# Ecological dominance in spatial distribution of avian influenza (H5N1) outbreaks [response]

Elsa Jourdain, Michel Gauthier-Clerc, Philippe Sabatier

► To cite this version:

Elsa Jourdain, Michel Gauthier-Clerc, Philippe Sabatier. Ecological dominance in spatial distribution of avian influenza (H5N1) outbreaks [response]. Emerging Infectious Diseases, 2007, 13 (8), pp.1270-1271. hal-03326094

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Submitted on 25 Aug 2021

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Distributed under a Creative Commons Attribution 4.0 International License
When all identified strains of *M. cosmeticum* are considered, this species is clearly present in diverse geographic regions and in healthcare institutions. These findings suggest that it may be widely distributed in the environment and should be regarded, along with other rapidly growing mycobacteria species, as a potential pathogen.

## Acknowledgment

We thank Lena Fischer of the Ohio Department of Health for technical contributions.

Robert C. Cooksey,*
Jacobus H. de Waard,†
Mitchell A. Yakrus,* Sean R. Toney,*
Omaira Da Mata,†
Scott Nowicki,‡ Kevin Sohner,‡
Elizabeth Koch,‡
Cathy A. Petti,§
Roger E. Morey,*
and Arjun Srinivasan*

*Centers for Disease Control and Prevention, Atlanta, Georgia, USA; †Instituto de Biomedicina, Caracas, Venezuela; ‡Ohio Department of Health, Columbus, Ohio, USA; and §ARUP Laboratories, Salt Lake City, Utah, USA

## References

1. Cooksey RC, de Waard JH, Yakrus MA, Rivera I, Chopite M, Toney SR, et al. *Mycobacterium cosmeticum* sp. nov., a novel rapidly growing species isolated from a cosmetic infection and from a nail salon. *Int J Syst Evol Microbiol.* 2004;54:2385-91.

2. Pfyffer GE, Brown-Elliott BA, Wallace RJ Jr. *Mycobacterium*: general characteristics, isolation, and staining procedures. In: Murray PR, Baron EJ, Pfaller MA, Jorgensen JH, Yolken RH, editors. Manual of clinical microbiology. Washington: ASM Press; 2003. p. 532-59.

3. Dombek PE, Johnson LK, Zimmerley ST, Sadowsky MJ. Use of repetitive DNA sequences and the PCR to differentiate *Escherichia coli* isolates from human and animal sources. *Appl Environ Microbiol.* 2000;66:2572-7.

4. Wagner D, Young LS. Nontuberculous mycobacterial infections: a clinical review. *Infection.* 2004;32:257-70.

Address for correspondence: Robert C. Cooksey, Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, 1600 Clifton Rd NE, Mailstop F08, Atlanta, GA 30333, USA; email: rcooksey@cdc.gov

# Ecoregional Dominance in Spatial Distribution of Avian Influenza (H5N1) Outbreaks

**To the Editor:** Recent articles in Emerging Infectious Diseases (1,2) and elsewhere (3,4) have highlighted the role of Anatidae migration in dispersal of the H5N1 subtype of highly pathogenic avian influenza (HPAI) virus. Although these articles point out that identifying the geographic origin of migrating waterfowl is needed to understand and predict pathogen dispersal, study analyses have been limited to pathways with nominal reference to climatic and vegetation patterns that control spatiotemporal patterns of this migration.

We propose that a better understanding of the threat of future spread can be obtained by identifying specific climatic and vegetation zones that are important in the life cycle of Anatidae, and which account for a disproportionately large number of HPAI outbreaks. The concept of ecoregions (5,6), i.e., distinct assemblages of natural communities determined by climate, geology, and evolution, is a useful zonal classification for evaluating HPAI outbreaks. A World Wildlife Fund classification delineating 825 terrestrial ecoregions (7), combined with a Google Earth map of 3,133 avian influenza outbreaks from November 24, 2003, to November 21, 2006 (8), provided the basis for this analysis.

All files were converted to shapefiles (Environmental Systems Research Institute, Redlands, CA, USA), and overlay analysis was performed by using ArcGIS software (Environmental Systems Research Institute).

The online Appendix Figure (available from www.cdc.gov/EID/content/13/8/1269-appG.htm) shows a chloropleth map (display of quantitative or qualitative information about subentities in terms of symbols or colors) of ecoregions with numbers of avian influenza cases (each spatially and temporally isolated set of individual events, regardless of number of deaths, is recorded as a case). Panels A, B, and C of this figure show enlargements of specific ecoregions with large numbers of known cases in regions of Eurasia, Southeast Asia, and Africa, respectively. Twenty-five ecoregions, representing 8.8% of the terrestrial surface area, accounted for 2,407 (76.8%) cases. A total of 132 of 825 ecoregional classifications had ≥1 recorded case of an avian influenza outbreak, but most (83) had <10 cases each.

Regionally, Southeast Asia has 12 ecoregions that collectively account for 1,651 cases (online Appendix Figure, panel B) that have occurred consistently, albeit cyclically, since 2003. Among these ecoregions, the freshwater wetlands of the Chao Phraya, Tonle Sap, and Red Rivers are known migratory waterfowl wintering habitats in which 719 cases were located. Recent phylogenetic evidence suggests that this area is a local hotspot for an endemic strain of avian influenza (H5N1) that demonstrates bidirectional dispersal among localities within the region (9).

In the Eurasian region (online Appendix Figure, panel A), 12 ecoregions accounted for 712 cases. The easternmost ecoregions, the Kazakh forest steppe (location of Lake Chany, an Anatidae habitat and breeding area) and the Kazakh Steppe, accounted for 132 cases, with the first case recorded
on July 18, 2005. Subsequent major outbreaks in this region occurred in July–August 2005 and December 2005–January 2006. Regions around the Black Sea, including Euxine-Colchic broadleaf forests (deltas of the Kizil and Yesil Rivers), westernmost Pontic steppe (Lake Sivash), and Balkan mixed forests (deltas of the Danube, Olt, and Siret Rivers) have been loci for outbreaks in the central Eurasian region since October 1, 2005. Additional outbreaks have occurred since October 21, 2005, in the Eastern Anatolia montane steppe and deciduous forests (location of Lakes Van and Urmia, and Karakaya and Keban Baraji Reservoirs). Mixed and broadleaf forests of central and western Europe account for the remaining European cases since October 19, 2005. Anatidae habitats in this area include freshwater wetlands formed by the Danube, Rhine, Rhone, and Saone Rivers, and the Baltic basin.

Two African ecoregions, the Nile Delta-flooded savanna (online Appendix Figure, panel A) and the West Sudanian savanna (online Appendix Figure, panel C), including part of the Lake Chad ecosystem, i.e., the Kano River and the Tiga Reservoir, accounted for 79 cases. The initial Sudanian savanna case was identified on January 10, 2006, and the initial Nile Delta case was identified on February 17, 2006.

Our results may be skewed by
several confounding factors, e.g., low
national surveillance capabilities re-
sulting in unreported cases and effects
of the poultry trade. Nonetheless, the
findings have implications for global
monitoring of avian influenza (H5N1)
outbreaks. Although migratory path-
ways and the poultry trade should
continue to be scrutinized, monitor-
ing efforts should focus on wintering
and breeding habitats of migrating
waterfowl, especially wetlands lo-
cated within ecoregions with a dis-
proportionately large number of avian
influenza outbreaks. These hotspots

are also likely to give rise to endemic
local strains with regional dispersal
characteristics (9).

Raja Sengupta,*
Lauren Rosenshein,*
Mark Gilbert,* and Claire Weiller*

*McGill University, Montreal, Quebec,
Canada

References

1. Gilbert M, Xiao X, Domenech J, Lu-broth J, Martin V, Slingenbergh J. Anatidae migration in the western Palearctic and spread of highly pathogenic avian influenza H5N1 virus. Emerg Infect Dis. 2006;12:1650–6.

2. Jourdain E, Gauthier-Clere M, Bicout DJ, Sabatier P. Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerg Infect Dis. 2007;13:365–72.

3. Kilpatrick AM, Chmura A, Gibbons DW, Fleischer RC, Marra PP, Daszak P. Predicting the global spread of H5N1 avian influenza. Proc Natl Acad Sci U S A. 2006;103:19368–73.

4. Olsen B, Munster VJ, Wallensten A, Waldenstro J, Osterhaus A, Fouchier R. Global patterns of influenza A virus in wild birds. Science. 2006;312:384–8.

5. Omernik J. Ecoregions of the conterminous United States. Annals of the Association of American Geographers. 1987;77:118–25.

6. Olson DM, Dinerstein E, Wikramanayake E, Burgess ND, Powell G, Underwood E, et al. Terrestrial ecoregions of the world: a new map of life on earth. Bioscience. 2001;51:933–8.

7. Conservation science: ecoregions. Washington: World WildLife Fund; 2007. [cited 2007 May 3]. Available from http://www.worldwildlife.org/science/ecoregions.cfm

8. Butler D. New Google earth maps of avian flu spread (updated September 2006). [cited 2007 Feb 21]. Available from http://declanbutler.info/flumaps1/avianflu.html

9. Wallace RG, Hodac H, Lathrop RH, Fitch WM. A statistical phylogeography of influenza A H5N1. Proc Natl Acad Sci U S A. 2007;104:4473–8.

**In Response:** Ecoregions are large units of land that reflect the distribution of species and communities and are used to define priority areas for biodiversity conservation. In their letter (1), Sengupta et al. suggest that ecoregions could help explain the spatial distribution of observed outbreaks of HPAI (H5N1). Since most outbreaks they observed occurred in ecoregions with waterfowl habitats, they concluded that monitoring efforts should focus on these areas.

Habitat mapping is useful for predicting the spread of wildlife-associated diseases. However, because ecoregions are large areas where agriculture and other human activities abound, many confounding variables exist. To assume that ecoregions with HPAI (H5N1) outbreaks are chiefly characterized by the natural biotopes is too simplistic.

In addition, the authors assume
that wild waterfowl are the main fac-
tors in the dispersal of HPAI (H5N1).
Although wild birds are known to be
involved in the dispersal of low patho-
genic strains of avian influenza viruses
(2,3), the precise role of these birds in
the dispersal of HPAI (H5N1) viruses
remains controversial. It is now clear
that the expansion of HPAI (H5N1)
in Asia and to Africa was primarily
associated with the poultry trade (4),
which is not represented on a map of
ecoregions. Also noteworthy is that
HPAI (H5N1) did not persist in wild
birds after the spring of 2006, and no
case has been detected in the wetlands
of America despite the migration of
wild ducks and waders from Siberia
(their main breeding ground) to Asia,
Europe, and North America.

We believe that human activity is
the primary vehicle for the spread of
HPAI (H5N1) virus. Rather than the
monitoring of waterfowl habitats, in-
creased surveillance of the legal and
illegal trade of birds and bird products
is more likely to help in predicting the
spread of this virus.

Address for corrrespondence: Raja Sengupta,
Department of Geography and School
of Environment, McGill University, 805
Sherbrooke St W, Montreal H3A2K6, Quebec,
Canada; email: sengupta@geog.mcgill.ca
Elsa Jourdain,*†
Michel Gauthier-Clerc,*
and Philippe Sabatier‡

*Station Biologique de la Tour du Valat, Ar-
les, France; and †Ecole Nationale Vétéri-
naire de Lyon, Marcy l'Etoile, France

References

1. Sengupta R, Rosenschein L, Gilbert M, Weiller C. Ecoregional dominance in spatial distribution of avian influenza (H5N1) outbreaks. Emerg Infect Dis. 2007;13:1269-70.

2. Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P. Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerg Infect Dis. 2007;13:365-72.

3. Olsen B, Munster VJ, Wallensten A, Waldenstro J, Osterhaus A, Fouchier R. Global patterns of influenza A virus in wild birds. Science. 2006;312:384-8.

4. Gauthier-Clerc M, Lebarbenchon C, Thomas F. Recent expansion of highly pathogenic avian influenza H5N1: a critical review. Ibis. 2007;149:202-14.

Address for correspondence: Elsa Jourdain,
Unité Environnement et Prédiction de la Santé
des Populations-Techniques de l'Ingénierie
Médicale et de la Complexité-Informatique,
Unité de Mixte de Recherche 5525, Ecole
Nationale Vétérinaire de Lyon, 1 Ave Bourgelat,
F-69280 Marcy l'Etoile, France; email:
e.jourdain@vet-lyon.fr

**In Response:** Sengupta et al. (1) discuss the role of ecoregions in the distribution of HPAI (H5N1) outbreaks. Although the concept of ecoregions is undoubtedly useful in global biogeography, we do not understand the point they are trying to make. In our article (2), which is cited in their letter, we undertook a descriptive study to determine whether spread of HPAI (H5N1) virus was consistent in time with ecologic drivers of bird migration and in space with distribution of major migratory flyways of Anatidae. It is obvious that the distribu-

tion pattern of Anatidae is dependent
on ecologic variables, and some of
these variables are summarized by the
ecoregion concept.

However, apart from a strictly
descriptive point of view, we do not
see how the ecoregion concept applies
to describe patterns in HPAI (H5N1)
spread and distribution. Sengupta et al.
list ecoregions where reports of HPAI
(H5N1) were concentrated. However,
what do they infer from this? They
observe regions with many reports of
HPAI (H5N1) and conclude that these
ecoregions are at risk. We find this
reasoning completely circular, and
any geographic zonation would pro-
vide the same observation. They may
mean that ecoregions define boundar-
ies within which secondary spread of
HPAI is more likely than across ecoreg-
gions. However, this hypothesis would
need to be more clearly demonstrated
and quantified before the ecoregion
concept can be used for global moni-
toring of HPAI (H5N1) outbreaks.

Marius Gilbert,*
Xiangming Xiao,†
and Jan Slingenbergh‡

*Free University of Brussels, Brussels, Belgium; †University of New Hampshire, Durham, New Hampshire, USA; and ‡Food and Agriculture Organization of the United Nations, Rome, Italy

References

1. Sengupta R, Rosenschein L, Gilbert M, Weiller C. Ecoregional dominance in spatial distribution of avian influenza (H5N1) outbreaks. Emerg Infect Dis. 2007;13:1269-70.

2. Gilbert M, Xiao X, Domenech J, Lu-
broth J, Martin V, Slingenbergh J. Ana-
tidae migration in the western Palearctic
and spread of highly pathogenic avian
influenza H5N1 virus. Emerg Infect Dis.
2006;12:1650-6.

Address for correspondence: Marius Gilbert,
Laboratory of Biological Control and Spatial
Ecology, Free University of Brussels, CP
160/12, 50 Ave F.D. Roosevelt, B-1050 Brussels,
Belgium; email: mgilbert@ulb.ac.be

Nephropathia
Epidemica in
Metropolitan Area,
Germany

**To the Editor:** Old World hantaviruses (family *Bunyaviridae*) are rodentborne pathogens that can cause hemorrhagic fever with renal syndrome (HFRS) (1). At least 3 different pathogenic hantavirus species have been detected in Europe: *Dobrava-Belgrade virus* (DOBV), *Tula virus*, and *Puumala virus* (PUUV) (1–3). Most human hantavirus infections in Europe are assigned to PUUV transmitted by bank voles (*Myodes glareolus*, formerly *Clethrionomys glareolus*). Although PUUV is thought to cause a mild form of HFRS, designated as nephropathia epidemica (NE), severe courses have been described with a case-fatality ratio of up to 0.6% (3).

Even though human hantavirus
infections have sporadically been re-
ported in Germany since 1983 (e.g.,
4-7), clinically apparent hantavirus
infections (HFRS, NE) did not be-
come notifiable diseases in Germany
until 2001. From 2001 through 2004,
~140 to 240 cases per year have of-
ficially been documented in Germany;
most were caused by PUUV. Regions
endemic for PUUV have been identi-
fied in southern Germany, especially
the Alb-Danube region (4,6,8). Since
2004, 2 aspects of the situation in Ger-
many have changed. First, the number
of clinical cases has increased dramat-
ically to a total of 448 in 2005. Sec-
ond, hantavirus infections have been
observed in regions previously not
recognized as endemic for hantavi-
ruses (9). An increased number of hu-
man cases were also observed in other
European countries (10).

Here we report the first, to our
knowledge, documented PUUV-as-
sociated urban NE outbreak, which
occurred in a city park in Germany.
In 2005, a total of 89 cases were re-
ported in the district of Cologne with