# ImportedPlasmodium vivax Malaria in the Russian Federation from Western Sub-Saharan Africa

Authors: Alla Baranova; Vladimir Sergiev; Lola Morozova; Natalia Turbabina; Evgeny Morozov
Journal: Journal of Tropical Medicine
 (2019)

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## Abstract

Background. Imported cases ofPlasmodium vivaxmalaria from western Africa are reported annually in the Russian Federation. Infected native African people moving from western Africa for different purposes (students, businessmen, specialists, etc.) or Russian citizens (tourists, diplomats, businessmen, etc.) incubate the pathogen until reaching their Russian destination.Methods. All imported and other confirmed malaria cases and the associatedPlasmodiumspecies recorded over the past twenty years throughout the Russian Federation were inventoried. These data were included in the national register. The data of imported malaria cases were analysed according to the species ofPlasmodium, case origin, dates of importation, and patient nationality.Results. A total of 267P. vivax-infected patients who contracted the disease in western Africa were diagnosed in the Russian Federation from 1984 to 2017. Among them, 3 cases had mixed infections (2 withP. vivax +P. falciparum and 1P. vivax +P. ovale). Conclusion. Our data reveal an existing risk of contractingP. vivax infections in towns of West sub-Saharan Africa despite the absence of localP. vivax infection records.


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## Body

## 1. Background

Plasmodium vivaxoccupies the largest malaria-endemic region of the world, followed byP. ovale [1].P. vivaxis almost absent in western sub-Saharan Africa, the epicentre of global malaria endemicity, due to genetic resistance of the local human population, which is in contrast with East Africa whereP. vivax malaria is distributed mainly in Ethiopia, but infrequent further south too.P. ovale is distributed throughout sub-Saharan Africa and South-East Asia, and in the western Pacific. It is responsible for 1-5% of all malaria cases in West Africa [2].There are several known genetic resistance mechanisms againstP. vivax. One of them is Duffy negativity, which is present in western sub-Saharan African populations. The Duffy antigen is located on the surface of red blood cells. The protein encoded by this gene is a glycosylated membrane protein. It is general receptor but has some specificity for chemokines. This genetic aberration is the only one among malaria genetic protection mechanisms without known negative affects to the health of human beings. Duffy negativity as a susceptibility factor had been speculated from epidemiological data before its function was discovered in the 1970s [3]. Duffy negativity in West Africa is attributed to erythrocytes only. The Duffy antigen is not abolished from the membranes of other cells.Nearly 100% of West Africans and their New World descendants, including the majority of Afro-Americans, have Duffy negativity in the form of heterozygotes; and the only place in the world with homozygotes for Duffy negativity are present. This genetic aberration is extremely rare in other ethnic groups. Duffy negativity is so effective in the protection againstvivaxmalaria that several investigators in the United States failed to intentionally infect volunteers withP. vivax[4]. A recent investigation proved the homozygotes for Duffy negativity experienced total protection fromP. vivax, and heterozygous individuals experienced partial protection [5].Therefore,P. vivax almost disappeared from West Africa, but complete elimination was not achieved [6]. Despite the common belief of totalP. vivax absence in West Africa and the lack of local records of the pathogen in western sub-Saharan countries, sporadic cases ofP. vivax malaria imported from the region have been registered in countries where malaria has been eliminated [7]. Data onP. vivax malaria cases in West Africa are absent from WHO documents from the last 10 years [8, 9]. Sporadic cases ofP. vivax malaria among Duffy negative subjects had been detected by PCR in West Cameroon recently [10]. Information regardingP. vivax malaria cases in Ethiopia, Eritrea, Somalia, Sudan, and Madagascar appeared in these documents, and some authors perceived the data as a recent development [5].A confirmation of the presence ofP. vivax in West Africa and imported cases ofP. vivax malaria recorded from that region would be surprising. Unfortunately, the wheel is too often reinvented and history is continually rewritten when there is a clear set of events to look back on, to get to know better, and to understand [11]. The first systematic efforts to map the global endemicity ofP. vivax were undertaken in 2012 only [12].The aim of this paper is to call attention to an existing risk of contractingP. vivax infection, even during a short stay, in towns of West sub-Saharan Africa despite the absence of local records ofP. vivax infection.We present data regarding the importation ofP. vivax malaria from West sub-Saharan Africa to the Russian Federation (1994-2017) and retrospective data (1984-1992) of the USSR.


## 2. Materials and Methods

The WHO Collaborating Centre for Research has been studyingvivax malaria and operating at the Martsinkovsky Institute of Medical Parasitology & Tropical Medicine of the Ministry of Health Russian Federation in Moscow since 1982. In addition to scientific research, the centre conducts epidemiological monitoring and the evaluation of antimalarial measures [13].Each diagnosed malaria case is required to be reported by any medical establishment in the Russian Federation to a local Rospotrebnadzor Department (State Sanitary and Epidemiological Organization) using the official form “Card of Epidemiological Investigation” that contains clinical, laboratory, entomological, and epidemiological information. In addition to reporting to local Rospotrebnadzor Department, thin and thick blood films together with a copy of the Card of Epidemiological Investigation for each identified malaria case are sent to the Reference Centre on Tropical Diseases at the Martsinkovsky Institute (Moscow) for microscopic confirmation by experts in malaria diagnoses. These data have been accumulated in the National Surveillance Register at the Martsinkovsky Institute since 1978. All imported cases are mapped to a country of origin.The information derived from standard cards is entered into a database and analysed annually. The annual report presents data on the aggregate of cases from all parts of the Russian Federation. The reports are distributed to all 85 administrative territories of the country as analytical information.The scope of malaria surveillance as a part of the general state surveillance system is as follows: malaria case reports are entered into a database; data is analysed and disseminated through an annual published analytical letter called “The Malaria Situation in the Russian Federation”; and planning, monitoring, and analysis of the efficacy of antimalarial measures are conducted. Malaria surveillance measures are carried out in all potential foci whenever imported malaria cases occur, as well as in new active foci when local transmission of malaria emerges. These measures include the following:(i)
detection of malaria patients(ii)
epidemiological investigation of cases and foci(iii)
entomological monitoring of breeding places and resting sites(iv)
larviciding with ecologically safe methods (according to the transmission season)(v)
indoor residual spraying of pyrethroids (in cases of local transmission of malaria only)(vi)
environmental measures, including hydroengineering and environmental control of breeding habitats(vii)
medical personnel training(viii)
health education of the foci population.Data on registered cases of malaria in Russia are published in a table with all the reportable pathogens that are transmitted each year, produced by the CISID (WHO/EURO).


## 3. Results

The importation ofP. vivax malaria to Russia from the countries of sub-Saharan Africa occurs almost annually by foreigners (students, businessmen) and Russian citizens (specialists on contracts, diplomats, sailors, and so on). According to the “National Register of Malaria in the Russian Federation” and the “Questionnaire of Epidemiological Survey of Malaria Foci,” 319 patients from sub-Saharan Africa withP. vivax malaria were identified from 1984 to 1992. Among them, 159 Russian citizens and foreigners were infected in 10 western African countries, with the majority infected in Nigeria (Table 1), and 160 patients were infected in eastern and Central Africa.Table 1
Origin of importedP. vivax cases in the USSR and Russian Federation from 1984-2008.
Countries Years TOTAL USSR Russian Federation 1984-1986 1987-1989 1990-1992 1994-1996 1997-1999 2000-2002 2003-2005 2006-2008 Benin 7 14 5 0 0 0 0 0 26  Gambia 4 0 2 0 0 0 0 0 6  Ghana 3 10 5 0 3 3 6 2 32  Guinea 1 4 0 6 3 4 4 2 24  Guinea-Bissau 8 6 1 0 2 3 2 1 23  Ivory Coast 0 0 0 0 5 6 4 4 19  Liberia 0 0 0 0 0 0 1 2 3  Mali 4 12 8 0 8 6 2 0 40  Nigeria 21 23 11 2 2 3 2 2 66  Sierra Leone 1 3 6 3 3 2 4 2 24  TOTAL 49 72 38 11 26 27 25 15 263Apart from imported malaria cases in Russia, Dr. G. Suleymanov (Martsinkovsky Institute, former Senior Researcher) detected three Russian citizen patients withP. vivax malaria that had been working on contracts during his time in West Africa (1991-1992) [14]. Two of them had mixedP. falciparum + P. vivax infections (confirmed microscopically).After the disintegration of the USSR, the number of travellers and persons working under contracts from the USSR/Russia decreased, and subsequently, the number of importedP. vivax malaria cases from West African countries to the Russian Federation decreased.From 1994 to 2008,135 imported cases ofP. vivax malaria from Africa were registered; among them, 104 were from West Africa [15], including 3 mixed infections: 2 -P. falciparum + P. vivaxand 1 -P. vivax + P. ovale (rare combination of two types of tertian malaria) (Table 1). There were998 imported cases ofP. falciparummalaria from Africa detected in the Russian Federation during these years, and among them,241 were from West Africa. One death attributable to malaria (P. falciparum + P. ovale) was reported in 2012 and occurred in a Russian resident visiting Sierra Leone.AllP. vivax malaria cases presented a fever, but none had severe and life-threatening conditions. All patients withP. vivax malaria received chloroquine for a 3-day period followed by a 14-day course of primaquine.Only twenty subjects reported compliance with malaria chemoprophylaxis (mefloquine or atovaquone/proguanil). All of them had visited West Africa and did not complete the drug regimen. No history of individual chemoprophylaxis was available for the remaining cases.ImportedP. vivax cases in 2009-2010 and 2013 originating in West African countries were not registered. One case from Guinea was recorded in 2011, one case from Cameroon was recorded in 2012, and two cases (Ivory Coast and Mali) were recorded in 2014. ImportedP. vivax cases from West African countries were not registered in 2015-2017. Thus, the total number of imported malaria cases from western sub-Saharan African countries for 1984-2017 is 267. The West African countries that served as the source of imported malaria cases are presented in Figure 1.Figure 1
Countries of western Africa served as a source of importedP. vivax malaria to the USSR and Russia.


## 4. Discussion

Imported cases ofP. vivax to Russia from the countries of sub-Saharan Africa differed from those of the Newly Independent States (NIS) countries by clinical manifestation. Among the latter were a higher number of manifestations after long-term incubation of the pathogen (45% of imported cases from Tajikistan and 50% from Azerbaijan) [16].Most imported cases of tertian malaria (P. vivax) by Russian citizens from sub-Saharan Africa presented the first clinical manifestation of the disease on the 12th-14th day after arrival in Russia. None of the importedP. vivax cases were followed by “introduced cases,” despite the susceptibility of endemic Russian mosquitoes toP. vivax from foreign countries [16].The great majority of the cases (92.5%) were located in cities where the conditions for transmission were not favourable and medical care was easily accessible, i.e., early detection of patients was possible. In addition, the return of foreign students and Ph.D. students after their summer vacations occurs in October, when the transmission season ofP. vivax by the mosquitoesAnopheles maculipennis, An. messeae, orAn. sacharovi is over in the Russian territory.The limitation of the study is travel histories of patients withP. vivax infection. Data of each case been collected for the last three years period, but we could not exclude that any individual presented his/her information incorrectly due to memory or other problems.


## 5. Conclusions

The results of the research analysis reveal an existing risk of contractingP. vivax infection in towns of West sub-Saharan Africa by local residents and foreigners despite the absence of local records ofP. vivax infection. The appearance of imported cases ofP. vivax malaria from that region of Africa should be considered in Russia and other countries.This article can be used by epidemiologists to refine the global area ofP.vivax distribution and by clinicians for the timely and correct diagnoses and treatment of malaria patients who arrive each year from African countries.A current understanding of the spatial epidemiology and geographical distribution ofP. vivax is far less developed than that forP. falciparum, representing a barrier to rational strategies for control and elimination of the disease. This communication may be considered important for studies onP. vivaxdistribution in sub-Saharan African countries.



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