Movement of people is the means by which human pathogens are dispersed,
so providing health care to mobile sectors of the community is vital to
disease control interventions.
Using malaria as a case study, our article examines types of migrant
transit and their significance for prevention and treatment of the
Asymptomatic untreated infections act as reservoirs for malaria
transmission. Malaria control programmes need to identify those migrant
streams with potential to transport malaria and to target prevention and
treatment measures appropriately.
Transit has also played a role in the dispersal of antimalarial drug
resistance, with the international transportation of
artemisinin-resistant parasites by human migration being the greatest
threat to the antimalarial treatments used in Africa today.
A geographic framework of human migration at local, national, and
international levels is needed so the potential speed and direction of
pathogen dispersal can be predicted, and for health policy and services
to respond appropriately to the needs of migrants and to threats of
This is one article in a six-partPLoS Medicineseries on Migration & Health.
There are many different types of migrants and types of movements and no single
commonly agreed definition for transit migration. Papadopoulou  describes it as “the
stage between emigration and settlement”, while in contrast, the assembly of
Inter-Parliamentary Union in Geneva  states that “transit migrants are…aliens who
stay in the country for some period of time while seeking to migrate permanently to
Although transit is often defined in terms of international borders, it is highly
likely that transit migrants undertake similar patterns of movement within their
countries of origin, and within the transit and settlement countries. Within a
country people can be moving permanently or multiple times towards urban areas and
back home, especially if they are internally displaced people (IDPs). In practice,
transitory migration is one component within a broad framework of movement
encompassing permanent, temporary, and circulatory migration, all of which can occur
in a bidirectional or in a stepwise sequence of moves ,.
This article examines types of transit migration and their significance for the
prevention and treatment of malaria in Africa, using a case study of migration in
People Movement and Malaria
Plasmodium falciparum malaria—responsible for the most severe
malaria—occurs across Africa, although the intensity of transmission varies
considerably. Half of Africans live in areas of high endemicity where more than
40% of the population have parasites in their blood ; the bulk of these infections are
asymptomatic. Transit between different areas exposes people to changing risks of
malaria infection, and the burden of infection often falls disproportionately on
mobile and migrant sectors of the community .
Migrants travelling from low to high transmission areas are at greater risk of
acquiring a malarial infection than those travelling in the opposite direction,
where also having no acquired immunity means they are much more vulnerable to
disease. Evidence from large-scale population resettlement programs in Ethiopia
Indonesia, and Brazil  show sharp increases in malaria morbidity and mortality
across all age groups in migrants from low to high transmission areas.
As such, migration has enormous significance for patterns of malaria infection and
disease, and for malaria control. When large groups of people move from high to low
transmission areas, the immediate result, as measurable by parasite prevalence,
would be an overall increase in transmission . But more common than
unidirectional permanent migrations are the regular and cyclical movements of
migrants or return migrants to areas of low transmission. In either case, a migrant
infected with malaria can serve as a reservoir and seed localised outbreaks or
epidemics in those areas, and thus migrants become “active transmitters”
of infection in low transmission areas .
Migration, Malaria, and Drug Resistance
International transit of people with malaria played a significant role in the global
dispersal of resistance to both chloroquine and sulphadoxine-pyrimethamine (also
known as SP or Fansidar), two drugs that were the mainstay of malaria treatment in
Africa for 30 years. In both cases, resistance mutations arose in Southeast Asia and
were subsequently imported into Africa during the 1970s for chloroquine, and during
the 1980s and 1990s for pyrimethamine and sulphadoxine, respectively ,. While there
was a 17-year lag between the appearance of chloroquine resistance in Southeast Asia
and its introduction to Africa, once established in Africa the dispersal of
resistance has been shown to follow the predictable process of incremental diffusion
In 2010, Tatem et al.  used permanent migration data derived from national
census statistics and measures of malaria endemicity to describe communities of
malaria-endemic African countries linked by higher levels of infection movement (see
Figure 1A). Their analysis
highlights “natural” migration regions where high levels of malaria
infection are interchanged. A comparison of malaria migration data (Figure 1A) with the geographic
distribution of parasite drug resistance lineages (Figure 1B) shows there is broad correspondence
between migration and resistance patterns.
The description of the geographic patterns of drug resistance dispersal comes from an
analysis  that
described five major lineages of sulphadoxine resistance at the
dhps gene in P. falciparum. These emerged
during the 1990s when the SP drug was widely used for treatment of malaria. Each
lineage occurred via a single mutation event, and has a distinctive geographical
distribution that reflects circulation and dispersal from their site of initial
The map in Figure 1b is a
snapshot of the distribution of these resistance lineages among 20 African
populations sampled during 2000–2007. The degree to which parasite populations
share resistance lineages is an indication of the extent of parasite mixing during
the 10–15 years they have been in circulation. The major regional distinctions
between parasite populations on the African mainland are between populations in the
east and west, and between the northern and southern populations in the east and the
The similarities between the geographical pattern of resistance mutation dispersal in
Africa and the levels of permanent migration between countries support the view that
parasite circulation through regionally distinct migration streams was central to
the spread of drug resistance mutations. However, permanent migration reported in
census data as “place of birth” captures only a fraction of the
migration and transit taking place. Furthermore, having been collated at the
national level, these data lack the spatial resolution to examine migration and
mobility within countries. Patterns of human circulation change
according to the dictates of war, trade, and transport infrastructure. These maps
suggest the existence of networks of high volume migration, whose boundaries are
unlikely to be national borders.
Case Study: Complex Migration Patterns and Drug-Resistant Malaria in Southwest
There has emerged a highly resistant form of P. falciparum in the
Kabale and Rukungiri districts of southwest Uganda  and in bordering areas of Rwanda
. The form
carries a mutation in the dhfr gene, which confers high level
resistance to a number of antifolate drugs in general use (including
sulfadoxine-pyrimethamine and chlorproguanil-dapsone). To predict the likely path of
dispersal of this resistant form of the parasite, we examined the types and
frequency of population movements in Uganda. The region of resistance emergence is
shown in red in Figure 2.
In 2005, Uganda hosted an international migrant pool of 2.25% of its total
population, with a reported net migration of 5,000 people . Internal migration is much
higher: nationally, 19.7% of the population of Uganda report to have lived in
another village, town, or district for more than 6 months at any one time in the
last 5 years .
And sub-national or district-level studies have shown that only 18% of heads
of households were born in their current areas of residence, and this proportion is
higher in rural areas (29%) .
Uganda also has a long history of hosting refugees from neighbouring countries. In
2008, the country was home to nearly 250,000 refugees from Sudan, the Democratic
Republic of the Congo, and Rwanda in camps containing upwards of 3,000 people each
, and an
additional 915,000 IDPs still remain after being displaced during the ongoing
conflict in northern Uganda . The location of refugee and IDP camps is illustrated by
shaded regions in Figure 2.
The interregional migrant streams in Figure 2 illustrate the central influence of the main city of Kampala.
Urbanization is a major component of permanent migration, although it has progressed
more slowly in East Africa than in other parts of the world. In 2002, just over
12% of the total Ugandan population was estimated to live in an urban area
for labour is now accepted as part of a household strategy to improve traditional
livelihood , and has been relatively well-documented in Uganda.
Migrant labour is characterised by circulatory rather than permanent movements, with
migrants returning to their areas of origin at the end of a formal contract or
wage-paying period . This migration system was disrupted with the economic
collapse in the 1970s and 1980s, with reports of reverse migration from major urban
areas, such as Kampala, back to rural areas . This reverse flow continued
until the mid-1980s , when urbanisation began to slowly increase again.
Apart from labour migration, the amount of circulatory migration associated with
other activities is difficult to establish. Return migration appears to be frequent
with an estimated 10% of urban dwellers making return visits to their home
areas of origin annually ,.
Migration in Southwest Uganda
The southwest of Uganda in particular has always suffered from scarcity of land,
as well as erosion and soil degradation , which has led to
out-migration from the region . More recently, improved roads and increased vehicle
numbers, as well as market liberalisation, has led to a further increase in
temporary mobility between rural and urban areas .
Another result of high population density has been migration and resettlement,
both programmed and spontaneous, into neighbouring areas. The first official
resettlement schemes took place in the late 1940s, and involved the transfer of
approximately 15,000 people from South Kigezi (now Kabale) into North Kigezi
(now Rukungiri) . Further resettlement schemes were undertaken to
relocate labour from Kabale and Rukungiri to Bunyoro in order to clear 500
square miles of bush as part of a tsetse barrier scheme .
While these schemes ended in the 1960s, migration between Kabale, Rukungiri, and
the Bunyoro region continued and the original scheme resulted in a strong
migration route opening between these areas . Around the same time (mid
to late 1950s) in Kabale, people had begun to encroach into the Bwindi forests
in the district . Migration data, based on birthplace information
taken during the 1969 population census in Uganda, clearly showed a large
migration stream from southwestern districts (Kigezi) into the western Toro and
Ankole regions as well as into Kampala and its surrounding areas.
These large northward migrant streams from the affected area of southwest Uganda
indicate that the highly drug-resistant malaria parasites have the means to
spread quickly within Southern Uganda. The maps in Figures 1 and 2 indicate that the future dispersal of
resistance has the potential to extend rapidly throughout east and southeast
Africa provided that selection in the form of continuing use of SP for treatment
is maintained. The relative importance of different types of travel for the
dispersal of malaria is difficult to quantify individually, but it is clear from
patterns of dispersal of drug resistance that the most significant migration
streams carry huge volumes of traffic and that these should be incorporated into
thinking about malaria control.
Geographical Framework of Migration for Malaria Elimination
Programmes for control and eradication of malaria in Africa during the 1950s were
undermined by failure to take account of population mobility, and by the
difficulties of access to and adequate health care provision for mobile sectors of
the population . A geographical framework of malaria dispersal is needed
for contemporary national planning and regional coordination of malaria control
measures directed towards elimination.
To build such a framework, there is an urgent need for better data on circulation
within countries and short-term circulation of populations around porous borders.
Countries that have multiple parasite populations, such as the Democratic Republic
of the Congo, require detailed surveys of travel behavior across their territory,
while countries with large populations of IDPs such as Uganda and Sudan (including
Darfur) are also key.
Data on permanent internal migration can be used to describe migration routes and
possible migration streams but cannot inform as to the frequency of travel between
different places. Permanent migration data from census are informative, but the
national scale of the data is not sufficiently high resolution to begin to
disentangle the movement of disease within national borders. In particular,
permanent migration data will not allow us to capture information on movements
between countries with leaky borders, or illegal movement between countries. Some
types of circulation in these situations are not captured in surveys because people
do not wish to disclose travel across border areas. One example is when IDPs may
make a series of return visits to their areas of origin for planting and harvesting
but report being present in IDP camps in order to fully avail themselves of food
Mapping the dispersal of drug resistance mutations has potential utility in defining
regions that encompass significant population mobility and quantifying population
connectivity. Such measures summarise the circulation of parasites through all types
of migration and have value in this respect, but they are not informative about
which migrant sectors of the population should be prioritized for malaria prevention
and treatment intervention.
Need for Migration Data in the Containment of Artemisinin Resistance
As we have noted, migration has historically played a pivotal role in the global
dissemination of drug resistance. Therefore, the recent confirmation of resistance
to artemisinins on the Cambodia–Thailand border  has triggered a concerted
effort to contain it. In the policy document “Global Planning Artemisinin
Resistance Containment” , the World Health Organization identifies three tiers of
risk, and implies that migration data are central to their definition. Tier I areas
have credible evidence of artemisinin resistance; Tier II areas have significant
inflows of people from Tier I; and Tier III areas have no evidence of artemisinin
resistance and limited contact with Tier I.
Although most of Africa can be comfortably classified as Tier III, the risk posed by
incoming migrants cannot be assessed without knowing the number and final
destination of travelers, together with their likelihood of carrying a malaria
infection. There is currently no policy for screening travelers to Africa and no
interventions to prevent the importation of artemisinin-resistant malaria into
Africa. Gathering data on malaria infection rates among incoming travelers should be
a priority for African national malaria control programmes.
Policy Needs and Recommendations
Clearly the current data on transit in Africa are limited, and more migration data
are needed. A geographic framework of human migration at local, national, and
international levels is particularly essential. It is only through the establishment
of such a framework that policy and services can respond appropriately to the needs
of migrants and at the same time sustain the gains made in malaria control
initiatives. For example, we need to:
1. Identify networks of high volume transit and migration within Africa. This
should include non-permanent and cyclical transit both within and between
2. Apply malaria control and elimination interventions across areas that
encompass significant volumes of migration.
3. Identify mobile communities and mobile sectors of the population who need to
be prioritized in the provision of malaria treatment and prevention
4. Provide targeted health care to these communities.
Transit at the inter-continental, national, and local level have all played a role in
the dispersal of antimalarial drug resistance in the past. Arguably, the
international transportation of artemisinin-resistant parasites by human migration
is the greatest threat to the antimalarial treatments used in Africa today. There
are currently no policy measures in place to prevent the importation of
artemisinin-resistant parasites to Africa. As a result, we also need to:
5. Gather data on the volume of migration between areas of confirmed artemisinin
resistance and African destinations.
6. Establish what the rate of malaria infection among such travelers is and what
proportion will travel to areas where transmission can potentially occur.
Once the risks of importation are quantified “a speedy, scientifically
sound, and coordinated response from affected countries, donors, and
international organisations” is needed .
7. When artemisinin resistance eventually emerges in Africa, apply migration
frameworks to guide strategies for the containment or management of
resistance through use of alternative treatment combinations.
Molecular markers for resistance to drugs of the past provide insight into the
drivers of resistance dispersal. If the rules governing the spread of resistance can
be elucidated now, then policy interventions to protect the efficacy of artesimin
combination therapies can be designed proactively rather than reactively and the
threat of resistance to new treatments managed with foresight.
Exploring the asylum-migration nexus: A case study of transit migrants
Global Commission on International Migration
Migration and Development
Inter-Parliamentary Union (IPU)
Disease and mobility: a neglected factor in
Int J Epidemiol
Migration and health: A framework for 21st century
A world malaria map: Plasmodium falciparum endemicity in
Malaria Control among Refugees and Displaced persons
Migration and malaria risk.
Health, Risk & Society
Economic and social consequences of malaria in new colonization
projects in Brazil.
Social Science and Medicine
Disease and dislocation: the impact of refugee movements on the
geography of malaria in NWFP, Pakistan.
Social Science & Medicine
Populations on the Move.
Third World Quarterly
The origins and spread of antimalarial drug resistance: lessons
for policy makers.
Following the path of most resistance: dhps K540E dispersal in
African Plasmodium falciparum.
International population movements and regional Plasmodium
falciparum malaria elimination strategies.
Proceedings of the National Academy of Sciences
14. PearceRJPotaHEveheMSBa elHMombo-NgomaG
Multiple origins and regional dispersal of resistant dhps in
African Plasmodium falciparum malaria.
Emergence of a dhfr mutation conferring high-level drug
resistance in Plasmodium falciparum populations from southwest
J Infect Dis
Molecular correlates of high level antifolate resistance in
Rwandan children with Plasmodium falciparum malaria.
Antimicrob Agents Chemother
A database of bilateral migrant stocks.
Available at http://www.migrationdrc.org/research/typesofmigration/global_migrant_origin_database.html
Uganda Demographic and Health Survey 2006. Kampala, Uganda and
Calverton, Maryland, USA
Uganda Bureau of Statistics (UBOS) and Macro International
Sustainable livelihoods, mobility and access needs
Transport Research Laboratory
United Nations High Commissioner for Refugees Global Appeal