... M. Kasenene, Mike Crandfield, Omar E. Cornejo, JeanMarc Chavatte, Clara Lin, [ . ... malarias in apes living in their natural habitat5 (M. Peeters pers. comm.).
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On the Diversity of Malaria Parasites in African Apes and the Origin of Plasmodium falciparum from Bonobos Sabrina Krief
, Ananias A. Escalante
, M. Andreina Pacheco, Lawrence Mugisha, Claudine André, Michel Halbwax, Anne Fischer,
JeanMichel Krief, John M. Kasenene, Mike Crandfield, Omar E. Cornejo, JeanMarc Chavatte, Clara Lin, [ ... ], Georges Snounou Published: February 12, 2010 Article
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DOI: 10.1371/journal.ppat.1000765
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Subject Areas Bonobos Chimpanzees Malarial parasites
ORIGINS AND PERSISTANCE OF HUMAN MALARIAS: CONTEXT MATTERS Posted by leendertzf on 23 Apr 2010 at 07:10 GMT
Mitochondria Parasite evolution Parasitic diseases Phylogenetic analysis
ORIGINS AND PERSISTANCE OF HUMAN MALARIAS: CONTEXT MATTERS Fabian H. Leendertz (1,2) and Thomas R. Gillespie (3,4) 1 Research Group ‘‘Emerging Zoonoses’’, Robert KochInstitut, Berlin, Germany 2 Department of Primatology, MaxPlanckInstitute for Evolutionary Anthropology, Leipzig, Germany 3 Department of Environmental Studies and Program in Population Biology, Ecology and Evolution, Emory University, Atlanta, Georgia USA 4Department of Environmental and Occupational Health, Rollins School of Public Health, Emory University, Atlanta, Georgia USA
Examination of the role of our closest phylogenetic relatives, the great apes, in the evolution and persistence of human malarias has been limited by a lack of data from wild ape populations where opportunities for humanmosquitoape malaria exchange are minimal. Interpretation of patterns of malaria infection in captive ape populations, such as sanctuaries, must consider the ample opportunities for human to ape transmission of such parasites as has been clearly demonstrated in cases of far lower overlap for respiratory and gastrointestinal viruses and bacteria (1,2). The recent study by Krief et al. (2010) (3) highlights the importance of context when interpreting the potential for zoonotic
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transmission of Plasmodium. This study examined great apes living in three distinct contexts: 1) captive bonobos living in a small sanctuary (500m x 500 m forested enclosure) far from natural bonobo habitat and surrounded by human settlements in the suburban area of Kinshasa, an urban center of more than 10 million people where malaria is common (Fig 1a, Lola ya Bonobo Sanctuary); 2) chimpanzees living on an isolated island in Lake Victoria with no permanent human settlements that chimpanzees have never naturally inhabited (Fig 1b, Ngamba Island Sanctuary); 3) semiwild chimpanzees living at a forest / village interface with high human overlap due to chimpanzee crop raiding and chimpanzees ranging at most times within 02 km of a village (Fig 1c, Kibale Forest). These are clearly not “natural settings”. With the exception of the Plasmodium strains of the reichenowi group (which is most likely a great ape group), it is far more likely that the apes examined in these contexts were infected with Plasmodium via mosquitoes carrying infected human blood. Human to ape Plasmodium transfer is further supported in these contexts, considering that chimpanzees living on Ngamba Island, a sanctuary situated on an isolated island with no permanent human settlements in Lake Victoria (Fig1b), demonstrate no Plasmodium infection3. Imagine confirming H1N1 in chimpanzees at the St Louis Zoo. Would we assume the chimpanzees are the reservoir? Founder individuals in sanctuaries are removed from the wild at the age of 24 and live for long periods in close proximity to humans before being confiscated and introduced to a sanctuary. Thus, Plasmodium parasites would have to be maintained chronically since youth in these animals or human variants of the parasite infect the apes while living in sanctuaries. Consider the case of the “Lola ya” bonobos who display high prevalence of human malarias, they are surrounded by infected vectors for human malaria for most of their life (human malaria prevalence in Kinshasa is 34%(4)) and are well separated from any natural bonobo populations. Conversely, Ngamba Island chimpanzees, who lack all human malarias, live in an environment where vectors are rare and the probability of infected vectors is also low due to the small temporary human presence. Human to ape malaria transmission is the most parsimonious explanation for the pattern of infection observed. The existence of human Plasmodium species in wild great apes inhabiting pristine contiguous forest with limited exposure to humans would be required to demonstrate the natural existence of these parasites in wild great apes. Recent detection of Plasmodium from noninvasively collected fecal samples from wild chimpanzees and gorillas provide important insights regarding the existence of human malarias in apes living in their natural habitat5 (M. Peeters pers. comm.). Systematic study of the ecological and epidemiological aspects of Plasmodium evolution and persistence using noninvasively collected samples of great apes living in remote regions, coupled with more detailed analyses of parasite strains detected in captive and wild great apes have great potential to shed light on the origin and zoonotic potential of these parasites (6). References 1. Köndgen S, Kühl H, N’Goran PK, Walsh PD, Schenk S, Ernst N, Biek R, Formenty P, MatzRensing K, Schweiger B, Junglen S, Ellerbrok H, Nitsche A, Briese T, Lipkin WI, Pauli G, Boesch C, Leendertz FH. (2008). Pandemic human viruses cause decline of endangered great apes. Curr Biol 18: 260–264. 2. Rwego, I.B., G. IsabiryeBasuta, T.R. Gillespie, and T.L. Goldberg. (2008) Gastrointestinal bacterial transmission among humans, mountain gorillas, and domestic livestock in Bwindi Impenetrable National Park, Uganda. Conservation Biology. 22:16001607. 3. Krief S, Escalante AA, Pacheco MA, Mugisha L, André C, et al. (2010) On the Diversity of Malaria Parasites in African Apes and the Origin of Plasmodium falciparum from Bonobos. PLoS Pathog 6: e1000765. 4. Kazadi W, Sexton JD, Bigonsa M, W’Okanga W, Way W (2004) Malaria in primary school children and infants in Kinshasa, Democratic Republic of the Congo: surveys from the 1980s and 2000 Am. J. Trop. Med. Hyg., 71: 97–102 5. Prugnollea, F. et. al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. PNAS 107,145863 (2010). 6. Gillespie TR, Nunn CL, Leendertz FH. (2008). Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. Yrbk Phys Anth 51, 5369. Acknowledgements This work was supported by the Robert KochInstitute, the MaxPlanckSociety, and Emory University.
Fig1 AC: Please see the referenced figure here: http://www.plospathogens.... Satellite image of territories and enclosures of great apes investigated (shaded areas). A: Bonobo sanctuary “Lola ya Bonobo” in the periphery of Kinshassa, DRC; B: Chimpanzee sanctuary “Ngamba Island” with no permanent human population; C: Complete territory of wild chimpanzees living in close contact to human settlements in Kibale Forest, Uganda. White bars represent 2500 meters. No competing interests declared.
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RE: ORIGINS AND PERSISTANCE OF HUMAN MALARIAS: CONTEXT MATTERS AnaniasEscalante replied to leendertzf on 23 Apr 2010 at 17:33 GMT
Comments ORIGINS AND PERSISTANCE OF HUMAN MALARIAS: CONTEXT MATTERS Posted by leendertzf