Climate, Environment and Transmission of Malaria

Le Infezioni in Medicina, n. 2, 93-104, 2016 Review 93

Climate, environment and transmission of malaria

Antonella Rossati1, Olivia Bargiacchi1, Vesselina Kroumova2, Marco Zaramella1, Annamaria Caputo3, Pietro Luigi Garavelli1 1Infectious Diseases Unit, “Maggiore della Carità” University Hospital, Novara, Italy; 2Infection Control Unit, “Maggiore della Carità” University Hospital, Novara, Italy; 3Internal Medicine, ASL TO3, Rivoli Hospital, Italy

SummaRY

Malaria, the most common parasitic disease in the tor Anopheles includes 465 formally recognised species. world, is transmitted to the human host by mosquitoes Approximately 70 of these species have the capacity to of the genus Anopheles. The transmission of malaria transmit Plasmodium spp. to humans and 41 are con- requires the interaction between the host, the vector sidered as dominant vector capable of transmitting and the parasite. The four species of parasites respon- malaria. The intensity of transmission is dependent sible for human malaria are Plasmodium falciparum, on the vectorial capacity and competence of local mos- Plasmodium ovale, Plasmodium malariae and Plasmodium quitoes. An efficient system for malaria transmission vivax. Occasionally humans can be infected by sever- needs strong interaction between humans, the ecosys- al simian species, like Plasmodium knowlesi, recognised tem and infected vectors. as a major cause of human malaria in South-East Asia Global warming induced by human activities has in- since 2004. While P. falciparum is responsible for most creased the risk of vector-borne diseases such as ma- malaria cases, about 8% of estimated cases globally are laria. Recent decades have witnessed changes in the caused by P. vivax. The different Plasmodia are not uni- ecosystem and climate without precedent in human formly distributed although there are areas of species history although the emphasis in the role of tempera- overlap. The life cycle of all species of human malar- ture on the epidemiology of malaria has given way to ia parasites is characterised by an exogenous sexual predisposing conditions such as ecosystem changes, phase in which multiplication occurs in several species political instability and health policies that have re- of Anopheles mosquitoes, and an endogenous asexual duced the funds for vector control, combined with the phase in the vertebrate host. The time span required presence of migratory flows from endemic countries. for mature oocyst development in the salivary glands is quite variable (7-30 days), characteristic of each spe- Keywords: malaria, climate changes, vector borne dis- cies and influenced by ambient temperature. The vec- eases.

n INTRODUCTION gion (12%) and the WHO Eastern Mediterranean Region (5%). Plasmodium falciparum is responsible alaria is the most common parasitic disease for most of the cases of malaria, but about 8% of Min the world. The parasite is transmitted estimated cases globally are caused by Plasmodi- to the human host by mosquitoes of the genus um vivax. Outside of the African continent this Anopheles. proportion increases to 47% [1]. The WHO reported in 2013 an estimated 198 mil- Although only P. falciparum is considered life- lion of cases of malaria occurred worldwide. Most threatening, the lack of severe complications as- of these cases (82%) were in the WHO African Re- sociated with P. vivax infection has been recently gion, followed by the WHO South-East Asia Re- questioned in several reports [2]. Indeed, it is an important cause of early pregnancy loss, reduced birth weight, severe disease and Corresponding author death in pregnant women and small children [3-6]. Antonella Rossati Vector borne diseases such malaria are highly in- E-mail: [email protected] fluenced by climatic factors, which enhance their 94 A. Rossati, et al.

transmission rate and extend their geographic high endemic countries to areas where the trans- presence. However to understand the epidemiol- mission is lower or absent. ogy of malaria others factors must be considered, Occasional focal outbreaks might occur when ma- like human activities and their impact on local laria transmission extends from the forest shade (ni- ecology. Climatic factors, especially temperature, dus) to peri-urban and urban areas, where the much play a crucial role on the survival of mosquitoes higher density of human population and presence and their longevity, but they also exert an influ- of vectors could fuel large epidemics [9, 10]. ence on the rate of multiplication of the parasite into the vector. In cold countries, mosquitoes and The Parasite parasite have developed strategies to survive Plasmodium species during the winter, and on the other extreme, to Approximately 250 species of Plasmodium are survive during the dry season [7]. presently believed to be parasites of mammals, Temperature, rainfall, and humidity are im- birds, and reptiles. More than 30 species of Plas- portant, as well as the wind and the duration of modium have been reported in non-human pri- daylight. The circadian rhythm affects other be- mates, including apes, gibbons, and New and haviours of the vector, such as feeding, resting, Old World monkeys. It is believed that all kind and oviposition which are restricted to optimum of malaria in the primates are transmitted only by times, regardless of ambient temperature. Anopheles mosquitoes [11]. Every single element that influences the climate Traditionally the four restricted or adapted spe- and with it the entire ecosystem, is strongly al- cies recognized as responsible of human malaria tered by humans and their activities. are P. falciparum, P. ovale, P. malariae and P. vivax. Although forest ecosystems are well known to Occasionally humans can be infected by several support transmission of malaria, significantly simian species such as P. cynomolgi cynomolgi, P. contributing to the global disease burden, the for- cynomolgi bastianelli, P. simiovale, P. brasilianum, P. est clearance can provide favourable conditions to schwetzi, P. inui and P. knowlesi that emerged as mosquitoes. Vectors that prefer temporary ground an important cause of human malaria in South- pools exposed to full sunlight like Anopheles can East Asia, especially the Malaysian Borneo since find a better condition to larval development, and 2004. The life cycle of all species of human ma- the proximity of vegetation near human habita- laria parasites is characterized by an exogenous tion can increases the population of forest vectors sexual phase (named sporogony) in which mul- of malaria [8]. tiplication occurs in several species of Anopheles Additional factors come from behaviour and cul- mosquitoes, and an endogenous asexual phase tural traits of the exposed population: daily activ- (named schizogony) which takes place in the ver- ity patterns, the location of homes in relation to tebrate host [12]. mosquito breeding sites, the kind of housing, the availability of bed nets and the access to the health Distribution of plasmodia care system. A crucial role is played by the water The different Plasmodia are not uniformly distrib- employed for agriculture and livestock. Drainage uted, although there are areas of overlap of the of wetlands can eliminate the breeding sites of the species. vector. Forest clearance provides a new habitat for vectors of malaria and changes the local microcli- Plasmodium falciparum mates by reducing the shade, altering the rainfall Eighty-five countries are actually classified as en- patterns, augmenting air movement. Humidity demic for P. falciparum malaria with 2.57 billion changes and proximity of cattle to human habi- people living in area at risk for transmission of tation can shift the behaviours of the anophelines this infection. Of these, 1.44 billion people lives in vectors from feeding on animals to feeding on hu- area of stable transmission, mainly in Africa (52% man host. of the global total) and Central, South and East Moreover, migration, urbanization, degradation Asia (46%) [13, 14]. of the health infrastructure, war, civil strife, and Once considered strictly human specific, P. falci- natural disasters can highly impact on malaria parum can infect bonobos, chimpanzees and goril- transmission by moving infected people from las and thus these African apes might serve also Climate, environment and transmission of malaria 95

as possible reservoir for the malignant form of sia, where P. vivax hibernans was present (in Fin- human malaria [15, 16]. land the last case of malaria was reported in 1954) [19]. Another hypothesis explaining the relapse Plasmodium vivax periodicity is that latent hypnozoites are activat- Of all malaria species that infect humans, P. vivax ed by a systemic febrile illness, thus interpreting is the most geographically widespread. Compared the large number of P. vivax relapses that follow P. with the more virulent P. falciparum, P. vivax toler- falciparum infections in tropical areas [20]. ates a wide range of temperature environmental (minimum: 16°C vs. 21°C for P. falciparum), which Plasmodium ovale may explain its broader distribution. Alternative- Humans are the only natural hosts of P. ovale. ly, this distribution may reflect a longer historical Their natural distribution is in Sub Saharan Africa association with humans. According with phy- and in the islands of the western Pacific. Anopheles logenetic analysis of Mu et al., P. vivax became a gambiae and A. funestus are the likely natural vec- human parasite via a host switch from Asian ma- tors. Infection to anopheline mosquitoes outside caques [17]. its geographic distribution is possible, and thus In endemic areas of Asia, Oceania, Central and the reasons for geographic isolation are not due to South America, and in the horn of Africa P. vivax vector incompetence [21]. Previous infection with malaria remain a major cause of morbidity [18]. It P. ovale did not prevent reinfection but resulted in is present throughout the tropics with low rate of reduced levels of parasitemia and fever. Previous infection in western and central sub-Saharan Afri- infection by other Plasmodium spp. did not prevent ca. The high proportion of Duffy-negative people infection; there was some reduction in the fre- in West and Central Africa has long be viewed as quency and intensity of fever and parasite counts. the most plausible explanation of the rarity of P. It has been estimated that the global burden of P. vivax malaria in those geographical areas [12]. ovale in Africa might exceed 15 million cases an- It is more difficult to control and eliminate P. vi- nually [22]. vax than P. falciparum because of its tendency to relapse after resolution of the primary infection. Plasmodium malariae There is significant geographical variation in the P. malariae has developmental cycles in the mos- rate at which a “strain” of P. vivax relapses. quito and in the primate host. P. malariae infection Temperate and subtropical strains often exhib- has been observed in all major malaria-endemic it either a long incubation or latent period of regions of the world where P. falciparum is also around eight to ten months. Tropical strains are present. In the recent past, it was prevalent in Eu- characterized by short incubation times and short rope and in southern parts of the United States. latency (approximately three to six weeks). Trop- Actually it is widespread throughout sub-Saharan ical strains relapse more rapidly than temperate Africa, much of southeast Asia, into Indonesia, strains and New World strains vary from those in and on many of the islands of the western Pacific. the Old World. It is also reported in areas of the Amazon Basin Relapse periodicity varies according with geo- of South America, along with Plasmodium brasil- graphic region and is categorized in nine global ianum, a parasite commonly found in New World regions with similar malaria transmission dy- monkeys. This parasite is apparently the same namics. species as P. malariae that has naturally adapted How hypnozoite relapse is triggered, and the to grow in monkeys following human settlement source of this phenotypic variation, is unresolved. of South America within the last 500 years. The One theory is that the mechanism is an adaptive ready passage of P. brasilianum to humans and trait of the parasite to sequester or “hibernate” the passage of P. malariae to New World monkeys during times when climatic conditions would be indicate that such interspecies transmission be- inhospitable to the parasite’s anopheline vectors. tween primates and humans is both feasible and This potential for long-term latency provides the probable [23]. obvious advantage of safe harbour during cold P. malariae has been characterized to exhibit op- winter months and this theory would explain the posing seasonal fluctuation with P. falciparum, presence of malaria in northern Europe and Rus- with prevalence of P. malariae and/or parasite 96 A. Rossati, et al.

densities increasing in the dry season. Outside Af- The vector rica there has been no report of opposing seasonal In nearly all mosquito species, the female obtains fluctuation in the prevalence of P. malariae and P. the protein she needs for the development of her falciparum infections [19]. eggs by feeding on vertebrate blood. During this meal, an infected anopheline vector can transmit Plasmodium knowlesi the parasite to a host. P. knowlesi, a simian plasmodium that infects for- The life cycle of all species of human malaria par- est macaque monkeys (Macaca fascicularis, Maca- asites is characterized by an exogenous sexual ca nemestrina, Trachypithecus obscurus, Presbytis- phase (named sporogony), occurring in several melalophus), is now recognized as an important species of Anopheles mosquitoes, and an endog- cause of human malaria not only in the Penin- enous asexual phase (named schizogony) which sular Malaysian Borneo but also in other parts of take place in the vertebrate host. South-East Asia. The sexual development of malaria parasite (spo- The first case of a naturally acquired P. knowlesi in- rogonic cycle) will be completed only when ma- fection was described in 1965, but it was not iden- ture female and male gametocytes of Plasmodium tified until 2004 when Singh et al. have detected spp. will be ingested by a biologically suitable spe- 120 individuals with malaria as single or mixed P. cies of female Anopheles mosquito during a blood knowlesi infections [24]. meal. Furthermore, although they are not epidemiolog- The genus Anopheles includes 465 formally rec- ically important, some plasmodia of monkeys can ognised species and more than 50 unnamed infect humans. Thuy et al. first have described a members of species complexes. Approximately woman with naturally acquired human infection 70 of these species have the capacity to transmit by Plasmodium cynomolgi [25]. human malaria parasites and 41 are considered

Figure 1 - Distribution of predominant malaria vectors. Climate, environment and transmission of malaria 97

Table 1 - The 41 dominant vector species/species Table 2 - Time required to development of mature complexes (DVS) per region. oocyst and temperature Anopheline species or species complex Sporogonic cycle Sporogonic cycle at 28°C at 20°C AMERICAS P. falciparum 9-10 days 22 days An. freeborni An. pseudopunctipennis P. vivax 8-10 days 16 days An. quadrimaculatus P. malariae 14 days 30-35 days An. albimanus P. ovale 12-14 days – An. albitarsis An. aquasalis An. darlingi An. marajoara as dominant vector species/species complexes An. nuneztovari (DVS), capable of transmitting malaria at a level of major concern to public health (Figure 1 and Total DVS: 9 Table 1) [26]. EUROPE AND MIDDLE-EST A mosquito blood meal is, on average, 2 to 3 μL, An. atroparvus and should contain at least one male and one fe- An. labranchiae male gametocyte to be infective. Host location by An. messeae the mosquito is mediated by physical (heat, mois- An. sacharovi An. sergentii ture, visual) and chemical cues that play a role An. superpictus during orientation and landing. It is known that Total DVS: 6 skin bacteria play an important role in the production of human body odour and that they convert AFRICA non-volatile compounds into volatile compounds An. arabiensis with characteristic smells [27]. An. funestus The time span required to development of ma- An. gambiae ture oocyst in the salivary glands is quite variable An. melas An. merus (7-30 days), characteristic of each species and in- An. moucheti fluenced by ambient temperature (Table 2) [12- An. nili 28,29,30]. Total DVS: 7 The temperature influence the cycle of Plasmo- ASIA dium because it affects the duration of the sporogonic cycle and the longevity of the vector. For An. barbirostris An. lesteri P. falciparum, the development stops at 16°C, but An. sinensis transmission below 18°C is unlikely because few An. aconitus adult mosquitoes survive the 56 days required to An. annularis complete sporogony at 16°C and because mosqui- An. balabacensis to abundance is limited by long larval duration. An. culicifacies Although the sporogonic cycle takes less than a An. dirus week above 32°C, the vector population turnover An. farauti C the daily survival An. flavirostris and mortality are high. At 40° An. fluviatilis of mosquitoes is not possible. The higher devel- An. koliensis opment threshold for the parasite is of 32°C for P. An. leucosphyrus falciparum and of 33°C for P. vivax [31]. An. maculatus group An. minimus Vectorial capacity An. punctulatus In human malaria, the intensity of transmission An. stephensi An. subpictus is highly dependent on the vectorial capacity An. sundaicus and competence of local mosquitoes. Most mosquitoes are dead ends for the parasite, and only Total DVS: 19 a limited number of Anopheles is able to transmit TOTAL: 41 plasmodium to humans. 98 A. Rossati, et al.

The major aspects of vectorial capacity and com- in 1848. Spleen rate is defined as proportion of a petence in Anopheles are: the vector longevity, the sampled population with palpable enlargement duration of sporogonic development, the contact of the spleen, reflecting the prevalence of the in- between the mosquito and vertebrate host suit- fection, found during a malariometric survey. If able for the parasite and the susceptibility/resis- splenomegaly in the 2-9 year-old age-group is tance of the vector to the parasite. found in more than 75% of the subjects examined Vectorial capacity and competence also present malaria is holoendemic, between 51-75% is hype- quantitative features in the sense that some spe- rendemic, 11-50% is mesoendemic and less than cies have a major role in malaria transmission 10% is hypoendemic. than others. Even at the species level, some popu- Another classification was developed by Macdon- lations or individual mosquitoes can have differ- ald. He showed that the stability of malaria was ent impacts on transmission. determined by the average number of feeds that Plasmodium infection can reduce the vectorial a mosquito takes on a human being during its life. longevity of Anopheles but this effect is balanced This vector-based index distinguish stable malar- when the vector live enough to become infec- ia (insensitive to natural and man-made pertur- tious [32]. bations, with values more than 2,5) from unstable malaria (very sensitive to climate and very Entomological parameters amenable to control, with values less than 0,5). Distribution, abundance, feeding behaviour, host Between these extremes is intermediate stability preference, parity status and human-biting, and [34]. infection rates are among the medical entomolog- The stable endemic malaria occurs in regions ical parameters essential factors in determining where the anophelines are anthropophilic and the vectorial competence of natural populations. have a high survival rate. Temperature and hu- An efficient system for malaria transmission needs midity are generally high and with relatively lit- a strong interaction between human and infected tle seasonal variation. vectors. In Africa the principal malaria vectors be- The great efficiency of the transmission makes long to the Anopheles gambiae complex and to the hard to control the spread of malaria. The trans- Anopheles funestus group. Humans, mosquitoes mission rate is high but severe and fatal illness and Plasmodium coexist from thousands of years are generally limited to children and people and have therefore developed and efficient sys- coming from non immune countries because tem for malaria transmission. These vectors feed older inhabitants who survived multiple infec- almost exclusively indoors at night, on sleeping tions maintain a high degree of immunity. humans. Changes in mosquito biting behaviour From the other side, unstable malaria occurs in re- have been shown to be immediately and directly gions where the anopheles are less anthropophilic induced by vector control tools, especially when and prefer to bite animals. Transmission rates can excito-repellent insecticides are used. vary greatly and when an epidemic occurs the The propensity to bite indoors is referred to as en- lack of immunity in the population is responsible dophagy, the propensity to bite during the night of more severe disease. when people usually sleep is referred to as noc- turnality and the propensity to bite human host is Entomological inoculation rate referred to as anthropophagy [33]. The most direct way of detecting human exposure Parity status is a proxy of the survival time of to infectious bites and mosquito population mon- adult female mosquitoes and determines wheth- itoring are the entomological inoculation rates er a parasite has sufficient time to complete its (EIR), defined as the product of man biting rates life cycle within the mosquito, thus determining (Ma) and the sporozoite rate (SR, proportion of whether the mosquito will serve as an effective mosquitoes carrying sporozoites): vector. EIR = Ma x SR The human host-epidemiology Unfortunately, under conditions of very low ma- The determination of the spleen rate to quantify laria transmission the EIR suffers from well recog- malaria endemicity was first introduced in India nized limitations [35-37]. Climate, environment and transmission of malaria 99

The environment ters that influence small-scale hydrology and mi- Malaria in urban setting croclimate. The process of urbanization includes physi- Vegetation has a critical role in determining rain- cal landscape modification and transformation. fall partitioning and is one of the primary deter- Moreover, urbanization involves significant so- minants of runoff because water availability in cio-economic change that generally improves temporary pools creates a breeding habitat for the health, housing and increase wealth. These fac- mosquitoes. tors, common to urban areas, cause marked ento- Variable amounts of shading, temperature, and mological, parasitological and behavioural effects evaporation are mechanisms by which land use and reduce malaria transmission both within the affects the surface microclimates that can influ- urban core and surrounding peri-urban areas [38]. ence malaria transmission. The need of clear water for the breeding site of Not only land use type, but also spatial relations Anopheles mosquito is believed to be a major between land use and breeding habitats may have factor that generally reduces the development an important influence on runoff, reaching malar- of anopheline larvae in urban setting. Although ia vector breeding habitats in water-limited envi- there is an evidence of decreasing from rural to ronments. urban areas, and transmission intensity is on the Vegetation and landscape characteristics are crit- average eight times greater in African rural areas ical environmental components that contribute than in urban centres, malaria transmission still to dynamic spatial variability in host, vector, and occurs in most urban settings. Where the urban- pathogen populations, by altering feeding pat- isation is rapid and unplanned, poverty, deterio- terns, habitat availability, dispersal and disper- rating infrastructure and overcrowding are some sion, and microclimates [45-47]. of the factors that contribute to the development To answer the need of food in the African con- of anopheline breeding sites. Anopheles gambiae tinent, many governments have sought ways of spp. can adapt to a wide range of polluted water. improving agricultural production by initiating Anopheline larvae can survive under conditions large-scale irrigation projects. The irrigation has that modify their habitat, like water contaminated often been blamed for aggravating malaria trans- with human faeces and oil from petrol tanks [39]. mission in local communities, but available evi- Anopheles gambiae spp. have developed tolerance dence suggests that this happens only in areas of to increasing levels of heavy metal such cadmi- unstable transmission. This apparent paradox is um, copper and lead, but this resistance has a sig- explained by a number of factors, including the nificant biological cost. previous immunity of the population and wide- Although pollution can adversely affect the mos- spread use of bednets and antimalarial drugs in quito’s ecological performance and fitness, grow- villages where the residents become wealthier ing evidence suggests that A. gambiae is expand- due to income generated from agricultural pro- ing its ecological niche into polluted habitats and duction. On the other hand, availability of water adaptation of this mosquito to the urban environ- increase the number of vectors and lead to in- ment is now a real threat [40]. creased cases of malaria in areas of unstable transmission, where people have little or no immunity Change in land use to malaria parasites [48]. Land use has been investigated as a driver of changes in mosquito population dynamics. Dif- Climate ferent studies in Kenya have shown a local in- Among five major factors characterizingAnophe - crease in temperature and humidity, altering the les population dynamics (temperature, moisture, development and densities of local vector popu- nutrient competition, predation and diseases, dis- lations as a consequence of deforestation [41-43]. persal), two are strictly connected with climate. In Uganda higher temperatures, higher mosquito Temperature is a critical regulator of growth and densities, and higher malaria transmission were development within each stage, in determining observed in cultivated than in natural swamps [44]. the end of one stage and the beginning of the next Changes in land cover affect land surface energy and in regulating the length of the gonotrophic and water balances, by altering physical parame- cycle [49]. 100 A. Rossati, et al.

Temperature affects the mosquitoes at each stage Because lower temperatures have a limiting effect of their life-cycle. If the temperature of the wa- on transmission of malaria, highland areas where ter where mosquitoes lay their eggs is too hot or average temperature is below a threshold are of- cold, then fewer eggs hatch. After the egg stage, ten malaria free. Although vectors such as A. gam- mosquitoes develop into larvae and then pupae. biae have been reported at altitudes up to 3,000 The temperature has also been shown to affect the m above sea level, endemic malaria disappears time it takes to transition between these stages above 1,800-2,000 m and human populations liv- with the optimum water temperature for survival ing in these areas have low degree of acquired and shortest transition between larvae and pupae immunity. These populations experience high being between 22°C and 26°C [50]. In the range of rates of morbidity and mortality as a result of epi- 18°C to 26°C, a change of only 1°C in temperature demics, and clinical picture of severe disease [57]. can change a mosquito’s life span by more than a The International Panel on Climate Change has week [51]. concluded that there is likely to be a net extension Specific temperature ranges are also important for in the distribution of malaria in areas of high al- the development of the parasite in the mosquito. titude where P. falciparum transmission is limited It has been shown that the optimum range for by low temperature. parasite development is between 25°C and 30°C. In recent decades, outbreaks of malaria have been The minimum temperature observed for surviv- reported from many mountain regions of Kenya, al for P. falciparum is 18°C and the maximum has Uganda and Rwanda, but a high degree of tem- been reported at 40°C [52]. poral and spatial variation in the climate of East However, while the temperature is a variable that Africa suggests further that claimed associations affects the development of both the vector popu- between local malaria resurgence and regional lation and the parasite within the vector, because changes in climate are overly simplistic [58-60]. the parasite develops inside the mosquito’s sali- Increases in malaria have been attributed to mi- vary glands, only the temperature is a factor lim- gration, breakdown in both health service provi- iting or favoring the growth of the parasite. The sion and vector control operations and to defor- life cycle of the parasite is therefore independent estation. Economic, social and political factors of the availability of water and moisture. can therefore explain recent resurgence in malaria Temperature close to 40°C recorded in small pools rather to climate change [61]. exceeds thermal death point of many species, in- Existing models will tend to underestimate mos- cluding A. funestus. This may help to explain why quito population growth under current condi- these species are rarely found in small pools and tions, and may overestimate relative increases in if the temperature of water is above 40°C [53]. population growth under future climate change. The cut-off of survival for Anopheles eggs in dry Paaijmans et al., suggest that although widely soil is of 15 days, but some African regions where used, air temperature alone does not provide an malaria is endemic experience drought periods appropriate variable for estimating immature longer than two months. Here the survival of mosquito development or for setting threshold Anopheles seems to be allowed by adult aestiva- temperatures. Mean water temperature in typical tion [54]. Survival rate may also be reduced when mosquito breeding sites was 4-6°C higher than the hot weather is accompanied by low humidity, but mean temperature of the adjacent air, resulting in in areas where such conditions are normal, local larval development rates, and hence population species have adapted to cope with them [55]. growth rates, that are much higher than predicted based on air temperature. A temperature-de- Global warming pendent population dynamic model demonstrate Climate changes induced by human activities that a small change in mean ambient air tempera- have focused the risk of increasing burden of vec- ture of just 0.5°C could translate into a 30-100% tor-borne diseases, and especially on malaria. increase in mosquito abundance. The use of air Climate based models have predicted that in- temperature rather than water temperature will creases in temperature and changes in rainfall tend to underestimate current mosquitoes growth patterns will result in a longer malaria season for rates, while strongly overestimating the impact of many sub-Saharan African regions [56]. warming on population growth rates [62]. Climate, environment and transmission of malaria 101

external temperature, the presence of vectors suitable for the transmission and susceptible hosts are the elements required by the parasite to complete its life cycle. Instead several are the factors required to ensure the survival of mosquitoes in the environment and the outdoor temperature is only one of many. The third actor, humans suffer only the indirect consequences of climate change in the case of vector-borne diseases. Extreme weather events such as floods and dry- ness can trigger migration of populations, but without the vector and the parasite, there will be no changes in transmission of the disease. Where malaria has been eradicated in the last century, the improvement of living conditions, the ability to clean up the environment, the access to drugs and the stability of borders have been crucial [65-68]. The reintroduction of malaria in already declared malaria-free countries has been indeed Figure 2 - Interactions between human host, vector the result of political instability (countries of the and parasite. former USSR) or the consequence of health policies that have reduced the funds for the vectors Models considering A. gambiae vector complex control joined to the presence of migratory flows species estimate that climate change effects on from endemic countries [69-73]. In contrast, the African malaria vectors shift their distributional distribution of mosquito nets, the wide availabil- potential from west to east and south. Although ity of highly effective antimalarial drugs such as is likely a reduction of the malaria burden, these artemisinin derivatives has led to the reduction of epidemiological changes will pose novel public malaria cases and mortality [74]. health problems in areas where it has not previously been common (Figure 2) [63]. n CONCLUSION n DISCUSSION The emphasis about the role of temperature on the epidemiology of malaria has been reduced Last decades have witnessed changes in the eco- in light of other conditions directly or indirectly system and climate without precedent in human linked to other aspects of climate, to changes of history. The implications of these changes on hu- the ecosystem, and to the improvement of sani- man health have been widely investigated and tary and economic conditions. If it is not possible especial emphasis has been placed on a potential to say in absolute terms that rising temperatures increase in distribution of vector-borne diseases will cause an increase in cases of malaria it must such as malaria [64]. be noted that it would lead to ideal conditions The transmission of malaria requires the interac- for malaria transmission also in regions where tion between the host, the vector and the parasite. the disease is not reported. In tropical regions the The parasite, which completes the sporogonic cy- temperature increase might even be unfavorable cle inside the mosquito and asexual cycle in the to the survival of the vector. To predict the future human host, cannot complete their development epidemiological scenarios we need more complex outside of a range of temperatures which are dif- models than those based merely on the tempera- ferent depending on the different Plasmodium spe- ture and above all it will be necessary ensure ac- cies. P. vivax has developed strategies that allow cess to treatment and health facilities to the peo- him to survive the winter in cold climates. The ple affected. 102 A. Rossati, et al.

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