A Review of Risk Factors for Imported Malaria in the European African Diaspora: Table 1

Imported malaria has been described as “an infection that was acquired in an endemic area by an individual (either a tourist or indigenous native) but diagnosed in a non‐endemic country after development of the clinical disease.” 1 In the UK, there was an average of 1,965 laboratory‐confirmed reports of imported malaria infections between 1987 and 2006, 2 and this country, together with France, Germany, and Italy, accounts for about three‐quarters of the 10,000 to 12,000 annual cases imported into the World Health Organization European region. 3 The majority of imported malaria infections reported in European countries are caused by Plasmodium falciparum, 3 the Plasmodium species associated with the most severe disease and mortality. Data from TropNetEurop, 4,5 a European sentinel surveillance system, describe how most cases originate from West Africa and affect travelers of African ethnicity. The most commonly reported reason for travel is to visit friends and relatives (VFRs), with 64.5% of all travelers citing this as a reason for travel in malaria reports between 1987 and 2006 to the UK's Malaria Reference Laboratory and 76.4% in reports to TropNetEurop in 2007. 5 Those VFRs who were born and lived for some time in malaria‐endemic countries before moving to Europe will have acquired partial immunity from exposure to malaria during childhood. Without repeated exposure, immunity appears to wane with time, although the time period during which this occurs is unknown. Bouchaud and colleagues 6 have demonstrated that levels of parasitemia and severe disease were lower in African migrants who were resident outside malarious areas for more than 4 years but acquired falciparum malaria on a short visit to a malaria‐endemic area, when compared to patients who had always lived outside these areas. However, a recent study of African migrants in Italy 7 suggests that living for more than 12 years outside a malarious area could result in a more serious clinical presentation with malaria. This highlights the importance for ex‐residents of malarious countries to maintain the same malaria preventative measures as other travelers. National and international malaria prevention policies recommend awareness of the risk of malaria, bite avoidance, the use of appropriate chemoprophylaxis, and early diagnosis of malaria‐type symptoms when traveling to a malarious country. A number of studies confirm that the use of chemoprophylaxis is low among VFRs. In a study of 302 malaria cases presenting at a hospital in Italy, Castelli and colleagues 8 found only 11% of “immigrants” compared to 55% of “non‐immunes” had used chemoprophylaxis on their last trip to an endemic area, whereas Driessen and colleagues 9 in a Dutch study reported that statistically fewer children of immigrants had used chemoprophylaxis compared to those children in the indigenous Dutch population (not all study authors use the term “VFR” although it is clear from the context that they are referring to those who are going to visit friends or relatives). Since many of the cases of imported malaria in Europe occur among those groups who have traveled to visit friends and relatives in endemic countries, it is of considerable public health importance to try to understand why so few VFRs protect themselves against malaria when they go to visit friends and relatives abroad. As a first step toward a better understanding of these behaviors, a review of the literature was undertaken to find out what is already known about this subject. English language articles published from 1990 (the approximate date from when cases of imported malaria began to increase) to December 2008 were searched, using the bibliographic databases “Pubmed,”“Web of Knowledge,” and “Embase”; search terms were: “migrants and malaria,”“immigrants and malaria,”“imported malaria,” and “visiting friends and relatives.” Reference lists from articles considered for inclusion were also searched. Articles set in European countries, in which primary research into the reasons for the high incidence of malaria in the African community were explored, focusing in particular on knowledge, attitudes, and behavior of travelers. Papers published before 1990; set in countries outside Europe; those which dealt only with the clinical management of individual imported cases; the main text (excluding abstract) was written in a non‐English language paper. Eighty‐six papers were identified by the search, of which three met the inclusion criteria and were selected for analysis (Table 1). Studies included along with methodology, design, and number of study participants *Whether “vaccinations” were taken was used as a proxy for seeking pre‐travel advice following focus group discussions showing study participants' confused pre‐travel advice with treatment. Studies included along with methodology, design, and number of study participants *Whether “vaccinations” were taken was used as a proxy for seeking pre‐travel advice following focus group discussions showing study participants' confused pre‐travel advice with treatment. The three studies which fitted the inclusion criteria were small scale, of differing designs, and used varying methodologies. Analysis was also hampered by a lack of uniformity in the definitions used. Despite the constraints encountered in synthesizing the research findings from these studies, it was possible to identify three specific areas that are relevant to the increased malaria risk in VFRs. These were: knowledge of how malaria is transmitted (n = 2), perceptions surrounding risk (n = 3), and attitudes affecting the use of chemoprophylaxis (n = 3). The data on each area are considered in turn. Pistone and colleagues 10 found that in a study of VFRs in Paris, 141/191 (74%) of subjects interviewed knew that malaria was transmitted by mosquitoes. This study also found no statistical difference in knowledge between those attending a travel agent and those visiting a travel clinic, with the other most commonly mentioned malaria transmission routes being dirty water (6%) and the sun (4%). In the study of immigrants from West Africa in the Netherlands, Schilthuis 11 found that only 81/292 (28%) named mosquitoes as the sole route of transmission. In this study, Schilthuis 11 categorized knowledge of the causes of malaria into “adequate,”“inadequate,” or “unclear,” the latter being a combination of “adequate” and “inadequate” knowledge. “Adequate” knowledge included perceptions of insufficient immunity and knowledge of transmission and exposure (virus or parasite, exposure outside in the evening) and blood transfusion, which occurred in 47/292 (16%) of respondents. “Inadequate knowledge” included drinking bad water, eating bad food, dirt/dirty environment, malnutrition, weather or climate, too much sun/heat, insects, standing water, too much thinking/overworking/stress, dirty water, contaminated air, taking too much antimalarial medicines for prevention, and change of environment. The proportion of participants with “inadequate” or “unclear” knowledge was 152/292 (52%). Travelers who received pre‐travel advice were significantly more likely to demonstrate “inadequate or unclear knowledge” (OR 2.22, CI 1.13–4.38). Perceptions about theoretical and personal risk of contracting malaria were compared in both the French and Dutch studies. 10,11 The French researchers found that 87% of respondents knew it was possible to get malaria in the country they were visiting; however, only 49% considered themselves at personal risk. While there was no difference between those attending the pre‐travel clinic and those visiting a travel agent in their general knowledge of the possibility of contracting malaria, there was a difference in perception of personal risk. Thirty‐three per cent of those who had visited a travel agency believed themselves to be at high risk of malaria compared to only 7% of those who had visited a travel clinic (p < 0.05). In the study of Dutch VFRs, 11 perceived risk of catching malaria was assessed as either “high” or “not high.” Overall, 54% considered it to be high, 33% having sought pre‐travel advice. To measure personal risk, participants were asked how dangerous the risk was for themselves, compared to specific risk groups (the definition of these groups was not provided). Forty‐six per cent categorized the risk to themselves as “very dangerous.” Two studies (in the Netherlands 11 and the UK 12 ) also provided data on how participants believed they would be protected from malaria and these included perceptions such as sustained immunity, 12 having had a malaria vaccine, 11,12 and never having suffered from malaria previously. 11,12 Biological factors, specifically sickle‐cell trait and/or G6PD deficiency, were also perceived as providing malaria protection. 11 A reduced perception of personal risk was also found among participants in the London study who had been brought up in the UK. Among this group, some participants believed that malaria caught while visiting friends and relatives in an endemic country would result in only a mild illness. 12 Both French and Dutch studies describe the proportion of travelers who intended to or had taken chemoprophylaxis. 10,11 Surprisingly, 201/292 (69%) of Dutch VFRs and 171/191 (94%) of French individuals affirmed their use of chemoprophylaxis. While overall 94% of French participants intended to use chemoprophylaxis, a significantly higher proportion of those attending the travel clinic (119/122; 97%) reported intending to take chemoprophylaxis than those attending a travel agent (60/69; 87%) (p < 0.05). When questioned on return, of the 106 interviewed, 80 (75%) had taken chemoprophylaxis and chemoprophylaxis use was significantly greater among those who had attended a travel clinic (55/64; 86%) than among those who had been only to a travel agent (25/42; 60%) (p < 0.05). Among those taking chemoprophylaxis, 15% had taken chloroquine, which is inadequate for sub‐Saharan Africa. The travel agent attendees were much more likely to be using chloroquine alone (13/42; 31%) than the 3/64 (5%) in the travel clinic group. Only 29% had used appropriate chemoprophylaxis (correct drug, dosage, and adherence including after return), more (p < 0.05) from the travel clinic (26/64:41%) group than the travel agent cohort (5/42; 12%). Several factors influencing the use of chemoprophylaxis among VFRs have been proposed. These include cost 11,12 ; fear of side effects 11 ; uncertainty about drug efficacy, either as a result of “getting used to them” or connected to mosquito resistance 12 ; feeling that the drugs are only effective against a more serious “type” of malaria; and distrust of doctors. 12 Practical concerns include the bitter taste and side effects experienced 12 ; traveling at short notice 11 ; or for short periods of time. 12 The opportunity for sharing chemoprophylaxis with friends and relatives living in the malarious area 10,12 may also influence correct adherence when chemoprophylaxis is obtained. A list of reasons for not “being vaccinated” (a˜proxy term used for taking pre‐travel advice) was described in the Dutch study. 11 In this study, more than 10 participants mentioned never taking preventive measures and buying medication in West Africa. Between five and nine respondents gave their reasons as: having had all vaccinations; not easily getting sick; it not being important or necessary. Less than five reported: “only taking tablets”; it being only necessary for children; cure being cheaper or easier to get; not knowing it was needed; the room being insect free; using traditional methods instead; avoidance of unhygienic food or water; a belief that the individual cannot die now; and protection from God. There have been several calls for more research to be undertaken to understand the reasons for the high incidence of imported malaria in the African community, and for targeted interventions to be implemented to reduce this. 2,13,14 Despite this, although many papers have discussed clinical issues in managing cases of imported malaria or described the epidemiology, very little qualitatively focused primary research, exploring factors that might influence the low use of preventive measures against malaria in these communities, has been carried out. Those studies which were identified were small scale, of differing designs, and the variation in methodologies used hindered true comparison. This means generalizable conclusions are difficult to make. Comparisons are also hampered by a lack of uniformity in definitions used. For example, residency status: The Dutch study included individuals who were presumed illegal immigrants and others who had been living in the country for at least 1 year, 11 whereas the French study described participants as “travelers of African ethnicity” 10 and Morgan 12 used the very broad definition of the “African community in London.” Investigating pre‐travel advice, 11 some participants misunderstood the difference between malaria prevention and treatment, and so the term “received vaccinations” was used as a proxy for seeking pre‐travel advice, a method not used by other authors. A definition of what constitutes accurate knowledge of malaria transmission is required to overcome the striking difference between numbers of respondents who were considered to know how malaria was transmitted in the two studies cited. Knowledge of malaria transmission and the presence of malaria in the country visited did not appear to relate to the uptake of chemoprophylaxis among VFRs. Importantly, perceptions of a reduced personal risk (due to factors such as sustained immunity and lack of susceptibility) were apparent among some VFRs. Understanding that a risk existed did not correlate to their perceived personal risk. Knowledge and experience acquired while living in Africa may have influenced these beliefs. A better understanding of the false paradox could provide useful background for those providing pre‐travel malaria advice. The finding that many believed they had received a vaccination reflects confusion among some VFRs. Some might mistake yellow fever vaccination for a malaria vaccination. Alternatively, vaccination may be considered as a term that includes oral chemoprophylaxis, thus creating misunderstanding between respondents and researchers. Perhaps surprisingly, in two of the three studies reviewed in this analysis, the reported use of chemoprophylaxis was fairly high—almost 70% in the Dutch study (69%) and over 60% among those reporting the lowest use in the French study. However, it was only in the French study that data were available on the reported appropriate use of chemoprophylaxis (drug, use, and duration) and this showed that the proportion of VFRs using chemoprophylaxis appropriately was considerably lower (ranging from 12% among those who had used a travel agent to 41% among those who had used a travel clinic). The range of beliefs influencing compliance to chemoprophylaxis including individual concerns such as the bitter taste are cited in two other studies of pediatric imported malaria. 15,16 Respondents focus on concerns about health care services, including a distrust of doctors, and structural barriers to health, when traveling at short notice. Migrants in many European countries often live in areas of high socioeconomic deprivation, 17,18 and money spent on travel may take priority over the expense of chemoprophylaxis. Some migrants may be unwilling to engage with the formal health care services. Ten per cent of respondents in the Netherlands did not have health insurance, and were assumed to be there illegally. The poor use of chemoprophylaxis is not restricted to African VFRs, and can occur irrespective of ethnicity. Fifty‐six patients with falciparum malaria who visited the Gambia (a popular tourist destination for indigenous British holidaymakers) had not used chemoprophylaxis. 19 The results from this review demonstrate that research among VFRs to date has focused on individual risk factors for malaria and on recent travel or planned journeys. Furthermore, the data available provide only a superficial understanding of some of the factors that may be influencing behaviors that result in the high incidence of imported malaria seen in the African Diaspora. However, in such research, it is important to recognize that VFRs are far from a homogenous group and additional research into the nature and extent of variation in knowledge, attitudes, and behaviors relating to malaria among the various groups that make up the African Diaspora across Europe is required. While there are some race‐based biological factors (sickle‐cell trait and G6PD deficiency) that contribute to perceptions of risk, in terms of ethnicity it is unlikely if there are discernible patterns of behavior that can be applied to the whole ethnic populations, let alone across populations from different backgrounds. This applies particularly to issues such as the taste of antimalarial tablets and fear of side effects which are not influenced by ethnicity, and care must be taken to not overly attribute failure to access malaria protection to cultural reasons alone. Although most impact on reducing the incidence of imported malaria can be made by focusing on interventions in the African community, understanding why other travelers put themselves at risk will also be important. The results from the review also suggest that there is a need for primary research using qualitative methodology to investigate the context within which personal decisions are made about malaria prevention. For example, the cumulative effect of disease‐free successive journeys may affect perceptions and reduce perceived risk of disease. Although there are differences in the etiology of disease, future themes could be drawn from research in other diseases that disproportionately affect the African Diaspora, such as HIV and TB. Studies into the former, in particular, have recognized the importance of the socioeconomic and structural contexts within which decisions are made about health. 20,21 Finally, research undertaken so far has focused on chemoprophylaxis. Mosquito bite prevention measures are also important with respect to malaria prevention, and there is a need to understand factors that restrict or influence VFRs from using these. The few researchers who have investigated knowledge, attitudes, and practices about malaria in the African Diaspora in Europe have made some valuable initial findings and have highlighted the need for agreement on definitions. Despite this, it is clear that there is no detailed understanding of the behavioral and cultural influences that predicate VFRs' risk of malaria. Understanding the context within which decisions are made by VFRs is important not only to inform public health policy but also to help in the appropriate design and targeting of the interventions. We thank Professor David Bradley, Department of Zoology, Oxford University, for commenting on early drafts of the paper. The authors state that they have no conflicts of interest.