Emerging Infectious Diseases
[Volume 6 No.2 / March - April 2000]

Perspectives

Malaria on the Move: Human Population Movement and Malaria
Transmission

Pim Martens and Lisbeth Hall
Maastricht University, Maastricht, the Netherlands

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 countries, with pockets of transmission in an
additional eight countries (1). Approximately 41% of the world's
population is at risk, and each year 300 million to 500 million
clinical cases of malaria, >90% of them in Africa, are reported.
Worldwide, approximately 2 million deaths per year can be
attributed to malaria, half of these in children under 5 years of age.

Historically, population movement has contributed to the spread of
disease (2). Failure to consider this factor contributed to failure of
malaria eradication campaigns in the 1950s and 1960s (3). The
movement of infected people from areas where malaria was still
endemic to areas where the disease had been eradicated led to
resurgence of the disease. However, population movement can
precipitate or increase malaria transmission in other ways as well.
As people move, they can increase their risk for acquiring the
disease through the ways in which they change the environment
and through the technology they introduce, for example, through
deforestation and irrigation systems (4). Such activities can create
more favorable habitats for Anopheles mosquitoes; at the same
time, workers may have increased exposure to the vector.
Furthermore, people can inadvertently transport infectious
mosquitoes to malaria-free areas, reintroducing disease. Population
movement is also increasingly implicated in the spread of drug
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 of reasons for increased mobility.
First, sophisticated forms of transport now permit the swift
movement of people over huge distances. Air travel has increased
by almost 7% a year in the last 20 years and is predicted to increase
by >5% a year during the next 20 years (6). Second, in the
developing world a rapidly increasing population is putting
pressure on scarce resources, leading to major population
redistribution. This particularly involves the movement from rural
to urban areas. Third, natural disasters such as droughts and floods
have created approximately 25 million environmental refugees (7).
Finally, conflict, often a result of population pressures and
environmental degradation, displaces vast numbers of people. We
examine the impact of population movement on malaria
transmission.

A Typology of Population Movement

The decision-making process leading to population movement can
best be understood in the light of "push and pull" forces (8). When
their needs can no longer be met in a particular environment,
people move elsewhere. The "push factor" could be environmental
degradation, population pressure on land, droughts, famines,
conflict, or loss or lack of employment. When people are satisfied
with their situation but believe that a move elsewhere will provide
new and attractive opportunities, a "pull factor" is involved. This
pull factor could be better political, economic, or social
opportunities or improved living conditions. Push and pull factors
can operate simultaneously; for example, people can be pushed by
environmental deterioration and scarce resources and pulled by the
economic opportunities offered by development projects.
Population movements can be differentiated by their temporal and
spatial dimensions. Temporal dimensions include circulation and
migration. Circulation encompasses a variety of movements,
usually short-term and cyclical and involving no longstanding
change of residence. Migration involves a permanent change of
residence (9). Circulation can be subdivided into daily, periodic,
seasonal, and long term (Table) (9). Daily circulation involves
leaving a place of residence for up to 24 hours. Periodic circulation
may vary from 1 night to 1 year, although it is usually shorter than
seasonal circulation. Seasonal circulation is a type of periodic
circulation in which the period is defined by marked seasonality in
the physical or economic environment. This type of circulation
involves persons or groups who are absent from their permanent
homes during a season or seasons of the year. Long-term
circulation, defined as absence from home for longer than a year,
affects groups such as wage laborers and traders, who maintain
close social and economic ties with their home area and intend to
return. In terms of spatial dimensions, the movements to and from
malarious areas are of epidemiologic importance. People who
move can be categorized as either active transmitters or passive
acquirers (2). Active transmitters harbor the parasite and transmit
the disease when they move to areas of low or sporadic
transmission. Passive acquirers are exposed to the disease through
movement from one environment to another; they may have low-
level immunity or may be nonimmune, which increases their risk
for disease.


Based on the above definitions, a typology can be devised that
identifies categories of population movement. Different activities
can be associated with these categories, and these activities, in
turn, can be associated with differing risks for malaria
transmission. All types of population movement can be
accommodated in this typology, and people may exhibit more than
one type of mobility.  Table. A typology of population movement
(adapted from [2])

Population Movement and Malaria

In developing countries, activities involving population movement
include urbanization, colonization, labor related to agriculture and
mining, and conflict. In industrialized countries, the impact of
population movements on malaria risk is mainly related to
intercontinental travel. In some regions, malaria risk may increase
as a result of a combination of different forms of mobility, as well
as other factors unrelated to population movements. For example,
in the African highlands, many of the issues described below act
concurrently (10). The categorization of the various examples
below simplifies a complex issue but is 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 population (11). Urban pull is prevalent throughout the
developing world, with rural-to-urban migration taking place faster
than ever before (12). Sub-Saharan Africa is the most rapidly
urbanizing region in the world (13), and the urban population in
India has 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 human-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 surface water, and use of
unprotected water reservoirs that increase human-vector contact
and vector breeding. Although water pollution in urban areas
usually leads to decreases in vector populations, some vectors,
such as An. arabiensis in the forest belt of West Africa, may adapt
to breeding in polluted waters (15). In Asia, An. stephensi is
proving adaptable to urban conditions, and in India it is a well-
established vector of urban malaria. In urban areas of 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 areas, where 25% to 40% of the urban
population live in poor housing without proper water supply and
drainage, another vector, An. culcifacies, also transmits malaria
(14). In India, the fact that the National Malaria Eradication
Program concentrated only on rural areas, ignoring the problem of
urban malaria, was one of the factors leading to a resurgence of
malaria in the 1970s (14). Several types of population movement
contributed to malaria transmission in India. First, circulation from
stable rural malaria areas to unstable urban areas had firmly
established malaria transmission in urban areas. 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 areas reintroduced malaria transmission.
Changes in vector behavior (exophilic and exophagic behavior
limiting the effectiveness of spraying), vector resistance to
insecticides, and increasing drug resistance, especially in
Plasmodium falciparum (14), also played a role. Population
movement also contributed to drug resistance, with people of
different 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 or sparsely populated areas may be accompanied by
an increase in malaria. Settlers, who have low-level immunity or
are nonimmune, may migrate into a disease-endemic area,
spreading the disease. Initially, housing tends to be basic, leading
to close human-vector contact. Moreover, housing is often near
rivers or lakes to facilitate water collection, increasing the exposure
of humans to mosquitoes. Activities to develop an area, such as
deforestation and irrigation, can increase the number of vector
breeding sites, contributing to an increase in malaria. Colonization
may be accompanied by major building projects, such as dams,
canals, highways, or mining activitiesreferred to as the tropical
aggregation of laborwhich can further enhance malaria
transmission.

Reemergence of malaria through mobility related to colonization
occurred in Brazil. Malaria had been practically eradicated from
most areas of the Amazon region by the national malaria campaign
in the 1950s and 1960s (16). Since the 1960s, however, the
incidence of malaria has increased dramatically because of massive
population movements to colonize new territory. New highways
were built in the 1960s, linking the 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
1980s, the discovery of gold led to a greater influx of people, along
with the establishment of hundreds of mines throughout the region.
The population of Rondnia State, which received the greatest
number of migrants, increased from 113,000 in 1970 to 1,200,000
in 1990. Malaria cases in Rondnia increased from 20,000 to
174,000 in the same period. In Brazil as a whole, approximately
50,000 cases of malaria were reported in 1970; by 1990, reports
had increased to 577,520, representing 10% of the world's reported
cases outside Africa (17). Of this total, >98% were recorded in the
Amazon region.

The types of population movement involved in the colonization of
the Amazons are migration and long-term circulation from malaria-
free areas of Brazil to the malaria-endemic Amazon region. The
people involved are nonimmune passive acquirers who on
becoming infected can become active transmitters. If these active
transmitters return to their initial place of residence in a malaria-
free but highly receptive area, they can reintroduce the parasite and
initiate an outbreak of malaria. For example, in 1985, 26 new
active foci of malaria were recorded in Brazilian states outside the
Amazon region (16). Settlers in the Amazon region are highly
mobile, moving with daily, periodic, and 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 laborers (17,18).

Agricultural Labor

Swaziland provides an example of how agricultural labor has
changed the spread of malaria. In the 1950s, control measures
(DDT spraying) were successfully implemented in the lowveld so
that agricultural development could take place, and by 1959,
malaria had been all but eradicated from Swaziland (19). However,
agricultural developments in the 1950s involving an irrigation
project for the cultivation of sugar cane created conditions
favorable for malaria. Vector density increased, along with a high
frequency of feeding on humans, as no domestic or wild animals
were around the project area to serve as alternative hosts. This
resurgence of malaria was catalyzed by the reintroduction 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 on the sugar estates in the 1960s and
early 1970s (19).

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

Refugees

The number of officially recognized refugees has steadily
increased, from approximately 5 million in 1980 to >20 million in
late 1994 (21). In addition, an estimated 25 million people have
fled their homes but remain internally displaced in their countries
of origin (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 and has caused high rates of both illness and death
among refugees and displaced persons in disease-endemic
countries, such as Thailand, Sudan, Somalia, Burundi, Rwanda,
and the Democratic Republic of Congo (23). In recent outbreak
among Burundian refugees at a refugee camp in northwestern
Tanzania, deaths from malaria and anemia in children under 5
years of age have increased 10-fold since the outbreak, reflecting
the lack of immunity in this age group (24). In the Sahel region of
Africa, where civil wars and conflicts have occurred for many
decades and large numbers of displaced people live in 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 thousands of people, Luanda, the capital of Angola,
underwent an unprecedented population increase in the 1980s. This
population movement resulted in a shift in malaria endemicity in
Luanda from hypoendemic to mesoendemic level within 5 years
(26). As a cause of child deaths, malaria moved from sixth to first
place. Increasing parasite resistance to chloroquine also became a
major problem. This situation arose because of the enormous
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 rural areas to an
unstable urban area.

Besides movements of large numbers of people, wars and civil
unrest tend to favor malaria transmission. The disruptive effect of
war on agriculture and water management can increase vector
breeding sites; the destruction of housing can increase human-
vector contact; the destruction of cattle can prompt zoophilic
vectors to become anthropophilic if their usual food supply is
disrupted (27); and control measures can be seriously 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, or through the movement of a
parasitemic person to a nonendemic-disease area, as in imported
malaria. Although the incidence of these cases is low, they account
for most malaria transmission in industrialized countries.

Airport Malaria

Airport malaria is defined as malaria acquired through the bite of
an infected tropical anopheline mosquito by persons whose
geographic history excludes exposure to this vector in its natural
habitat (28). The vector is usually introduced into a nonendemic-
disease country on an international flight. For example, random
searches of airplanes at Gatwick Airport (London) found that 12 of
67 airplanes from tropical countries contained mosquitoes (29).
After a mosquito leaves the aircraft, it may survive long enough to
take a blood meal and transmit the disease, usually in the vicinity
of an airport. In temperate climates, temperature and humidity can
be favorable in the summer for the mosquito not only to survive
but also to move around and perhaps lay eggs. With 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
around Roissy-Charles-de-Gaulle Airport (30). Four of the patients
were airport workers, and the others lived in Villeparisis,
approximately 7.5 km away. Anopheline mosquitoes were thought
to have traveled in the cars of airport workers who lived next door
to two of the patients. In 1989, two cases of P. falciparum malaria
were identified in Italy in two persons who lived in Geneva (31).
Another five cases of airport malaria were reported in Geneva in
the summer of 1989 (32). High minimum temperatures were
thought to have allowed the survival of infected anophelines
introduced by aircraft. In Britain, two cases of P. falciparum
malaria were observed in persons living 10 km and 15 km from
Gatwick Airport (33). Hot, humid weather in Britain may have
facilitated 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).

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, and the mosquito
responsible is thought to have acquired the parasite after biting a
parasitemic girl who had acquired malaria in India. Airport malaria
was ruled out because of the distance from the nearest airport. This
may be the first case of malaria introduced to Europe in 20 years
and demonstrates the hazards of population movement (the parasite
had been introduced from India) combined with human activities
(providing vector breeding sites).

In the United States, recent outbreaks of presumed local mosquito-
borne transmission have been reported in California, with
migration from a disease-endemic area (38). The people involved
were migrant workers from malaria-endemic areas. An outbreak in
1986 involved 28 cases (26 in Mexican migrant workers) of P.
vivax during a 3-month period (39). The epidemic curve indicated
secondary spread, which confirmed local mosquito-borne
transmission. In the early 1990s, outbreaks were identified in
neighborhoods of Houston with many immigrants from countries
with malaria transmission. These outbreaks occurred when the
weather was hot and humid and thus conducive to the completion
of the sporogonic cycle and the survival of female anophelines
(38). Given that climate change could lead to more favorable
conditions for vector survival in Europe and the United States (40),
the increase in incidence in both airport and imported malaria is
cause for concern. If temperatures increase, uninfected introduced
or local mosquitoes could survive long enough after taking a blood
meal from a parasitemic person for the completion of the
sporogonic cycle of the parasite, thus enabling transmission.

Figure. Imported cases of malaria in Europe (34,35).

Conclusions

Population movements that either place people at risk for malaria
or cause them to pose a risk to others cannot be stopped. However,
prevention measures can address the causes of these movements
which, in developing countries, are often prompted by need rather
than choice; if living conditions and opportunities improved in
their place of residence, people would not be forced to move. In
cases where movements are unavoidable, people should be made
aware of the risks and have adequate access to treatment.

Epidemics are more likely to take place in areas where health care
may be poor or lacking. Areas at risk for epidemics through the
influx of infected people should be identified to avoid or control
epidemics. Particular attention should be paid to urban areas, given
the increasing number of cases of urban malaria and the ongoing
trend toward uncontrolled urbanization.

The risk for increased malaria transmission through economic
development of an area should be analyzed thoroughly before
development begins. For example, sound environmental
management can restrict vector breeding and reduce human-vector
contact. Such management could include proper maintenance of
irrigation systems and adequate water supply and sanitation
facilities for workers. Personal vector-control measures, such as
bed nets, and antimalarial drugs should be used. Regarding the
risks that airport and imported malaria pose for industrialized
countries, measures should be taken to ensure that cases of malaria
are promptly diagnosed and treated. Strengthened surveillance
would help prevent the reintroduction of malaria transmission by
local mosquitoes, which could acquire the infection by biting
persons with airport or imported malaria. Given the economic
resources and quality of health care in industrialized countries, the
likelihood is low that isolated outbreaks of malaria will lead to
reestablishment of transmission.

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

Acknowledgments

Comments on earlier versions of this paper from Bas Amelung,
Steve Lindsay, Saskia Nijhof, Mansell Prothero, Piebe de Vries,
and two anonymous referees are gratefully appreciated.


This work was supported by the United Nations Environment
Programme (Project Number FP/3210-96-01- 2207), the Dutch
National Research Program on Global Air Pollution and Climate
Change (Project Number 952257), and the Netherlands Foundation
for the Advancement of Tropical Research (Project Number WAA
93-312/313).

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

Ms. Hall studied environmental health sciences at Maastricht
University and toxicology and pharmacology at the University of
London. The focus of her research is behavioral change in relation
to environmental impact.

Address for correspondence: Pim Martens, International Centre for
Integrative Studies, Maastricht University, P.O. Box 616, 6200
MD Maastricht, the Netherlands; fax: 31-43- 388-4916; e-mail:
p.martens@icis.unimaas.nl.

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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA

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