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Tropical Medicine and International Health

doi:10.1111/j.1365-3156.2011.02734.x

volume 16 no 5 pp 598607 may 2011

Dengue transmission in the Asia-Pacific region: impact of


climate change and socio-environmental factors
Shahera Banu1, Wenbiao Hu2, Cameron Hurst1 and Shilu Tong1
1 School of Public Health, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Qld, Australia
2 School of Population Health, University of Queensland, Brisbane, Qld, Australia

Summary

objective To review the scientific evidence about the impact of climate change and socioenvironmental factors on dengue transmission, particularly in the Asia-Pacific region.
methods Search of the published literature on PubMed, ISI web of Knowledge and Google Scholar.
Articles were included if an association between climate or socio-environmental factors and dengue
transmission was assessed in any country of the Asia-Pacific region.
results Twenty-two studies met the inclusion criteria. The weight of the evidence indicates that global
climate change is likely to affect the seasonal and geographical distribution of dengue fever (DF) in the
Asia-Pacific region. However, empirical evidence linking DF to climate change is inconsistent across
geographical locations and absent in some countries where dengue is endemic.
conclusion Even though climate change may play an increasing role in the transmission of DF, no
clear evidence shows that such impact has already occurred. More research is needed across countries to
better understand the relationship between climate change and dengue transmission. Future research
should also consider and adjust for the influence of important socio-environmental factors in the
assessment of the climate change-related effects on dengue transmission.
keywords dengue transmission, climate change, socio-environmental factors, the Asia-Pacific

Introduction
Global climate is changing rapidly, due primarily to
anthropogenic greenhouse gas emissions (IPCC 2007).
Global mean temperature is projected to increase between
1.16.4 C by the end of this century relative to 1980
1999. There is growing evidence that climate change has
already affected and will increasingly impact on human
health (Epstein 2005; Haines et al. 2006; McMichael et al.
2006; Costello et al. 2009). The changes in global temperature, precipitation and humidity that are expected to
occur because of projected climate change will affect the
biology and ecology of vectors and consequently the risk of
vector-borne disease transmission (Gubler et al. 2001;
Tong et al. 2008; Shuman 2010). Dengue fever (DF) is the
most important arboviral disease in the world (Gubler
2002a; WHO 2006). About 2.5 billion people live in
endemic areas and an additional 120 million people travel
to affected areas every year. The annual number of dengue
infections is estimated to be 50100 million. Case fatality
rates vary between 0.5 and 3.5% in Asian countries
(Guzman & Kouri 2002; Halstead 2007; Suaya et al.
2009). Cases reported to the World Health Organization
598

(WHO) over the past four decades show an upward trend,


especially in urban areas (WHO 2006).
Climate variability, lack of effective vector control
programmes, uncontrolled urbanization and increased
international travel are suggested to be the important risk
factors for increased activity of dengue (Gubler 2002a;
Sutherst 2004). Temperature, rainfall and relative humidity
are thought as important climatic factors contributing
towards the growth and dispersion of the mosquito vector
and potential of dengue outbreaks (Patz et al. 2005).
Temperature is also capable of affecting pathogen replication, maturation and period of infectivity (Patz et al. 1998).
As global temperatures continue to increase, it has
predicted that the endemic range of DF will expand
geographically (Githeko et al. 2000; Hopp & Foley 2001;
Woodruff & McMichael 2004). Warmer temperatures will
also allow for increased reproduction and activity and
decreased incubation time of larvae, resulting in an
increased capacity for producing offspring. Thus, an
increase in the transmission potential and prevalence of DF
seems likely (Jetten & Focks 1997; Barbazan et al. 2010).
The increasing temperatures could also increase DF transmission by extending the season in which transmission

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Tropical Medicine and International Health

volume 16 no 5 pp 598607 may 2011

S. Banu et al. Dengue transmission in the Asia-Pacific region

occurs (Patz & Reisen 2001). Lengthy drought conditions


in endemic areas without a stable drinking water supply
may encourage the storage of drinking water, thereby
increasing the number of breeding sites for the mosquito
vector Aedes aegypti (Beebe et al. 2009). Conversely, high
rainfall will ensure that small artificial containers used as
larval mosquito habitat would remain flooded, thereby
expanding adult mosquito population (Patz et al. 1998).
Moreover, climate change associated with El Nino-Southern Oscillation (ENSO) may trigger outbreak of DF in
populated areas where the disease is endemic (Hales et al.
1999; Johansson et al. 2009b).
As climate change may have a significant impact on the
transmission and incidence of DF, it is essential to examine
the association between climatic variables and DF epidemic. Recently, a few studies have explored the impact of
climate variability and climate change on dengue transmission (Hales et al. 2002; Johansson et al. 2009a). Others
assessed the influence of socio-ecological factors on dengue
epidemics (McBride et al. 1998; Bohra & Andrianasolo
2001; Thammapalo et al. 2005a; Cummings et al. 2009;
Johansson et al. 2009b). However, the link between
dengue and climate change remains inconclusive because
the potential influence of socio-demographic factors on
dengue transmission has rarely been considered seriously in
previous research (Patz et al. 1998; Reiter 2001; Semenza
& Menne 2009). In this paper, we review the reported

Methods
A literature search using PubMed, ISI Web of Knowledge
and Google scholar was conducted in December 2009.
Keywords such as Dengue, Dengue fever, Dengue
hemorrhagic fever, climate change*, climate variability,
climate model*, Risk factors and socio-environmental
factors were used in different combinations to identify
potential articles and references. Search terms included
MeSH terms and free text terms. Limits were set for
language (English) and publication year (19902009). In
Google Scholar, we limited our search by subject (Biology,
Life Science and Environmental science) as it gives huge
number of irrelevant references. However, we searched all
fields for PubMed and Web of Science. Table 1 shows the
search results from each database. The initial search
generated 1931 references including duplicates. All titles
and 466 abstracts were reviewed to identify potential
epidemiological studies. Then, 290 full-text articles were
retrieved based on abstracts reviewed and critically analysed by the first author.

Search terms

PubMed

ISI web of
knowledge

# 1 (Dengue OR Dengue
fever OR Dengue
Hemorrhagic fever)
AND (climate change*
OR climate variability
OR climate model*)
# 2 (Dengue OR Dengue
fever OR Dengue
Hemorrhagic fever)
AND (Risk factors OR
Socio-environmental
factors)
#1 AND #2 (Dengue OR
Dengue fever OR
Dengue Hemorrhagic
fever) AND (climate
change* OR climate
variability OR climate
model*) AND (Risk
factors OR
Socio-environmental factors)
Total (including duplicates)

310

134

167

611

325

216

584

1125

47

19

129

195

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Google
Scholar

effects of climate change and other socio-environmental


factors on dengue transmission in the Asia-Pacific region to
draw attention to the methodological challenges in this
area. Additionally, we provided recommendations for
future research directions.

Total (including
duplicates)

Table 1 Search strategy

1931

599

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volume 16 no 5 pp 598607 may 2011

S. Banu et al. Dengue transmission in the Asia-Pacific region

Inclusion criteria
Articles were included in the review if they (i) evaluated the
effects of climate variability or the influence of other socioenvironmental factors on dengue transmission (ii) conducted in countries of the Asia-Pacific region and (iii) used
an epidemiological study design. Only studies conducted in
the Asia-Pacific region were included because many countries of this region are prone to dengue transmission but no
systematic review has focused on this region in the
literature yet. Epidemiological study designs included time
series analysis, spatial or spatio-temporal analysis and

descriptive study which applied to identify the influence of


climate variables (temperature, humidity, precipitation,
wind speed and El Nino events) and socio-environmental
factors (population density, urbanization, housing, family
income, transport and vector control) on dengue transmission. Figure 1 illustrates article inclusion process.
Results
Of 290 full-text articles, 22 articles met the inclusion criteria
and the major findings of these studies were reviewed and
summarized in Tables 2 and 3. All articles included in this

1931 references were found after searching PubMed, ISI


Web of knowledge and Google scholar databases

1465 references rejected (studies describing


virological or serological features of dengue and
treatment or vaccine development)

466 abstracts were read and 290 full text articles were
retrieved

Inclusion criteria used were:

From the Asia-Pacific region


Reports association between dengue and
climatic or non-climatic factors
Observational study design
Published in English

268 articles rejected due to irrelevant research


question and inappropriate study design

22 articles found potentially relevant


18 modelled climatic factors
4 modelled environmental factors except climate
variables

600

Figure 1 Flow diagram of article selection


process.

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Tropical Medicine and International Health

volume 16 no 5 pp 598607 may 2011

S. Banu et al. Dengue transmission in the Asia-Pacific region

Table 2 Characteristics of studies on the association between climatic variables and dengue transmission
Study

Location
(study period)

Statistical
method

Johansson et al.
2009a

Thailand
(19831996)

Risk factors

Major findings

Wavelet analysis

ENSO
Precipitation &
temperature

Tipayamongkholgul Thailand
et al. 2009
(19962005)

Poisson regression

ENSO
Temperature
Relative humidity
Wind speed

Cazelles et al. 2005 Thailand


(19831997)

Wavelet analysis

ENSO

Nakhapakorn &
Tripathi 2005

Thailand
(19972001)

Multiple regression Rainfall


Temperature
Humidity
Land use

Thammapalo
et al. 2005b

Thailand
(19781997)

Linear least square Monthly total


regression
rainfall
Rain days
Daily temperature
Daily relative
humidity

Nagao et al. 2003

Thailand
(19921996)

Multiple regression Temperature,


Rainfall
Water wells
Tin houses

Hsieh &
Chen 2009

Taiwan
(2007)

Richards model
Distributed lag
model

Typhoon
Temperature
Precipitation

Wu et al. 2007

Taiwan
(19982003)

ARIMA model

Temperature
Rainfall
Relative humidity
Vector density

The direct relationship


Further research is
between ENSO and
needed to explain the
dengue was non-stationary non-stationarity in ENSO
and ENSO appeared to be and dengue incidence
associated with local tem
perature and precipitation
The effects of El Nino on Only southern coastal and
dengue transmission were northern inland regions
varied according to
were included
geographical location
within Thailand
The dynamics of El Nino The magnitude of the
were strongly associated
El Nino and dengue
with dengue incidence but relationship needs
non-stationary existed in to be viewed within a
this relation which might wider context of
influenced by the
socio-environmental
synchrony of previous
variability
dengue epidemic
Built-up area had highest Only one province was
risk of dengue incidence
included
and temperature, rainfall
and humidity were likely
to be key determinants of
DF
Increased temperature was Spatial variation was not
positively associated with examined
dengue incidence in
central and northern parts
of Thailand where in
creased rainfall was
negatively associated in
southern Thailand
Larval abundance of Aedes Only 18 province of
mosquito was positively
Northern Thailand were
associated with house
included
conditions, water supply
and transport services. In
creased rainfall in 2
months earlier and
temperature were also
correlated with larval
indices
The multiwave dengue
Further research is required
outbreak in Taiwan in
to explore the relationship
2007 was appeared to be between extreme weather
influenced by rainfall and events and dengue
temperature variation as a transmission
consequence of two
consecutive typhoons
The incidence of DF was Only one metropolitan city
negatively associated with was included
monthly temperature
variation and reversely
with relative humidity at
lags of 2 months

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Comments

601

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S. Banu et al. Dengue transmission in the Asia-Pacific region

Table 2 (Continued)
Location
(study period)

Statistical
method

Wu et al. 2009

Taiwan
(19982002)

Spatial analysis
Logistic regression

Halide &
Ridd 2008

Indonesia
(19982005)

Multiple regression

Arcari et al.
2007

Indonesia
(19922001)

Multiple regression

Study

Risk factors

Major findings

Comments

Temperature
Rainfall
Level of
urbanization
Percentage of elder
population
Temperature
Relative humidity
Rainfall

Number of warm months


and degree of urbanization
were found to be
associated with increasing
risk of DF incidence at
township level
Relative humidity at
34 months lags and
current number of dengue
cases appeared to be major
determinants for
prediction of DF outbreak
in Indonesia
Rainfall and temperature
observed as important
predictor of DF transmission in Indonesia, al
though the association
differed across geographical region of the country
ENSO driven increased
temperature exhibited
greater impact on dengue
transmission by the vector
population
Temperature, rainfall and
relative humidity were
major determinants for
dengue transmission and
outbreak coincided in
post-monsoon period
Increase minimum
temperature and decreased
wind velocity were
associated with increase
dengue incidence
Dengue incidence seemed to
have no relationship with
climatic factors. However,
negatively associated with
vector control
Weekly mean temperature
and total precipitation
were related to increased
dengue incidence
Decreased mean of SOI at
lags of 312 months
earlier was inversely asso
ciated with dengue
incidence in Queensland
Monthly mean minimum
temperature was the major
contributor for dengue
outbreak in Townsville

Both climatic variables and


socio-demographic factors
were considered

Temperature
Rainfall
Relative humidity
SOI

Bangs et al.2006 Indonesia


Descriptive analysis Temperature
(1997 & 1998)
Relative humidity
Rainfall, ENSO
House index
Chakravarti &
Kumaria 2005

India (2003)

Descriptive analysis Temperature


Rainfall
Relative humidity

Lu et al. 2009

China
(20012006)

Poisson regression

Yang et al. 2009 China


(July October
2004)

Temperature,
rainfall
Relative humidity
Wind velocity

Descriptive analysis Temperature,


precipitation
Humidity
Breteau index
House index
Poisson regression
Temperature
Precipitation

Hii et al. 2009

Singapore
(20002007)

Hu et al. 2010

Australia (1993 SARIMA model


2005)

ENSO

Bi et al. 2001

Australia
(19901994)

Temperature
Precipitation
Relative humidity

ARIMA model

Only one city was included

Socio-environmental
factors were not included

Only one city was included

Only one outbreak in one


city was considered

Only one province was


included

Non-endemic nature of DF
in Cixi city may biased the
relationship between
climate variables and DF
Socio-environmental
factors were not included

Only SOI was considered

Only 4 years dataset used

Arranged by location of study.


ENSO, El Nino-Southern Oscillation Index; ARIMA, autoregressive integrated moving average; SARIMA, seasonal autoregressive
integrated moving average; SOI, Southern Oscillation Index; DF, dengue fever.

602

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S. Banu et al. Dengue transmission in the Asia-Pacific region

Table 3 Characteristics of studies on the association between Socio-environmental factors and Dengue transmission

Study

Location
(study period) Statistical method

Cummings
et al. 2009

Thailand
Linear regression
(19802005) Wavelet analysis

Both socio-demographic
and climatic factors
were considered

Thammapalo
et al. 2005a

Thailand
(1999)

A complex relationship
was revealed between
Aedes larval
abundance and socioenvironmental factors

McBride
et al. 1998

Australia
(1993)

India
Bohra &
Andrianasolo (1990)
2001

Risk factors

Major findings

Population data (age, birth Changes in the birth rate


rate, death rate, household and death rate in
size, education level,
Thailand can explain
sanitation)
the changes in the age
Climatic data (rainfall)
distribution of dengue
cases and its periodicity
Logistic regression Housing style
Housing style, window
Window screen
screen and ethnicity
Ethnicity
seemed to affect the
Education level
presence of Aedes
Occupation
mosquito larva in the
Age, gender
house
Logistic regression House hold cases, neighViral serotypes, vector
populations, unscreened
bour cases
houses and hard
Window screen
immunity emerged as
Travel history
important risk factors
Mosquito control
Presence of water tank
for dengue increased
dengue incidence in
Charter Tower in 1993
Spatial analysis
Uncovered water container Housing pattern,
Multiple regression Presence of solid waste
mosquito control
Mosquito control
facility, presence of solid
Housing pattern
waste and uncovered
Water supply
water container were
most important sociocultural risk factors for
dengue transmission

Comments

Climatic factors were


not included

Climatic factors were


not considered.

Arranged by location of study.

review were published between 1998 and 2010. Eight


studies from Thailand, three each from Australia, Taiwan
and Indonesia, two each from China and India and one from
Singapore. There was no study conducted in some countries
of the Asia-Pacific region where dengue is endemic, such as,
Bangladesh, Sri Lanka, and Myanmar.
Association between climatic factors and DF
Of the 22 published studies, 18 evaluated the relationship
between climatic variables and dengue incidence (Bi et al.
2001; Nagao et al. 2003; Cazelles et al. 2005; Chakravarti
& Kumaria 2005; Nakhapakorn & Tripathi 2005;
Thammapalo et al. 2005b; Bangs et al. 2006; Arcari et al.
2007; Wu et al. 2007, 2009; Halide & Ridd 2008; Hii
et al. 2009; Hsieh & Chen 2009; Johansson et al. 2009a;
Lu et al. 2009; Tipayamongkholgul et al. 2009; Yang et al.
2009; Hu et al. 2010). Among them, only three studies
considered both climatic and social factors (Nagao et al.
2003; Nakhapakorn & Tripathi 2005; Wu et al. 2009).
The main outcome variables assessed in these studies were

2011 Blackwell Publishing Ltd

the number of dengue cases and mosquito density


(Breteau index, house index and container index). Most
studies collected data on temperature, amount of precipitation and relative humidity as climatic variables (Cazelles
et al. 2005; Nakhapakorn & Tripathi 2005; Thammapalo
et al. 2005b; Wu et al. 2007). Several used ENSO as an
independent variable (Cazelles et al. 2005; Johansson et al.
2009a; Tipayamongkholgul et al. 2009). Only one study
assessed the influence of extreme weather event (Typhoon)
on DF (Hsieh & Chen 2009).
Different methods were used to evaluate the association
between climatic variables and dengue incidence or mosquito density. Of the 18 studies reviewed, two used spatial
analyses (Nakhapakorn & Tripathi 2005; Wu et al. 2009),
13 time series analyses (Bi et al. 2001; Nagao et al. 2003;
Cazelles et al. 2005; Thammapalo et al. 2005b; Arcari
et al. 2007; Wu et al. 2007; Halide & Ridd 2008; Hii et al.
2009; Hsieh & Chen 2009; Johansson et al. 2009a; Lu
et al. 2009; Tipayamongkholgul et al. 2009; Hu et al.
2010) and three descriptive analyses (Chakravarti &
Kumaria 2005; Bangs et al. 2006; Yang et al. 2009).
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S. Banu et al. Dengue transmission in the Asia-Pacific region

Various multiple regressions analyses like logistic regression and Poisson regression were mostly used to analyse
and predict DF transmission. These time series regression
analyses provide a way to establish the relationship
between changes of weather parameters, environmental
factors and the occurrence of dengue cases which might be
used for forecasting future dengue outbreak based on
model scenarios (Wu et al. 2007). Both classical autoregressive integrated moving average (ARIMA) model and
seasonal ARIMA model were also applied to link between
weather variation and dengue (Bi et al. 2001; Wu et al.
2007; Hu et al. 2010). Spatial analysis of dengue occurrence was used to identify the high-risk area for dengue
outbreaks (Wu et al. 2009). However, none of the previous
studies included both spatial and temporal data into their
models. The identification of high-risk areas through
spatio-temporal modelling may assist existing surveillance
and control efforts by permitting limited resources in areas
where dengue outbreaks are most likely to occur.
An association between climatic factors and dengue
incidence or mosquito density was reported in most studies
(Bi et al. 2001; Nagao et al. 2003; Cazelles et al. 2005;
Chakravarti & Kumaria 2005; Nakhapakorn & Tripathi
2005; Thammapalo et al. 2005b; Bangs et al. 2006; Arcari
et al. 2007; Wu et al. 2007; Halide & Ridd 2008; Hii et al.
2009; Hsieh & Chen 2009; Johansson et al. 2009a;
Lu et al. 2009; Tipayamongkholgul et al. 2009; Hu et al.
2010). However, the direction and intensity of this
association varied by time and location (Thammapalo
et al. 2005b; Arcari et al. 2007; Tipayamongkholgul et al.
2009). Temperature, rainfall and relative humidity were
often major determinants of dengue transmission. There
was no association between dengue incidence and climate
variability in Cixi, China, which might be attributed to the
non-endemic nature of DF in Cixi and the short study
period (4 months) (Yang et al. 2009).
Several non-climatic factors, such as, urbanization, land
use, vector-control programme, human movement, housing quality and population immunity, were identified as
potential confounders for assessing the climate-dengue
relationship. Only 1 of 18 studies reviewed was adjusted
for socio-environmental factors (Nagao et al. 2003),
apparently because the lack of relevant datasets makes it
difficult to control these variables (Bi et al. 2001; Arcari
et al. 2007; Wu et al. 2007).
Most studies examining the temperature influence on
dengue transmission or mosquito density reported a
positive association (Bi et al. 2001; Nagao et al. 2003;
Thammapalo et al. 2005b; Arcari et al. 2007; Hii et al.
2009; Lu et al. 2009; Wu et al. 2009). Higher temperature
favours virus replication, vector proliferation and feeding
frequency of mosquito (Jetten & Focks 1997; Patz et al.
604

1998). Therefore, rising temperature may enhance dengue


transmission. However, the impact of increased temperature on dengue outbreak was not immediate. Various lag
times were reported for this relationship, ranging from 4 to
16 weeks (Bi et al. 2001; Arcari et al. 2007; Wu et al.
2007; Hsieh & Chen 2009; Lu et al. 2009; Hu et al. 2010).
Bi et al. 2001 found that monthly mean minimum
temperatures impacted on the transmission of DF through
a 4-month lagged period which includes the period of
replication and development of mosquito, the extrinsic
incubation period (time of replication of virus within
vector) and intrinsic incubation period of the virus (time of
virus replication within the host)(Bi et al. 2001). Therefore, observed lags were biologically plausible.
Associations between rainfall and dengue transmission
are inconsistent across geographical locations. Dengue
outbreaks were usually coincided with wet season and
positive associations between dengue incidence and precipitation were reported in many countries of the AsiaPacific region (Nagao et al. 2003; Nakhapakorn &
Tripathi 2005; Arcari et al. 2007). Rainfall may increase
the breeding sites of Aedes mosquito and therefore increase
dengue transmission. However, excess rainfall was found
negatively associated with dengue incidence in Thailand,
Indonesia and Taiwan (Thammapalo et al. 2005b; Halide
& Ridd 2008; Wu et al. 2009). The plausible explanation
might be the mosquito larvae washed away by heavy
rainfall (Thammapalo et al. 2005b; Arcari et al. 2007).
The ENSO is a periodic variation in the atmospheric
conditions and ocean surface temperatures of the tropical
Pacific and hypothesized to have influence on multiyear
variation in dengue incidence (Johansson et al. 2009a).
Among the studies reviewed, four examined the impact of
ENSO on the synchrony of dengue epidemics in Thailand
and Australia (Cazelles et al. 2005; Johansson et al. 2009a;
Tipayamongkholgul et al. 2009; Hu et al. 2010). They
reported a significant but non-stationary influence of
ENSO on dengue transmission (Cazelles et al. 2005;
Johansson et al. 2009a; Tipayamongkholgul et al. 2009;
Hu et al. 2010). Spatial heterogeneity and various lag
effects were also apparent in this relation (Tipayamongkholgul et al. 2009; Hu et al. 2010). In Thailand, ENSO
was associated with local temperature and precipitation
changes. It was suggested that decreased ENSO could
result in increased temperature and decreased rainfall
leading to increased water storage, increased mosquito
breeding sites and therefore, increased dengue transmission
(Johansson et al. 2009a). Moreover, further research is
necessary to explain the non-stationarity and spatial
variation in the ENSOdengue relationship to effectively
support the hypothesis of inter annual variation in dengue
transmission.

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Association between socio-environmental factors and DF


Four studies have examined the impact of socio-environmental factors on dengue incidence in the Asia-Pacific
region (Table 2) (McBride et al. 1998; Bohra & Andrianasolo 2001; Thammapalo et al. 2005a; Cummings et al.
2009). The increasing trends in population growth,
uncontrolled urbanization, spread of mosquito vector and
movement of virus through international travel were
suggested to be the major contributing factors for the
recent dengue expansion in endemic areas (Gubler et al.
2001; Campbell-Lendrum & Reithinger 2002; Kyle &
Harris 2008). Influences of different socio-environmental
factors on dengue transmission were illustrated in this part
of the paper from a global perspective as very little
evidence is available from the Asia-Pacific region.
Socio-economic condition.
Dengue transmission might be influenced by peoples socioeconomic status (Gubler et al. 2001; Reiter et al. 2003).
People in developed countries usually live in better houses
with glazed windows, piped water, insect screening and
air-conditioning than those in developing countries (Reiter
2001). These facilities may effectively reduce their contacts
with vector mosquitoes and even if infected mosquitoes
gain entry to these buildings, the low ambient temperature
and artificially dry atmosphere may decrease their survival
rate and reduce the risk of transmission (Reiter 2001).
Besides these, many activities, particularly social gatherings
which occur in outdoor situations such as balconies,
courtyards and outdoor restaurants, might facilitate contact with vector (Gubler et al. 2001; Reiter 2001). It has
been suggested that the large difference in disease incidence
between United States and Mexico Border States is
probably caused by differences in living standards and
human behaviours (Gubler et al. 2001).
A spatial analysis of dengue in Thailand reported that
the risk of DF was quite geographically homogenous and
associated with housing types and poor garbage disposal
(Thammapalo et al. 2007). Housing style was strongly
related to the number of water jars and discarded items.
Town houses and slum houses in Phuket had relatively
fewer discarded wet containers than single houses on
rubber plantations. Therefore, single houses had a 315
times higher risk of dengue, because these dwelling types
have sufficient open space where discarded items could be
easily filled with rain water which can create mosquito
breeding sites (Thammapalo et al. 2005a).
International travel.
International trade and transports were suggested to have
potential influence on the geographical distribution of

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vectors and pathogen (Gubler et al. 2001; Reiter 2001;


Sutherst 2004). Commercial shipping might be linked to
the spread of both A. aegypti and Aedes albopictus
between regions (Romi et al. 1997). For example, after the
introduction of used tires, an American species of A. albopictus has established in Italy (Romi et al. 1997). In
addition, air-travel has greatly increased the dissemination
of dengue viruses via rapid transit of viraemic individuals
around the world (Kyle & Harris 2008). As a result, the
worldwide movement of dengue virus has been greatly
facilitated by air travel (Reiter 2001). Introduction of new
dengue viruses by travellers was one of the important
factors for causing hyper-endemicity in Puerto Rico and
increased severity of the disease (Gubler & Trent 1993;
Gubler et al. 2001).
Public health intervention.
The health risk arising from climate change may differ
between countries depending on the quality of public
health infrastructures (Githeko et al. 2000). In Canada and
USA, good surveillance and vector control programmes
limited the endemic transmission of DF, whereas in Mexico
and other less developed countries the health infrastructures are still ineffective (Githeko et al. 2000). The
majority of dengue endemic countries in Asia do not have
laboratory based active surveillance system that can
provide accurate early warning for epidemic DF (Gubler
2002b). In the pacific, only Australia, Tahiti and New
Caledonia have good laboratory surveillance (Gubler
2002b). Recently, there have been considerable improvements in surveillance and vector control in Australia
(Ritchie et al. 2002). Therefore, it seems unlikely that DF
will become re-established as an endemic disease in
Australia (McMichael 2003).
Conclusion
The review indicates that global climate change is likely to
affect the seasonal and geographical distribution of DF in
the Asia-Pacific region. The complex nature of the dengue
transmission which involves vector ecology, viral factors,
population immunity and socio-demographic changes
makes it difficult to quantify how climate change affects
dengue transmission. However, the impact of socio-environmental changes on dengue transmission is less well
studied. Therefore, relative importance and interaction
between socio-environmental and climatic factors remain
to be elucidated and need further exploration. Biological
judgement and caution are also necessary in interpreting a
direct relationship between climatic factors or non-climatic
factors and dengue transmission. We hope this review
inspires further work to elucidate the relative importance
605

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S. Banu et al. Dengue transmission in the Asia-Pacific region

and interaction between climatic or non-climatic factors in


the transmission of dengue.
There is the lack of data in many countries where dengue
is endemic. To demonstrate the regional variation in the
climate-dengue relationship, a multidisciplinary approach
incorporating region-specific predicted climate changes and
non-climatic factors could help to identify consistencies in
interactions between dengue and certain climatic and nonclimatic factors. Thus, a more sophisticated multivariable
predictive model may be constructed for control and
prevention of DF. Furthermore, multicentre or multicountry studies using both climatic and socio-environmental
data could help to reveal the potential impact of climate
change on dengue transmission in the Asia-Pacific region.
References
Arcari P, Tapper N & Pfueller S (2007) Regional variability in
relationships between climate and dengue DHF in Indonesia.
Singapore Journal of Tropical Geography 28, 251272.
Bangs MJ, Larasati RP, Corwin AL, Wuryadi S & Jakarta I (2006)
Climatic factors associated with epidemic dengue in Palembang,
Indonesia: implications of short-term meteorological events on
virus transmission. Southeast Asian Journal of Tropical Medicine and Public Health 37, 11031116.
Barbazan P, Guiserix M, Boonyuan W, Tuntaprasart W, Pontier D
& Gonzalez JP (2010) Modelling the effect of temperature on
transmission of dengue. Medical and Veterinary Entomology
24, 6673.
Beebe NW, Cooper RD, Mottram P & Sweeney AW (2009)
Australias dengue risk driven by human adaptation to climate
change. PLoS Neglected Tropical Diseases 3, e429. DOI:
10.1371/journal.pntd.0000429.
Bi P, Tong S, Donald K, Parton KA & Hobbs J (2001) Climate
variability and the dengue outbreak in Townsville, Queensland,
199293. Enviornmental Health 1, 5460.
Bohra A & Andrianasolo H (2001) Application of GIS in modeling
of dengue risk based on sociocultural data: case of Jalore,
Rajasthan, India. Dengue Bulletin 25, 92102.
Campbell-Lendrum D & Reithinger R (2002) Dengue and climate
change. Trends in Parasitology 18, 524.
Cazelles B, Chavez M, McMichael AJ & Hales S (2005) Nonstationary influence of EI Nino on the synchronous dengue epidemics in Thailand. PLoS Medicine 2, 313318.
Chakravarti A & Kumaria R (2005) Eco-epidemiological
analysis of dengue infection during an outbreak of dengue
fever, India. Virology Journal 2, 32. DOI: 10.1186/1743-422X2-32.
Costello A, Abbas M, Allen A et al. (2009) Managing the
health effects of climate change: Lancet and University College
London Institute for Global Health Commission. Lancet 373,
16931733.
Cummings DAT, Iamsirithaworn S, Lessler JT et al. (2009) The
impact of the demographic transition on dengue in Thailand:

606

insights from a statistical analysis and mathematical modeling.


PLoS Medicine 6, e1000139.
Epstein PR (2005) Climate change and human health. New England Journal of Medicine 353, 14331436.
Githeko AK, Lindsay SW, Confalonieri UE & Patz JA (2000)
Climate change and vector-borne diseases: a regional analysis.
Bulletin of the World Health Organization 78, 11361147.
Gubler DJ (2002a) Epidemic dengue dengue hemorrhagic fever
as a public health, social and economic problem in the 21st
century. Trends in Microbiology 10, 100103.
Gubler DJ (2002b) How effectively is epidemiological surveillance
used for dengue programme planning and epidemic response?
Dengue Bulletin 26, 96106.
Gubler DJ & Trent DW (1993) Emergence of epidemic dengue dengue hemorrhagic fever as a public health problem in the
Americas. Infectious Agents and Disease 2, 383393.
Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R & Patz JA (2001)
Climate variability and change in the United States: potential
impacts on vector- and rodent-borne diseases. Environmental
Health Perspectives 109(Suppl. 2), 223233.
Guzman MG & Kouri G (2002) Dengue: an update. Lancet
Infectious diseases 2, 3342.
Haines A, Kovats RS, Campbell-Lendrum D & Corvalan C (2006)
Climate change and human health: impacts, vulnerability, and
mitigation. Lancet 367, 21012109.
Hales S, Weinstein P, Souares Y & Woodward A (1999) El Nino
and the dynamics of vectorborne disease transmission. Environmental Health Perspectives 107, 99102.
Hales S, de Wet N, Maindonald J & Woodward A (2002)
Potential effect of population and climate changes on global
distribution of dengue fever: an empirical model. Lancet 360,
830834.
Halide H & Ridd P (2008) A predictive model for dengue hemorrhagic fever epidemics. International Journal of Environmental Health Research 18, 253265.
Halstead SB (2007) Dengue. The Lancet 370, 16441652.
Hii YL, Rocklov J, Ng N, Tang CS, Pang FY & Sauerborn R
(2009) Climate variability and increase in intensity and magnitude of dengue incidence in Singapore. Global Health Action 2.
doi: 10.3402/gha.v2i0.2036.
Hopp MJ & Foley JA (2001) Global-scale relationships between
climate and the dengue fever vector, Aedes aegypti. Climatic
Change 48, 441463.
Hsieh YH & Chen CWS (2009) Turning points, reproduction
number and impact of climatological events for multi-wave
dengue outbreaks. Tropical Medicine and International Health
14, 628638.
Hu W, Clements A, Williams G & Tong S (2010) Dengue fever
and El Nino Southern Oscillation in Queensland, Australia: a
time series predictive model. Occupational and Environmental
Medicine 67, 307311.
IPCC (2007) Climate Change 2007: The Physical Science Basis:
Contribution of Working Group I to the Fourth Assessment
Report of the Intergovernmental Panel on Climate Change.
Cambridge University Press, Cambridge, United Kingdom and
New York, NY, USA.

2011 Blackwell Publishing Ltd

Tropical Medicine and International Health

volume 16 no 5 pp 598607 may 2011

S. Banu et al. Dengue transmission in the Asia-Pacific region

Jetten TH & Focks DA (1997) Potential changes in the distribution


of dengue transmission under climate warming. American
journal of tropical medicine and hygiene 57, 285297.
Johansson MA, Cummings DAT & Glass GE (2009a) Multiyear
climate variability and dengue El Nino southern oscillation,
weather, and dengue incidence in Puerto Rico, Mexico, and
Thailand: a longitudinal data analysis. PLoS Medicine 6,
e1000168.
Johansson MA, Dominici F & Glass GE (2009b) Local and global
effects of climate on dengue transmission in Puerto Rico. PLoS
Neglected Tropical Diseases 3, e382.
Kyle JL & Harris E (2008) Global spread and persistence of
dengue. Annual Review of Microbiology 62, 7192.
Lu L, Lin H, Tian L, Yang W, Sun J & Liu Q (2009) Time series
analysis of dengue fever and weather in Guangzhou, China.
BMC Public Health 9, 395. DOI: 10.1186/1471-2458-9-395.
McBride WJ, Mullner H, Muller R, Labrooy J & Wronski I (1998)
Determinants of dengue 2 infection among residents of Charters
Towers, Queensland, Australia. American Journal of Epidemiology 148, 11111116.
McMichael AJ (2003) Global climate change: will it affect
vector-borne infectious diseases? Internal Medicine Journal
33, 554.
McMichael AJ, Woodruff RE & Hales S (2006) Climate change
and human health: present and future risks. Lancet 367,
859869.
Nagao Y, Thavara U, Chitnumsup P, Tawatsin A, Chansang C &
Campbell-Lendrum D (2003) Climatic and social risk factors for
Aedes infestation in rural Thailand. Tropical Medicine and
International Health 8, 650659.
Nakhapakorn K & Tripathi NK (2005) An information value
based analysis of physical and climatic factors affecting dengue
fever and dengue haemorrhagic fever incidence. International
Journal of Health Geographics 4, 13. DOI: 10.1186/1476072X-4-13.
Patz JA & Reisen WK (2001) Immunology, climate change and
vector-borne diseases. Trends In Immunology 22, 171172.
Patz JA, Martens WJM, Focks DA & Jetten TH (1998) Dengue
fever epidemic potential as projected by general circulation
models of global climate change. Environmental Health
Perspectives 106, 147153.
Patz JA, Campbell-Lendrum D, Holloway T & Foley JA (2005)
Impact of regional climate change on human health. Nature
438, 310317.
Reiter P (2001) Climate change and mosquito-borne disease.
Environmental Health Perspectives 109, 141161.
Reiter P, Lathrop S, Bunning M et al. (2003) Texas lifestyle limits
transmission of dengue virus. Emerging Infectious Diseases 9,
8689.
Ritchie SA, Hanna JN, Hills SL et al. (2002) Dengue control in
north Queensland, Australia: case recognition and selective
indoor residual spraying. Dengue Bulletin 26, 713.

Romi R, Sabatinelli G, Savelli LG, Raris M, Zago M & Malatesta


R (1997) Identification of a North American mosquito species,
Aedes atropalpus (Diptera: Culicidae), in Italy. Journal of the
American Mosquito Control Association 13, 245246.
Semenza JC & Menne B (2009) Climate change and infectious
diseases in Europe. Lancet Infectious diseases 9, 365375.
Shuman EK (2010) Global climate change and infectious diseases.
New England Journal of Medicine 362, 10611063.
Suaya JA, Shepard DS, Siqueira JB et al. (2009) Cost of dengue
cases in eight countries in the Americas and Asia: a prospective
study. American Journal of Tropical Medicine and Hygiene 80,
846855.
Sutherst RW (2004) Global change and human vulnerability to
vector-borne diseases. Clinical Microbiology Reviews 17,
136173.
Thammapalo S, Chongsuwiwatwong V, Geater A, Lim A &
Choomalee K (2005a) Socio-demographic and environmental
factors associated with Aedes breeding places in Phuket, Thailand. Southeast Asian Journal of Tropical Medicine and Public
Health 36, 426433.
Thammapalo S, Chongsuwiwatwong V, McNeil D & Geater A
(2005b) The climatic factors influencing the occurence of dengue hemorrhagic fever in Thailand. Southeast Asian Journal of
Tropical Medicine and Public Health 36, 191196.
Thammapalo S, Chongsuvivatong V, Geater A & Dueravee M
(2007) Environmental factors and incidence of dengue fever and
dengue haemorrhagic fever in an urban area, Southern Thailand.
Epidemiology and Infection 136, 135143.
Tipayamongkholgul M, Fang CT, Klinchan S, Liu CM & King
CC (2009) Effects of the El Nino-Southern Oscillation on
dengue epidemics in Thailand, 19962005. BMC Public Health
9, 422. DOI: 10.1186/1471-2458-9-422.
Tong S, Dale P, Nicholls N, Mackenzie JS, Wolff R & McMichael
AJ (2008) Climate variability, social and environmental factors,
and Ross River virus transmission: research development and
future research needs. Environmental Health Perspectives 116,
15911597.
WHO (2006) Scientific Working Group Report on Dengue.
WHO, Geneva, Switzerland.
Woodruff RE & McMichael T (2004) Climate change and human
health: all affected bit some more than others. Social Alternatives 23, 1722.
Wu PC, Guo HR, Lung SC, Lin CY & Su HJ (2007) Weather as an
effective predictor for occurrence of dengue fever in Taiwan.
Acta Tropica 103, 5057.
Wu PC, Lay JG, Guo HR, Lin CY, Lung SC & Su HJ (2009)
Higher temperature and urbanization affect the spatial patterns
of dengue fever transmission in subtropical Taiwan. Science of
the Total Environment 407, 22242233.
Yang T, Lu L, Fu G et al. (2009) Epidemiology and vector efficiency
during a dengue fever outbreak in Cixi, Zhejiang Province, China.
Journal of Vector Ecology 34, 148154.

Corresponding Author Shilu Tong, School of Public Health, Institute of Health and Biomedical Innovation, Queensland University of
Technology, Kelvin Grove, Qld-4059, Australia. Tel.: +61 7 3138 9745; Fax: +61 7 3138 3369; E-mail: s.tong@qut.edu.au

2011 Blackwell Publishing Ltd

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