Introduction

The Intergovernmental Panel on Climate Change (IPCC) has reported the existence of abundant evidence of climate change on a global scale [1]. According to the IPCC’s fourth assessment in 2007, global average surface temperature will increase by 1.1-6.4°C by 2100, 2-9 times more than globally averaged warming during last century [1]. Furthermore, the frequency and extent of extreme weather events; such as heat waves, bushfires, floods, and cyclones, can be highly impacted by the changing climate. Anthropogenic climate change has also been identified as an important risk factor for population health [2], including transmission of infectious diseases, and most importantly suspected impacts distribution and occurrence of vector borne diseases [1]. Despite the ongoing debate over the influence climate factors have on mosquito-borne disease occurrence, it is widely assumed that distribution and occurrence of these diseases, such as malaria, are determined by climate and that global warming trends will lead to higher incidence and wider geographic range [3–10]. In contrast, some studies hold that the current evidence is insufficient to clearly attribute local resurgences or such geographic spread to regional changes in climate [11–14]. More research is needed to better understand the relationship between climate change and transmission of mosquito-borne diseases, and to further promote adaptive policies formulation to reduce unexpected climate-related risk at a global, regional or local level.

Mosquito-borne diseases in China remain a serious public health problem. For example, 46,988 malaria cases and 18 deaths were reported in 1,097 counties in 2007 [15]. In 2002, the most serious outbreak of dengue fever occurred in Taiwan with 5,285 diagnosed cases [16]. In 2006, an outbreak of Japanese encephalitis occurred in Shanxi Province causing 19 deaths [17]. As the largest develo** country, China has experienced considerable changes in climate over during the last decade with more rapid changes in the past 50 years [18]. The annual average temperature has risen by 0.5-0.8°C, which is slightly higher than the global average level. These variation and fluctuation in weather patterns and extreme climatological phenomena (e.g. droughts, storms, floods etc.) may have a detrimental effect on frequency and distribution of mosquito-borne diseases.

In recent years, the impact of climate change on the transmission of mosquito-borne diseases has been studied in China. However, the quantitative relationship between meteorological variables and the spatial and temporal distributions of these infectious diseases is still not clear. Study findings are inconsistent, which may be due to methodological limitations, unavailability of relevant data and many uncertainties about the range and magnitude of influences of climate change. Moreover, there remains no adaptive mechanism to reduce adverse consequences of mosquito-borne diseases under the changing climate in China. It is urgent to improve our understanding of current evidence, knowledge gaps and development of adaptation options. Our aims were to summarize previous research exploring climate change-related impacts on mosquito-borne diseases in China by reviewing the published studies examining the relationship between climate variability and the transmission of malaria, dengue fever and Japanese encephalitis, and to give some suggestions for the development of adaptation strategies and measures to lessen the adverse impacts on mosquito-borne diseases in China.

Methods

Search strategy

The PubMed electronic database and China Hospital Knowledge Database (CHKD) were used in December 2011 to retrieve original studies published in English and Chinese, respectively. Searches of the “Google” search engine and “Google Scholar” were also conducted. Combinations of the key terms “malaria”, “dengue”, “dengue fever”, “dengue hemorrhagic fever”, “Japanese encephalitis”, “climate”, “weather”, “climate change”, “climate variability”, “climatic factors”, “temperature”, “rainfall”, and “humidity” were used to maximize search yield. Titles, abstracts and keywords were first screened for relevance and full texts were obtained to evaluate for inclusion criteria. Reference lists of each included article were then evaluated if missed in the in the initial electronic database search. Figure 1 illustrates the systematic search and inclusion/exclusion process.

Figure 1
figure 1

Flow chart of literature search strategy.

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Inclusion criteria

Studies were included on the basis of the following criteria:

  1. 1.

    Articles must evaluate the effects of climatic factors on the distribution and transmission of malaria, dengue fever or Japanese encephalitis. Meteorological variables (e.g. temperature, rainfall etc.) or ecological proxy indicators (e.g. Normalized Difference Vegetation Index, South Oscillation Index) had to be included. Disease variables (e.g. incidence, cases) or entomologic variables (e.g. Breteau Index, House Index etc.) had to be included.

  2. 2.

    The papers had to use an epidemiological study design (e.g. time series analysis, spatial and/or temporal analysis and descriptive study) to identify the association between climatic variables and incidence of mosquito-borne diseases and/or vector factors (e.g. mosquito density, distribution, infectious life span).

  3. 3.

    Only studies published before December 2012 and conducted in China (including Chinese Autonomous Regions, Hong Kong, Macau and Taiwan) were examined.

Results and discussion

Literature search

To avoid language bias, studies published in English and Chinese were considered for inclusion (Table 1). The initial search generated 3769 articles from PubMed, CHKD and Google Scholar databases. Review of the titles, abstracts and keywords excluded 2989 articles, leaving 780 studies identified as potential epidemiological papers. Then, 517 full-text articles were identified based on the abstracts and evaluated for inclusion. Of these, fifty-four articles met the inclusion criteria and 3 papers were included after cross-referencing. The methodologies and major findings of the final 57 studies are summarized in Tables 2, 3 and 4.

Table 1 Numbers of selected studies published in English and Chinese
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Table 2 Characteristics of studies on the association between climatic variables and malaria transmission
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Table 3 Characteristics of studies on the association between climatic variables and dengue transmission
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Table 4 Characteristics of studies on the association between climatic variables and JE transmission
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Study sites mainly included Yunnan Province (n = 9), Hainan Province (n = 8), Anhui Province (n = 7), Taiwan (n = 7), Guizhou Province (n = 5), Shandong Province (n = 3), Guangdong Province (n = 3), Henan Province (n = 2), Hubei Province (n = 2), Jiangsu Province (n = 2), and Liaoning Province (n = 2). Other locations included Jiangxi Province, Hebei Province, Shanxi Province, Shaanxi Province, Sichuan Province, Gansu Province, Zhejiang Province, Fujian Province, Bei**g Municipality, Chongqing Municipality, Tian** Municipality, Inner Mongolian Autonomous Region, and Tibetan Autonomous Region. However, there was no study conducted in some regions where mosquito-borne diseases are endemic, such as Guangxi and Hunan Province.

All included studies examined the relationship between climatic variables and mosquito-borne diseases. Of these, only 6 studies evaluated of the impacts of both meteorological factors and other relevant determinants, such as urbanization, agriculture and vaccination [51, 54, 64, 71, 73]. Several studies used ecological proxy indicators including Normalized Difference Vegetation Index (NDVI) and South Oscillation Index (SOI) as risk variables [28, 29, 35, 23, 31, 35, 19, 23, 47, 56]. Other statistical methods used included study designs utilizing Principle Component Analysis (PCA), Back propagation artificial neural network and CLIMEX model etc.

Associations between climatic variables and mosquito-borne diseases

Malaria

Despite considerable reductions in the overall burden of malaria in the 20th century, this ancient disease still represents a significant public health problem in China, especially in the southern and central regions. In 2010, 7,855 diagnosed malaria cases and 34,082 suspected cases with 19 deaths were reported in 1191 counties of 239 Provinces/Municipalities/Autonomous Regions in China. The annual incidence was 0.66/10,000 population [76]. Only sixteen percent of malaria cases were caused by Plasmodium falciparum[76] mostly occurring in Yunnan Province, which is located in southern China. Yunnan remains a hypo-endemic region with persistent cases of both P. falciparum and P. vivax malaria.

To identify risk factors related to climate change and its role in malaria transmission, a series of studies were conducted in mainland China to investigate the relationships between meteorological variables and malaria [19–46]. Except for a single study that found no association, all studies showed correlations between climatic variables and malaria in different locations and study periods in China. The contradictory study likely resulted from a short (6-month) study period [36]. In Yunnan province, two studies were conducted in 2009 to clarify potential risk factors of malaria transmission [26, 31]. Clements et al. (2009) demonstrated that for P. vivax the relative risk appeared to cycle every 3 to 4 years, whereas for P. falciparum the pattern was less regular [26]. Hui et al. (2009) found that the influence of meteorological variables on P. vivax malaria was greater than that of P. falciparum malaria, especially in cluster areas, indicating P. vivax malaria may be more climate-sensitive [31].

Almost all of these analyses identified a positive association between temperature indices and malaria transmission. Some studies also reported that temperature was the most important climatic determinant in the transmission of malaria. For example, a study conducted in **an, which is a temperate city in northern China, showed that a 1°C rise in maximum temperature may be related to a 7.7% to 12.7% increase in the number of malaria cases, while a 1°C rise in minimum temperature may result in approximately 11.8% to 12.7% increase in cases [22]. Zhou et al. (2010) revealed that temperature was a key meteorological factor correlated to malaria incidence, implying the potential role of global warming in malaria re-emergence in central China early in the 21th century, especially in Anhui, Henan and Hubei Provinces along the Huang-Huai River [21]. However, the association between temperature variables and malaria incidence may not be constant year-round. Tian et al. (2008) emphasized the stronger effect of minimum temperature on malaria incidence in the cool months in the rain forest area of Mengla County, Yunnan province, indicating increased risk of transmission as a result of warmer winters [27]. Although global warning could make more areas climatologically suitable for malarial transmission; because higher temperature promotes mosquito development, virus replication and feeding frequency of mosquitoes, extreme high temperature can also restrict the growth of mosquitoes and reduce the spread of malaria. Typically, temperatures lower than 16°C or higher than 30°C have a negative impact on the development and activities of mosquitoes [30].

High relative humidity is expected to prolong the life of the mosquito enabling it to transmit the infection to several persons. Correlations between relative humidity and malarial transmission were also detected in some regions in China [19, 20, 23–25, 30, 32, 23]. In Motou County of Tibet, Huang et al. (2011) found that relative humidity, which was greatest relative to malaria incidence among meteorological variables as it is a result of temperature, rainfall and other climatic indicators and influenced the activity of mosquito directly such as biting rate and breeding rate [20]. The distribution of mosquitoes, which also is also dependent on relative humidity, determines the extent of malarial spread. Thus, no malaria transmission occurs where the monthly average relative humidity is lower than 60% [23]. Conversely, it was reported that relative humidity is not a restricting factor in areas where it is higher than 60%, but temperature then becomes the major driver [23]. For example, no association of relative humidity and malaria transmission was detected in Hainan province [19–21, 23–26, 30–35, 94, 95], which may affect the development and infection capacity of both the mosquito and the virus. Relative humidity is also important in the transmission of JE because mosquitoes can survive longer and disperse further in areas with suitable relative humidity [96]. Studies in different areas of Asia have also shown the likely influence of climate on the incidence of JE [97–99]. However, little research has been conducted to examine the effect of climatic variables, along with mass vaccination and other non-climatic drivers in China. Bi et al. (2007) have identified positive relationships between climatic variables (monthly maximum temperature, minimum temperature and total rainfall) and JE transmission in a rural region of Anhui Province [65] and a metropolitan area of Shangdong Province [63] where no rice was grown and the role of pigs in disease transmission was not fully understood [63]. Unfortunately, the effects of vaccination on JE control in the two areas were very limited during the study periods. In the metropolitan area of **an city, a potential threshold of the effect of temperature on JE was also detected by the Hockey Stick model which is based on the assumption that temperature has no effect on JE cases until a threshold value. When the monthly mean maximum temperature was higher 25.2°C or the minimum temperature was over 21.0°C, an obvious increase in JE cases occurred [63]. These findings are consistent with the threshold temperature detection in previous Chinese studies [87]. Using ARIMA models, Lin et al. (2011) suggested that monthly average temperature and relative humidity at 0-month lag were positively associated with JE incidence in Linyi, another city of Shangdong Province after adjusting for mass vaccination in this area [62]. Time lag-0 of climate variables was perhaps because the behaviour of pig breeding in Linyi, along with the high density of mosquitoes help to shorten the transmission cycle [62]. With adjustment of more interactional factors including seasonal pattern, time trend, pig density, 23 geographic areas representing location of farm and paddy cultivation, and vaccination coverage, HSU et al. (2008) identified the significant effects of monthly temperature and rainfall with two months lag on the monthly occurrence of JE in Taiwan [64]. Similarly, temperature and rainfall were two significant determinants of JE spread with control of vaccination coverage and paddy field areas [71].

Few analyses, without controlling for non-climatic factors that potentially affect JE transmission, also reported associations between different climatic variables such as temperature, rainfall and JE annual incidence by correlation and regression analyses [66–69, 72, 100]. Based in part on recommendations and established approaches in recent studies of adaptation to climate change [81, 101–105], as well as on the status of mosquito-borne diseases in China, we highlight five principles to guide timely development of adaptation mechanism to reduce the adverse impacts of climate change on the control of mosquito-borne diseases. These guidelines may also be applicable in addressing the threat to other health outcomes from climate change.

Improving current surveillance and monitoring systems integrated with climate-sensitive conditions

In recent years, the Chinese government has paid great attention to the prevention and control of mosquito-borne diseases. Since 2004, cases of infectious diseases have been electronically recorded and the data collected at the national level by the Chinese Center for Diseases Control and Prevention (China CDC). This important step means the disease surveillance system is more sensitive and efficient than in previous years. However, unavailability of good quality long-term data sets has hampered our understanding of the likely impacts of climate change on mosquito-borne diseases and vector distribution. Kovats et al. (2001) have pointed out that climate change and health researches require at least 30 years of data because short- and medium- term associations may not provide an accurate picture of the impact of climate change occurring over many decades [106]. In China, imperfect data collected by passive surveillance systems restrict such climate-health relationship analysis. For example, onset dates rather than notification dates are not available, which may lead to considerable information bias. According to a national report in 2005, it was also estimated that only 1/18 (5.6%) malaria cases in China are reported [107]. Furthermore, lack of routine data collection of vectorial indicators has restricted our understanding of real geographic and temporal distributions of mosquito vectors.

Under the circumstance of the changing climate, truly effective surveillance systems and monitoring systems can be used to identify changes in the range and incidence of diseases; determine whether these changes are to be the result of climate change; assist the development of response measures and develop hypotheses about the climate-health relationship [108]. We believe that there are also many gaps for improving current surveillance and monitoring of infectious diseases in China in response to climate variation. Surveillance for early detection of epidemics of mosquito-borne diseases based on readily climatic data, such as daily temperature records, in combination with other interactional factors are of paramount importance [108]. For example, an effective early warning system for outbreaks of mosquito-borne diseases based on predicted extreme weather conditions, such as extreme temperature or rainfall, can be considered as an immediate opportunity for adaptation by strengthening the preparedness of emergency response before periods of high-risk [100]. Careful tracking of imported cases, in conjunction with relevant meteorological data, is also of assistance in providing earlier warning signals for emerging indigenous epidemics [109, 110]. In short, coherent surveillance systems integrated with climate-sensitive conditions are urgently needed to improve scientific knowledge about the health risks of climate change, and to prioritize needs for intervention and adaptation options.

Focusing adaptation strategies and policies on vulnerable communities

Some populations and geographical regions will be particularly vulnerable to climate change. Although climate change is a global threat to public health, it is well acknowledged that poorer nations and communities who have contributed least to greenhouse gas emissions are most vulnerable to the effects [111]. Higher malaria risk in China has also been associated with poverty, poor quality housing, unhygienic surroundings and agricultural activities in rural and remote areas. Chinese farmers in rural regions who usually work in fields and sleep in the open are at higher risk of mosquito biting especially in summer and autumn, when the peak times of malaria occurred due to favorable climate conditions and active propagation of mosquitoes. However, urban populations may also share some increased vulnerabilities in the context of climate change. For example, populations living in cities located on the coast or on small islands may be particularly vulnerable to frequent rainfall and storms and are also exposed to changes in the spread of mosquito-borne diseases, such as Taiwan. Additionally, metropolitan regions may be experiencing two types of warming trends;warmer temperatures caused by the urban heat island effect as well as global climate change, which could make more urban areas suitable for the transmission of mosquito-borne diseases by reducing development times, increasing survival probabilities and biting frequency for the mosquitoes [102, 112].

Due to limited funding, resources, and time, effective adaptive action is required to protect the most vulnerable individuals and communities, due to geographic locations and low adaptive capacity, from inevitable effects of climate change on mosquito-borne diseases. Firstly, better identification of real vulnerable groups needs to be based on more comprehensive factors, such as political rigidity, population growth, poverty, culture, dependency, geographic isolation, population immunity and human perceptions, behaviours and activities etc. This requires both qualitative and quantitative assessing methods in future adaptation research. The next step is the development and implementation of timely and efficient adaptive strategies in those targeted communities by collective coordination of all relevant sectors. Adaptive options may include expanding mosquito control, improving vaccination coverage, enhancing existing elimination programs and conducting health education programs in a relative short term, and the establishing an early warning system, improving housing quality, strengthening preparedness and response of extreme weather events (e.g. better and adequate urban drainage systems) in a long run.

Strengthening the capacity of public health system to adapt climate change

In the Chinese context, an efficient network system of mosquito-borne diseases control has been established and CDCs at national, province, and city level take the major responsibility in the network. Although the public health system has credible skills and experience ranging in disease control and prevention, public health management and emergency preparedness services, the status of the resources and capacity of mosquito-borne diseases control at local levels is not optimistic, especially in rural counties, townships and communities. For example, Chen et al. (2010) pointed out that lack of additional funding, additional staff, staff straining and equipment currently has become the major hamper of improving ability of local public health sectors in malaria surveillance, diagnosis and treatment, and mosquito control [114]. Moreover, inaccessible information and training on health influences of climate change may restrict awareness, knowledge, attitude and decisions of local public health departments. In brief, adaptation to climate change will require the public health system has a key leadership role to take in health adaptation strategy making and implementation in China. Stable funding, additional staff and better information access will be needed to best prepare the public health sectors to manage the health risks associated with climate change.

Develo** multidisciplinary approaches sustained by a new mechanism of intersectoral coordination and collaboration

What makes addressing the range and magnitude of health impacts of climate change even more difficult is unavoidable complexities and uncertainties in multi-factorial causal webs. We can not deal with climatic variables or health outcomes or any other potential interacting drivers in isolation and need to integrate scientific knowledge from various disciplines to tackle these interactions by develo** a better collaborated mechanism across all relevant governmental and non-governmental sectors and institutions which are responsible for the prevention and control of climate-sensitive disease [101, 112]. Although the existing national plans and policies about climate change clearly indicate that adaptation to health burdens from climate-sensitive diseases is a multiple-sector responsibility, mechanisms of intersectoral decision making and coordination do not yet operated to guarantee free and open exchange of information, adequate compliance and participation, ongoing financial and technological support.

For the control and prevention mosquito-borne diseases under condition of climate change, it is even more urgent to produce multidisciplinary insights from diverse public and private sectors. Although some health risks can be reduced largely by health sector interventions such as surveillance, mosquito control, spraying, vaccination, sanitation activities and health education, many adverse impacts require concerted adaptive options with other relevant sectors such as meteorology, environmental, urban designing and planning, water, agriculture and housing [101]. Unfortunately, health sectors in China which invest greater financial and resources support, are often the only ones responsible for disease prevention and control. Therefore, there is a particular need for a multidisciplinary approach sustained by ongoing intersectoral coordination and collaboration, which not only allow us to have a bettering understanding of the complex climate-health relationship, but will provide integrated and practical adaptive strategies to minimize climate-sensitive disease impairments, and further influence policy-formulation and decision-making [115, 116].

Promoting awareness and mobilization of the public and individuals

An important step in the development and promotion of successful local adaptation options is raising public and professional awareness. Governments, institutions, and organizations play indispensable roles in those adaptive actions but so do the public and individuals if they are receptive to behavior change to adapt to a world altered by climate change [101]. It is well acknowledged that the perceived risk of climate change in the population is the strongest motivator of health behaviour change, that is, it is only when individuals feel vulnerable and threatened to the impacts of climate change that they will take autonomous adaptation seriously [117]. In China, climate change has traditionally been treated as an environmental threat rather than a public health issue. We highlight that awareness programs about the health aspects of climate change are urgently needed, coupled with high-quality baseline investigations to examine public perception of adverse health effects from climate change in China.

Mobilization of the public to adapt to climate change also depends on availability of information about effective adaptation measures as well as social capacity to deal with these problems. A recent cross-sectional survey conducted in the U.S. showed that people who report knowledge of the necessary information to prepare for adverse health impacts of climate change were more likely to have an adaptive plan for their household [118]. For the prevention of mosquito-borne diseases, scientific knowledge and information, such as risk behaviour and self-protection measures, should be rapidly dispersed during high-risk periods to strengthen the adaptive capacity of the public. For example, relevant health intervention campaigns can be conducted to warn and educate local communities to change personal behaviour, e.g. use of mosquito nets in the field at peak time of mosquito-borne diseases; cleaning living conditions as soon as an increase in cases; emptying artificial containers with stagnant water timely. Moreover, better implementation of planned adaptation to climate change requires good social capability which depends on resource availability and cultural acceptability, indicating that successful adaptation strategies much be suitable for local conditions and accepted by local populations [101].

Conclusions

This study included scientific evidence of impacts of climate change on the transmission of mosquito-borne diseases, resulting in increase in incidence and geographic spread in China. Variability in temperature, precipitation, wind and extreme weather events has been observed to be linked with changes of spatial and temporal distribution of malaria, dengue fever, Japanese encephalitis in some regions in China. However, research to date has limitations and challenges in attributing changes in the status of mosquito-borne diseases to climate change. Potential adverse effects heighten the urgent need to conduct more high-quality research for assessing risks of these climate-sensitive vector-borne diseases, to improve current control policies from a weather-based direction, and to develop targeted policies for adapting short-term and long-term climate shifts in China.

Based on summarization of what is known about the likely impacts of climate change on these diseases in China we highlight five principles to guide policy formulation to enhance adaptation mechanism to reduce the adverse impacts of climate change on the control of mosquito-borne diseases. These recommendations include: 1) improving current surveillance and monitoring systems integrated with climate-sensitive conditions; 2) focusing adaptation strategies and policies on vulnerable communities; 3) strengthening public health system capacity to adapt to climate change; 4) develo** multidisciplinary approaches sustained by a new mechanism of intersectoral collaboration; and 5) promoting awareness and mobilization of the public as well as health and other professionals.