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Volume 18, Number 10—October 2012

Letter

Duffy Phenotype and Plasmodium vivax infections in Humans and Apes, Africa

Suggested citation for this article

To the Editor: Benign tertian malaria, caused by Plasmodium vivax, has long been considered absent, or at least extremely rare, in western and central Africa. In these regions, 95%–99% of humans are of the Duffy negative phenotype, a condition that is thought to confer complete protection against the parasite during the blood stages of its life cycle (1,2). Sporadic reports throughout the latter half of the 20th century, however, have hinted at the presence of the parasite in these regions, the most convincing of which were the steady and consistent numbers of non-African travelers who returned to their countries of origin infected with malarial parasites that were subsequently identified as P. vivax (2).

More recently, evidence has emerged regarding the transmission of P. vivax in regions of Africa where the local human population is predominantly Duffy negative (36). In 4 (3.5%) of 155 patients from western Kenya (6), 7 (0.8%) of 898 persons from Angola (4), and 8 (8.2%) of 97 persons from Equatorial Guinea (4), P. vivax parasites were detected in the blood of apparently Duffy-negative persons, suggesting that the parasite might not be as absolutely dependent on the Duffy receptor for erythrocyte invasion as previously thought. These findings are supported by a report from Madagascar (where the human population is composed of a mixture of Duffy-positive and Duffy-negative persons), in which 42 (8.8%) of 476 Duffy-negative persons who had symptoms of malaria were reported to be positive for P. vivax by both microscopy and PCR (7). The prevalence of P. vivax in Duffy-negative persons was significantly lower than its prevalence in Duffy-positive persons residing in the same area, suggesting that Duffy negativity is a barrier to the parasite to some degree. Given the extremely high rates of malaria transmission in western and central Africa, a P. vivax parasite that could efficiently invade Duffy-negative erythrocytes would, presumably, become highly prevalent very rapidly.

With the exception of the cases reported from Angola and Kenya, which lie outside the area where the proportion of the population with Duffy negativity is highest, the reports of the transmission of P. vivax within predominantly Duffy-negative populations all come from regions inhabited by chimpanzees and gorillas (i.e., Democratic Republic of the Congo [3], Uganda [4], and Equatorial Guinea [5]). During our seroepidemiologic study from the Democratic Republic of the Congo, in which P. vivax sporozoite–specific antibodies were detected in ≈10% of the population, we found that women were significantly more likely than men to have been exposed to P. vivax sporozoites (3). Women in this region typically spend more time than men near the forest fringe, where they work in crop fields. This forest is within the known habitat range of the chimpanzee Pan troglodytes and the gorilla, Gorilla gorilla gorilla, both of which have been reported to be natural hosts of the malaria parasite P. schwetzi, which is a P. vivax–like or P. ovale–like parasite that might also be unable to invade the erythrocytes of persons who are Duffy negative (8). These animals have recently been shown to be infected occasionally with parasites that have mitochondrial genomes closely resembling those of P. vivax (9,10).

We have argued that, given the high malaria transmission rates in sub-Saharan Africa, it is plausible that the 1%–5% of the human population who are Duffy positive might maintain the transmission of the parasite (2). The discovery of P. vivax parasites (or P. vivax–like parasites) in the blood of African great apes leads to a question: could nonhuman primates in Africa be acting as Duffy-positive reservoirs of P. vivax in regions where the human population is almost entirely insusceptible? This possibility warrants further investigation. Given the increasing rarity of the great apes, however, their capacity to act as zoonotic reservoirs could be limited. It would be informative, in any case, to determine how the regions that P. vivax–positive travelers visit during their stay in Africa correspond with the ranges of chimpanzees and gorillas.

If African great apes do, indeed, constitute a zoonotic reservoir of P. vivax parasites, what are the repercussions for human health? Given that 95%–99% of humans possibly exposed to such a reservoir are Duffy negative, and therefore resistant to the parasite, these would appear to be slight. However, as humans encroach more frequently into ape habitats, the chances of humans encountering the parasite will increase. In the short term, the risks are probably limited to Duffy-positive persons who enter areas where apes are present, such as tourists and migrant workers.

Richard Leighton CulletonComments to Author  and Pedro Eduardo Ferreira
Author affiliations: Nagasaki University, Nagasaki, Japan (R.L. Culleton, P.E. Ferreira); University of Algarve, Faro, Portugal (P.E. Ferreira); and Karolinska Institutet, Stockholm, Sweden (P.E. Ferreira)

References

  1. Miller LH, Mason SJ, Clyde DF, McGinniss MH. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med. 1976;295:3024. DOIPubMed
  2. Culleton RL, Mita T, Ndounga M, Unger H, Cravo P, Paganotti G, Failure to detect Plasmodium vivax in West and Central Africa by PCR species typing. Malar J. 2008;7:174. DOIPubMed
  3. Culleton R, Ndounga M, Zeyrek FY, Coban C, Casimiro PN, Takeo S, Evidence for the transmission of Plasmodium vivax in the Republic of the Congo, West Central Africa. J Infect Dis. 2009;200:14659. DOIPubMed
  4. Dhorda M, Nyehangane D, Renia L, Piola P, Guerin PJ, Snounou G. Transmission of Plasmodium vivax in south-western Uganda: report of three cases in pregnant women. PLoS ONE. 2011;6:e19801. DOIPubMed
  5. Mendes C, Dias F, Figueiredo J, Mora VG, Cano J, de Sousa B, Duffy negative antigen is no longer a barrier to Plasmodium vivax–molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl Trop Dis. 2011;5:e1192. DOIPubMed
  6. Ryan JR, Stoute JA, Amon J, Dunton RF, Mtalib R, Koros J, Evidence for transmission of Plasmodium vivax among a Duffy antigen negative population in western Kenya. Am J Trop Med Hyg. 2006;75:57581.PubMed
  7. Ménard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, Ratsimbasoa A, Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci U S A. 2010;107:596771. DOIPubMed
  8. Coatney GR, Collins WE, Warren M, Contacos PG. Plasmodium schwetzi. In: Coatney GR, Collins WE, Warren M, Contacos PG, editors. The primate malarias. Bethesda (MD): US Department of Health, Education, and Welfare; 1971. p. 141–52.
  9. Krief S, Escalante AA, Pacheco MA, Mugisha L, Andre C, Halbwax M, On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. 2010;6:e1000765. DOIPubMed
  10. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:4205. DOIPubMed

Suggested citation for this article: Culleton RL, Ferreira PE. Duffy phenotype and Plasmodium vivax infections in humans and apes, Africa [letter]. Emerg Infect Dis [Internet]. 2012 Oct [date cited]. http://dx.doi.org/10.3201/eid1810.120120

DOI: 10.3201/eid1810.120120

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Table of Contents – Volume 18, Number 10—October 2012

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Richard Leighton Culleton, Malaria Unit, Institute of Tropical Medicine, Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan





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