Malaria and the mobile and migrant population in Cambodia: a population movement framework to inform strategies for malaria control and elimination

Migration and health have become a major concern in the last few years in the context of globalization and has drawn attention from policy makers both from governments and from international institutions [1, 2]. In 2010, at global level, it was estimated that migrants represented almost one billion people, consisting of 214 million international migrants (40% moving between neighbouring countries) and 740 million internal migrants [1]. The most general definition of “migrants” refers to individuals who changed their usual place of residence for more than 1 year. This can be refined and adjusted depending on the lens used to look at population movement [2]. In addition to people who may, on a more longer term basis, move primary place of residence (migrate), there are also people who are mobile for short periods of time, for work, cultural, social or tourism reasons. In this paper, the term HPM is used when referring to the processes involved in population movement and mobile and migrant population (MMP) when referring to people (individuals) in movement, although this is not a homogeneous or fixed group [3]. HPM in relation to health outcomes and potential health threats (emerging or re-emerging diseases) is a global concern, fuelled by globalization and demographic and socio-economic disparities [1, 2, 4, 5]. From a global health perspective, population movement, has been and continues to be considered one of the main drivers of major infectious disease transmission, as MMP are exposed to higher risks of infectious diseases or risks of not receiving adequate treatment compared to non-migrant population [4]. This is illustrated historically by plague and cholera and related quarantine measures and more recently by the severe acute respiratory syndrome (SARS) in 2003, the influenza H1N1 pandemic in 2009 and the Ebola outbreak in 2014 [4]. Three main factors need to be considered when looking at migration and health: (1) disparity of health environments (2) movement of population between regions of different prevalence of health indicators (3) vulnerability of migrants population during the various phases of migration [6]. The complexity of the migration processes, the lack of common terminology, the importance of health determinants (biological, behavioural, environmental and socio-economic) have led to the development of population-based frameworks to inform policy-makers and strategies relating to the migrant population, at various spatial and temporal scales [2, 4, 7]. Population movements can be categorized according to spatial and temporal characteristics: spatially, migration can occur within a country (rural/urban, rural/rural and urban/urban) or between countries (contiguous and non-contiguous international movement) [8]; while temporally, distinctions are made between migration (permanent/very long term change of residence) and circulation (shorter-term and cyclical movements, no change of residence) [9]. As defined by Gushulak [6]: “A population health-based approach considers the relationship between migration and health as a progressive, interactive process influenced by temporal and local variables”.

Population movement has historically posed a huge challenge to the control and elimination of malaria. In 1957, at the time of the Global Malaria Eradication Programme, the WHO Malaria Expert Committee stated that “mass movements within or through a malarious country in the malaria season are likely to cause an exacerbation of the disease to the extent of often precipitating a severe epidemic”. [10]. More recently, following the renewal of the malaria elimination paradigm [11, 12], the critical need to address population movement to achieve and sustain malaria elimination has been recognized in view of the central role it plays in the reintroduction of imported cases into malaria-free areas and in the spread of drug resistant parasites to new areas [8, 13‐17]. In relation to malaria, Prothero and others have described the importance of the distinction between migration and circulation, and the need to apply various temporal and spatial dimensions to distinguish different categories of human mobility depending on seasonality of agricultural or forest related activities [9, 18]. These concepts have been applied to describe mobility patterns in northern Thailand [9, 19]. The recent identification of artemisinin drug resistance on the Thai–Cambodia border along with the renewed calls for the elimination of malaria have once again, brought to the fore the relevance of HPM to National Malaria Control Programmes (NMCPs) and stakeholders in the region [13, 20, 21]. These have led to further studies based on the typology of HPM developed by Prothero and aimed at inform global, regional and national strategies both in the context of the spread of anti-malarial drug resistance, and malaria elimination [7, 8, 16, 22‐26].

In the World Health Organization’s Global Plan for Artemisinin Resistance Containment (GPARC), operational research into MMPs is highlighted as a vital part of containing and preventing resistance and this has been further emphasized in the Emergency Response to Artemisinin Resistance (ERAR) framework [14, 15]. According to the strategy document, building scalable models to reach MMPs should be the highest priority for research. In the GMS, individuals moving from areas of high to low transmission hinder control and elimination of malaria by importing infections and acting as sources of local transmission, while facilitating the spread of drug resistance parasites [27‐30]. High frequency of cross-border movement has been documented between Cambodia and its neighbours: Thailand, Laos and Vietnam [27, 29]; and the frequency of border-crossing among Cambodian people has previously been associated with malaria infection [31].

The concept of “push and pull factors” has been used to better understand the factors affecting population movement [2, 6, 29, 30, 32, 33]. In Cambodia, as elsewhere in Asia [34], poverty is closely related to migration, with most internal migration being due to economic reasons [35‐37]. Initially pushed to migrate due, for instance to landlessness (sometimes related to catastrophic health expenditures) or lack of economic opportunities at the place of origin, MMPs at their destination still lack land ownership, proper housing and basic assets, and have access only to non-permanent or short-term jobs, “3D jobs (Dirty, Dangerous and Disliked)” which allow them only to maintain the status quo rather than improving their standard of living [36]. Land use and land resources are therefore the main drivers of population movement from the densely populated central areas to the less densely populated forested and border areas, rich in natural resources [35‐37]. Mobile populations come to the new place, attracted by land development, with a variety of purposes which include farming work, mining, investment, trade, visiting relatives, and eventually the prospect of finding a new settlement [35]. Poverty affects families in both the place of origin as a push factor and at the place of destination where migrants and mobile populations can get caught further in a poverty cycle, especially when as non-immune individuals they are exposed to malaria.

Vulnerability is a complex concept and has been used in different settings (disaster management, climate change, poverty, HIV/AIDS). Bates et al. described vulnerability in terms relevant to malaria and MMPs as: “Vulnerability encompasses the factors that lead to variation in the impact of disease between different communities and individuals”. Those factors have been identified at various levels: individual level (biological and disease related factors); household and community level (social and economic factors); meso/macro level (environmental and institutional factors) [38].

At a macro level, the malaria ecosystem in Cambodia, as in most of South-East Asia, is mainly related to the forests, and has been described as “forest malaria” [39]. This is because the main malaria vectors in Cambodia are forest vectors: Anopheles dirus (usually found in thick forest or forest fringe) and Anopheles minimus (present in edges of flowing waters such as foothill streams, and springs). The highly anthropophilic and exophagic characteristics of An. dirus combined with early biting behaviour makes it a highly efficient malaria vector and raises the issue of outdoor and residual transmission and the importance of the type of housing. Although the size of forested areas has drastically reduced over the past few years, forest-related activities are still important sources of income for a significant proportion of Cambodians. Therefore at an individual level, individuals living close to the forest and forest goers, including those staying overnight in forest huts, have a higher risk of being parasitaemic than people further away from forest or village residents [40‐44]. Working primarily in the forest or residing in the forest have also been identified as important risk factors for malaria infection in Vietnam [45‐48] and Thailand [49‐52]. Housing types (types of wall, roof) and constructions conditions have been shown to be associated with mosquito entry, and individuals living in poorly constructed houses, bamboo or mud houses have been found to be at higher risk of malaria than those living in wooden, concrete or cement houses [46, 53‐61]. Housing conditions in forest settings are often basic; sometimes there are no houses so temporary visitors simply sleep in a hammock between two trees.

At the household and community level, malaria has been found to affect the poorest of the poor with 58% of malaria deaths occurring among the 20% poorest of the world population [62], although a review published in 2005 found mixed evidence on the link between poverty and malaria incidence at individual and households levels [63]. A more recent systematic review found that the odds of malaria infection among the poorest children was higher than among the least poor [64]. More specifically in South-East Asia, a higher risk of infection has been shown among the poorest and among forest goers or migrants seeking work in the forest in Cambodia [41, 42], Thailand [65, 66] and Vietnam [47, 48].

MMPs are biologically more vulnerable to malaria because they often come from non-forested areas where they are not exposed to malaria, to forested areas where they are. Compared to the local population who will have developed a relative immunity to malaria through repeated exposure, non-immune travellers and migrants, bitten by an infected mosquito, have a higher risk of becoming parasitaemic, having a high parasitaemia, clinical malaria, severity and death [9, 32, 38, 67‐71]. This increase in risk has been described in the context of forest malaria, in Thailand [19, 50, 72], Cambodia [41], India [73], and Brazil [74]. Studies conducted in Indonesia among migrants from Java to Irian Jaya demonstrated that in such a situation, non-immune migrants would develop protective immunity towards malaria within 12–24 months after moving to the new area [75, 76].

Education and knowledge are key factors in influencing malaria prevention and treatment-seeking behaviour although the relationship between knowledge and behaviour is complex and the result of the interaction of social, cultural and economic factors [35, 38, 69]. Mobile and migrant population are less likely to be aware of existing health services than local long term residents [29, 34, 68, 77] and if they arrive from non-malaria areas are less likely to have heard health education messages for malaria than local population living in malaria transmission areas [35, 78]. In the Mekong Subregion, poor knowledge of malaria transmission and prevention has been shown to be a risk factor of malaria infection [48, 50, 65, 66].

The effectiveness of insecticide-treated nets (ITN) in reducing malaria morbidity and mortality is clearly recognized [79] and the universal coverage of this intervention is now one of the two main pillars of the malaria control strategy globally [12]. However ownership and actual use of different types of prevention measures will affect exposure to mosquito bites [61, 80‐82]. There is evidence that ITNs are effective in protecting migrants and/or forest goers, and that conversely the lack of ownership or use of ITN or insecticide-treated hammock nets (ITHN) is a risk factor of infection as shown in Thailand [51, 52, 66, 83, 84] and Vietnam [45‐47]. Furthermore, the use of ITHN by forest goers has been shown to reduce incidence and prevalence among forest goers in Vietnam [85] and to reduce mosquito bites in Cambodia [86]. However, in the Cambodia Malaria Survey 2010, the use of nets by forest goers, travellers or visitors was slightly lower than the general population and the proportion of forest goers, living more than 2 kms from the forest, using a long lasting insecticide net (LLIN) when they stayed overnight in the forest was low at 13.6% [42].

Since the Alma Ata declaration [87] the importance of the access in determining use of health services use has been well recognized. The concept of “access” is often described as consisting of the following dimensions: availability, accessibility, accommodation, affordability and acceptability [88‐90]. Distance, or more importantly, travel time from population settlements to health facilities or health providers are an important component of access to health care and have been described or modelled in various settings [91‐94]. This issue is particularly important for mobile and migrants population working in remote forested areas, in Cambodia and in the GMS and constitute one of the major barriers to reaching these population and for them to access diagnosis and treatment services [28, 29, 34, 78, 95‐97]. The high mobility of the MMP is known as one of the main limitations for malaria control and elimination in the GMS and the mobility of the work location has been identified as an important determinant of access and outreach [28, 95, 98].

Many of these factors contribute to the high incidence of malaria amongst MMPs in Cambodia when compared with the more “static or less mobile” population of similar socio-economic and demographic profile typically captured in standard household surveys: the results of a national malaria survey conducted in Cambodia in 2010 showed that the prevalence of malaria among mobile populations (including travellers, visitors, and forest goers) is generally higher than the resident population and that the odds of having a positive blood slide increase three-fold for forest goers compare to non-forest goers [42].

To address this challenge and to support the goals of the National Malaria Elimination Strategy 2025, the Cambodian NMCP proposed the development of an MMP strategy aimed at adapting and better targeting interventions to these hard-to reach populations [99]. In order to contribute to this process and as a first step towards further planning and research, a population movement framework (PMF) was developed in the context of malaria in Cambodia. This was needed to differentiate between different types of MMPs, based on key characteristics that would help to determine the most effective strategies to target and reach these populations with the most appropriate interventions. The process involved characterising and defining the MMPs in Cambodia, identifying the different activities and risks as well as the types of intervention strategies needed to appropriately target this high malaria risk group.

This paper describes the process and the resulting framework, starting with a formulation of the key research questions based upon the need to have a more refined and user friendly means of classifying risk and vulnerability for MMPs. The research questions were formulated as follows: