Impact of Anthropogenic Environmental Alterations on Vector-Borne Diseases

Abstract

The spread of infectious vector-borne diseases involves at least 3 organisms: a parasite, a vector, and a host. Alterations to the natural environment may change the context within which these entities interact, thus potentially affecting vector-borne disease epidemiology. In this review, examples are presented in which human-driven ecological changes may be contributing to the spread of vector-borne diseases. Such changes include deforestation, agriculture and animal husbandry, water control projects, urbanization, loss of biodiversity, introduction of alien species, and climate change. The global environment is currently being degraded at an alarming pace, potentially placing human populations at increasing risk for unnecessary and preventable outbreaks of vector-borne diseases. Further research is needed to improve our ability to predict and prevent emergence and reemergence of vector-borne diseases from environmental alterations.

Introduction

Over the past several decades, a number of vector-borne diseases have reemerged in locations in which they were declining or have emerged in areas in which the disease was previously not known.[1] Understanding the factors contributing to these alarming observations is vital to preventing further spread of vector-borne diseases. Vector-borne diseases are unique among human diseases because of the extent to which they depend on the natural environment. Ecological alterations directly or indirectly affecting populations of the pathogen, the vector, or the nonhuman hosts of the pathogen may culminate in altered epidemiology of vector-borne diseases afflicting humans.[2]

This paper reviews human-driven ecosystem alterations that may increase the transmission of vector-borne diseases. The term “vector” refers to organisms that transfer a pathogen from one host to another.[3] The environmental disturbances to be discussed include: (1) deforestation, (2) agriculture and animal husbandry, (3) water control projects, (4) urbanization, (5) loss of biodiversity, (6) introduction of alien species, and (7) climate change. These alterations are diverse but are often interrelated.[2] While some have primarily local effects (such as water control projects) and others global (such as climate change), all of these disturbances are exacerbated by a rapidly expanding human population.[4–6]

The inherent complexities of the global environment and infectious disease transmission make predictions regarding the impact of the former on the latter at times uncertain and imprecise.[6] Nonetheless, through an interdisciplinary approach, the major ecological variables and patterns affecting transmission of vector-borne diseases can be identified.[2,4,7,8]

Deforestation

Deforestation may bring about whole-scale ecosystem reconstitution. This in turn may influence vector-borne disease transmission through altered vegetation, introduction of livestock, development of human settlements, and loss of biodiversity. Forest-related activities, such as mining and logging, have been associated with increased exposure to the vectors of yellow fever, malaria, and leishmaniasis.[2,8,9]

Deforestation may create ecological niches favoring proliferation of vectors and parasites.[9] For example, water puddles in deforested areas tend to have lower salinity and acidity than puddles in forests. Such deforested water puddles may be more conducive for the larval development of certain Anopheles mosquito species (the vectors of malaria), particularly A darlingi, the most effective vector of malaria in the Amazon.[1,2,9]

The blackfly vectors of onchocerciasis found in savannahs preferentially transmit the more severe form of the disease compared with forest blackflies. Reports from several African countries show that the geographical distribution of savannah blackflies has increased after deforestation.[10] Loiasis is another vector-borne disease (transmitted by tabanid flies) in which deforestation has contributed to the emergence of more efficient vector species.[2]

Increased malaria transmission has coincided with deforestation in Africa, Asia, and Latin America.[1,9] In a study of the human biting rate and distribution of A darlingi in relation to deforestation and ecological alteration in the Amazon, it was reported that the A darlingi biting rate increased in deforested areas compared with predominantly forested areas after controlling for the presence of humans.[11] In another study of Anopheles distribution, areas that were both altered and unaltered by human activity were surveyed, and A darlingi was found in all of the altered sites but in none of the unaltered sites.[12]

Agriculture and Animal Husbandry

The growing worldwide demand for food has increased the conversion of natural ecosystems into agrarian ones that suit the raising of both plants and animals.[6] The ecosystem disturbances caused by farming may favor vector-borne disease transmission through a variety of mechanisms.

Land cover changes due to agriculture can alter local microclimates. In a study conducted at high altitudes in Uganda, areas in which natural swamp vegetation were replaced by agricultural crops experienced higher temperatures. This microenvironmental change was thought to be a contributing factor to the increased risk for malaria in those cultivated areas.[13]

Animal husbandry may also increase the transmission of some vector-borne diseases. Vector populations may grow with the additional feeding options livestock offer; a larger vector population may in turn result in increased frequency of feeding on humans. Furthermore, farm animals are potential reservoir hosts, thus making pathogens more widespread.[9] When grazing extends into recently altered natural habitats, livestock may contribute to the emergence of vector-borne disease by facilitating the exchange of a pathogen from nonhuman reservoirs to humans.[2,8,9]

Transmission of Japanese encephalitis is increasing in parts of Southeast Asia and the western Pacific, largely because of increased irrigated agriculture (especially rice paddies) and pig husbandry (an important natural host of the virus). Furthermore, breeding sites within human-made structures are deemed more important for the mosquito vectors of Japanese encephalitis than natural sites.[14,15]

Water Control Projects

There are numerous examples of artificial bodies of water contributing to vector and parasite proliferation. Dams and canals form breeding sites for mosquitoes.[2,9] Smaller water impoundments are especially conducive to vector proliferation given the expansive aggregate surface area they occupy and shallow depth they provide for larval breeding.[8]

The emergence of Plasmodium falciparum malaria, the most deadly form of malaria, in the Thar Desert of India coincided with the construction of irrigation canals.[1] In addition, while there was just one anopheline mosquito species before the construction of the canals, several anopheline mosquito species have since been established.[16]

In another damaging example, an outbreak of schistosomiasis affecting thousands of people occurred after the construction of the Diama Dam on the Senegal River.[1,2,17] In Egypt, the prevalence of Schistosoma mansoni infection nearly doubled in a desert that was altered by construction of irrigation projects. Several factors are thought to have contributed to the increased prevalence of this parasite. The irrigation water originated from the Nile River and may have introduced snail vectors to the irrigated area. Furthermore, some settlers to the irrigated area may have been infected when they arrived and inadvertently contaminated the local water supply due to inadequate treatment of sewage. In contrast, other settlers may have had little or no immunity to schistosomiasis if they were not previously exposed and thus were highly susceptible to infection.[18,19]

Urbanization

Urbanization represents an ecosystem disturbance directly through the conversion of natural habitat into human settlements and indirectly through waste generation. The concentration of new urbanization in developing countries, which often lack the infrastructure to support a large, dense urban population, will present many challenges to public health.[1,4,20]

Vector-borne diseases may flourish with rapid urbanization. Expanding cities encroaching upon neighboring environments may increase exposure to some vectors and nonhuman hosts of vector-borne diseases, as has occurred with yellow fever, trypanosomiasis, and Kyasanur Forest disease.[2,4,8,9] Furthermore, migrants to new areas may lack immunity to the prevalent endemic vector-borne diseases, thus increasing their susceptibility to illness; alternatively, migrants may introduce new pathogens and vectors to their resettled locations.[1,2,9, 21–23]

Drainage of waste water is another important determinant of vector-borne disease transmission in urban locales. In resource-limited settings undergoing rapid urbanization, there is often inadequate clearance of standing water collected in used containers and tires, thus facilitating mosquito vector reproduction, a problem particularly evident for dengue and yellow fever.[2,4]

An example of disease proliferation arising from urbanization includes outbreaks of leishmaniasis in Brazil. Formerly, visceral leishmaniasis was predominantly a rural disease. However, outbreaks of the disease have recently occurred in several Brazilian cities due to massive population movement from rural areas to cities.[19,24,25] Also, some forms of cutaneous leishmaniasis typically occur as epidemics in densely populated cities in central and western Asia.[21]

Loss of Biodiversity

In simple terms, biodiversity refers to the variety of species on Earth.[5] The threats to biodiversity from human activities are many, including stratospheric ozone depletion; pollution; introduction of invasive species; global warming; and most important, habitat degradation.[5] The rate of species loss today is the highest it has been since the dinosaurs went extinct.[4]

Reduction in global biodiversity is likely to contribute to vector-borne disease transmission. One theory of how biodiversity protects against vector-borne diseases is termed the “dilution effect.” Locales with few species capable of sustaining vectors will have higher disease risk because vectors feed more frequently on the species that serve as hosts of the pathogen. In contrast, “dilution” occurs in areas with high biodiversity because more species (not all of which harbor parasites) are available to sustain vectors.[2,26] This model seems consistent with observations of the epidemiology of several vector-borne diseases, including leishmaniasis, African trypanosomiasis, Chagas' disease, West Nile virus, and Rocky Mountain spotted fever.[2,5]

Lyme disease is a bacterial infection passed through the bite of the Ixodes tick and is the most common vector-borne disease in the United States. The risk for Lyme disease is lower in areas with higher vertebrate-species diversity because not all vertebrates transmit the bacteria to the tick vector equally well, thus breaking the disease cycle. Furthermore, the population of the main reservoir host of Lyme disease, the white-footed mouse, is lower in ecosystems with more biodiversity due to the presence of mouse predators, thus lowering disease risk.[5,26] Similarly, in Lake Malawi, over-fishing has disrupted the foodweb such that snail populations have blossomed, thus increasing the prevalence of schistosomiasis.[2]

Introduction of Alien Species

Human introduction of alien species to an ecosystem occurs for a variety of reasons, from the accidental escape of an offending species to the intentional release for pest control. A nonindigenous species becomes invasive when, after establishing itself in a new environment, it subsequently begins to spread.[3] The environmental impact of invasive species can be great; invasive species are the second largest cause of biodiversity loss after habitat degradation.[27]

Nonindigenous species impact vector-borne disease epidemiology in several ways. Through their role in biodiversity loss, invasive species indirectly contribute to vector-borne disease risk. Nonindigenous species introduced by humans play a direct role in vector-borne disease transmission when the introduced species is itself a vector. This is increasingly a concern with widespread use of modern technology, such as air and sea travel, which remove the geographic barriers that previously limited vector migration.[22,28]

The Asian tiger mosquito, Aedes albopictus, is the most invasive mosquito in the world.[29] It has spread in the past 2 decades from the western Pacific and Southeast Asia to Africa, the Middle East, North and South America, and Europe.[30] This spread has occurred largely due to the international trade of used tires in which mosquito eggs have been laid. In addition to the inherent ecological problems associated with this rapid mosquito invasion, the global expansion of A albopictus poses a threat to human health. This mosquito is a potential vector for at least 22 viruses.[29,30]

A albopictus was implicated as a vector of the chikungunya virus on several Indian Ocean islands involved in a 2006 chikungunya fever outbreak. A albopictus is not the vector typically associated with chikungunya fever, but it is thought that a new variant of the chikungunya virus better adapted to A albopictus was partially responsible for the outbreak.[22,28,31] This example highlights the role shifting vector populations may play in the emergence of vector-borne diseases. More recently, in 2007 there was an outbreak of chikungunya fever in Italy by the virus variant adapted to A albopictus. This was the first-ever reported outbreak in a temperate country. This mosquito was first introduced in Italy in 1990 through tires imported from the United States; it is now widespread in Italy.[31,32]

Climate Change

There is a wealth of evidence that human activities, in particular the emission of greenhouse gases, are causing climate change.[33,34] Climate change will have a wide-ranging impact, from warmer global temperatures to altered hydrological patterns.[9,35] Vector-borne disease epidemiology is inherently dependent on climate, as the life cycles of many vectors are affected by ambient meteorologic conditions.[34]

The overall effect of anthropogenic climate change on vector-borne diseases remains debated, and the outcome may vary regionally.[4,8,9, 34–38] Nonetheless, there appears to be an overall expansion of the global distributions of malaria, various mosquito- and tick-borne encephalitides, and yellow fever that is at least partially attributable to rising global temperatures.[2]

Modeling serves an important role in predicting the impact of anthropogenic climate change on vector-borne disease epidemiology. One such model predicts that transmission of schistosomiasis may be increasing in nonendemic areas of China due to climate change.[33] Another model anticipates that dengue fever incidence will increase worldwide secondary to climate change.[39]

Warmer temperatures are associated with altered rates at which mosquitoes reach sexual maturity, frequency of mosquito blood meals, and rates at which parasites are acquired, as well as shortened incubation time of parasites within mosquitoes. These factors together can favor transmission of mosquito-borne diseases.[2,4,9,13,23,35, 37–39] Similarly, increased precipitation associated with global warming may benefit mosquito populations by increasing the number of breeding sites.[1,9]

The impact of climate change on malaria is of special concern given its high global distribution.[4] Although in the past the lower temperatures at high altitudes in Africa have limited the expansion of malaria vectors, there are recent reports of malaria epidemics occurring in these previously unaffected areas, perhaps in part due to higher temperatures and increased precipitation.[4,34] The International Panel on Climate Change has warned that climate change may continue to increase the incidence of malaria in areas of high altitude.[36,40]

Climate change may alter the distribution of vector-borne disease by affecting nonhuman hosts. Plague is a bacterial disease transmitted to humans typically by fleas from rodents. In a study of the incidence of human plague in New Mexico in relation to precipitation, the number of human plague cases was positively associated with higher-than-normal winter-spring precipitation, perhaps because the wetter conditions favored rodent breeding.[41]

The El Niño weather cycle provides further evidence of the importance of climate on vector-borne disease transmission. While differences exist in the changes effected by anthropogenic climate change and El Niño and the time scale over which they occur, El Niño is a helpful model to investigate the impact of climate on infectious diseases given the short period over which it exerts its effects.[4] El Niño has driven heat waves and drought in parts of Africa and Asia as well as heavy rains and floods in South America.[4] In the Asia-Pacific region, El Niño has impacted dengue fever outbreaks.[23] In South America, Asia, and Africa, malaria transmission is sensitive to the climate variability from El Niño. Additionally, the frequency and severity of El Niño events is expected to increase with anthropogenic climate change.[34,35]

Conclusion

The pace at which we are degrading the global environment is accelerating. Under these circumstances, vector-borne diseases represent a significant risk to public health due to their inherent dependence on the global environment. The evidence reviewed here indicates that in many instances the transmission of vector-borne diseases will increase with human-driven environmental alteration. We must remain cautious in our interactions with the biosphere to ensure that we do not bring about unnecessary outbreaks of serious vector-borne diseases. Further research is necessary so that we can predict and prevent emerging and reemerging vector-borne diseases due to environmental damage.