35

Vector-borne Infectious Diseases and Climate Change
Ichiro KURANE*, Akira KOTAKI, Tomohiko TAKASAKI
Department of Virology I, National Institute of Infectious Diseases
1-23-1 Toyama, Shinjuku-ku Tokyo, 162-8640 Japan*e-mail: kurane@nih.go.jp

Abstract
Climate change has a variety of impacts on human health including spread of infectious diseases.
Vector-borne and water-borne infectious diseases are two main categories of diseases which are forecasted
to be most affected.
It has been reported that climate change has altered the distribution of some infectious disease vectors
such as mosquitoes and ticks. Many papers have also reported that the climate has influenced epidemics ofvector-borne infectious diseases such as dengue fever and malaria. It is forecasted that epidemic andendemic regions of dengue fever and malaria will expand in many areas and probably increase the numberof patients. It is also likely that the endemic region of Japanese encephalitis (JE) virus will expand northward and the activity of JE virus will increase in northern Japan. On the other hand, it should be noted thatin addition to climate change, multiple biological and sociological factors also influence epidemics ofvector-borne infectious diseases. Our current understanding of the effects of climate change on humanhealth, including infectious diseases, is insufficient. Further extensive studies are warranted.
Key words: climate change, dengue fever, global warming, Japanese encephalitis, malaria,
vector-borne infectious diseases

1. Introduction
Global warming is an unequivocal phenomenon
today and is evident from observations of increases in
global average air and ocean temperatures. Global
warming is associated with other climate changes, e.g.,changes in rainfall, increases in storms. Climate change
has a variety of impacts on human health. Many effects
have been reported; however, many of the emerging andforecasted effects have yet to be clearly confirmed with
scientific data. The emerging evidence of the effect ofclimate change/global warming on human health andprojected trends are summarized in the 4th report of theIntergovernmental Panel on Climate Change (IPCC)(Confalonieri et al., 2007). This report states that climate change has altered the distribution of some infectious disease vectors (medium confidence), altered theseasonal distribution of some allergenic pollen species(high confidence), and increased heat wave-related
deaths (medium confidence). The projected trends inclimate change-related effects include: (1) an increase inmalnutrition and consequent disorders, including thoserelating to child growth and development (high confidence), (2) an increase in the number of people sufferingfrom mortality, disease or injury from heat waves,
floods, storms, fires and droughts (high confidence), (3)a change of the range of some infectious disease vectors
Global Environmental Research
12: 35-40 (2008)
printed in Japan(high confidence), (4) mixed effects on malaria; in someplaces the geographical range will contract, elsewhere
the geographical range will expand and the transmission
season may be changed (very high confidence), (5) anincrease in the burden of diarrheal diseases (medium
confidence), (6) an increase in cardio-respiratory morbidity and mortality associated with ground-level ozone(high confidence), (7) an increase in the number ofpeople at risk of dengue fever (low confidence), and (8)some benefits to health, including fewer deaths fromcold, although it is expected that these will be outweighed by the negative effects of rising temperatures
worldwide, especially in developing countries (highconfidence). These effects on human health can bedivided into direct and indirect ones (Table 1). The
direct effects include an increase in mortality especiallyamong those with cardiovascular and and/or respiratory
diseases, and an increase in cases of heat stroke due toheat waves. The indirect effects include an increase in
the number infectious disease patients, and possibly
changes in the patterns of allergies.
Vector-borne and water-borne infectious diseases are
two main categories of infectious diseases which are
forecasted to be most affected (Fig. 1). There will be anincrease in vector-borne infections as a result of an
expansion of arthropod-infested areas, an increase infeeding behavior of mosquitoes, an increased rate of©2008 AIRIES36

I. KURANE et al.

Table 1 Some of the emerging and forecasted effects of climatechange on infectious diseases and other human healthconditions in the world.
Effects on infectious diseases• Expansion of mosquito-infested areas and increase inmosquito activity: increase in the number of patients withmosquito-borne infectious diseases (i.e., dengue andmalaria) and expansion of epidemic areas.
• Contamination of water and foods with bacteria: increase in
the number of patients with water-borne and food-borne
infectious diseases.
• Deterioration of environmental and social conditions:increased risk of infectious diseases
Direct effects on other health conditions• Heat waves: short-term increase in mortality especiallyamong those with cardiovascular and/or respiratory
diseases, and increase in heat-shock patients• Co-effects with air pollution: increases in asthma andallergy patients• Storms and floods: increases in morbidity and accidental
deathsFig. 1 Projected effects of global warming on infectious diseases.

larval development and an increased speed of virus
replication in infected mosquitoes. There will be anincrease in diarrheal diseases from bacterial infections
due to contamination of water and foods.

2. Effects of Climate Change on Vector-borne
Infectious Diseases
Vector-borne infectious diseases are transmitted by
infected arthropods. The vectors include mosquitoes,
ticks, sandflies, blackflies and triatomid bugs. Major
mosquito-borne infectious diseases include dengue
fever/dengue hemorrhagic fever, Japanese encephalitis,
West Nile fever, Murray Valley encephalitis, Ross Riverfever, Rift Valley fever and yellow fever, which arecaused by viruses, and malaria caused by protozoa.
Tick-borne infectious diseases include tick-borne
encephalitis, which is caused by tick-borne encephalitis
viruses. There is evidence suggesting that some of these
vector-borne infectious diseases are affected by climatechange.
2.1 Dengue fever (DF) and dengue hemorrhagic
fever (DHF)
Dengue fever and dengue hemorrhagic fever are themost important vector-borne viral infectious diseases in
the world (Kurane & Takasaki, 2001; Kurane, 2007).
There are four serotypes of dengue virus, dengue virus
types 1, 2, 3 and 4. Although these are called the four

serotypes of the dengue virus, it is generally acceptedthat these four dengue viruses are antigenically-relateddifferent species. Humans are natural hosts of dengue
viruses, and dengue viruses are maintained between
mosquitoes and humans in nature. Dengue viruses aretransmitted to humans by infected mosquitoes, mainly
Aedes aegypti and Aedes albopictus. Dengue virus infection can be asymptomatic or cause two forms of
illness, dengue fever and dengue hemorrhagic fever,
although the majority of dengue viral infections are
asymptomatic. Dengue fever is a self-limited febrile illness accompanied by retro-orbital or frontal headache,etc. Myalgia and bone pain occur soon after the onset ofthe fever. A small percentage of patients infected withthe dengue virus demonstrate plasma leakage into interstitial spaces, thrombocytopenia and also hemorrhagic
manifestation. This severe life-threatening syndrome iscalled dengue hemorrhagic fever. Dengue fever anddengue hemorrhagic fever are a serious cause ofmorbidity and mortality in most tropical and subtropicalareas of the world: mainly Southeast and South Asia,
Central and South America, and the Caribbean (Fig. 2).
There are approximately 2.5 billion people at risk in theworld for infection with dengue viruses. Nearly 100
countries and areas are at risk for domestic dengue virus
infections. Dengue cases are estimated to occur in up to
100 million people annually. A total of approximately
500,000 cases of DHF occur annually. Large epidemics
of DF/DHF are usually caused by Aedes aegypti, while
Aedes albopictus causes only small outbreaks.
It has been reported that there is an association
between epidemics of dengue fever and climate (Hales
et al., 1999; Hales et al., 2002; Corwin et al., 2001;
Gagnon et al., 2001; Cazelles et al., 2005). However,these reported associations are not always consistent,
probably due to the complexity of climatic effects ontransmission, and also due to the presence of other factors. Heavy rainfall or high temperature can lead to anincrease in transmission; however, there are reports thatdrought can also be a cause of an increase in dengue
epidemics, when household water storage increases thenumber of suitable mosquito breeding sites (Pontes etal., 2000; Depradine & Lovell, 2004; Guang et al.,2005). It has been reported that density maps of Aedes
aegypti based on temperature, rainfall, cloud cover are
consistent with the distribution of dengue fever (Hopp &Foley, 2003). The model of vector abundance has
demonstrated a good agreement with the distribution ofreported dengue cases in some areas of the world (Hopp& Foley, 2003).
2.2 Malaria
Malaria is considered to be the most important
vector-borne infectious disease in the world. There havebeen many reports which suggest climate change affects
malaria. Climate has had an influence on the distribution,
intensity of transmission and seasonality of malaria in
sub-Saharan Africa (Hay et al., 2002; Craig et al., 2004).
The El Niño Southern Oscillation (ENSO) phenomenon

Infectious Diseases and Climate Change

37

Fig. 2 Distributions of dengue epidemics worldwide. Red: areas where dengue epidemics have been reported.
Yellow: areas where presence of Aedes aegypti is confirmed. (from the Website of Center for Disease Control
and Prevention, U.S.A.)

has had an impact on the risk of malaria epidemics insouthern Asia and South America (Kovats et al., 2003).
Associations between interannual variability in temperature and malaria transmission were reported in Africa. It
has also been reported that the minimum temperature at
the start of the transmission season accounted for thevariability in malaria epidemics between years in
Madagascar (Bouma, 2003). The number of cases
admitted with malaria was associated with rainfall andhigh maximum temperatures 3-4 months previously in
Kenya (Githeko & Ndegwa, 2001). Malaria morbidity
data from the late 1980s to the early 1990s in Ethiopia
indicated that epidemics were associated with highminimum temperatures in the preceding months (Abeku
et al., 2003). On the other hand, there has been no clear
evidence that malaria has been affected by climatechange in South America (Confalonieri et al., 2007) orin the Russian Federation (Semenov et al., 2002).
Although many reports have indicated a relationshipbetween climate and malaria transmission dynamics, it
should be stressed that there is still much uncertainty
about the potential impact of climate change on malaria
at local and global levels (Confalonieri et al., 2007)
2.3 Japanese encephalitis (JE)
2.3.1 Epidemiology of JE in Japan
Japanese encephalitis (JE) is a serious viral encephalitis with a high mortality rate and a high percentage ofneuro-psychiatric sequelae. JE occurs endemically andin annual epidemics in many Asian countries (Oya &Kurane, 2007). Approximately 50,000 cases are reported
annually worldwide. The disease is caused by the bite ofJE virus-infected mosquitoes. JE is an especially important disease in East, Southeast and South Asia (Fig. 3).
The endemic regions have expanded recently to New

Guinea and northern Australia. JE virus is the only
mosquito-borne virus that is endemic and causes humandisease in Japan at this point.
JE virus is maintained in nature between vector
mosquitoes and domestic pigs in endemic regions. The
principal vector of JE virus is Culex tritaeniorhynchus
in most endemic areas of Asia, including Japan. C.
tritaeniorhynchus reproduces in rice paddies and theconnecting canals. Pigs are also considered an amplifier
for JE virus in the temperate zone. Thus, pigs are theamplifier as well as the natural host of JE virus in thetransmission cycle of JE virus in human residential areas.
In temperate areas, the vector mosquitoes start to be
detected in May, then seroconversion of pigs occurs andoccurrence of human cases follows.
It is understood that the number of JE patients is
affected by multiple factors; the activity and numbers of
JE virus-infected mosquitoes, location of pig farms,
immune status of humans, preventive measures against
mosquitoes, etc. Especially in countries like Japan
where JE vaccination has been strongly implemented
and most of the people have protective immunity against
JE virus, the threat of JE is not reflected by the numberof patients. Pigs are not immunized with JE vaccine
except for sows expected to give birth. Pigs are usually
killed to be shipped to market before six months of age
in Japan. Most pigs are born after the JE season is overin the previous year; thus, they are naïve to JE virus
before the current year’s epidemic season starts. Naïve
pigs are highly susceptible to JE virus and easily
infected with it by the bite of infected mosquitoes. Pigs
develop high and sustained levels of viremia after infection, and high levels of specific antibodies. These indicate that the seroconversion rate among sentinel seronegative pigs reflects the prevalence of JE virus in the

38

I. KURANE et al.

Fig. 3 Distribution of Japanese encephalitis (JE) worldwide.

area. In Japan, seroconversion rates of sentinel pigs havebeen checked in most prefectures every year. Seroconversion usually starts in May or June in Okinawa,
the southernmost prefecture, and in July in othersouthern prefectures. The sero-positive area gradually
moves up north. Seroconversion is detected in most
prefectures by the end of October. Thus, the sentinel pig
system is useful for estimating the JE risk in humans
and activity of JE virus-infected mosquitoes.
2.3.2 Effects of climate change on the
seroconversion rate to JE virus in pigs
JE surveillance was implemented in 1965 under the
National Epidemiological Surveillance of Vaccine
Preventable Diseases program by the Ministry of Healthand Welfare (currently the Ministry of Health, Labourand Welfare) in Japan (Arai et al., 2008). This surveillance includes (i) confirmation of notified JE cases, (ii)prevalence of JE antibodies among the general population, and (iii) seroconversion rates of sentinel pigs
nationwide. Seroconversion rates to JE virus among
sentinel pigs are assessed by measuring specific antibodies to JE virus approximately 2-3 times a monthfrom May or June to October. Seroconversion rates insentinel pigs of the year are shown for each participating
prefecture from 1972 to 1995 (Fig. 4). Although seroconversion rates differed year by year especially innorthern Japan, high levels of seroconvertion rates wereobserved every year in southern Japan.
For further analysis, the average percentages of seroconversion rates among sentinel pigs were calculated foreach participating prefecture in 1982, 1990, and1993-2000. Meteorological data at multiple sites in eachprefecture are available from the 1980s. The data of (1)average day temperature, (2) highest temperature of theday, (3) number of days with the highest temperature
being 30oC or higher and (4) average amount of rainfall,

were collected for 47 prefectures during three summer
months including July, August and September in 1982,
1990 and 1993-2000. The meteorological data obtainedat the same or closest sites to the pig farms or slaughterhouses were used for the analyses along with the final
seroconversion data in pigs.
The relationship between the seroconversion rate to
JE virus and categories of meteorological data during
the summer season were examined by linear regression
analysis. There were positive relationships between
seroconversion rates in pigs and each of three categoriesof meteorological data: the highest daytime temperature,
average temperature during the three months and thenumber of days with the highest day temperature being
30oC or higher. No significant positive relationship was
found between the seroconversion rate and average rainfall. These results indicate that in years when thetemperature is high during summer, seroconversion rates
in sentinel pigs are higher and high levels of seroconversion in sentinel pigs are observed even in prefectures
located in northern Japan. Thus, if global warming
continues, it is possible that the activity of JE virus, i.e.,
activity of JE virus-infected mosquitoes, will become
constantly high even in northern Japan, probably
including Hokkaido, the northernmost island. These
trends, however, will not directly increase the number of
JE patients if appropriate countermeasures are taken, i.e.,strong implementation of JE vaccination.
2.4 Other vector-borne infectious diseases
There is some evidence of climate-related shifts inthe distribution of tick vectors. Northern or altitudinal
shifts in tick distribution have been reported in Sweden
and Canada (Lindgren & Talleklint, 2000; Lindgren &Gustafson, 2001; Barker & Lindsay, 2000), and also
altitudinal shifts in the Czech Republic (Daniel et al.,2004). Geographical changes in tick-borne infections

Infectious Diseases and Climate Change

39

Year
(Reported No.
of JE cases）

1972
（22）

1973
（70）

1974
（6）

1975
（27）

1976
（13）

1977
（5）

1978
（88）

1979
（86）

1980
（40）

1981
（23）

1982
（21）

1983
（32）

1984
（27）

1985
（39）

1986
（26）

1987
（37）

1988
（32）

1989
（27）

1990
（54）

1991
（13）

1992
（2）

1993
（4）

1994
（4）

1995
（2）

1996
（4）

1997
（4）

1998
（2）

1999
（5）

2000
（7）

2001
（5）

2002
（8）

2003
（1）

2004
（5）

2005
（7）

Fig. 4 Seroconversion rates to Japanese encephalitis virus in sentinel pigs in each prefecture from 1972 to 2005. The numbers inparentheses indicate reported human JE cases. Red: 80%, yellow: 50%-80%, green: <50%, blue: no seroconversion, white: nottested. (Data from National Epidemiological Surveillance of Vaccine Preventable Diseases program, the Ministry of Health,Labour and Welfare, Japan)

were also observed in Denmark (Skarphedinsson et al.,2005). A severe outbreak of Murray Valley encephalitis
reportedly occurred after heavy rainfall and flooding insouthern Australia, and ENSO has been proposed as apredictive tool (Nicholls, 1986). Heavy rain or floods
can cause outbreaks of Ross River fever, due to increased breeding of mosquitoes (Mackenzie, J. et al.,2000)

3. Some Considerations to be Addressed
It is expected that research on the effects of climatechange on infectious diseases will become much more
active. There are some concerns to be addressed in thisresearch. The number of patients with infectious diseases can be affected by multiple factors. It is generally
agreed that infection with pathogens does not always
lead to disease. The asymptomatic infection rate is often
greater than the symptomatic one with many pathogens.
There are differences in virulence among strains in eachspecies of pathogen. Thus, the number of symptomatic
infections can vary depending on the level of virulenceof the dominant strains within each pathogen. Furthermore, changes in human disease can be modified bylevels of accuracy of surveillance and reporting systems,
disease control measures, the immune status of theaffected population, population changes and other factors such as changes in land-use and agricultural techniques (Kovats et al., 2001; Rogers & Randolph, 2006).
Thus, in the studies of the effects of climate change on

infectious diseases, multiple biological and sociologicalfactors should be taken into account.

4. Conclusions
It is expected that the levels of impacts of climatechange on infectious diseases will differ among regions,depending on their infrastructure. In Japan, we cannot
say that the impacts of global warming on infectious
diseases are apparent at this point yet. However, it isexpected that these impacts will appear in one form or
another if climate change/global warming continue toprogress in the future. Although studies of the effects ofclimate change on vector-borne infectious diseases havemade much progress in recent years, there is still a lackof evidence rather than an absence of effects (Kovats etal. 2001). At the present time as well, research on theimpacts of climate change/global warming on infectious
diseases and on future prospects should be conducted ina wide range of research fields.

Acknowledgements
This study was partially supported by a grant from
“Global Environment Research Fund” by Ministry of
the Environment, Japan.

40

I. KURANE et al.

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Ichiro KURANE
Ichiro KURANE is the Director of Department of Virology 1, National Institute of
Infectious Diseases. He obtained his M.D.
and Ph.D. degrees from the Tohoku University School of Medicine, Sendai, Japan.
His major scientific interests are hostdefense mechanisms against arthropodborne viruses, and the pathogenesis ofthese viral diseases; in particular, dengue
fever, dengue hemorrhagic fever, Japanese encephalitis and West Nile
encephalitis. He has recently expanded his research field, and has started
to study the effect of climate change on infectious diseases. He served as amember of a council organized by the Ministry of the Environment toelucidate the effects of global warming on human health. He is the Chairof the Japanese panel of the U.S.-Japan Cooperative Medical Science
Program.

(Received 19 June 2008, Accepted 1 July 2008)