Migrants as a Major Risk Group for Imported Malaria in European Countries Patricia Schlagenhauf, Robert Steffen, and Louis Loutan cation with surveillance groups provided additional information. It has been estimated that at the end of the twentieth century, some 150 million people were living outside the country of their birth. International travel and migration are changing the epidemiology of imported malaria in Europe. A growing proportion of imported cases is seen in immigrants and refugees arriving and in settled migrants returning to their country of origin to visit friends and relatives (VFR). Physicians in industrialized countries need to be aware of the malaria risk in these communities from both a prevention and treatment perspective.1 The goal of this research was to quantify the current situation in Europe. Proportion of Nonnationals Depending on the country of origin of the report, the proportion of cases varied from 33% in the United Kingdom to 86% in a region of France, reflecting the profile of immigration in various areas at different time points. On pooling the reports, 43% of malaria cases registered in important European centers occur in nonnationals, frequently settled immigrants VFR. In Italy, where 44% of cases were related to foreigners, VFRs accounted for 72% of the cases reported in this group.2 Methods and Results Increasing Proportion of Nonnationals All reports describe an increasing proportion of malaria cases occurring in nonnationals. In the report describing imported malaria cases in northern Italy,4 the proportion of immigrants increased from 34% in 1991 to 59.9% in 1995 (p = .002). In the Netherlands, for the period 1979 to 1988, only 15% of cases were in persons originating in a malaria-endemic area, whereas for the period 1991 to 1994, 40% of cases were in persons from malaria-endemic areas, and 8% of cases were in children born to settled immigrants resident in the Netherlands.5 Systematic searches of MEDLINE and available national malaria statistics were scanned to identify studies and reports showing the proportions of malaria cases occurring in nonnationals in European countries. Nonnationals were defined as being foreign born residents, which embraces various categories of migrants, including immigrants, refugees, asylum seekers, foreign workers, illegal migrants, or aliens. Only reports describing more than 250 malaria cases were included in the analysis. The period of the search was January 1991 to September 2001. A total of five MEDLINE reports2–6 were found that satisfied the inclusion criteria, and personal communi- Comment Data from the aforementioned studies show that residents of foreign origin represent a growing proportion of imported cases, reflecting to some extent the increasing number of migrants in western Europe. In Britain, an older study has shown that migrants VFRs have a malaria incidence rate almost three times higher that that of tourists to Africa,7 suggesting a higher risk of exposure and/or insufficient protection measures. Although no prospective studies exist that confirm the hypothesis, migrants VFRs may be more exposed as they visit their families in rural areas with higher transmission rates and simple nonair-conditioned living conditions. Many return home during summer holidays, a period corresponding to the rainy season in West Africa or to the monsoon season in India when malaria transmission is at its peak. Many migrants VFRs mistakenly believe that they retain lifetime immunity and although immunity does wane when constant reexposure stops, some immunologic memory remains that partly explains the lower case fatality in Patricia Schlagenhauf, PhD, Robert Steffen, MD: University of Zürich Travel Clinic and World Health Organization Collaborating Center for Travelers’ Health, Institute for Social and Preventive Medicine, University of Zürich, Zürich, Switzerland; Louis Loutan, MD, MPH: Travel and Migration Medicine Unit, Department of Community Medicine, University Hospital of Geneva, Geneva, Switzerland. The authors had no financial or other conflicts of interest to disclose. Correspondence: Patricia Schlagenhauf, PhD, University of Zürich Travel Clinic and World Health Organization Collaborating Center for Travelers’ Health, Institute for Social and Preventive Medicine, University of Zürich, Sumatrastrasse 30, 8006 Zürich, Switzerland. J Travel Med 2003; 10:106–107. 106 Schlagenhauf et al., Migrants as a Major Risk Group for Imported Malaria in European Countries 107 Table Major Reports on Imported Malaria Cases in Europe (1991 to 2001) Paper/report* Total no. of cases Nonnationals Proportion of nonnationals Romi 2001 Italy TropNetEurop† 2001 Europe Minodier 1999 France Matteelli 1999 N.Italy CNRMI‡ 1999 France Wetsteyn 1997 Netherlands Bradley 1994 UK Total 5,898 2,595 2,679 884 315 271 694 416 3,069 1,596 286 137 3,551 1,172 16,492 7,071 44 % 33% 86% 60% 52% 48%§ 33% 43% *Selection criteria for papers and reports: reports on imported malaria cases in Europe with n > 250 with specified proportion of nonnationals. † Personal communication Tomas Jelinek. TropNetEurop Sentinel Surveillance Report on Plasmodium falciparum September 2001. Notification centers in 15 European countries (accounts for approximately 10% of European cases). ‡ Personal communication Fabrice Legros. Centre National de Référence pour les Maladies d’Importation (CNRMI) report calculates that an estimated 5,940 cases are imported. The number here refers to the notified number of cases. § 40% originally from malaria endemic areas; 8% were children born to immigrants resident in The Netherlands. migrants. This is not the case in children born of settled immigrants who are particularly at risk of acquiring malaria when visiting relatives.3,5 The evidence here points to a growing proportion of cases of imported malaria seen in foreign-born residents and migrants VFRs in Europe. It is necessary to specifically target malaria prevention for such groups on a European scale. New communication channels need to be explored, and we suggest simple immediate measures highlighting malaria risk, such as (1) stickers for airline tickets in the migrants’ languages designed in a culturally sensitive way and (2) in-flight messages both to and from malaria destinations detailing malaria prevention measures on the in-flight and providing advice on coping with suspected malaria on the return flight, respectively. Acknowledgment PS did the search, collated, and analyzed the data and drafted the paper. LL and RS contributed to the concept and background information and to revising the paper. References 1. Loutan L. Malaria in migrants. In: Schlagenhauf P, ed. Travelers’ malaria. Hamilton, ON: BC Decker, 2001:285–302. 2. Romi R, Sabatinelli G, Majori G. Malaria epidemiological situation in Italy and evaluation of malaria incidence in Italian Travelers. J Travel Med 2001; 8:6–11. 3. Minodier P, Lanza-Silhol F, Piarroux R, et al. Imported pediatric malaria in Marseille (French). Archives de Pediatrie 1999; 6:935–943. 4. Matteelli A, Colombini P, Gulletta M, et al. Epidemiological features and case management practices of imported malaria in northern Italy 1991-1995. Trop Med Int Health 1999; 4:653–657. 5. Wetsteyn JCFM, Kager PA, van Gool T. The changing pattern of imported malaria in the Academic Medical Center , Amsterdam. J Travel Med 1997; 4:171–175. 6. Bradley D, Warhurst D, Blaze M, Smith V. Malaria imported into the United Kingdom in 1992 and 1993. Communicable Disease Report. CDR Review 1994; 13:169 –172. 7. Phillips Howard PA, Radalowicz A, Mitchell J, Bradley D. Risk of malaria in British residents returning from malarious areas. BMJ 1990; 300:499–503. Venice, Italy. Submitted by Charles D. Ericsson, MD.
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