Year of the Monkey, Implications for Malaria

As human population expands and people move into once seemingly remote wilderness, there is greater contact between people and various animals and the greater chance for the spread of zoonotic disease. The West African Ebola outbreak is a case in point.[i] Now as the Lunar Year of the Monkey has begun, it is an important time to highlight the potential of shared disease between humans and their primate cousins.

 

image001The most widely known form of malaria that people acquire from monkeys occurs in Southeast Asia, Plasmodium knowlesi. The blame has been laid squarely on the shoulders of deforestation caused by human expansion into what was previously the primary domain of macaque monkeys. The discovery of the parasite is credited to Giuseppe Franchini in 1927[ii]. Published studies in English date back to the late 1930s.[iii],[iv] and for the next seven decades the primary focus of most research was on the effect on monkeys themselves as well as use of the parasite to model human disease.

 

African primates have been implicated in malaria transmission also. Researchers working in Gabon foundPlasmodium falciparum, the most common species of malaria in Africa in the greater spot-nosed monkey (Cercopithecus nictitans).[v] Today wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax, with the implication that, “All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.” [vi]

 

Duval and colleagues studied malaria in chimpanzees and gorillas in Cameroon. They found that, “One chimpanzeePlasmodium strain was genetically identical, on all three markers tested, to variant P. ovale type,” found in humans.[vii]Again in Cameroon, Duval and co-researchers identified samples of Plasmodium species in gorillas and chimpanzees that related to Plasmodium falciparum.[viii]

 

As long as the potential for zoonotic malaria transmission from primates to humans exists along with the potential for adaptation of such parasites to humans and subsequent transmission among humans, our goals of eliminating malaria as a human disease by 2030 are at risk.[ix] Ironically it is human activity that heightens this risk.

 

To date it does not appear that primate to human malaria transmission is occurring in Africa. Unlike the Plasmodium knowlesi situation Southeast Asia, “African apes harboring parasites do not seem to serve as a recurrent source of human malaria.” This is an important finding and potential reprieve for ongoing control and eradication measures in Africa.[x]

 

In a broader context Faust and Dobson explain that, “The diversity and distribution of primate malaria are an essential prerequisite to understanding the mechanisms and circumstances that allow Plasmodium to jump species barriers, both in the evolution of malaria parasites and current cases of spillover into humans,”[xi] implying it is not a matter of if humans and primates might share malaria disease in Africa, but when it will happen on the scale seen in Southeast Asia.

 

[i] Pigott DM, Golding N, Mylne A, Huang Z, Henry AJ, Weiss DJ, Brady OJ, Kraemer MUG, Smith DL, Moyes CL, Bhatt S, Gething PW, Horby PW, Bogoch II, Brownstein JS, Mekaru SR, Tatem AJ, Khan K, Hay SI. Mapping the zoonotic niche of Ebola virus disease in Africa. eLife 2014;10.7554/eLife.04395. http://dx.doi.org/10.7554/eLife.04395

[ii] Franchini G (1927) Su di un plasmodio pigmentato di una scimmia (On a pigmented plasmodium of a monkey). Arch Ital Sci Med Colon 8:187–90. http://www.cabdirect.org/abstracts/19272901681.html

[iii] Coggeshall LT and Kumm HW. Effect of repeated superinfection upon the potency of immune serum of monkeys harboring chronic infections of Plasmodium knowlesi. J Exp Med. 1938 Jun 30; 68(1): 17–27. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2133656/

[iv] Eaton MD, Coggeshall LT. Complement fixation in human malaria with an antigen prepared from the monkey parasitePlasmodium knowlesi. J Exp Med. 1939 Feb 28;69(3):379-98. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2133745/

[v] F.Prugnolle, B.Ollomo, P.Durand, E.Yalcindag, C.Arnathau, E.Elguero, A.Berry, X.Pourrut, J-P.Gonzalez, D.Nkoghe, J.Akiana, D.Verrier, E.Leroy, F.J.Ayala and F.Renaud. African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. PNAS, 4 July 2011

[vi] Liu W, Li Y, Shaw KS, et al. African origin of the malaria parasite Plasmodium vivax. Nature Communications. 2014; 5:3346, DOI: 10.1038/ncomms4346, www.nature.com/naturecommunications

[vii] Duval L, Nerrienet E, Rousset D, Sadeuh Mba SA, Houze S, et al. (2009) Chimpanzee Malaria Parasites Related to Plasmodium ovale in Africa. PLoS ONE 4(5): e5520. doi:10.1371/journal.pone.0005520

[viii] Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, Goodman SM, Andriaholinirina NV, Randrianarivelojosia M, Paul RE, Robert V, Ayalak FJ, Ariey F. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. PNAS 2010; 107(23): www.pnas.org/cgi/doi/10.1073/pnas.1005435107

[ix] Ouma C. How can we defeat malaria by 2030? World Economic Forum. Friday 11 September 2015. https://www.weforum.org/agenda/2015/09/how-can-we-defeat-malaria-by-2030/ (accessed 2016-02-20)

[x] Sundararaman SA, Liu W, Keele BF, Learn GH, Bittinger K, Mouacha F, Ahuka-Mundeke S, Manske M, Sherrill-Mix S, Li Y, Malenke JA, Delaporte E, Laurent C, Mpoudi Ngole E, Kwiatkowski DP, Shaw GM, Rayner JC, Peeters M, Sharp PM, Bushman FD, Hahn BH. Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc Natl Acad Sci USA. 2013; 110(17): 7020-5. doi: 10.1073/pnas.1305201110.

[xi] Faust C and Dobson AP. Primate malarias: Diversity, distribution and insights for

zoonotic Plasmodium. One Health 2015 1:66–75. http://dx.doi.org/10.1016/j.onehlt.2015.10.001

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