-blood
at farm-bulk milk
NR

ELISA
PCR

PCR
PCR

ELISA
ELISA
ELISA

513
31
.

4
0
.

0.8
0.0
.

Switzerland
Indirect Immunofluorescence assay (IFA), Enzyme Linked Immunosorbent assay (ELISA), Polymerase Chain Reaction
(PCR), Complement fixation Test (CFT)
* Investigation in relation to clinical symptoms in the population (animals)

EFSA Journal 2010; 8 (5):1595

108

Q fever
a

The data was extracted from a EFSA ad hoc consultation (2010) and relate to data collection classifiers Surveillanceobjective sampling
** herd level data
NA – information not available; NR – no reply to the consultation in 2010

Table 18: Selected number of human outbreaks of Q fever in Germany
Year

Area

No of
cases
235

Source

2010

BadenWürtemb
erg

2009

Paderbor
n,
Westphal
ia

5

sheep

2008

Aschaffe
nburg,
Bavaria

>56

sheep

living near infected herds

01/2008
to
3/2008

LahnDillKreis,
Hesse

>46

sheep

living or working near infected
herds;
walking over grazing grounds

07/2005
to
08/2005

Jena,
Thuringia

>331

sheep

living near the grazing, grounds
(400m);
hot and dry weather;
male gender;
age of 25-64 years

2003

BadenWürttem
berg
Not
specified

8

cattle

calving; contact to stable

2003

Soest,
Nordrhin
eWestphal
ia

299

sheep

contact to super spreading ewe
and contaminated pen at 4th.05.;
duration of contact; age (children
had an attack rate of 3%, adults of
>20%); high seroprevalence and
positive PCR results in sheep
flocks; susceptibility of human
population; no correlation: wind,
tick bites, consumption of
unpasteurised goat or sheep

EFSA Journal 2010; 8 (5):1595

Risk factors

Comments

Reference

being a farmer or waste control
worker; seeing rodents regularly
during work; close and direct
contact to animals e.g. goats,
cattle and (pet) rats; living in sight
of a goat or sheep stable; sheep
densitiy; increasing age
handling of pregnant animal,
abortion

seroprevalence
study and risk
factor analysis;
three years study

Brockmann
et al., in
press

aquired during
animal experiment
(obstetrics); other
earlier cases have
been described for
the university of
Giessen, Hesse
15% children and
youngsters

Henning
et al., 2009

16% children and
youngsters;
26 of 30 tested
sheep had an
active C.burnetii
infection; 5 sheep
were ‗positive‘ for
C. burnetii
Case definition:
a. CFT Phase II
antigen titer > 1:80
or ELISA Phase II
IgM positive
b. fever > 38.5°C,
myalgy or
headache lasting
longer than 1 day
during 13.06. and
28.07.
family members
visiting the farm;
calf died; ELISA
and culture
positive
farmers‘ market;
25% of the
animals of the
herd tested
positive in ELISA;
case definition:
symptom onset
4th.05. to 3rd.June,
exclusion
criterion: negative

RKI, 2008
Hamann
et al., 2009

RKI, 2008

Gilsdorf
et al., 2008
RKI, 2006

RKI, 2004

Porten
et al., 2006
RKI, 2003

109

Q fever
cheese, pregnancy, heart valve

07/2001
till
08/2001

Munich,
Bavaria

3

sheep

exposure to contaminated dust

12/2000
till
05/2001

Hochsaue
rlandkrei
s
Nordrhin
eWestphal
ia;
WaldeckFrancken
berg,
Hesse
Dortmun
d,
Nordrhin
eWestphal
ia

75

sheep

contaminated dust

82

sheep
manure

1997

BadenWürttem
berg
not
specified

12

fallow
deer

exposure to farm, faeces and
contaminated manure; steady
wind; duration time of exposure;
contact to dogs and cats; smoking
cigarettes; no correlation: type of
outdoor activity, precipitation and
temperature, exposure to
meadows with grazing sheep,
consumption of unpasteurised
goat or sheep cheese (another
farm nearby located), contact to
other farm animals or pigeons,
tick bites, consumption of raw
milk
contact

01/1996
to
06/1996

Rollshaus
en,
county of
Lohra,

56

sheep

05/1999
till
08/1999

EFSA Journal 2010; 8 (5):1595

contact to sheep, walking near by
sheep farm; outdoor lambing; dry
season; no correlation: drinking

IgM titer for Phase
II antigens;
shortest onset of
disease 2 days;
25% hospitalised,
no deaths
4 of 11 pregnant
women were
infected without
further
complications
movie team:
working in a barn
with wind
generators for
more than 10h;
75% of sheep
tested serological
positive, Coxiella
positive placenta
was found; 17
further human
cases in
neighbouring areas
found
serological
positive animals in
herds

RKI, 2002

RKI, 2001

700 sheep;
lambing within a
barn on farm;
manure was stored
in lambing barn
till 3rd till 15th of
May then
displaced on fields
nearby; 57% of
herd animals were
ELISA positive in
serology;

Reintjes
et al., 2000

abortions,
abnormal fetuses,
high mortality
(50%) of offspring
in a herd of 71
fallow deer
(Cervus dama);
attack rate of 92%
in humans
75% of sheep
tested were
seropositive; small

RKI, 1997

Lyytikäine
n et al.,
1997

110

Q fever
Hesse

1994

4/1992
to
5/1992

1982/19
83

raw milk, tick bites, contact with
other domestic animals, living on
a farm with cattle, sheep, or goats,
outdoor leisure activities
hot and dry weather; wind; age
(young persons being affected:
average 38 years)

town with 300
inhabitants

contact to diseased
animals during aid
or section; contact
to animal
transporting van;
contact to
personnel of the
hospital;
serological and
culture positive
herd
the only reported
outbreak in the
GDR

Düsseldo
rf,
Nordrhin
eWestphal
ia
Berlin

>18

sheep

80

sheep

direct or indirect contact to a
clinically diseased sheep herd at
an animal hospital
wind and dry season

Suhl,
Thuringia
, GDR

156

various
rumina
nt
species

direct or indirect contact

Lyytikäine
n et al.,
1998
Schulze
et al., 1996

Schneider
et al., 1993
Molle
et al.,
1995b

Stelzner
et al., 1986
Kramer,
1990

Table 19: C. burnetii infection in animals -Germany
location

Year

Animals
/herds

Tests

Lower Saxony

nd

nd / 95

BadenWürtemberg

nd

3.460 sheep
/nd

Nd,
seropreva
lence
CFT
>1:10
ELISA
>0.4

Northerrn
BadenWürttemberg

19982000

1.167 cattle /
105

ELISA
antigen
capture
ELISA

1.4 to 2 / nd

BadenWürtemberg

1996/
97

826 cattle /
38

CFT
antigen
capture
ELISA

6.7 / nd
8.5 / nd

Hannover,
Lower Saxony

1992/
93

500 cattle
(random) /
nd
665 cattle /

CFT
>1:10

7.6 / nd
9.6 / 76.9
19.3 / 78.8
5.6 / 100

EFSA Journal 2010; 8 (5):1595

Prevalence
animals/herds
%/%
2.7 / nd

Comments

Reference

Prevalence of
the agent:0.7

Runge and
Ganter, 2008

0 to 1.4 (total:
0.5)/ nd
0.9 to 10.2 (total:
8.7) / nd

Samples
collected in the
four districts of
BW; correlation
CFT and
ELISA 90.5%
Q fever
correlated with
abortion; herds
with fertility
problems
In th group
fertility
problems:
14.3% were
positive with
the Ag-ELISA
versus 0.6%
without
problems; in
CFT 9.0%
versus 3.4%
Correlation
with herd size

Sting et al.,
2004

Sting et al.,
2002

Sting et al.,
2000

Wittenbrink
et al., 1994

111

Q fever

Southern Bavaria

1991

Arnsberg,
NorthrhineWestphalia

1989/
90

39
383 (fertility
problems)/
33
612 bulls / 1
1.095 cattle /
21
3.500 cattle /
155

ELISA

11.8 / 81.0

ELISA,

13.3 / 57.4 (within
herd 24.7)
12.9 / 53.5 (within
herd 21.0)

IFT >1:8

Northern Bavaria

3.884 cattle/
246

CFT

7.6 / 30.0

Stuttgart, BadenWürtemberg

2.109 cattle /
125
Farms with
fertility
problems:
1.064 cattle/
208
7.580 cattle /
17
4.337 sheep
/ nd

CFT
>1:5

8 / 35.2

Thuringia, GDR
Thuringia, GDR

1980ti
es
19801989

EFSA Journal 2010; 8 (5):1595

24.4 / 48.1

Survey also on
reservoir
animals
Correlation
coefficient was
0.79;
prevalence
increased with
herd size
prevalence
increased with
herd size: big
farms
61.1%
and 9.5% of
animals
positive; small
farms: 12.1%
and 3.1% of
animals
positive
describes
eradication
strategies

Rehacek et al.,
1993
Klemt
and
Krauss, 1991

Roth
and
Bauer, 1986

Woernle and
Müller, 1986

CFT
>1:10

CFT

19.4 /100

CFT
>1:20

1.1 / 47.0

Correlation to
herd size and
bad mangement

Lange
1992
Lange
1992

et al.,
et al.,

112

Q fever

GLOSSARY AND ABBREVIATIONS
Ab

antibodies

CD

Council Decision

CFT

Complement fixation test

DIVA

Differentiate Infected from Vaccinated Animals

EC

European Commission

ECDC

European Center for Disease Prevention and Control

EFSA

European Food safety Authority

ELISA

Enzyme-Linked Immunosorbent Assay

FITC

Fluorescein isothiocyanate

IFA

Indirect Fluorescent Antibody

IHC

Imunohistochemistry

LCV

Large cell variant

MAT

Micro agglutination test

MIFT

Microimmunofluorescence test

MLVA

Multiple Loci VNTR Analysis

MS

Member states

MST

Multispacer sequence typing

NRL

National Reference Laboratory

OIE

World Organisation for Animal Health

PCR

Polymerase Chain Reaction

SCV

Small cell variant

SDC

Small dense cell

ToR

Terms of reference

VNTR

Variable Number of Tandem Repeats

WG

Working group

EFSA Journal 2010; 8 (5):1595

113

Q fever

Burden of disease - the impact of a health problem in an area measured by financial cost, mortality,
morbidity, or other indicators.
Monitoring - system of collecting, analysing and disseminating data on the occurrence of disease,
infectious agents and contamination. As opposed to surveillance, no active control options are taken
when positive cases are detected (Dir. 2003/99).
Positive result - situation stating when the sample is considered to be positive for the agent.
Prevalence - the proportion of existing cases in a population at the specified time of testing.
Sample - set composed of one or several units or a portion of matter selected by different means in a
population or in an important quantity of matter, which is intended to provide information on a given
characteristic of the studied population or matter and to provide a basis for a decision concerning the
population or matter in question or concerning the process which has produced it (Reg. (EC) No
2073/2005).
Sampling strategy - planned procedure for selecting samples from a population and for conducting
the sampling in order to obtain the information needed.
Sampling unit - the unit which the specimens taken represent and which is considered either infected
(contaminated) or not, based on the analyses result. For animal data, the sampling unit may be
―Animal‖, ―Flock”, ―Herd”, ―Holding‖ or ―Slaughter batch”; for food data, the sampling unit might
be ―Single” or ―Batch”.
Surveillance - a close and continuous observation for the purpose of control. As opposed to
monitoring, control options are taken when positive cases are detected. This type of programme does
often but not always have a defined target for diseases / contamination reduction.
Survey - study involving a sample of units selected from a well-delineated population. This (target)
population is the entire set of units to which findings of the survey are to be extrapolated. The units to
examine are to be selected randomly (Rothman, 1986 and Noordhuizen et al., 2001).
Suspect sampling following a recent case - unplanned selection of a sample, where the individual
units are selected based on the recent judgement and experience regarding the occurrence of infection
or contamination in the population, lot, or sampling frame, e.g. earlier positive samples. The samples
obtained from this procedure are not randomly extracted.

EFSA Journal 2010; 8 (5):1595

114