The impact of increasing temperatures due to climate change on infectious diseases
BMJ 2024; 387 doi: https://doi.org/10.1136/bmj-2024-079343 (Published 04 October 2024) Cite this as: BMJ 2024;387:e079343
- Olga Anikeeva, research fellow1,
- Alana Hansen, research associate1,
- Blesson Varghese, postdoctoral researcher1,
- Matthew Borg, postdoctoral researcher1,
- Ying Zhang, associate professor2,
- Jianjun Xiang, professor3,
- Peng Bi, professor1
- 1Department of Public Health, University of Adelaide, Adelaide, South Australia SA 5005, Australia
- 2University of Sydney, Sydney, New South Wales, Australia
- 3Fujian Medical University, Fuzhou, Fujian, China
- Correspondence to: P Bi peng.bi{at}adelaide.edu.au, J Xiang jianjun.xiang{at}fjmu.edu.cn
Abstract
Global temperatures will continue to rise due to climate change, with high temperature periods expected to increase in intensity, frequency, and duration. Infectious diseases, including vector-borne diseases such as dengue fever and malaria, waterborne diseases such as cholera, and foodborne diseases such as salmonellosis are influenced by temperature and other climatic variables, thus contributing to higher disease burden and associated healthcare costs, particularly in socioeconomically disadvantaged regions. Targeted efforts and investments are therefore needed to support low and middle income countries to prepare for and respond to the increasing infectious disease threats posed by rising temperatures. This can be facilitated by the development and refinement of robust disease and entomological surveillance and early warning systems with integration of climatic information that promote enhanced understanding of the geographic distribution of disease risk. To enhance healthcare workforce capacity and capability to respond to these public health threats, medical curricula and continuing professional education programmes for healthcare providers must include evidence based components on the impacts of climate change on infectious diseases.
Introduction
Heatwaves and high temperature periods have been increasing in intensity, frequency, and duration, and these trends are expected to worsen due to climate change.1 Climate change, with associated high temperatures and irregular rainfall, has multifaceted impacts on the transmission of infectious diseases, leading to changes in pathogen development, vector distribution, and human behaviour, with increases in some infectious diseases (fig 1).23
Effects of climate change on transmission of infectious diseases
Global warming expedites melting of glaciers and ice sheets, and expands oceans by warming them, increasing sea levels, rainfall, and flooding. Vector-borne illnesses increase due to both drought and flooding increasing stagnant water, as well as decreased extrinsic incubation periods, which improve mosquito breeding conditions.4 Vector-borne diseases such as dengue fever, malaria, West Nile virus, and Japanese encephalitis are particularly influenced by high temperature and other climatic variables such as rainfall and relative humidity, in part due to their impact on mosquito breeding and lifespan and pathogen replication rates within mosquitos.3567
Flooding and heavy rainfall can lead to contamination of water and food supplies by mixing them with faecal pathogens from sewers, negatively affecting water and food hygiene and predisposing to foodborne and waterborne diseases such as cholera and salmonellosis.89 Droughts from global warming may also lead to increased faecal concentrations in water supplies.10 Climate change is associated with both human and animal migration, leading to increasing population densities that promote increased pathogen transmission rates. Importantly, disease burden due to increasing temperatures varies across populations and geographic locations, with heavier disease burden observed in lower sociodemographic index regions and more densely populated areas in the context of climate change.11 In China, for instance, a northward shift of endemic areas of vector-borne diseases was observed due to climate change.12 Older individuals are particularly vulnerable to the negative impacts of increasing temperatures on infectious disease risk, posing additional challenges in the context of ageing populations globally.313
This review summarises the impact of increasing temperatures due to climate change on the burden of a broad range of vector-borne, foodborne, and waterborne diseases of public health concern. These diseases include dengue fever (responsible for 29 200 deaths and 2.08 million disability-adjusted life years globally in 2021), malaria (749 000 deaths globally in 2021, with 57% occurring among children under 5 years of age), and shigella infection (212 000 deaths globally in 2016, the second leading cause of diarrhoeal morality).14
The emergence and re-emergence of infectious diseases, including novel pathogens, due to climate change have the potential to increasingly affect populations globally and spread to previously unaffected regions. The review summarises the infectious disease challenges posed by increasing temperatures and climate change and considers the responses needed from global health systems and health professionals to minimise the negative impacts.15
Sources and selection criteria
We conducted literature searches between February and April 2024 using PubMed and Embase. We used the following search terms, with appropriate database-specific modifications (addition of MeSH terms when searching PubMed), to identify relevant peer reviewed articles: high temperature, heatwave, hot weather, climate change, global warming, infectious disease, and communicable disease, as well as disease-specific keywords for the conditions discussed in this review. We searched the reference lists of relevant systematic reviews to identify additional publications. Articles were included if they were peer reviewed; published in English; and were systematic reviews, randomised controlled trials, or observational studies reporting on the impacts of high temperatures on at least one of the selected infectious diseases. Articles were excluded if they were not peer reviewed, were not available in English, or did not report on the impact of high temperatures or heatwaves on at least one of the infectious diseases discussed in this review. Articles published between 1990 and 2024 were considered for inclusion, with those published in the past 10 years prioritised.
Results of literature search
Table 1 summarises the overall findings from the included studies about the impacts of high temperatures and, where relevant, other climatic factors such as rainfall and flooding on the selected infectious diseases. The sections that follow present a detailed overview of the impacts of increasing temperatures on vector-borne, waterborne, and foodborne diseases, discuss the quality and strength of the available evidence, and, where appropriate, highlight future research directions.
Summary of the impacts of high temperature on selected infectious diseases
Impacts of increasing temperatures on vector-borne and zoonotic diseases
Vector-borne diseases are influenced by climatic variables, including temperature, humidity, and precipitation. The following sections detail the epidemiological evidence linking these climatic factors with specific mosquito-borne, parasitic and zoonotic diseases, such as dengue fever, malaria, Japanese encephalitis, West Nile fever, Zika virus disease, schistosomiasis, leishmaniasis, and haemorrhagic fever with renal syndrome.
Dengue fever
Dengue, a mosquito-borne viral infection transmitted by Aedes mosquitoes, poses a global health threat, affecting 3.8 billion people (53% of the global population), with an estimated 100-400 million infections and over 20 000 deaths annually.116117 Dengue is predominantly prevalent in tropical and subtropical climates, especially in urban and semi-urban areas, with a high concentration of cases (about 70%) in the Asia-Pacific region.117118
Various factors influence dengue transmission, with climatic factors such as temperature, rainfall, and humidity, as well as macroclimate phenomena such as the Indian Ocean Dipole and El Nino Southern Oscillation, playing a crucial role by accelerating mosquito breeding, extending mosquito lifespan, and enhancing the replication rate of the dengue virus within mosquitoes.567119
A 2023 systematic review and meta-analysis16 of 54 peer reviewed, original research studies including quantitative observational time series and case-crossover designs showed a 13% increase in risk of dengue infection (95% confidence interval 11% to 16%) for each 1°C increase in high temperatures, with recent studies171819 reinforcing this association. Positive associations between rainfall, relative humidity, and dengue cases have been documented,46 yet negative associations19120 are observed during periods of extremely heavy rainfall and very high humidity levels. This is likely due to the washing away of mosquito breeding sites, reduced mosquito activity, and reduced viability of the dengue virus.5
Malaria
Malaria is an Anopheles mosquito-borne infectious disease caused by parasites of the Plasmodium genus. Current empirical evidence suggests that climatic factors can have both direct and indirect effects on malaria transmission and burden, although the direction and magnitude of changes in transmission vary across social and ecological systems, both within and between countries.121122 Rising temperatures, altered rainfall patterns, and changing ecological conditions affect the distribution and abundance of malaria vectors, contributing to the expansion of transmission zones geographically.20 Warmer temperatures enable mosquitoes to proliferate in areas previously unsuitable for their survival, including higher altitudes and cooler regions.
A northward shift of the malaria epidemic belt in North America, Europe, and Asia and the occurrence of new cases in some African highlands have been reported.21 This expansion potentially exposes millions of people to the risk of malaria, particularly in regions where populations lack immunity. Conversely, increasing temperatures may reduce the environmental suitability for malaria transmission by Anopheles mosquitos in sub-Saharan Africa.123
Indirect effects of climate change on malaria transmission (and other vector-borne diseases such as dengue fever) can be mediated through socioeconomic factors such as poor living conditions, reduced access to healthcare services, population displacements due to climate change, and rising food insecurity leading to malnutrition.121 In addition, fluctuations in temperature and humidity may compromise the efficacy of antimalarial drugs, posing a significant challenge to malaria control programmes, particularly in low and middle income countries.124125
Japanese encephalitis
Japanese encephalitis (JE) is a mosquito-borne zoonotic disease transmitted by Culex mosquitoes, which acquire the Japanese encephalitis virus by feeding on infected pigs or poultry.126 Globally, an estimated three billion people reside in regions where JE is endemic, predominantly across 24 countries in South East Asia and the Western Pacific.126 Annually, approximately 68 000 clinical cases are recorded, with a case fatality rate of 25-30% and chronic neurological effects in 30-50% of JE survivors.126
Climatic factors play a crucial role in creating conditions favourable for mosquito breeding and viral activity, which can substantially influence the transmission dynamics of JE.34127 Observational studies have consistently reported positive associations between JE cases and climatic variables such as temperature, relative humidity, and rainfall.22232425262728293031323334 For example, a time series analysis study in a region with a humid subtropical climate in India estimated that each 1 unit increase in average daily mean temperature, rainfall, and relative humidity led to increases in JE hospital admissions by 22.2% (95% CI 20.1% to 24.4%), 0.6% (0.4% to 0.9%), and 5.2% (4.7% to 5.8%), respectively; and in JE mortality by 13.3% (11.2% to 15.4%), 0.9% (0.5% to 1.3%), and 3.3% (2.7% to 3.8%), respectively.128 Similarly, a case-crossover analysis study in Taiwan reported that a 1°C increase in temperature correlated with a 14.4% (7.4% to 21.4%) rise in JE case counts, while a 5% increase in relative humidity was associated with a 9.8% (1.0% to 18.6%) increase in JE cases.31
West Nile fever
West Nile fever is caused by West Nile virus (WNV), a mosquito-borne flavivirus sensitive to climatic variations, characterised by a global distribution maintained through an enzootic cycle involving Culex species mosquitoes and avian hosts.129 Climate change exerts influence on multiple facets of WNV transmission, including the vector, amplifying host, and virus. A warming climate can accelerate mosquito and pathogen development, heighten vector competence for WNV, and alter mosquito traits such as longevity, blood feeding behaviour, and fecundity,36130 with often non-linear effects.131 Driven by climate change, alterations in the timing of bird migration and breeding patterns may further contribute to shifts in long range virus movement.131132
Predictions suggest a broadened WNV distribution and elevated risk worldwide in the context of climate change, albeit with considerable regional variability.3536 Europe, for instance, anticipates up to a fivefold increase in WNV risk by 2040-60 under different demographic and climate change scenarios, and areas reporting the disease would increase from 15% to 23-30%, which will disperse to previously WNV-naïve areas such as northern Europe.3738 In North America, a 5°C increase in mean maximum weekly temperature was associated with a 32-50% surge in reported WNV infections.39 Moreover, recent perspective and experimental studies have highlighted the potential impact of climate change on the epidemiology of WNV co-infections and co-circulation with other arboviruses, such as Usutu virus (a flavivirus serologically closely related to Japanese encephalitis and West Nile viruses, which is found in parts of Africa, Europe, and the Middle East), Zika virus, and dengue virus, particularly in regions where multiple vectors and hosts overlap.133134 Co-infections with other pathogens may influence disease severity, clinical outcomes, and public health responses, presenting additional challenges for disease surveillance and control.
Zika virus disease
Zika virus (ZIKV) disease is a mosquito-borne viral disease transmitted by infected Aedes aegypti and Aedes albopictus mosquitoes.135 An estimated 3.6 billion people (42% of the global population) live in tropical and subtropical regions where ZIKV disease risk is elevated, and, without preventive measures such as vector controls, the virus could potentially affect over 6.2 billion people globally (79% of the global population).135136137138 Since 2015, ZIKV disease has emerged as an important global health threat, with 89 countries across five of the six WHO regions (excluding the Eastern Mediterranean region) reporting evidence of autochthonous ZIKV disease with over 1.4 million suspected and confirmed cases.135
ZIKV disease is particularly concerning due to its potential to cause severe birth defects such as microcephaly and other congenital anomalies (however, it should be noted that cases of microcephaly have predominantly been reported in Brazil over a relatively short time), and many infections go undetected as roughly 75% of cases are asymptomatic.135139140
Similar to dengue virus, which is transmitted by the same mosquito species, evidence suggests climatic factors can influence ZIKV disease outbreaks, with mechanistic models from laboratory studies showing maximal transmission occurring at temperatures between 26° and 30°C.4041 However, compared with dengue, direct evidence linking ZIKV disease and climatic factors such as temperature, humidity, and precipitation is limited. An ecological study in Colombia applying Bayesian structured additive regression modelling to assess high risk areas of ZIKV disease found a significant positive association between the disease and meteorological factors (temperature, rainfall, and relative humidity), with nearly half of the 32 regions assessed (15-17 regions) showing a significant positive association.141 However, more research is needed to establish definitive links between climatic factors and Zika virus infections.
Schistosomiasis
With 207 million cases globally (more than 90% of those in Africa), schistosomiasis, a neglected tropical and subtropical parasitic disease, is caused by six different species of Schistosoma, which use freshwater snails as necessary intermediate hosts. The snails release the larval forms of the parasites (cercariae), which can penetrate skin during contact with infested water, thus leading to human infection. In endemic areas farmers can become infected during routine agricultural, domestic, and occupational activities, and people undertaking recreational activities such as swimming or fishing can also be at risk.
The impact of climate change on schistosomiasis is complex, as the disease’s response to climatic factors not only depends on snail types and schistosome species but also ecological and socioeconomic determinants such as dam building and agricultural expansion.43142 The reproduction, survival, and dispersal of the intermediate host snails, as well as the development of the worm within the host, are highly sensitive to temperature variations.143 Within the optimal temperature range of 15-31°C, elevated temperatures are associated with increased snail infection, egg laying, egg hatching, snail maturation, and human infection.42
A study in China projected an expansion of schistosomiasis transmission into currently non-endemic areas in the north of the country, with an additional risk area of 783 883 km2 by 2050, translating to 8.1% of the total surface area of China.144 Similarly, transmission is expected to increase in the current marginal transmission areas with potential for greater transmission at the edge of the cooler temperature range, such as in Mediterranean countries.43 Moderate precipitation facilitates snail breeding, while heavy rainfall may disrupt snail habitats and reduce cercariae survivability.145 Climate change related flooding, drought, and alterations in water salinity and pH have also been identified as influencing factors in schistosomiasis transmission.42
Leishmaniasis
Leishmaniasis, caused by the Leishmania genus of parasitic protozoa, is a zoonotic disease of increasing public health concern. Symptoms range from mild (such as, skin sores, fatigue, loss of appetite) to severe (such as, persistent fever, anaemia, and liver and spleen enlargement) and are influenced by the host’s immune response as well as the species of Leishmania.146 It is transmitted to humans through the bites of infected female sandflies and has a variety of reservoirs, including humans, domestic animals, horses, rodents, birds, and reptiles.
Leishmaniasis is endemic in 90 countries, predominantly in South America, East and West Africa, the Mediterranean region, Central Asia, and the Indian subcontinent.146 However, higher temperatures due to climate change, as well as the rapid movement of people and animals facilitated by mass transit networks, have led to sandflies increasingly appearing in countries and regions with traditionally colder climates, with cases of leishmaniasis detected in previously unaffected countries in recent years.146 An ecological study in China of two leishmaniasis outbreaks that occurred between 2005 and 2015 found higher temperatures and lower relative humidity increased leishmaniasis risk.45 Similarly, an ecological study in Sri Lanka found that high temperature, as well as lower humidity and wind speed, were significantly associated with leishmaniasis cases.46 A study in Iran analysed demographic, environmental, and geographic data using geographic information systems and regression models to identify several environmental and ecological factors that influence leishmaniasis distribution, with warmer temperatures and lower altitudes, rainfall, and humidity associated with increased cases.47
Haemorrhagic fever with renal syndrome
Haemorrhagic fever with renal syndrome (HFRS), a rodent-borne viral disease caused by the Hantavirus genus of the family Bunyaviridae, has an estimated global incidence of 60 000 to 150 000 cases annually, with mainland China accounting for nearly 90% of cases.147148 The fatality rate of HFRS varies by virus strain, ranging between 1% and 15%.149 Humans typically contract the viruses through inhalation of or contact with contaminated rodent droppings, urine, faeces, and saliva.48150
Environmental factors, especially climate, significantly influence HFRS transmission by affecting rodent populations and their interaction with humans.61 Several epidemiological studies have shown a positive association between temperature, rainfall, humidity and HFRS cases, with a non-linear relationship between temperature and HFRS found in temperate and warm temperate zones, while a linear relationship was observed in the subtropical zone.484950515253545556575859606162 For example, a study across 19 Chinese cities found that a 1°C increase in maximum temperature led to a 1.6% (95% CI 1.0% to 2.2%) rise in HFRS cases; a 1 mm increase in weekly precipitation resulted in a 0.2% (0.1% to 0.3%) increase; and a 1% rise in average relative humidity was associated with a 0.9% (0.5% to 1.2%) increase in HFRS cases.56
Impacts of increasing temperatures on foodborne and waterborne diseases
Higher temperatures and increased occurrences of flooding due to climate change can negatively affect water quality and influence human behaviour and food hygiene, resulting in increased risks of waterborne and foodborne diseases.
Bacterial infections
Cholera
Cholera is an acute diarrhoeal disease caused by the bacterium Vibrio cholerae. This waterborne disease occurs in over 40 countries and can be fatal, especially in developing countries.151 There has been a recent global emergence of cholera, and climate change and associated extreme weather events could be one of the drivers.152153 Cholera transmission can be enhanced with inadequate access to safe water and basic sanitation, and increasing flooding due to climate change may play an important role. Warmer temperatures can also favour growth of bacteria and produce a higher concentration of pathogens in water8; a narrative review and experimental studies consistently found increased risks of cholera associated with higher temperatures.6364
Incorporating climatic factors into monitoring and projection modelling could be effective for early warning and preparedness initiatives.10 Despite evidence of geographic expansion of pathogenic Vibrio species in water supplies, there has been insufficient research on the impacts of climate change on cholera in developing countries, thus further investigation is warranted.154
Salmonellosis
Salmonellosis is one of the most prevalent bacterial forms of gastroenteritis, causing over 90 million cases and 155 000 deaths worldwide each year.155 Cases are most commonly reported in hot seasons.156 The optimal temperature for Salmonella species is 35-37°C. High temperatures can boost the transmission and replication of the bacteria to contaminate food such as eggs and meat, causing human infections when consumed.9 A consistent positive relationship between temperature and salmonellosis has been reported in all continents except the Antarctic at various time lags ranging from a few days to six weeks.89656667686970
Studies have shown that a 1°C increase in temperature increases the estimated risk of salmonellosis to between 3% and 13%, with an estimated pooled relative risk of 1.05 (95% CI 1.04 to 1.07) reported in a recent meta-analysis.71 The impacts can be more evident in tropical zones, as well as socioeconomically disadvantaged and rural regions, with food handling and consumption behaviours also playing a role. Increasing temperatures in future years may increase the health burden and economic costs of salmonellosis, warranting interventions that incorporate both socioeconomic and ecological factors.157158
Campylobacteriosis
The WHO recognises Campylobacter infection as “the most common bacterial cause of human gastroenteritis worldwide.”155 The relationship between temperature and Campylobacter infection is less clear than for salmonellosis. Although most studies included in 2024 systematic review reported increased risks with higher temperatures, some studies revealed a negative or null impact.72
Rising temperatures accounted for 33.3% of cases of campylobacteriosis in England and Wales,73 while in Germany campylobacteriosis incidence correlated positively with temperatures between −5°C and 28°C.74 A time series study in Israel showed a 1°C increase above a threshold of 27°C can increase cases by 15%.75 It is estimated that cases in four countries in Europe (Denmark, Finland, Norway, and Sweden) may double by the end of the 2080s due to climate change.76 However, in South Korea campylobacteriosis was not significantly associated with any combination of climatic factors,77 and was inversely associated with temperature rise in South Australia.78 These findings reflect more complicated pathways and interconnections between climate, eco-environment, food contamination, and human behaviour which merit further research.
Shigellosis (bacillary dysentery)
Shigellosis is caused by Shigella bacteria and often results in mild diarrhoea, but severe cases with bloody diarrhoea can be fatal. Quantitative studies are too limited to show that shigellosis is a climate sensitive disease as the effects of temperature vary across different areas.79 A 2023 global risk mapping and prediction model study using individual participant data from multiple studies among children in lower and middle income countries found that shigellosis is sensitive to climatic factors, including temperature, with infections peaking at 33°C and decreasing above this point.159 Temperature is one of the driving factors for bacillary dysentery transmission in various climatic zones and in rural and urban areas of China.80818283 A study in Iran showed correlations between climate and dysentery, particularly in young children and older adults.160 A meta-analysis has estimated that the risk of shigellosis incidence increases by 7.0% per 1°C increase in temperature.71
Escherichia coli infection
Escherichia coli is a common bacterium that can cause diarrhoeal diseases. E coli O157 is of particular public health concern as it can cause severe stomach ache, bloody diarrhoea, and kidney failure.161 Although cases are usually mild, young children and the elderly can be at high risk and complications can be life threatening.162 In a meta-analysis of 18 studies of E coli using temperature modelling, a positive association was found in 15 studies, with a pooled risk estimate of an 8% (95% CI 5% to 11%) increase in the incidence of diarrhoeagenic E coli for a 1°C increase in mean monthly temperature.84 This increase was 10% (5% to 10%) when not controlling for precipitation.84
Legionellosis
Legionellosis is a form of pneumonia caused by Legionella bacteria, which is found in freshwater and in water systems in the built environment. The number of cases in developed countries has been increasing.163 Multiplication and virulence of Legionella can be significantly increased when temperatures are high.164 Rising temperatures have been reported to increase legionellosis in some regions, but the effects are small and inconsistent.71858687 Most studies are based in the northern hemisphere, with few conducted in the southern hemisphere. Evidence suggests that high temperatures combined with heavy rainfall or humidity could be better predictors than temperature alone.888990
Viral gastroenteritis
The interconnections among viruses that cause enteric infections, climate factors, ecology, and human behaviours are complex processes that have not been sufficiently examined and understood. The relationship between ambient temperature and viral diarrhoea could be positive, negative, or not significant,165 and further research is needed.
Rotavirus infection
Rotavirus infection is the leading cause of severe, acute diarrhoea in children less than 5 years old. Annually, it is estimated there are over 25 million outpatient visits and more than 2 million hospitalisations worldwide, predominantly in developing countries.166 Some observational studies in Nepal, South Korea, Spain, Great Britain, the Netherlands, Bangladesh, and Costa Rica have indicated a reduced risk for rotavirus cases associated with warmer temperatures, with a time lag of up to two months.9293949596979899 However, time series and cross-sectional studies in China and Africa have reported more cases associated with higher temperatures.100101 A meta-analysis found no positive relationship between rotavirus infection and temperature.91 Findings suggest a more holistic approach should be taken to investigate climatic and hydrological impacts on rotaviruses.167
Norovirus infection
Norovirus is a leading cause of gastroenteritis for all age groups and a major public health concern, causing 200 000 deaths each year and an estimated annual global economic cost of £48 billion.168 As with rotavirus, the impact of warmer temperatures on norovirus infections is unclear, even though temperature has been identified as a key variable affecting virus persistence in surface waters.102
Increases in norovirus outbreaks (>70%) have been reported in cold and dry seasons,103104 indicating that lower temperatures may favour the survival of the pathogen in the environment. This negative association between temperatures and norovirus infection (relative risk 0.85 (95% CI 0.83 to 0.86)), showed a lagged effect of up to seven weeks.105106 Rather than temperature, humidity and rainfall may be a more sensitive and stronger predictor of norovirus in Africa.169170171 Projections of norovirus outbreaks for coastal regions of China could be more accurate by incorporating temperature, precipitation, elevation, latitude, and longitude in the modelling.172
Hand, foot, and mouth disease (HFMD)
HFMD is a highly contagious viral infection, and often infects young children predominantly through person-to-person contact. There have been recent outbreaks in the Asia-Pacific region. China had about 430 000 reported HFMD cases between January and May 2021.173 As a result, there has been a sharp increase in studies on the impacts of meteorological factors on HFMD since 2020, covering almost all regions of China. Both high and low temperatures (non-optimal ambient temperature) may promote the transmission of HFMD, demonstrating an M-shaped relationship with two peaks on both ends of the temperature spectrum.107108109
Some systematic reviews and ecological studies in China, Vietnam, and the US reported a positive association between temperature and HFMD, with a short lag effect of up to a few days in various climatic zones, and interactions with other climatic variables such as humidity, wind speed, air pressure, and sunshine.110111112113114115 Higher temperatures may also have acute short term effects on reduced risks of HFMD.174 In addition, the impact of temperature could be mediated by a range of demographic and socioeconomic factors, such as gender, greenspace in parks, per capita GDP, urbanisation rate, density of healthcare institutions, and student density in schools and kindergartens.175176177 A study in Malaysia, showed that rainfall and wind speed variably influence HFMD risk.178
International agency and healthcare system response
Disease surveillance, notification, and information sharing
Climate change will continue to pose considerable challenges to already overloaded global healthcare and disease surveillance systems. This is particularly problematic for traditional surveillance systems that rely on historical case notification data and do not adequately consider climatic and demographic variables, thus limiting their effectiveness in tracking the impact of increasing temperatures on disease spread and predicting future disease burden.179
Developing and refining integrated surveillance and early warning systems can address this issue by enhancing the capacity of health systems to prepare for and respond to infectious diseases sensitive to climate.180181 These systems integrate multiple data sources such as traditional disease surveillance, vector surveillance, and weather data to enable more accurate detection, investigation, and response to infectious disease outbreaks, as illustrated in figure 2. They rely on timely and transparent information sharing and cooperation between agencies, including health and agricultural departments, meteorological agencies, and vector and animal disease surveillance efforts, both nationally and internationally.182183
Requirements for an integrated surveillance system for climate sensitive infectious diseases
Adopting a “One Health” approach by prioritising and facilitating cooperation, collaboration, and information sharing across sectors and regions is central to the development of effective disease surveillance systems, as well as prevention, mitigation and control actions, and interventions.184 By taking into account the influence of climatic variables on disease risk, integrated surveillance systems can enhance preparedness and adaptive capacity via early warning systems that anticipate risks based on routinely collected epidemiological, climatic, entomological, environmental, and demographic data.179180181185
The use of satellite remote sensing and geographic information systems technologies enables the identification of spatial and temporal climatic patterns that may influence infectious disease risk, which can be applied to predict epidemics based on these risk conditions.186 Understanding the geographic distribution of cases is central to enabling resources and preventive efforts to be proactively targeted to at-risk locations and populations.187 Furthermore, promoting digital disease surveillance with online disease notification is critically important, particularly in low and middle income countries.
Similarly, enhancing entomological surveillance systems, especially in low and middle income countries, to provide timely and accurate information on vector density and distribution is central to enabling prediction and mitigation of climate sensitive vector-borne diseases. Moreover, recent rapid developments in artificial intelligence and machine learning could be incorporated into integrated infectious disease and vector surveillance systems and early warning systems. These technologies have the potential to yield solutions to challenges pertaining to integrating and unifying data from different sources, and further research in this area is warranted.
Targeting surveillance and response systems in at risk regions
A narrative review of climate driven and weather driven early warning systems around the world found that improving the timing and accuracy of seasonal climate forecasting paired with comprehensive and timely surveillance data on vector exposure-response relationships can be applied to identify conditions conducive to infectious disease outbreaks weeks to months in advance. This allows active surveillance efforts, preventive strategies, and response resources to be targeted to the identified at-risk regions.185
An ecological study evaluating the effectiveness of an early warning signal model for dengue in Colombia using climate, population, and dengue notification datasets, which incorporated temperature, precipitation, humidity, elevation, and population density data, found that it successfully detected 75% of outbreaks between one to five months ahead of time, 12.5% within the month of the outbreak, and missed 12.5% of outbreaks.188 Additionally, the system could be applied to identify at-risk populations at small spatial scales, enabling scarce resources, preventive actions, and vector control efforts to be effectively targeted.188
Similarly, in Mexico the integration of the Early Warning and Response System tool co-developed with the WHO Tropical Diseases Unit into the national surveillance system has led to measurable improvements in dengue surveillance. This resulted in more accurate prediction of climate sensitive disease outbreaks to trigger earlier implementation of mitigation and prevention measures, and highlighted the importance of collaboration and information sharing across sectors and institutions.183 However, while these climate based early warning systems are used in some regions for certain infectious diseases such as dengue, malaria, leishmaniasis, and cholera, gaps in data availability and insufficient research in this field has so far limited their integration into existing surveillance systems, and wider application to other infectious diseases.183185187188189190
Healthcare workforce knowledge and capacity
It is important to consider the healthcare workforce’s knowledge and capacity to respond to infectious disease challenges posed by climate change. As higher temperatures due to climate change contribute to the geographic spread and increasing cases of infectious diseases, health service providers, particularly in regions not previously routinely affected by these conditions, may lack knowledge and experience in identifying and treating them.191 A narrative review of global evidence on climate change and health in medical education found that, although most medical students acknowledged that climate change negatively affected health outcomes, the majority (including over 80% of Chinese and 90% of Ethiopian medical students) felt they lacked the necessary knowledge and were inadequately prepared to deal with climate related health risks.192 Similarly, a survey of general practitioners in rural New South Wales, Australia, found that only around 60% felt that they could provide advice to their patients on the health impacts of climate change.193 A survey of health professionals in India found that, although over 80% of respondents were aware of the immediate health impacts of heat exposure, fewer than 60% had adequate knowledge of delayed or indirect health impacts of climate change.194 A survey of Centres for Disease Control and Prevention staff in China found that only 27% felt they had a good understanding of climate change, with 85% expressing a need for more information about the health impacts of climate change.195 In Vietnam, a survey of healthcare professionals, medical students, and community workers found that participants had moderate to low awareness of the impacts of climate change on infectious disease epidemics, with those working in provincial areas having lower levels of awareness compared with their metropolitan counterparts.196
Increases in general practitioner consultations, emergency department presentations, and hospital admissions for infectious diseases as a result of rising temperatures and other climate extremes may contribute to increased and potentially unsustainable workloads among healthcare providers, thus reducing their capacity to respond to the health challenges posed by rising temperatures. Concerningly, between 33% and 44% of surveyed general practitioners in rural New South Wales, Australia reported being unsure or not believing their general practice had the capacity to adequately respond to the health consequences of an extreme weather event, such as a severe heatwave.193
However, while increasing temperatures may initially expose health workforce knowledge gaps and contribute to increasing and unstainable workloads, they also present an important opportunity to adapt healthcare professional education and training to include a stronger focus on the impacts of extreme heat on infectious disease risk and the health consequences of climate change more broadly. The aforementioned narrative review found that most (60-80%) of medical students wanted the topic of climate change and its impacts on health outcomes to be integrated into their curriculum, while a minority expressed concern that it would add additional time pressure to their already demanding studies.192 Similarly, over 70% of surveyed healthcare providers in India expressed an interest in learning about the impacts of climate change on infectious disease outbreaks.194 Among surveyed general practitioners in rural New South Wales, 71% expressed a preference for locally based seminars or workshops to provide continuing professional development and education on the health impacts of climate change.193 As the impacts of high temperatures on infectious disease become more pronounced globally, there is likely to be greater demand for healthcare providers with knowledge and experience in this field, which presents an important opportunity to develop specialised education and training programmes as part of medical curricula and professional development packages. It is critical that these programmes include material to develop and enhance health professionals’ data collection and disease surveillance knowledge, thus positively contributing to capacity building and improving the accuracy and timeliness of infectious disease surveillance data.
Healthcare system response: resourcing and collaboration
The impacts of climate change on infectious disease outcomes pose challenges to the allocation of finite health resources and necessitate greater collaboration between countries and across sectors to adequately prepare for and respond to infectious disease outbreaks.179197 A systematic review of 21 studies (including narrative reviews, evaluations, case studies, qualitative studies, and mixed methods study designs) on the adaptation of the South African health sector to climate change found scant evidence of the country’s already strained health system’s capacity to prepare for and respond to extreme weather events. It called for health sector leadership in reframing climate change as an urgent health issue requiring a comprehensive, adequately resourced response.191
A 2015 pilot study of an electronic tool to facilitate health and wellbeing risk assessments in Tasmania, Australia found that healthcare system stakeholders were concerned about the capacity of the health sector to adapt to increasing temperatures and the impacts of climate change.198 The study proposed the use of tools incorporating decision support modules to support stakeholders to develop their knowledge about health sector adaptation to climate change and improve health sector preparedness and resilience.198 It is also important to facilitate and promote collaboration between different sectors, including but not limited to, health, agriculture, meteorology, and work health and safety.
Health systems of low and middle income countries may be particularly disadvantaged with regard to their capacity to translate policies and programmes related to climate change into tangible actions due to limited interdisciplinary and intersectoral collaboration and resource constraints.199200201 Similarly, rural health departments and providers may be particularly disadvantaged with respect to the financial and human resources needed to engage in climate change preparedness and mitigation initiatives.202 Thus, additional efforts and investments may be needed to support low and middle income countries and rural and regional communities to enhance their capacity and capability to prepare for and respond to the increasing infectious disease challenges posed by climate change.202 Such efforts could include the development and implementation of targeted training courses and educational workshops for frontline healthcare workers and researchers to improve infectious disease prevention, diagnosis, treatment, and management both in the short and longer term. Additionally, infectious disease surveillance efforts could be strengthened by facilitating the sharing of information and expertise between countries through the involvement of the WHO and its regional offices.
It is equally important to engage with local communities to participate in and deliver infectious disease control and mitigation interventions. These include education about temperature related health risks and preventive strategies such as distributing mosquito nets and identifying and removing vector breeding sites, particularly in socioeconomically disadvantaged communities.198 Increasing population adaptive capacity and knowledge of the broader health impacts of increasing temperatures rather than focusing specifically on infectious diseases may promote greater community resilience to the far reaching consequences of climate change.203
Strengths and limitations of this review
This review has comprehensively summarised the impacts of increasing temperatures on a broad range of vector-borne, waterborne, and foodborne diseases of public health importance. It has also synthesised the evidence on global health and education system responses to increasing infectious diseases challenges due to rising global temperatures and climate change more broadly. The synthesis and analysis of the evidence has informed the development of key considerations and recommendations aimed at healthcare professionals, policy makers, and researchers, including the critical need to develop and refine location-specific, targeted early warning systems with integration of climatic information to support preparedness and response planning and actions, including resource allocation and workforce capacity building, particularly in low and middle income countries.
Limitations of the review include the fact that it was not a systematic review. It prioritised recent, high quality, systematic reviews and meta-analyses and observational studies. However, some important studies in this area may have been overlooked. Also, as the focus of the review was on the influence of temperature on infectious disease risk, it did not include a detailed discussion of the influence of other climatic variables such as humidity, rainfall, flooding, and wind speed that contribute to and mediate these associations. Finally, as the review was limited to a range of selected climate sensitive infectious diseases of public health importance, several other diseases that are influenced by temperature were not included, such as tick-borne diseases (such as Lyme disease), and other waterborne and foodborne diseases such as cryptosporidiosis and giardiasis.
Practical implications
As temperatures continue to increase globally due to climate change, it is critical to develop and refine robust integrated surveillance and early warning systems to enhance the capacity of health systems to prepare for and respond to temperature sensitive infectious diseases. Incorporating satellite remote sensing and geographic information systems technologies into these systems would promote enhanced understanding of the geographic distribution of cases, thus enabling resources and preventive efforts to be proactively targeted to at-risk locations and populations. Given that infectious diseases disproportionately affect socioeconomically disadvantaged regions, additional efforts and investments are needed to support low and middle income countries and rural and regional communities to prepare for and respond to increasing infectious disease challenges.
Additionally, timely and dynamic quantitative assessment of the risk of climate sensitive infectious diseases is needed to ensure that accurate, high equality evidence is available to inform targeted mitigation and control decisions and actions. Advances in artificial intelligence and machine learning technologies have the potential to contribute to enhancing timely risks assessments for infectious diseases and should be the focus of future research in this field.
Changes in healthcare systems and organisations
Given the importance of timely and transparent information sharing and collaboration within and across sectors, organisations, and agencies, barriers to efficient information and knowledge exchange must be addressed, while ensuring that confidentially and data security are protected.
Finally, greater availability and acceptance of climate change education as part of medical and health curricula and continuing professional development is needed to enable healthcare professionals to recognise and effectively respond to infectious disease challenges in the context of climate change. Including evidence based components on the multifaceted impacts of climate change on infectious diseases and other health outcomes will enhance the capability and capacity of the healthcare workforce to respond to these public health threats.
Emerging treatments
As the impacts of temperature vary considerably across different infectious diseases, pathogen-specific adaptations and treatments such as vaccinations, are needed to effectively address the challenges posed by infectious diseases in the context of rising global temperatures.71 Recent advances in this area, such as the introduction of Wolbachia into Aedes mosquitoes to prevent them transmitting dengue and Zika, as well as the introduction of a dengue vaccine (currently limited to individuals fulfilling specific criteria such as previous dengue infection), may provide additional solutions to dealing with infectious disease challenges.204 Further research focusing on the identification of host factors that interact with Wolbachia to prevent replication and transmission of dengue and Zika may inform and enable the development of novel control strategies for vector-borne diseases.204
Guidelines
No specific guidelines for the prevention, treatment, and management of infectious diseases due to high temperatures and climate change have been developed to date. However, general guidelines pertaining to reducing the negative health impacts of heat exposure have been developed, including the WHO European Region Heat-Health Action Plan Guidance, which highlights the importance of information sharing and collaboration across sectors to facilitate timely medical and public health advice, health and social system improvements, and advances in housing cooling infrastructure and urban planning.205 Additionally, general guidance from the WHO is available on the establishment of an Early Warning, Alert and Response System (EWARS) to detect infectious disease outbreaks during humanitarian emergencies more broadly, including conflicts and natural disasters; however, these systems do not specifically consider phenomena related to climate change such as increasing temperatures.206
Conclusion
Vector-borne diseases, including dengue fever, malaria, Japanese encephalitis, schistosomiasis, leishmaniasis, haemorrhagic fever with renal syndrome, West Nile fever and Zika virus disease, are notably influenced by climatic variables such as temperature, humidity, and precipitation. While there is substantial evidence on the influence of higher temperatures on the risk of many of these conditions, more research is needed to address knowledge gaps, such as to establish definitive links between climatic factors and Zika infections. From the perspective of climate change adaptation, recent advances in targeted, pathogen-specific adaptation and treatment approaches, such as dengue vaccines, are promising, although currently limited in their application. As emerging infectious diseases are often zoonotic in origin, a One Health approach fostering collaboration between the human health, animal health and environment sectors can aid in the establishment of integrated surveillance and response systems to address climate change driven disease threats.207
The review highlighted that the relationship between temperature and waterborne and foodborne diseases is complex. Higher temperatures and non-optimal temperatures could increase the number of cases. Future research warrants a more comprehensive approach that considers other environmental, social, demographic, economic, cultural, and behavioural factors, and the interactions between these factors and rising temperatures, contributing to the transmission of these diseases. The impacts of large scale policies and interventions on mitigating increasing temperatures and infectious disease risk, such as those focused on biodiversity restoration and increasing greenspace in urban settings warrant further investigation.
Questions for future research
How can the incorporation of artificial intelligence and machine learning approaches into integrated disease and vector surveillance and early warning systems enhance their predictive capacity and utility to deal with climate change impacts?
Can a One Health approach be used more effectively to promote intersectoral collaboration between human health, animal health, and environment sectors to minimise challenges from zoonotic infectious disease posed by climate change?
Should regional collaborative centres be established to project future infectious disease burdens under different climate change scenarios to assist low and middle income countries to prepare for the increasing infectious disease challenges due to climate change?
Patient involvement
While patients and the public were not directly involved in this review due to its wide scope and focus on the findings and implications of previous studies and systematic reviews on the topic, the authors acknowledge the importance of actively involving community members in future research on addressing the wide ranging negative impacts of increasing temperatures on infectious diseases to ensure consumer perspectives and lived experiences inform study designs as well as policy and practice recommendations.
Footnotes
State of the Art Reviews are commissioned on the basis of their relevance to academics and specialists in the US and internationally. For this reason they are written predominantly by US authors.
Contributors: All authors contributed to the planning, conduct, and reporting of this review. BV and JX led the conduct and reporting of the vector-borne diseases section of the review, MB and YZ led the waterborne and foodborne diseases section, and OA and PB led the healthcare systems response section. OA, AH, and PB were responsible for the initial drafting and editing of the full review, while AH and PB led the identification of future research directions. All authors read, edited, and approved the final version of the manuscript. PB, as the guarantor, accepts responsibility for the overall content of this review.
Competing interests: We have read and understood the BMJ policy on declaration of interests and declare that we have no competing interests.
Provenance and peer review: Commissioned; externally peer reviewed.