The geography of imported malaria to non-endemic countries: a meta-analysis of nationally reported statistics

Abstract

Background: Malaria remains a problem for many countries classified as malaria free through cases imported from endemic regions. Imported cases to non-endemic countries often result in delays in diagnosis, are expensive to treat, and can sometimes cause secondary local transmission. The movement of malaria in endemic countries has also contributed to the spread of drug resistance and threatens long-term eradication goals. Here we focused on quantifying the international movements of malaria to improve our understanding of these phenomena and facilitate the design of mitigation strategies.

Methods: In this meta-analysis, we studied the database of publicly available nationally reported statistics on imported malaria in the past 10 years, covering more than 50 000 individual cases. We obtained data from 40 non-endemic countries and recorded the geographical variations.

Findings: Infection movements were strongly skewed towards a small number of high-traffic routes between 2005 and 2015, with the west Africa region accounting for 56% (13 947/24 941) of all imported cases to non-endemic countries with a reported travel destination, and France and the UK receiving the highest number of cases, with more than 4000 reported cases per year on average. Countries strongly linked by movements of imported cases are grouped by historical, language, and travel ties. There is strong spatial clustering of plasmodium species types.

Interpretation: The architecture of the air network, historical ties, demographics of travellers, and malaria endemicity contribute to highly heterogeneous patterns of numbers, routes, and species compositions of parasites transported. With global malaria eradication on the international agenda, malaria control altering local transmission, and the threat of drug resistance, understanding these patterns and their drivers is increasing in importance.

Funding: Bill & Melinda Gates Foundation, National Institutes of Health, UK Medical Research Council, UK Department for International Development, Wellcome Trust.

Figure 1

Origins, destinations, and flows of imported cases of malaria from endemic to non-endemic countries (A) Of the non-endemic countries that reported the origin country of imported cases, the average annual number of malaria cases (all species) between 2005 and 2015 exported from endemic to non-endemic countries (red) and imported cases to non-endemic from endemic countries (blue). (B) Malaria endemic to non-endemic country connectivity through cases imported to the non-endemic country. Of the non-endemic countries that reported the origin country of imported cases, the average annual number of malaria cases (all species) between 2005 and 2015 moving from endemic to non-endemic country pairs are mapped as flow lines. Only average annual flows of >50 cases are mapped, with >200 in red, 100–200 in pink, and 50–100 in yellow. The flow lines are overlaid on a map of Plasmodium falciparum prevalence.

Figure 2

Results of community detections on the network of malaria endemic–non-endemic imported malaria pairs Countries mapped in the same colour belong to a unique community, with imported malaria case movements being larger within the communities than between them. Fewer cases in Asia and the Americas had origin–destination information available, making the community detection results less robust. Moreover, with substantially fewer non-endemic countries outside of Europe with strong reporting, analyses simply show the regions as homogeneous single communities.

Figure 3

Plasmodium falciparum prevalence in 2010 versus average annual number of P falciparum cases imported to non-endemic countries for all endemic countries, 2005–15 The circles are coloured by region (green=Americas, pink=Africa, blue=Asia), and their sizes correspond to numbers of outgoing migrants to non-endemic countries. Linear model fit to P faciparum parasite rate (PfPR) against P faciparum cases: r2=0·32; p<0·01.

Figure 4

Pooled data for imported malaria species breakdown to non-endemic regions from endemic ones The figure shows proportions of total imported case numbers, rather than absolute numbers, which are shown in figure 1A.

Figure 5

Species composition of reported imported malaria cases to non-endemic countries mapped by endemic country of origin of the cases