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Malaria on the move: human population movement and malaria transmission.

Reports of malaria are increasing in many countries and in areas thought free of the disease. One of the factors contributing to the reemergence of malaria is human migration. People move for a number of reasons, including environmental deterioration, economic necessity, conflicts, and natural disasters. These factors are most likely to affect the poor, many of whom live in or near malarious areas. Identifying and understanding the influence of these population movements can improve prevention measures and malaria control programs.

Malaria, the world's most prevalent vector-borne disease, is endemic in 92 [ILLEGIBLE TEXT] with pockets of transmission in an additional eight countries (1). Approximately the world's population is at risk, and each year 300 million to 500 million [ILLEGIBLE TEXT] of malaria, [is greater than] 90% of them in Africa, are reported. Worldwide, approximately 2 m deaths per year can be attributed to malaria, half of these in children under 5 year age.

Historically, population movement has contributed to the spread of disease (2). [ILLEGIBLE TEXT] to consider this factor contributed to failure of malaria eradication campaigns in [ILLEGIBLE TEXT] 1950s and 1960s (3). The movement of infected people from areas where malaria still endemic to areas where the disease had been eradicated led to resurgence of disease. However, population movement can precipitate or increase malaria [ILLEGIBLE TEXT] in other ways as well. As people move, they can increase their risk for acquiring disease through the ways in which they change the environment and through the technology they introduce, for example, through deforestation and irrigation [ILLEGIBLE TEXT] Such activities can create more favorable habitats for Anopheles mosquitoes; at [ILLEGIBLE TEXT] time, workers may have increased exposure to the vector. Furthermore, people [ILLEGIBLE TEXT] inadvertently transport infectious mosquitoes to malaria-free areas, reintroducing disease. Population movement is also increasingly implicated in the spread of [ILLEGIBLE TEXT] resistance in malaria (5).

The unprecedented increase in mobility in the last few decades has led to greater concern about the relationship between mobility and malaria. There are a number reasons for increased mobility. First, sophisticated forms of transport now permit swift movement of people over huge distances. Air travel has increased by [ILLEGIBLE TEXT] year in the last 20 years and is predicted to increase by [is greater than] 5% a year during the [ILLEGIBLE TEXT] years (6). Second, in the developing world a rapidly increasing population is [ILLEGIBLE TEXT] pressure on scarce resources, leading to major population redistribution. This particularly involves the movement from rural to urban areas. Third, natural [ILLEGIBLE TEXT] such as droughts and floods have created approximately 25 million environment refugees (7). Finally, conflict, often a result of population pressures and [ILLEGIBLE TEXT] degradation, displaces vast numbers of people. We examine the impact of [ILLEGIBLE TEXT] movement on malaria transmission.

A Typology of Population Movement

The decision-making process leading to population movement can best be [ILLEGIBLE TEXT] the light of "push and pull" forces (8). When their needs can no longer be met in particular environment, people move elsewhere. The "push factor" could be environmental degradation, population pressure on land, droughts, famines, [ILLEGIBLE TEXT] loss or lack of employment. When people are satisfied with their situation but be that a move elsewhere will provide new and attractive opportunities, a "pull [ILLEGIBLE TEXT] involved. This pull factor could be better political, economic, or social [ILLEGIBLE TEXT] improved living conditions. Push and pull factors can operate simultaneously; [ILLEGIBLE TEXT] example, people can be pushed by environmental deterioration and scarce [ILLEGIBLE TEXT] pulled by the economic opportunities offered by development projects.

Population movements can be differentiated by their temporal and spatial [ILLEGIBLE TEXT] Temporal dimensions include circulation and migration. Circulation [ILLEGIBLE TEXT] variety of movements, usually short-term and cyclical and involving no [ILLEGIBLE TEXT] change of residence. Migration involves a permanent change of residence (9). Circulation can be subdivided into daily, periodic, seasonal, and long term ([ILLEGIBLE TEXT] Daily circulation involves leaving a place of residence for up to 24 hours. [ILLEGIBLE TEXT] circulation may vary from 1 night to 1 year, although it is usually shorter than [ILLEGIBLE TEXT] circulation. Seasonal circulation is a type of periodic circulation in which the [ILLEGIBLE TEXT] defined by marked seasonality in the physical or economic environment. This [ILLEGIBLE TEXT] circulation involves persons or groups who are absent from their permanent [ILLEGIBLE TEXT] during a season or seasons of the year. Long-term circulation, defined as absence home for longer than a year, affects groups such as wage laborers and traders, [ILLEGIBLE TEXT] maintain close social and economic ties with their home area and intend to return[ILLEGIBLE TEXT]

[TABULAR DATA NOT REPRODUCIBLE IN ASCII]

In terms of spatial dimensions, the movements to and from malarious areas are [ILLEGIBLE TEXT] epidemiologic importance. People who move can be categorized as either active transmitters or passive acquirers (2). Active transmitters harbor the parasite and [ILLEGIBLE TEXT] the disease when they move to areas of low or sporadic transmission. Passive [ILLEGIBLE TEXT] are exposed to the disease through movement from one environment to another; [ILLEGIBLE TEXT] may have low-level immunity or may be nonimmune, which increases their risk disease.

Based on the above definitions, a typology can be devised that identifies [ILLEGIBLE TEXT] population movement. Different activities can be associated with these [ILLEGIBLE TEXT] these activities, in turn, can be associated with differing risks for malaria [ILLEGIBLE TEXT] All types of population movement can be accommodated in this typology, and [ILLEGIBLE TEXT] may exhibit more than one type of mobility.

Population Movement and Malaria

In developing countries, activities involving population movement include urban colonization, labor related to agriculture and mining, and conflict. In [ILLEGIBLE TEXT] countries, the impact of population movements on malaria risk is mainly related [ILLEGIBLE TEXT] intercontinental travel.

In some regions, malaria risk may increase as a result of a combination of [ILLEGIBLE TEXT] forms of mobility, as well as other factors unrelated to population movements. [ILLEGIBLE TEXT] example, in the African highlands, many of the issues described below act [ILLEGIBLE TEXT] (10). The categorization elf the various examples below simplifies a complex [ILLEGIBLE TEXT] useful for indicating major processes related to mobility and malaria risk.

Urbanization

The world's urban population is growing at four times the rate of the rural [ILLEGIBLE TEXT] (11). Urban pull is prevalent throughout the developing world, with rural-to-[ILLEGIBLE TEXT] migration taking place faster than ever before (12). Sub-Saharan Africa is the [ILLEGIBLE TEXT] rapidly urbanizing region in the world (13), and the urban population in India [ILLEGIBLE TEXT] doubled in the last 2 decades (14). When accompanied by adequate housing and sanitation, urbanization can lead to a decrease in malaria through reductions in [ILLEGIBLE TEXT] vector contact and vector breeding sites. However, in developing countries, rapid unregulated urbanization ,often leads to an increase in or resumption of malaria transmission because of poor housing and sanitation, lack of proper drainage of [ILLEGIBLE TEXT] water, and use of unprotected water reservoirs that increase human-vector [ILLEGIBLE TEXT] vector breeding.

Although water pollution in urban areas usually leads to decreases in vector [ILLEGIBLE TEXT] some vectors, such as An. arabiensis in the forest belt of West Africa, may adapt breeding in polluted waters (15). In Asia, An. stephensi is proving adaptable to [ILLEGIBLE TEXT] conditions, and in India it is a well-established vector of urban malaria. In urban India, water is not supplied regularly and is stored in houses, providing extensive breeding places for An. stephensi in overhead tanks and cisterns. In periurban are where 25% to 40% of the urban population live in poor housing without proper supply and drainage, another vector, An. culcifacies, also transmits malaria (14).

In India, the fact that the National Malaria Eradication Program concentrated [ILLEGIBLE TEXT] rural areas, ignoring the problem of urban malaria, was one of the factors leading resurgence of malaria in the 1970s (14). Several types of population movement contributed to malaria transmission in India. First, circulation from stable rural [ILLEGIBLE TEXT] areas to unstable urban areas had firmly established malaria transmission in [ILLEGIBLE TEXT] Then, after the National Malaria Eradication Program, rural areas became free of endemic malaria but were receptive, so circulation from urban areas back to rural reintroduced malaria transmission. Changes in vector behavior (exophilic and [ILLEGIBLE TEXT] behavior limiting the effectiveness of spraying), vector resistance to insecticides, increasing drug resistance, especially in Plasmodium falciparum (14), also [ILLEGIBLE TEXT] Population movement also contributed to drug resistance, with people of [ILLEGIBLE TEXT] immune status moving from endemic- to nonendemic-disease areas, accelerating transmission of resistant strains.

Colonization of New Territory

Through the interaction of a number of factors, the colonization of unpopulated [ILLEGIBLE TEXT] sparsely populated areas may be accompanied by an increase in malaria. Settlers, have low-level immunity or are nonimmune, may migrate into a disease-endemic spreading the disease. Initially, housing tends to be basic, leading to close human contact. Moreover, housing is often near rivers or lakes to facilitate water [ILLEGIBLE TEXT] increasing the exposure of humans to mosquitoes. Activities to develop an area, deforestation and irrigation, can increase the number of vector breeding sites, contributing to an increase in malaria. Colonization may be accompanied by [ILLEGIBLE TEXT] building projects, such as dams, canals, highways, or mining activities--referred [ILLEGIBLE TEXT] tropical aggregation of labor--which can further enhance malaria transmission.

Reemergence of malaria through mobility related to colonization occurred in [ILLEGIBLE TEXT] Malaria had been practically eradicated from most areas of the Amazon region [ILLEGIBLE TEXT] national malaria campaign in the 19508 and 19608 (16). Since the 19608, [ILLEGIBLE TEXT] incidence of malaria has increased dramatically because of massive population movements to colonize new territory. New highways were built in the 19608, [ILLEGIBLE TEXT] Amazon region to the rest of the country and attracting laborers to work on road construction. In the 1970s, many more people were attracted to the region by agricultural settlements and hydroelectric projects. Finally, in the 19808, the [ILLEGIBLE TEXT] of gold led to a greater influx of people, along with the establishment of hundred mines throughout the region. The population of Rondonia State, which received [ILLEGIBLE TEXT] greatest number of migrants, increased from 113,000 in 1970 to 1,200,000 in 19 Malaria cases in Rondonia increased from 20,000 to 174,000 in the same period. Brazil as a whole, approximately 50,000 cases of malaria were reported in 1970; 1990, reports had increased to 577,520, representing 10% of the world's reported outside Africa (17). Of this total, [is greater than] 98% were recorded in the Amazon region.

The types of population movement involved in the colonization of the Amazons migration and long-term circulation from malaria-free areas of Brazil to the [ILLEGIBLE TEXT] endemic Amazon region. The people involved are nonimmune passive acquirers becoming infected can become active transmitters. If these active transmitters [ILLEGIBLE TEXT] their initial place of residence in a malaria-free but highly receptive area, they [ILLEGIBLE TEXT] reintroduce the parasite and initiate an outbreak of malaria. For example, in 1985 new active foci of malaria, were recorded in Brazilian states outside the Amazon (16). Settlers in the Amazon region are highly mobile, moving with daily, period seasonal circulation from settlements in unstable disease-endemic regions to hyperendemic-disease regions of the rainforests. This mobility keeps settlements unstable and at high risk for epidemics through the constant flow of parasitemic [ILLEGIBLE TEXT] (17,18).

Agricultural Labor

Swaziland provides an example of how agricultural labor has changed the spread malaria. In the 19508, control measures (DDT spraying) were successfully [ILLEGIBLE TEXT] in the lowveld so that agricultural development could take place, and by 1959, [ILLEGIBLE TEXT] had been all but eradicated from Swaziland (19). However, agricultural develop the 19508 involving an irrigation project for the cultivation of sugar cane created conditions favorable for malaria. Vector density increased, along with a high [ILLEGIBLE TEXT] of feeding on humans, as no domestic or wild animals were around the project [ILLEGIBLE TEXT] serve as alternative hosts. This resurgence of malaria was catalyzed by the [ILLEGIBLE TEXT] of parasite carriers in the form of migrant workers from disease-endemic areas of Mozambique, who were involved in migration or long-term circulation to work [ILLEGIBLE TEXT] sugar estates in the 1960s and early 1970s (19).

In Colombia, the annual parasite index (defined as the ratio between the number reported and the population at risk) has increased threefold since the 1960s (20). increase seems to be related to the migration of nonimmune people to areas such Naya basin, where malaria is endemic, and to the circulation of groups within the basin. The circulation is predominantly seasonal, related to agriculture. People [ILLEGIBLE TEXT] from hills and terraces, where malaria risk is minimal, to the malarious delta [ILLEGIBLE TEXT] cultivate and harvest their crops. In doing so, they are exposed to the anopheline population of the area and are at high risk for malaria. A large number of people involved in this circulation (approximately 60% of the area's population is [ILLEGIBLE TEXT] approximately 4 months of the year), and this population density, combined with large vector population, maintains transmission at high levels (20).

Refugees

The number of officially recognized refugees has steadily increased, from [ILLEGIBLE TEXT] 5 million in 1980 to [is greater than] 20 million in late 1994 (21). In addition, an estimated 25 m people have fled their homes but remain internally displaced in their countries of (22). The displacement of large numbers of people and their circulation can favor malaria transmission. If refugees are nonimmune, they could travel through or to malarious regions and acquire the infection, and if they are infectious, they could disseminate the disease to other areas.

Malaria is one of the most commonly reported causes of death among refugees a caused high rates of both illness and death among refugees and displaced persons disease-endemic countries, such as Thailand, Sudan, Somalia, Burundi, Rwanda, Democratic Republic of Congo (23). In recent outbreak among Burundian refuge refugee camp in northwestern Tanzania, deaths from malaria and anemia in child under 5 years of age have increased 10-fold since the outbreak, reflecting the lac immunity in this age group (24). In the Sahel region of Africa, where civil wars a conflicts have occurred for many decades and large numbers of displaced people resettlement or refugee camps often located in lowland disease-endemic areas, epidemics are common (25).

As a result of 15 years of continuous war, which displaced hundreds of thousand people, Luanda, the capital of Angola, underwent an unprecedented population [ILLEGIBLE TEXT] in the 1980s. This population movement resulted in a shift in malaria endemicity Luanda from hypoendemic to mesoendemic level within 5 years (26). As a cause child deaths, malaria moved from sixth to first place. Increasing parasite [ILLEGIBLE TEXT] chloroquine also became a major problem. This situation arose because of the [ILLEGIBLE TEXT] influx of displaced people of low socioeconomic status into an environment with stagnant water reservoirs. The population movements that increased malaria transmission in Luanda were long-term circulation and migration from stable [ILLEGIBLE TEXT] to an unstable urban area.

Besides movements of large numbers of people, wars and civil unrest tend to [ILLEGIBLE TEXT] malaria transmission. The disruptive effect of war on agriculture and water [ILLEGIBLE TEXT] can increase vector breeding sites; the destruction of housing can increase human contact; the destruction of cattle can prompt zoophilic vectors to become [ILLEGIBLE TEXT] if their usual food supply is disrupted (27); and control measures can be [ILLEGIBLE TEXT] diminished if health-care facilities are reduced or unavailable.

Intercontinental Travel

The intercontinental transfer of malaria can occur through the introduction of an infective vector into a nonendemic-disease area, as in so-called airport malaria, [ILLEGIBLE TEXT] through the movement of a parasitemic person to a nonendemic-disease area, as [ILLEGIBLE TEXT] imported malaria. Although the incidence of these cases is low, they account for malaria transmission in industrialized countries.

Airport Malaria

Airport malaria is defined as malaria acquired through the bite of an infected [ILLEGIBLE TEXT] anopheline mosquito by persons whose geographic history excludes exposure to vector in its natural habitat (28). The vector is usually introduced into a [ILLEGIBLE TEXT] disease country on an international flight. For example, random searches of [ILLEGIBLE TEXT] Gatwick Airport (London) found that 12 of 67 airplanes from tropical countries contained mosquitoes (29). After a mosquito leaves the aircraft, it may survive [ILLEGIBLE TEXT] enough to take a blood meal and transmit the disease, usually in the vicinity of a airport. In temperate climates, temperature and humidity can be favorable in the for the mosquito not only to survive but also to move around and perhaps lay egg the enormous and continuing increase in air traffic, cases of airport malaria may increase. Several such cases are described below.

During a hot summer in 1994, six cases of airport malaria were identified in and Roissy-Charles-de-Gaulle Airport (30). Four of the patients were airport workers the others lived in Villeparisis, approximately 7.5 km away. Anopheline [ILLEGIBLE TEXT] were thought to have traveled in the cars of airport workers who lived next door [ILLEGIBLE TEXT] of the patients. In 1989, two cases of P. falciparum malaria were identified in [ILLEGIBLE TEXT] two persons who lived in Geneva (31). Another five cases of airport malaria [ILLEGIBLE TEXT] reported in Geneva in the summer of 1989 (32). High minimum temperatures we thought to have allowed the survival of infected anophelines introduced by [ILLEGIBLE TEXT] Britain, two cases of P. falciparum malaria were observed in persons living 10 [ILLEGIBLE TEXT] 15 km from Gatwick Airport (33). Hot, humid weather in Britain may have [ILLEGIBLE TEXT] the survival of an imported mosquito.

Imported Malaria

Throughout the world, many countries are reporting an increasing number of cases of imported malaria (Figure) because of the great increase in long-distance travel in recent decades. For example, cases imported from Africa to the United Kingdom rose from 803 in 1987 to 1,165 in 1993, and the ratio of all imported cases of falciparum to vivax malaria rose from 0.76 in 1984 to 1.52 in 1993 (36).

[Figure ILLUSTRATION OMITTED]

Recently, a woman in Italy was infected with malaria through a bite from a local species, An. labranchiae (37). This species was a common malaria vector in Italy until the country was declared malaria free in 1970. Local breeding sites, including isolated pools in dried-up irrigation channels, were identified, an mosquito responsible is thought to have acquired the parasite after biting a [ILLEGIBLE TEXT] girl who had acquired malaria in India. Airport malaria was ruled out because of distance from the nearest airport. This may be the first case of malaria introduced Europe in 20 years and demonstrates the hazards of population movement (the [ILLEGIBLE TEXT] had been introduced from India) combined with human activities (providing [ILLEGIBLE TEXT] breeding sites).

In the United States, recent outbreaks of presumed local mosquito-borne [ILLEGIBLE TEXT] have been reported in California, with migration from a disease-endemic area (3[ILLEGIBLE TEXT] people involved were migrant workers from malaria-endemic areas. An outbreak 1986 involved 28 cases (26 in Mexican migrant workers) of P. vivax during a 3-period (39). The epidemic curve indicated secondary spread, which confirmed [ILLEGIBLE TEXT] mosquito-borne transmission.

In the early 1990s, outbreaks were identified in neighborhoods of Houston with immigrants from countries with malaria transmission. These outbreaks occurred the weather was hot and humid and thus conducive to the completion of the [ILLEGIBLE TEXT] cycle and the survival of female anophelines (38). Given that climate change [ILLEGIBLE TEXT] to more favorable conditions for vector survival in Europe and the United States the increase in incidence in both airport and imported malaria is cause for [ILLEGIBLE TEXT] temperatures increase, uninfected introduced or local mosquitoes could survive [ILLEGIBLE TEXT] enough after taking a blood meal from a parasitemic person for the completion [ILLEGIBLE TEXT] sporogonic cycle of the parasite, thus enabling transmission.

Conclusions

Population movements that either place people at risk for malaria or cause them [ILLEGIBLE TEXT] a risk to others cannot be stopped. However, prevention measures can address [ILLEGIBLE TEXT] of these movements which, in developing countries, are often prompted by need than choice; if living conditions and opportunities improved in their place of [ILLEGIBLE TEXT] people would not be forced to move. In cases where movements are unavoidable, should be made aware of the risks and have adequate access to treatment. Epide more likely to take place in areas where health care may be poor or lacking. Area for epidemics through the influx of infected people should be identified to avoid control epidemics. Particular attention should be paid to urban areas, given the increasing number of cases of urban malaria and the ongoing trend toward [ILLEGIBLE TEXT] urbanization.

The risk for increased malaria transmission through economic development of an should be analyzed thoroughly before development begins. For example, sound environmental management can restrict vector breeding and reduce human-[ILLEGIBLE TEXT] contact. Such management could include proper maintenance of irrigation [ILLEGIBLE TEXT] adequate water supply and sanitation facilities for workers. Personal vector-[ILLEGIBLE TEXT] measures, such as bed nets, and antimalarial drugs should be used.

Regarding the risks that airport and imported malaria pose for developed [ILLEGIBLE TEXT] measures should be taken to ensure that cases of malaria are promptly diagnosed treated. Strengthened surveillance would help to prevent the reintroduction of [ILLEGIBLE TEXT] transmission by local mosquitoes, which could acquire the infection by biting [ILLEGIBLE TEXT] with airport or imported malaria. Fortunately, given the economic resources and of health care available in the developed world, the likelihood is low that isolate outbreaks of malaria will lead to reestablishment of transmission.

The relationship between malaria transmission and population movement is [ILLEGIBLE TEXT] but future attempts to eradicate or control malaria will be futile if they are not [ILLEGIBLE TEXT] understanding of this link. Because the current magnitude and diversity of [ILLEGIBLE TEXT] movements are unprecedented, this issue is worthy of attention.

Acknowledgments

Comments on earlier versions of this paper from Bas Ameltmg, Steve Lindsay, S[ILLEGIBLE TEXT] Nijhof, Mansell Prothero, Piebe de Vries, and two anonymous referees are [ILLEGIBLE TEXT] appreciated.

This work was supported by the United Nations Environment Programme ([ILLEGIBLE TEXT] Number FP/3210-96-01-2207), the Dutch National Research Program on Global Pollution and Climate Change (Project Number 952257), and the Netherlands Foundation for the Advancement of Tropical Research (Project Number WAA 9[ILLEGIBLE TEXT]312/313).

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(40.) Martens P, Kovats RS, Nijhof S, De Vries P, Livermore MTJ, Bradley DJ, Climate change and future populations at risk of malaria. Global [ILLEGIBLE TEXT] Change 1999;S9:89-107.

Dr. Martens is director of the Global Assessment Centre, International Centre for Integrative Studies, Maastricht University. His area of expertise includes [ILLEGIBLE TEXT] the health impact of globalization and global environmental changes. He is [ILLEGIBLE TEXT] chief of the journal Global Change and Human Health.

Ms. Hall studied enviromnental health sciences at Maastricht University and [ILLEGIBLE TEXT] and pharmacology at the University of London. The focus of her research is [ILLEGIBLE TEXT] change in relation to environmental impact.

Address for correspondence: Pim Martens, International Centre for Integrative [ILLEGIBLE TEXT] Maastricht University, P.O. Box 616, 6200 MD Maastricht, the Netherlands; fax: 388-4916; e-mail: p.martens@icis.unimaas.nl
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Date:Mar 1, 2000
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