Articles | Volume 4, issue 1
https://doi.org/10.5194/pb-4-47-2017
© Author(s) 2017. This work is distributed under
the Creative Commons Attribution 3.0 License.
the Creative Commons Attribution 3.0 License.
Special issue:
https://doi.org/10.5194/pb-4-47-2017
© Author(s) 2017. This work is distributed under
the Creative Commons Attribution 3.0 License.
the Creative Commons Attribution 3.0 License.
Review article
| 
14 Mar 2017
Review article |
| 14 Mar 2017
Wild African great apes as natural hosts of malaria parasites: current knowledge and research perspectives
Hélène Marie De Nys
Project group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany
current address: UMI 233, Institut de Recherche pour le Développement (IRD), INSERM U1175, and University of Montpellier, Montpellier, France
Therese Löhrich
Project group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany
Doris Wu
Project group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany
Sébastien Calvignac-Spencer
Project group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany
Fabian Hubertus Leendertz
Project group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany
Related authors
No articles found.
Karen Lampe, Jens-Christian Rudnick, Fabian Leendertz, Martina Bleyer, and Kerstin Mätz-Rensing
Primate Biol., 4, 39–46, https://doi.org/10.5194/pb-4-39-2017, https://doi.org/10.5194/pb-4-39-2017, 2017
Related subject area
Infection biology
Seroprevalence of viral infections in captive rhesus and cynomolgus macaques
Limited susceptibility of rhesus macaques to a cowpox virus isolated from a lethal outbreak among New World monkeys
Revisiting a quarter of a century of simian immunodeficiency virus (SIV)-associated cardiovascular diseases at the German Primate Center
Detection systems for antibody responses against herpes B virus
Lymphocryptovirus-dependent occurrence of lymphoma in SIV-infected rhesus macaques with particular consideration to two uncommon cases of non-Hodgkin's lymphoma
Prions
Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar
Immunodeficiency viruses and prion disease
Artur Kaul, Uwe Schönmann, and Stefan Pöhlmann
Primate Biol., 6, 1–6, https://doi.org/10.5194/pb-6-1-2019, https://doi.org/10.5194/pb-6-1-2019, 2019
Short summary
Short summary
Monitoring macaque health requires the detection of infectious diseases. Here, we report the screening of a macaque colony for antibodies which indicate selected viral infections. Our results show that infection with beta- and gamma-herpesviruses was frequent, while infection with simian retrovirus type D and simian T cell leukemia virus was not. Measles virus infection was more frequent in animals with extensive contact with humans, but no firm correlation could be established.
Kerstin Mätz-Rensing, Constanze Yue, Jeanette Klenner, Heinz Ellerbrok, and Christiane Stahl-Hennig
Primate Biol., 4, 163–171, https://doi.org/10.5194/pb-4-163-2017, https://doi.org/10.5194/pb-4-163-2017, 2017
Short summary
Short summary
The research into therapeutic agents for prevention and treatment of orthopoxvirus (OPXV) infections requires adequate animal models to investigate the efficacy and safety of new vaccines and antiviral compounds against smallpox and other highly pathogenic OPXVs. This study was undertaken to investigate the susceptibility of rhesus monkeys towards the calpox virus, an orthopoxvirus of the species Cowpox virus, which is uniformly lethal in common marmosets, in order to define a new animal model.
Matthias Mietsch, Ulrike Sauermann, Kerstin Mätz-Rensing, Antonina Klippert, Maria Daskalaki, Nicole Stolte-Leeb, and Christiane Stahl-Hennig
Primate Biol., 4, 107–115, https://doi.org/10.5194/pb-4-107-2017, https://doi.org/10.5194/pb-4-107-2017, 2017
Stefan Pöhlmann, Astrid Krüger, Wali Hafezi, Stefan Schneider, Jens Gruber, Michael Winkler, and Artur Kaul
Primate Biol., 4, 9–16, https://doi.org/10.5194/pb-4-9-2017, https://doi.org/10.5194/pb-4-9-2017, 2017
Short summary
Short summary
Transmission of macaque herpes B virus (BV) to humans can induce severe disease. Therefore, diagnostic tests for detecting BV infection are needed. Here, we show that antigens of BV-related non-human primate herpes viruses allow for the detection of antibodies elicited against BV with a higher sensitivity than antigens of human herpes simplex viruses (HSV). Moreover, we provide evidence that using recombinant viral glycoproteins may allow us to discriminate antibody responses against BV and HSV.
Antonina Klippert, Martina Bleyer, Ulrike Sauermann, Berit Neumann, Artur Kaul, Maria Daskalaki, Nicole Stolte-Leeb, Frank Kirchhoff, and Christiane Stahl-Hennig
Primate Biol., 3, 65–75, https://doi.org/10.5194/pb-3-65-2016, https://doi.org/10.5194/pb-3-65-2016, 2016
Short summary
Short summary
Despite effective antiviral therapy, HIV infection frequently leads to blood cell tumors known as lymphoma in the final disease stage. We have observed the same tumors in monkeys infected with simian immunodeficiency virus. Tumor development coincided with and was fostered by co-infection with the tumorigenic simian homolog to human Epstein–Barr virus. Two cases of lymphoma are presented, one exhibiting an unusual cell surface marker composition and the other obstructing the urogenital tract.
Walter Bodemer
Primate Biol., 3, 47–50, https://doi.org/10.5194/pb-3-47-2016, https://doi.org/10.5194/pb-3-47-2016, 2016
Short summary
Short summary
Inheritance by DNA and RNA as genetic elements has been known for decades. However, inheritance by proteins was completely unexpected. Proteins as carrier of genetic information have been identified in yeast where non-Mendelian inheritance could not be explained by transfer of chromosomes (DNA). Prions in yeast helped to understand structure and function of mammalian prions. The rhesus monkey has been found to be a valid animal model for prion infection and the epigenetically controlled disease.
Andrea Springer and Peter M. Kappeler
Primate Biol., 3, 51–63, https://doi.org/10.5194/pb-3-51-2016, https://doi.org/10.5194/pb-3-51-2016, 2016
Short summary
Short summary
Parasites play important roles in ecosystems, ultimately by affecting host health and survival. Several host traits generate differences in parasite diversity among host species living in the same habitat. We examine these traits in relation to intestinal parasitism of six sympatric lemur species. We highlight the opportunities of exploring the parasitic fauna of wildlife from a community ecology and evolutionary perspective, and identify avenues for future research on lemur parasitism.
W. Bodemer
Primate Biol., 2, 65–69, https://doi.org/10.5194/pb-2-65-2015, https://doi.org/10.5194/pb-2-65-2015, 2015
Short summary
Short summary
Lentiviral immunodeficiency viruses cause AIDS in humans and in non-human primates. Macaques are a suitable animal model to study infection, disease and the immune response against the retrovirus. As to prion disease, we established a rhesus monkey infection model for this unique infectious pathogen. Animals were experimentally infected with human and bovine prions. Unlike in human prion disease (Creutzfeldt-Jakob disease), we observed early and late stages of disease.
Cited articles
Adler, S.: Malaria in chimpanzees in Sierra Leone, Ann. Trop. Med. Parasit., 17, 13–19, 1923.
Ansell, J., Hamilton, K. A., Pinder, M., Walraven, G. E., and Lindsay, S. W.: Short-range attractiveness of pregnant women to Anopheles gambiae mosquitoes, T. Roy. Soc. Trop. Med. H., 96, 113–116, 2002.
Ayouba, A., Mouacha, F., Learn, G. H., Mpoudi-Ngole, E., Rayner, J. C., Sharp, P. M., Hahn, B. H., Delaporte, E., and Peeters, M.: Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans), Int. J. Parasitol., 42, 709–713, https://doi.org/10.1016/j.ijpara.2012.05.004, 2012.
Blacklock, B. and Adler, S.: A parasite resembling Plasmodium falciparum in a chimpanzee, Ann. Trop. Med. Parasit., 160, 99–106, 1922.
Blanquart, S. and Gascuel, O.: Mitochondrial genes support a common origin of rodent malaria parasites and Plasmodium falciparum's relatives infecting great apes, BMC Evol. Biol., 11, 70, https://doi.org/10.1186/1471-2148-11-70, 2011.
Boundenga, L., Ollomo, B., Rougeron, V., Mouele, L. Y., Mve-Ondo, B., Delicat-Loembet, L. M., Moukodoum, N. D., Okouga, A. P., Arnathau, C., Elguero, E., Durand, P., Liégeois, F., Boué, V., Motsch, P., Le Flohic, G., Ndoungouet, A., Paupy, C., Ba, C. T., Renaud, F., and Prugnolle, F.: Diversity of malaria parasites in great apes in Gabon, Malaria J., 14, 111, https://doi.org/10.1186/s12936-015-0622-6, 2015.
Bray, R. S.: Studies on malaria in chimpanzees. V. The sporogonous cycle and mosquito transmission of Plasmodium vivax shcwetzi, J. Parasitol., 44, 46–51, 1958a.
Bray, R. S.: Studies on malaria in chimpanzees. VI. Laverania falciparum., Am. J. Trop. Med. Hyg., 7, 20–24, 1958b.
Bray, R. S.: Studies on malaria in chimpanzees. VIII. The experimental transmission and pre-erythrocytic phase of Plasmodium malariae, with a note on the host-range of the parasite, Am. J. Trop. Med. Hyg., 9, 455–465, 1960.
Bray, R. S.: The Malaria Parasites of Anthropoid Apes, J. Parasitol., 49, 888–891, 1963.
Broderick, C., Nadjm, B., Smith, V., Blaze, M., Checkley, A., Chiodini, P. L., and Whitty, C. J. M.: Clinical, geographical, and temporal risk factors associated with presentation and outcome of vivax malaria imported into the United Kingdom over 27 years: observational study, BMJ, 350, h1703, https://doi.org/10.1136/bmj.h1703, 2015.
Brumpt, E.: Les parasites du paludisme des chimpanzés, Comptes Rendus Soc. Biol., 130, 834–840, 1939.
Carter, R.: Speculations on the origins of Plasmodium vivax malaria, Trends Parasitol., 19, 214–219, https://doi.org/10.1016/s1471-4922(03)00070-9, 2003.
Carter, R. and Mendis, K. N.: Evolutionary and historical aspects of the burden of malaria, Clin. Microbiol. Rev., 15, 564–594, 2002.
CDC: Anopheles mosquitoes, available at: http://www.cdc.gov/malaria/about/biology/mosquitoes/ (last access: 2015), 2012.
Coatney, G. R.: Simian malarias in man: facts, implications, and predictions, Am. J. Trop. Med. Hyg., 17, 147–155, 1968.
Coetzee, M.: Distribution of the African malaria vectors of the Anopheles gambiae complex, Am. J. Trop. Med. Hyg., 70, 103–104, 2004.
Collins, W. E., Skinner, J. C., Pappaioanou, M., Broderson, J. R., and Mehaffey, P.: The sporogonic cycle of Plasmodium reichenowi, J. Parasitol., 72, 292–298, 1986.
Contacos, P. G., Coatney, G. R., Orihel, T. C., Collins, W. E., Chin, W., and Jeter, M. H.: Transmission of Plasmodium schwetzi from the chimpanzee to man by mosquito bite, Am. J. Trop. Med. Hyg., 19, 190–195, 1970.
Culleton, R. L., Mita, T., Ndounga, M., Unger, H., Cravo, P. V, Paganotti, G. M., Takahashi, N., Kaneko, A., Eto, H., Tinto, H., Karema, C., D'Alessandro, U., do Rosario, V., Kobayakawa, T., Ntoumi, F., Carter, R., and Tanabe, K.: Failure to detect Plasmodium vivax in West and Central Africa by PCR species typing, Malaria J., 7, 174, https://doi.org/10.1186/1475-2875-7-174, 2008.
Davies, C. R., Ayres, J. M., Dye, C., and Deane, L. M.: Malaria infection rate of Amazonian primates increases with body weight and group size, Funct. Ecol., 5, 655–662, 1991.
Délicat-Loembet, L., Rougeron, V., Ollomo, B., Arnathau, C., Roche, B., Elguero, E., Moukodoum, N. D., Okougha, A.-P., Mve Ondo, B., Boundenga, L., Houzé, S., Galan, M., Nkoghé, D., Leroy, E. M., Durand, P., Paupy, C., Renaud, F., and Prugnolle, F.: No Evidence for Ape Plasmodium Infections in Humans in Gabon, PLoS One, 10, e0126933, https://doi.org/10.1371/journal.pone.0126933, 2015.
De Nys, H. M., Calvignac-Spencer, S., Thiesen, U., Boesch, C., Wittig, R. M., Mundry, R., and Leendertz, F. H.: Age-related effects on malaria parasite infection in wild chimpanzees, Biol. Lett., 9, 20121160, https://doi.org/10.1098/rsbl.2012.1160, 2013.
De Nys, H. M., Calvignac-Spencer, S., Boesch, C., Dorny, P., Wittig, R. M., Mundry, R., and Leendertz, F. H.: Malaria parasite detection increases during pregnancy in wild chimpanzees, Malaria J., 13, 413, https://doi.org/10.1186/1475-2875-13-413, 2014.
Desai, M., ter Kuile, F. O., Nosten, F., McGready, R., Asamoa, K., Brabin, B., and Newman, R. D.: Epidemiology and burden of malaria in pregnancy, Lancet Infect. Dis., 7, 93–104, https://doi.org/10.1016/s1473-3099(07)70021-x, 2007.
Doolan, D. L., Dobaño, C., and Baird, J. K.: Acquired Immunity to Malaria, Clin. Microbiol. Rev., 22, 13–36, 2009.
Duval, L., Nerrienet, E., Rousset, D., Sadeuh Mba, S. A., Houze, S., Fourment, M., Le Bras, J., Robert, V., and Ariey, F.: Chimpanzee malaria parasites related to Plasmodium ovale in Africa, PLoS One, 4, e5520, https://doi.org/10.1371/journal.pone.0005520, 2009.
Duval, L., Fourment, M., Nerrienet, E., Rousset, D., Sadeuh, S. A., Goodman, S. M., Andriaholinirina, N. V, Randrianarivelojosia, M., Paul, R. E., Robert, V., Ayala, F. J., and Ariey, F.: African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus, P. Natl. Acad. Sci. USA, 107, 10561–10566, https://doi.org/10.1073/pnas.1005435107, 2010.
Ekvall, H., Arese, P., Turrini, F., Ayi, K., Mannu, F., Premji, Z., and Bjorkman, A.: Acute haemolysis in childhood falciparum malaria, T. Roy. Soc. Trop. Med. H., 95, 611–617, 2001.
Escalante, A. A. and Ayala, F. J.: Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences, P. Natl. Acad. Sci. USA, 91, 11373–11377, 1994.
Escalante, A. A., Barrio, E., and Ayala, F. J.: Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene, Mol. Biol. Evol., 12, 616–626, 1995.
Escalante, A. A., Cornejo, O. E., Freeland, D. E., Poe, A. C., Durrego, E., Collins, W. E., and Lal, A. A.: A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite, P. Natl. Acad. Sci. USA, 102, 1980–1985, https://doi.org/10.1073/pnas.0409652102, 2005.
Faure, E.: Malarial pathocoenosis: beneficial and deleterious interactions between malaria and other human diseases, Front. Physiol., 5, 441, https://doi.org/10.3389/fphys.2014.00441, 2014.
Garnham, P. C., Lainson, R., and Gunders, A. E.: Some observations on malaria parasites in a chimpanzee, with particular reference to the persistence of Plasmodium reichenowi and Plasmodium vivax, Ann. Soc. Belg. Med. Tr., 36, 811–821, 1956.
Gautret, P., Legros, F., Koulmann, P., Rodier, M. H., and Jacquemin, J. L.: Imported Plasmodium vivax malaria in France: Geographical origin and report of an atypical case acquired in Central or Western Africa, Acta Trop., 78, 177–181, 2001.
Graham, A. L.: Ecological rules governing helminth-microparasite coinfection, P. Natl. Acad. Sci. USA, 105, 566–570, https://doi.org/10.1073/pnas.0707221105, 2008.
Guyatt, H. L. and Snow, R. W.: Malaria in pregnancy as an indirect cause of infant mortality in sub-Saharan Africa, T. Roy. Soc. Trop. Med. H., 95, 569–576, 2001.
Hayakawa, T., Culleton, R., Otani, H., Horii, T., and Tanabe, K.: Big bang in the evolution of extant malaria parasites, Mol. Biol. Evol., 25, 2233–2239, https://doi.org/10.1093/molbev/msn171, 2008.
Hayakawa, T., Arisue, N., Udono, T., Hirai, H., Sattabongkot, J., Toyama, T., Tsuboi, T., Horii, T., and Tanabe, K.: Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees, PLoS One, 4, e7412, https://doi.org/10.1371/journal.pone.0007412, 2009.
Herbert, A., Boundenga, L., Meyer, A., Moukodoum, D. N., Okouga, A. P., Arnathau, C., Durand, P., Magnus, J., Ngoubangoye, B., Willaume, E., Ba, C. T., Rougeron, V., Renaud, F., Ollomo, B., and Prugnolle, F.: Malaria-like symptoms associated with a natural Plasmodium reichenowi infection in a chimpanzee, Malaria J., 14, 220, https://doi.org/10.1186/s12936-015-0743-y, 2015.
Hill, A. V, Allsopp, C. E., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P. A., Bennett, S., Brewster, D., McMichael, A. J., and Greenwood, B. M.: Common west African HLA antigens are associated with protection from severe malaria, Nature, 352, 595–600, https://doi.org/10.1038/352595a0, 1991.
Hughes, A. L. and Verra, F.: Malaria parasite sequences from chimpanzee support the co-speciation hypothesis for the origin of virulent human malaria (Plasmodium falciparum), Mol. Phylogenet. Evol., 57, 135–143, https://doi.org/10.1016/j.ympev.2010.06.004, 2010.
Junglen, S., Kurth, A., Kuehl, H., Quan, P. L., Ellerbrok, H., Pauli, G., Nitsche, A., Nunn, C., Rich, S. M., Lipkin, W. I., Briese, T., and Leendertz, F. H.: Examining landscape factors influencing relative distribution of mosquito genera and frequency of virus infection, Ecohealth, 6, 239–249, https://doi.org/10.1007/s10393-009-0260-y, 2009.
Kaiser, M., Lowa, A., Ulrich, M., Ellerbrok, h., Goffe, A. S., Blasse, A., Zommers, Z., Couacy-Hymann, E., Babweteera, F., Zuberbuhler, K., Metzger, S., Geidel, S., Boesch, C., Gillepsie, T., and Leendertz, F.: Wild Chimpanzees Infected with 5 Plasmodium Species, Emerg. Infect. Dis., 16, 1956–1959, https://doi.org/10.3201/eid1612.100424, 2010.
Keele, B. F., Jones, J. H., Terio, K. A., Estes, J. D., Rudicell, R. S., Wilson, M. L., Li, Y., Learn, G. H., Beasley, T. M., Schumacher-Stankey, J., Wroblewski, E., Mosser, A., Raphael, J., Kamenya, S., Lonsdorf, E. V, Travis, D. A., Mlengeya, T., Kinsel, M. J., Else, J. G., Silvestri, G., Goodall, J., Sharp, P. M., Shaw, G. M., Pusey, A. E., and Hahn, B. H.: Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz, Nature, 460, 515–519, https://doi.org/10.1038/nature08200, 2009.
Koops, K., McGrew, W. C., Matsuzawa, T., and Knapp, L. A.: Terrestrial nest-building by wild chimpanzees (Pan troglodytes): implications for the tree-to-ground sleep transition in early hominins, Am. J. Phys. Anthropol., 148, 351–361, https://doi.org/10.1002/ajpa.22056, 2012.
Kotepui, M., Piwkham, D., PhunPhuech, B., Phiwklam, N., Chupeerach, C., and Duangmano, S.: Effects of malaria parasite density on blood cell parameters, PLoS One, 10, e0121057, https://doi.org/10.1371/journal.pone.0121057, 2015.
Krebs, B. L., Anderson, T. K., Goldberg, T. L., Hamer, G. L., Kitron, U. D., Newman, C. M., Ruiz, M. O., Walker, E. D., and Brawn, J. D.: Host group formation decreases exposure to vector-borne disease: a field experiment in a “hotspot” of West Nile virus transmission, P. Roy. Soc. B-Biol. Sci., 281, 20141586, https://doi.org/10.1098/rspb.2014.1586, 2014.
Krief, S., Escalante, A. A., Pacheco, M. A., Mugisha, L., Andre, C., Halbwax, M., Fischer, A., Krief, J. M., Kasenene, J. M., Crandfield, M., Cornejo, O. E., Chavatte, J. M., Lin, C., Letourneur, F., Gruner, A. C., McCutchan, T. F., Renia, L., and Snounou, G.: On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos, PLoS Pathog., 6, e1000765, https://doi.org/10.1371/journal.ppat.1000765, 2010.
Krief, S., Levrero, F., Krief, J.-M., Thanapongpichat, S., Imwong, M., Snounou, G., Kasenene, J. M., Cibot, M., and Gantier, J.-C.: Investigations on anopheline mosquitoes close to the nest sites of chimpanzees subject to malaria infection in Ugandan Highlands, Malaria J., 11, 116, https://doi.org/10.1186/1475-2875-11-116, 2012.
Kwiatkowski, D. P.: How malaria has affected the human genome and what human genetics can teach us about malaria, Am. J. Hum. Genet., 77, 171–192, https://doi.org/10.1086/432519, 2005.
Larremore, D. B., Sundararaman, S. A., Liu, W., Proto, W. R., Clauset, A., Loy, D. E., Speede, S., Plenderleith, L. J., Sharp, P. M., Hahn, B. H., Rayner, J. C., and Buckee, C. O.: Ape parasite origins of human malaria virulence genes, Nat. Commun., 6, 8368, https://doi.org/10.1038/ncomms9368, 2015.
Lee, K. S., Divis, P. C., Zakaria, S. K., Matusop, A., Julin, R. A., Conway, D. J., Cox-Singh, J., and Singh, B.: Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques, PLoS Pathog., 7, e1002015, https://doi.org/10.1371/journal.ppat.1002015, 2011.
Lindsay, S., Ansell, J., Selman, C., Cox, V., Hamilton, K., and Walraven, G.: Effect of pregnancy on exposure to malaria mosquitoes, Lancet, 355, 1972, https://doi.org/10.1016/S0140-6736(00)02334-5, 2000.
Liu, W., Li, Y., Learn, G. H., Rudicell, R. S., Robertson, J. D., Keele, B. F., Ndjango, J. B., Sanz, C. M., Morgan, D. B., Locatelli, S., Gonder, M. K., Kranzusch, P. J., Walsh, P. D., Delaporte, E., Mpoudi-Ngole, E., Georgiev, A. V, Muller, M. N., Shaw, G. M., Peeters, M., Sharp, P. M., Rayner, J. C., and Hahn, B. H.: Origin of the human malaria parasite Plasmodium falciparum in gorillas, Nature, 467, 420–425, https://doi.org/10.1038/nature09442, 2010.
Liu, W., Li, Y., Shaw, K. S., Learn, G. H., Plenderleith, L. J., Malenke, J. A., Sundararaman, S. A., Ramirez, M. A., Crystal, P. A., Smith, A. G., Bibollet-Ruche, F., Ayouba, A., Locatelli, S., Esteban, A., Mouacha, F., Guichet, E., Butel, C., Ahuka-Mundeke, S., Inogwabini, B.-I., Ndjango, J.-B. N., Speede, S., Sanz, C. M., Morgan, D. B., Gonder, M. K., Kranzusch, P. J., Walsh, P. D., Georgiev, A. V, Muller, M. N., Piel, A. K., Stewart, F. A., Wilson, M. L., Pusey, A. E., Cui, L., Wang, Z., Färnert, A., Sutherland, C. J., Nolder, D., Hart, J. A., Hart, T. B., Bertolani, P., Gillis, A., LeBreton, M., Tafon, B., Kiyang, J., Djoko, C. F., Schneider, B. S., Wolfe, N. D., Mpoudi-Ngole, E., Delaporte, E., Carter, R., Culleton, R. L., Shaw, G. M., Rayner, J. C., Peeters, M., Hahn, B. H., and Sharp, P. M.: African origin of the malaria parasite Plasmodium vivax, Nat. Commun., 5, 3346, https://doi.org/10.1038/ncomms4346, 2014.
Liu, W., Sundararaman, S. A., Loy, D. E., Learn, G. H., Li, Y., Plenderleith, L. J., Ndjango, J.-B. N., Speede, S., Atencia, R., Cox, D., Shaw, G. M., Ayouba, A., Peeters, M., Rayner, J. C., Hahn, B. H., and Sharp, P. M.: Multigenomic Delineation of Plasmodium Species of the Laverania Subgenus Infecting Wild-Living Chimpanzees and Gorillas, Genome Biol. Evol., 8, 1929–1939, https://doi.org/10.1093/gbe/evw128, 2016.
MacFie, T. S., Nerrienet, E., Bontrop, R. E., and Mundy, N. I.: The action of falciparum malaria on the human and chimpanzee genomes compared: absence of evidence for a genomic signature of malaria at HBB and G6PD in three subspecies of chimpanzee, Infect. Genet. Evol., 9, 1248–52, https://doi.org/10.1016/j.meegid.2009.06.025, 2009.
Makanga, B., Yangari, P., Rahola, N., Rougeron, V., Elguero, E., Boundenga, L., Moukodoum, N. D., Okouga, A. P., Arnathau, C., Durand, P., Willaume, E., Ayala, D., Fontenille, D., Ayala, F. J., Renaud, F., Ollomo, B., Prugnolle, F., and Paupy, C.: Ape malaria transmission and potential for ape-to-human transfers in Africa., P. Natl. Acad. Sci. USA, 113, 5329–5334, https://doi.org/10.1073/pnas.1603008113, 2016.
Mapua, M. I., Qablan, M. A., Pomajbíková, K., Petrželková, K. J., Hůzová, Z., Rádrová, J., Votýpka, J., Todd, A., Jirků, M., Leendertz, F. H., Lukeš, J., Neel, C., and Modrý, D.: Ecology of malaria infections in western lowland gorillas inhabiting Dzanga Sangha Protected Areas, Central African Republic, Parasitology, 142, 890–900, https://doi.org/10.1017/S0031182015000086, 2015.
Martin, M. J., Rayner, J. C., Gagneux, P., Barnwell, J. W., and Varki, A.: Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid, P. Natl. Acad. Sci. USA, 102, 12819–12824, https://doi.org/10.1073/pnas.0503819102, 2005.
Martinsen, E. S., Perkins, S. L., and Schall, J. J.: A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches, Mol. Phylogenet. Evol., 47, 261–273, https://doi.org/10.1016/j.ympev.2007.11.012, 2008.
Mooring, M. S. and Hart, B. L.: Animal Grouping for Protection from Parasites: Selfish Herd and Encounter-Dilution Effects, Behaviour, 123, 173–193, https://doi.org/10.1163/156853992X00011, 1992.
Mu, J., Joy, D. A., Duan, J., Huang, Y., Carlton, J., Walker, J., Barnwell, J., Beerli, P., Charleston, M. A., Pybus, O. G., and Su, X. Z.: Host switch leads to emergence of Plasmodium vivax malaria in humans, Mol. Biol. Evol., 22, 1686–1693, https://doi.org/10.1093/molbev/msi160, 2005.
Mühlberger, N., Jelinek, T., Gascon, J., Probst, M., Zoller, T., Schunk, M., Beran, J., Gjørup, I., Behrens, R. H., Clerinx, J., Björkman, A., McWhinney, P., Matteelli, A., Lopez-Velez, R., Bisoffi, Z., Hellgren, U., Puente, S., Schmid, M. L., Myrvang, B., Holthoff-Stich, M. L., Laferl, H., Hatz, C., Kollaritsch, H., Kapaun, A., Knobloch, J., Iversen, J., Kotlowski, A., Malvy, D. J. M., Kern, P., Fry, G., Siikamaki, H., Schulze, M. H., Soula, G., Paul, M., Gómez i Prat, J., Lehmann, V., Bouchaud, O., da Cunha, S., Atouguia, J., and Boecken, G.: Epidemiology and clinical features of vivax malaria imported to Europe: sentinel surveillance data from TropNetEurop, Malaria J., 3, 5, https://doi.org/10.1186/1475-2875-3-5, 2004.
Ngoubangoye, B., Boundenga, L., Arnathau, C., Mombo, I. M., Durand, P., Tsoumbou, T.-A., Otoro, B. V., Sana, R., Okouga, A.-P., Moukodoum, N., Willaume, E., Herbert, A., Fouchet, D., Rougeron, V., Bâ, C. T., Ollomo, B., Paupy, C., Leroy, E. M., Renaud, F., Pontier, D., and Prugnolle, F.: The host specificity of ape malaria parasites can be broken in confined environments, Int. J. Parasitol., 46, 737–744, https://doi.org/10.1016/j.ijpara.2016.06.004, 2016.
Nunn, C. and Eckhard, W. H.: Malaria infection and host behavior: a comparative study of Neotropical primates, Behav. Ecol. Sociobiol., 59, 30–37, https://doi.org/10.1007/s00265-005-0005-z, 2005.
Oni, G. A. and Oguntibeju, O. O.: Relationships between the Malaria Parasite Density and Children Anaemia: Brief Communication, Int. J. Pathol., 4, available at: http://www.researchgate.net/publication/267367309_Relationships_between_the_Malaria_Parasite_Density_and_Children_Anaemia_Brief_Communication (last access: 28 June 2015), 2006.
Pacheco, M. A., Cranfield, M., Cameron, K., and Escalante, A. A.: Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens, Malaria J., 12, 328, https://doi.org/10.1186/1475-2875-12-328, 2013.
Patnaik, P., Jere, C. S., Miller, W. C., Hoffman, I. F., Wirima, J., Pendame, R., Meshnick, S. R., Taylor, T. E., Molyneux, M. E., and Kublin, J. G.: Effects of HIV-1 serostatus, HIV-1 RNA concentration, and CD4 cell count on the incidence of malaria infection in a cohort of adults in rural Malawi, J. Infect. Dis., 192, 984–991, https://doi.org/10.1086/432730, 2005.
Paupy, C., Makanga, B., Ollomo, B., Rahola, N., Durand, P., Magnus, J., Willaume, E., Renaud, F., Fontenille, D., and Prugnolle, F.: Anopheles moucheti and Anopheles vinckei Are Candidate Vectors of Ape Plasmodium Parasites, Including Plasmodium praefalciparum in Gabon, PLoS One, 8, e57294, https://doi.org/10.1371/journal.pone.0057294, 2013.
Pedersen, A. B. and Fenton, A.: Emphasizing the ecology in parasite community ecology, Trends Ecol. Evol., 22, 133–139, https://doi.org/10.1016/j.tree.2006.11.005, 2007.
Prugnolle, F., Durand, P., Neel, C., Ollomo, B., Ayala, F. J., Arnathau, C., Etienne, L., Mpoudi-Ngole, E., Nkoghe, D., Leroy, E., Delaporte, E., Peeters, M., and Renaud, F.: African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum, P. Natl. Acad. Sci. USA, 107, 1458–1463, https://doi.org/10.1073/pnas.0914440107, 2010.
Prugnolle, F., Ollomo, B., Durand, P., Yalcindag, E., Arnathau, C., Elguero, E., Berry, A., Pourrut, X., Gonzalez, J. P., Nkoghe, D., Akiana, J., Verrier, D., Leroy, E., Ayala, F. J., and Renaud, F.: African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains, P. Natl. Acad. Sci. USA, 108, 11948–11953, https://doi.org/10.1073/pnas.1109368108, 2011.
Prugnolle, F., Rougeron, V., Becquart, P., Berry, A., Makanga, B., Rahola, N., Arnathau, C., Ngoubangoye, B., Menard, S., Willaume, E., Ayala, F. J., Fontenille, D., Ollomo, B., Durand, P., Paupy, C., and Renaud, F.: Diversity, host switching and evolution of Plasmodium vivax infecting African great apes, P. Natl. Acad. Sci. USA, 110, 8123–8128, https://doi.org/10.1073/pnas.1306004110, 2013.
Rayner, J. C., Liu, W., Peeters, M., Sharp, P. M., and Hahn, B. H.: A plethora of Plasmodium species in wild apes: a source of human infection?, Trends Parasitol., 27, 222–229, https://doi.org/10.1016/j.pt.2011.01.006, 2011.
Reichenow, E.: Über das Vorkommen der Malariaparasiten des Menschen bei den Afrikanischen Menschenaffen, Cent. f. Bakt. I. Abt. Orig., 85, 207–216, 1920.
Rich, S. M., Leendertz, F. H., Xu, G., LeBreton, M., Djoko, C. F., Aminake, M. N., Takang, E. E., Diffo, J. L., Pike, B. L., Rosenthal, B. M., Formenty, P., Boesch, C., Ayala, F. J., and Wolfe, N. D.: The origin of malignant malaria, P. Natl. Acad. Sci. USA, 106, 14902–14907, https://doi.org/10.1073/pnas.0907740106, 2009.
Rodhain, J.: Contribution a l'étude des plasmodiums des singes africains, Ann. Soc. Belg. Med. Tr., 16, 237–253, 1936.
Rodhain, J.: Les plasmodiums des anthropoïdes de l'Afrique centrale et leurs relations avec les plasmodiums humains, Ann. Soc. Belge Med. Tr., 19, 563–572, 1939.
Rodhain, J.: Les plasmodium des anthropoids de l'Afriqe centrale et leurs relations avec les plasmodiums humains, Ann. Soc. Belg. Med. Tr., 35, 69–73, 1940.
Rodhain, J. and Dellaert, R.: L'infection a Plasmodium malariae du chimpanze chez l'homme. Etude d'une premiere souche isolee de l'anthropoide Pan satyrus verus, Ann. Soc. Belg. Med. Tr., 23, 19–46, 1943.
Rodhain, J. and Dellaert, R.: Contribution a l'etude du Plasmodium schwetzi E. Brumpt (2me note). Transmission du Plasmodium schwetzi a l'homme, Ann. Soc. Belg. Med. Tr., 35, 73–76, 1955.
Rogerson, S. J., Hviid, L., Duffy, P. E., Leke, R. F. G., and Taylor, D. W.: Malaria in pregnancy: pathogenesis and immunity, Lancet Infect. Dis., 7, 105–117, https://doi.org/10.1016/s1473-3099(07)70022-1, 2007.
Rudicell, R. S., Holland Jones, J., Wroblewski, E. E., Learn, G. H., Li, Y., Robertson, J. D., Greengrass, E., Grossmann, F., Kamenya, S., Pintea, L., Mjungu, D. C., Lonsdorf, E. V, Mosser, A., Lehman, C., Collins, D. A., Keele, B. F., Goodall, J., Hahn, B. H., Pusey, A. E., and Wilson, M. L.: Impact of simian immunodeficiency virus infection on chimpanzee population dynamics, PLoS Pathog., 6, e1001116, https://doi.org/10.1371/journal.ppat.1001116, 2010.
Rynkiewicz, E. C., Pedersen, A. B., and Fenton, A.: An ecosystem approach to understanding and managing within-host parasite community dynamics, Trends Parasitol., 31, 212–221, https://doi.org/10.1016/j.pt.2015.02.005, 2015.
Sabbatani, S., Manfredi, R., and Fiorino, S.: Malaria infection and human evolution, Infez. Med., 18, 56–74, 2010.
Samson, D. R., Muehlenbein, M. P., and Hunt, K. D.: Do chimpanzees (Pan troglodytes schweinfurthii) exhibit sleep related behaviors that minimize exposure to parasitic arthropods? A preliminary report on the possible anti-vector function of chimpanzee sleeping platforms, Primates, 54, 73–80, https://doi.org/10.1007/s10329-012-0329-z, 2013.
Schaer, J., Perkins, S. L., Decher, J., Leendertz, F. H., Fahr, J., Weber, N., and Matuschewski, K.: High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa, P. Natl. Acad. Sci. USA, 110, 17415–17419, https://doi.org/10.1073/pnas.1311016110, 2013.
Schwetz, J.: Contribution à l'étude des parasites malariens des singes supérieurs africains, Rev. di Malariol., 13, 143–147, 1934.
Sharp, P. M., Rayner, J. C., and Hahn, B. H.: Evolution. Great apes and zoonoses, Science, 340, 284–286, https://doi.org/10.1126/science.1236958, 2013.
Sinka, M. E., Bangs, M. J., Manguin, S., Coetzee, M., Mbogo, C. M., Hemingway, J., Patil, A. P., Temperley, W. H., Gething, P. W., Kabaria, C. W., Okara, R. M., Van Boeckel, T., Godfray, H. C., Harbach, R. E., and Hay, S. I.: The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis, Parasite Vector., 3, 117, https://doi.org/10.1186/1756-3305-3-117, 2010.
Skarbinski, J., James, E. M., Causer, L. M., Barber, A. M., Mali, S., Nguyen-Dinh, P., Roberts, J. M., Parise, M. E., Slutsker, L., and Newman, R. D.: Malaria surveillance – United States, 2004, MMWR (Morbidity and Mortality weekly report), Surveillance summaries, 2002, Washington, D.C., USA, 55, 23–37, 2006.
Smith, J. D., Rowe, J. A., Higgins, M. K., and Lavstsen, T.: Malaria's deadly grip: cytoadhesion of Plasmodium falciparum-infected erythrocytes, Cell. Microbiol., 15, 1976–1983, https://doi.org/10.1111/cmi.12183, 2013.
Springer, A., Fichtel, C., Calvignac-Spencer, S., Leendertz, F. H., and Kappeler, P. M.: Hemoparasites in a wild primate: Infection patterns suggest interaction of Plasmodium and Babesia in a lemur species, Int. J. Parasitol.-Parasites Wildl., 4, 385–395, https://doi.org/10.1016/j.ijppaw.2015.10.006, 2015.
Sundararaman, S. A., Liu, W., Keele, B. F., Learn, G. H., Bittinger, K., Mouacha, F., Ahuka-Mundeke, S., Manske, M., Sherrill-Mix, S., Li, Y., Malenke, J. A., Delaporte, E., Laurent, C., Mpoudi Ngole, E., Kwiatkowski, D. P., Shaw, G. M., Rayner, J. C., Peeters, M., Sharp, P. M., Bushman, F. D., and Hahn, B. H.: Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria, P. Natl. Acad. Sci. USA, 110, 7020–7025, https://doi.org/10.1073/pnas.1305201110, 2013.
Tanabe, K., Mita, T., Jombart, T., Eriksson, A., Horibe, S., Palacpac, N., Ranford-Cartwright, L., Sawai, H., Sakihama, N., Ohmae, H., Nakamura, M., Ferreira, M. U., Escalante, A. A., Prugnolle, F., Bjorkman, A., Farnert, A., Kaneko, A., Horii, T., Manica, A., Kishino, H., and Balloux, F.: Plasmodium falciparum accompanied the human expansion out of Africa, Curr. Biol., 20, 1283–1289, https://doi.org/10.1016/j.cub.2010.05.053, 2010.
Tarello, W.: A fatal Plasmodium reichenowi infection in a chimpanzee?, Rev. Méd. Vét., 156, 503–505, 2005.
Taylor, D. W., Wells, R. A., Vernes, A., Rosenberg, Y. J., Vogel, S., and Diggs, C. L.: Parasitologic and immunologic studies of experimental Plasmodium falciparum infection in nonsplenectomized chimpanzees (Pan troglodytes), Am. J. Trop. Med. Hyg., 34, 36–44, 1985.
Tazi, L. and Ayala, F. J.: Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P. brasilianum, Infect. Genet. Evol., 11, 209–221, https://doi.org/10.1016/j.meegid.2010.08.007, 2011.
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S., and Begon, M.: Species interactions in a parasite community drive infection risk in a wildlife population, Science, 330, 243–246, https://doi.org/10.1126/science.1190333, 2010.
Thurber, M. I., Ghai, R. R., Hyeroba, D., Weny, G., Tumukunde, A., Chapman, C. A., Wiseman, R. W., Dinis, J., Steeil, J., Greiner, E. C., Friedrich, T. C., O'Connor, D. H., and Goldberg, T. L.: Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community, Int. J. Parasitol., 43, 613–619, https://doi.org/10.1016/j.ijpara.2013.03.002, 2013.
Trimnell, A. R., Kraemer, S. M., Mukherjee, S., Phippard, D. J., Janes, J. H., Flamoe, E., Su, X. Z., Awadalla, P., and Smith, J. D.: Global genetic diversity and evolution of var genes associated with placental and severe childhood malaria, Mol. Biochem. Parasit., 148, 169–180, https://doi.org/10.1016/j.molbiopara.2006.03.012, 2006.
van Duivenvoorde, L. M., Voorberg-van der Wel, A., van der Werff, N. M., Braskamp, G., Remarque, E. J., Kondova, I., Kocken, C. H., and Thomas, A. W.: Suppression of Plasmodium cynomolgi in rhesus macaques by coinfection with Babesia microti, Infect. Immun., 78, 1032–1039, https://doi.org/10.1128/IAI.00921-09, 2010.
Verhulst, N. O., Smallegange, R. C., and Takken, W.: Mosquitoes as potential bridge vectors of malaria parasites from non-human primates to humans, Front. Physiol., 3, 197, https://doi.org/10.3389/fphys.2012.00197, 2012.
Verrelli, B. C., Tishkoff, S. A., Stone, A. C., and Touchman, J. W.: Contrasting histories of G6PD molecular evolution and malarial resistance in humans and chimpanzees, Mol. Biol. Evol., 23, 1592–1601, https://doi.org/10.1093/molbev/msl024, 2006.
Volkman, S. K., Barry, A. E., Lyons, E. J., Nielsen, K. M., Thomas, S. M., Choi, M., Thakore, S. S., Day, K. P., Wirth, D. F., and Hartl, D. L.: Recent origin of Plasmodium falciparum from a single progenitor, Science, 293, 482–484, https://doi.org/10.1126/science.1059878, 2001.
Voorberg-vd Wel, A., Kocken, C. H., Zeeman, A. M., and Thomas, A. W.: Detection of new Babesia microti-like parasites in a rhesus monkey (Macaca mulatta) with a suppressed Plasmodium cynomolgi infection, Am. J. Trop. Med. Hyg., 78, 643–645, 2008.
White, N. J.: Malaria, Manson's tropical diseases, 21st ed., edited by: Cook, G. C. and Zumla, A., Saunders, London, UK, 1205–1295, 2003.
Whitworth, J., Morgan, D., Quigley, M., Smith, A., Mayanja, B., Eotu, H., Omoding, N., Okongo, M., Malamba, S., and Ojwiya, A.: Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study, Lancet, 356, 1051–1056, https://doi.org/10.1016/s0140-6736(00)02727-6, 2000.
WHO: Malaria – Fact sheet #94, available at: http://www.who.int/mediacentre/factsheets/fs094/en/index.html (last access: 2016), 2015.
Williams, T. N.: Red blood cell defects and malaria, Mol. Biochem. Parasit., 149, 121–127, https://doi.org/10.1016/j.molbiopara.2006.05.007, 2006.
Short summary
Humans and African great apes (AGAs) are naturally infected with several species of closely related malaria parasites. Research on AGA malaria has been driven by the need to understand the origins of human malaria and the risk of transmission of malaria parasites infecting AGAs to humans. The understanding of the ecology of AGA malaria parasites and their impact on AGA health remains relatively poor. We review current knowledge on AGA malaria and identify gaps and future research perspectives.
Humans and African great apes (AGAs) are naturally infected with several species of closely...
Special issue