Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T08:15:15.923Z Has data issue: false hasContentIssue false
  • English
  • Français

Ecology of malaria infections in western lowland gorillas inhabiting Dzanga Sangha Protected Areas, Central African Republic

Published online by Cambridge University Press:  04 March 2015

MWANAHAMISI I. MAPUA ,
MONEEB A. QABLAN ,
KATEŘINA POMAJBÍKOVÁ ,
KLÁRA J. PETRŽELKOVÁ ,
ZUZANA HŮZOVÁ ,
JANA RÁDROVÁ ,
JAN VOTÝPKA ,
ANGELIQUE TODD ,
MILAN JIRKŮ  and
FABIAN H. LEENDERTZ
...Show all authors
MWANAHAMISI I. MAPUA
Affiliation:
Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
MONEEB A. QABLAN*
Affiliation:
Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Central European Institute for Technology (CEITEC), University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
KATEŘINA POMAJBÍKOVÁ
Affiliation:
Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic
KLÁRA J. PETRŽELKOVÁ
Affiliation:
Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic Institute of Vertebrate Biology, Czech Academy of Sciences, 603 00 Brno, Czech Republic Liberec Zoo, 460 01 Liberec, Czech Republic
ZUZANA HŮZOVÁ
Affiliation:
Health Institute in Ústí nad Labem, Sokolovska 60, Prague 8 180 00, Czech Republic
JANA RÁDROVÁ
Affiliation:
Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic Department of Parasitology, Faculty of Science, Charles University, 128 44 Prague, Czech Republic
JAN VOTÝPKA
Affiliation:
Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic Department of Parasitology, Faculty of Science, Charles University, 128 44 Prague, Czech Republic
ANGELIQUE TODD
Affiliation:
WWF, Dzanga Sangha Protected Areas, BP 1053 Bangui, Central African Republic
MILAN JIRKŮ
Affiliation:
Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, 370 05 České Budějovice, Czech Republic
FABIAN H. LEENDERTZ
Affiliation:
Project Group Epidemiology of Highly Pathogenic Microbiology, Robert Koch-Institut, Nordufer 20, 13353 Berlin, Germany
JULIUS LUKEŠ
Affiliation:
Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, 370 05 České Budějovice, Czech Republic Canadian Institute for Advanced Research, Toronto ON, M5G 1Z8, Canada
CECILE NEEL
Affiliation:
Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
DAVID MODRÝ
Affiliation:
Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Central European Institute for Technology (CEITEC), University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Institute of Parasitology, Biology Centre, Czech of the Academy of Sciences, 370 05 České Budějovice, Czech Republic
*
*Corresponding author. Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic and Central European Institute for Technology (CEITEC), University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic. E-mail: moneeb_78@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

African great apes are susceptible to infections with several species of Plasmodium, including the predecessor of Plasmodium falciparum. Little is known about the ecology of these pathogens in gorillas. A total of 131 gorilla fecal samples were collected from Dzanga-Sangha Protected Areas to study the diversity and prevalence of Plasmodium species. The effects of sex and age as factors influencing levels of infection with Plasmodium in habituated gorilla groups were assessed. Ninety-five human blood samples from the same locality were also analysed to test for cross-transmission between humans and gorillas. According to a cytB PCR assay 32% of gorilla's fecal samples and 43·1% human individuals were infected with Plasmodium spp. All Laverania species, Plasmodium vivax, and for the first time Plasmodium ovale were identified from gorilla samples. Plasmodium praefalciparum was present only from habituated individuals and P. falciparum was detected from human samples. Although few P. vivax and P. ovale sequences were obtained from gorillas, the evidence for cross-species transmission between humans and gorillas requires more in depth analysis. No association was found between malaria infection and sex, however, younger individuals aged ≤6 years were more susceptible. Switching between two different Plasmodium spp. was observed in three individuals. Prolonged monitoring of Plasmodium infection during various seasons and recording behavioural data is necessary to draw a precise picture about the infection dynamics.

Keywords

African great apesmalarialowland gorillaPlasmodium spp
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 890 - 900
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adler, S. (1923). Malaria in chimpanzees in Sierra Leone. Annals of Tropical Medicine and Parasitology 17, 13–19.Google Scholar
Baird, J. K. (2009). Malaria zoonoses. Travel Medicine and Infectious Disease 7, 269–277.CrossRefGoogle ScholarPubMed
Blacklock, B. and Adler, S. (1922). A parasite resembling Plasmodium falciparum in a chimpanzee. Annals of Tropical Medicine and Parasitology 160, 99–106.Google Scholar
Blom, A., Cipolletta, C., Brunsting, A. M. and Prins, H. H. (2004). Behavioral responses of gorillas to habituation in the Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 25, 179–196.Google Scholar
Bray, R. (1958). Studies on malaria in chimpanzees. V. The sporogonous cycle and mosquito transmission of Plasmodium vivax schwetzi. The Journal of Parasitology 44, 46–51.Google Scholar
Breuer, T., Hockemba, M. B., Olejniczak, C., Parnell, R. J. and Stokes, E. J. (2008). Physical maturation, life-history classes and age estimates of free-ranging western gorillas insights from Mbeli Bai, Republic of Congo. America Journal of Primatology 71, 106–119.CrossRefGoogle Scholar
Chapman, C. A., Gillespie, T. R. and Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology: Issues, News, and Reviews 14, 134–144.CrossRefGoogle Scholar
Cipolletta, C. (2003). Ranging patterns of a western gorilla group during habituation to humans in the Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 24, 1207–1226.Google Scholar
Collins, W. E. (2012). Plasmodium knowlesi: a malaria parasite of monkeys and humans. Annual Review of Entomology 57, 107–121.Google Scholar
De Beaudrap, P., Nabasumba, C., Grandesso, F., Turyakira, E., Schramm, B., Boum, Y. and Etard, J. F. (2011). Heterogeneous decrease in malaria prevalence in children over a six-year period in south-western Uganda. Malaria Journal 10, 132.CrossRefGoogle Scholar
De Nys, H. M., Calvignac-Spencer, S., Thiesen, U., Boesch, C., Wittig, R. M., Mundry, R. and Leendertz, F. H. (2013). Age-related effects on malaria parasite infection in wild chimpanzees. Biology Letters 9, 20121160.CrossRefGoogle ScholarPubMed
Doolan, D. L., Dobano, C. and Baird, J. K. (2009). Acquired immunity to malaria. Clinical Microbiology Reviews 22, 13–36.CrossRefGoogle ScholarPubMed
Doran-Sheehy, D. M., Derby, A. M., Greer, D. and Mongo, P. (2007). Habituation of western gorillas: the process and factors that influence it. American Journal of Primatology 69, 1354–1369.CrossRefGoogle Scholar
Duval, L., Nerrienet, E., Rousset, D., Mba, S. A. S., Houze, S., Fourment, M., Le Bras, J., Robert, V. and Ariey, F. (2009). Chimpanzee malaria parasites related to Plasmodium ovale in Africa. PLoS One, 4: e5520.CrossRefGoogle ScholarPubMed
Duval, L. and Ariey, F. (2012). Ape Plasmodium parasites as a source of human outbreaks. Clinical Microbiology and Infection 18, 528–532.CrossRefGoogle ScholarPubMed
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. (2010). African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proceedings of the National Academy of Sciences 107, 10561–10566.Google Scholar
Escalante, A. A. and Ayala, F. J. (1994). Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proceedings of the National Academy of Sciences 91, 11373–11377.CrossRefGoogle ScholarPubMed
Garnham, P., Lainson, R. and Gunders, A. (1956). Some observations on malaria parasites in a chimpanzee, with particular reference to the persistence of Plasmodium reichenowi and Plasmodium vivax . Annales de la Societe Belge de Medecine Tropicale 36, 811–821.Google Scholar
Goselle, O. N., Onwuliri, C. O. and Onwuliri, V. A. (2009). Malaria infection in HIV/AIDS patients and its correlation with packed cell volume (PCV). Journal of Vector Borne Diseases 46, 205–211.Google Scholar
Hasegawa, H., Modrý, D., Kitagawa, M., Shutt, K. A., Todd, A., Kalousová, B., Profousová, I. and Petrželková, K. J. (2014). Humans and Great Apes Cohabiting the Forest Ecosystem in Central African Republic Harbour the Same Hookworms. PLoS Neglected Tropical Diseases 8, e2715.Google Scholar
Hayakawa, T., Arisue, N., Udono, T., Hirai, H., Sattabongkot, J., Toyama, T., Tsuboi, T., Horii, T. and Tanabe, K. (2009). Identification of Plasmodium malariae, a human malaria parasites, in imported chimpanzees. PLoS ONE 4, e7412.CrossRefGoogle ScholarPubMed
Janatova, M., Albrechtova, K., Petrzelkova, K. J., Dolejska, M., Papousek, I., Masarikova, M., Cizek, A., Todd, A., Shutt, K., Kalousova, B., Profousova-Psenkova, I., Modry, D. and Literak, I. (2014). Antimicrobial-resistant Enterobacteriaceae from humans and wildlife in Dzanga-Sangha Protected Area, Central African Republic. Veterinary Microbiology 171, 422–431.Google Scholar
Jensen, S. A., Mundry, R., Nunn, C. L., Boesch, C. and Leendertz, F. H. (2009). Non-invasive body temperature measurement of wild chimpanzees using fecal temperature decline. Journal of Wildlife Disease 45, 542–546.Google Scholar
Kaiser, M., Löwa, A., Ulrich, M., Ellerbrok, H., Goffe, A. S., Blasse, A., Zommers, Z., Couacy-Hymann, E., Babweteera, F., Zuberbühler, K., Metyger, S., Geidel, S., Boesch, C., Gillespies, T. R. and Leendertz, F. H. (2010). Wild chimpanzees infected with 5 Plasmodium species. Emerging Infectious Diseases 16, 1956–1959.CrossRefGoogle ScholarPubMed
Kalema-Zikusoka, G., Rothman, J. M. and Fox, M. T. (2005). Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates 46, 59–63.CrossRefGoogle ScholarPubMed
Keele, B. F., Van Heuverswyn, F., Li, Y., Bailes, E., Takehisa, J., Santiago, M. L., Bibollet-Ruche, F., Chen, Y., Wain, L. V., Liegeois, F., Loul, S., Ngole, E. M., Bienvenue, Y., Delaporte, E., Brookfield, J. F., Sharp, P. M., Shaw, G. M., Peeters, M. and Hann, B. H. (2006). Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313, 523–526.Google Scholar
Klailova, M., Hodgkinson, C. and Lee, P. C. (2010). Behavioral responses of one western lowland gorilla (Gorilla gorilla gorilla) group at Bai Hokou, Central African Republic, to tourists, researchers and trackers. American Journal of Primatology 72, 897–906.CrossRefGoogle ScholarPubMed
Köndgen, S., Kühl, H., N'Goran, P. K., Walsh, P. D., Schenk, S., Ernst, N., Biek, R., Formenty, P., Mätz-Rensing, K., Schweiger, B., Junglen, S., Ellerbrok, H., Nitsche, A., Briese, T., Lipkin, W. I., Pauli, G., Boesch, C. and Leendertz, F. H. (2008). Pandemic human viruses cause decline of endangered great apes. Current Biology 18, 260–264.CrossRefGoogle ScholarPubMed
Krief, S., Escalante, A. A., Pacheco, M. A., Mugisha, L., André, C., Halbwax, M., Fischer, A., Krief, J.-M., Kasenene, J. M., Crandfield, M., Cornejo, O. E., Chavatte, J. M., Lin, C., Letourneur, F., Grüner, A. C., McCutchan, T. F., Rénia, L. and Snounou, G. (2010). On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathogens 6, e1000765.CrossRefGoogle ScholarPubMed
Krief, S., Levrero, F., Krief, J. M., Thanapongpichat, S., Imwong, M., Snounou, G., Kasenene, J. M., Cibot, M. and Gantier, J. H. (2012). Invetigation in anopheline mosquitoes close to the nest sites of chimpanzees subject to malaria infection in Ugandan Highlands. Malaria Journal 11, 116.Google Scholar
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. (2010). Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420–425.Google Scholar
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., 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. et al. (2014). African origin of the malaria parasite Plasmodium vivax . Nature Communications 5, 3346.CrossRefGoogle ScholarPubMed
Masi, S. (2009) Habituation, ecotourism and research for conservation of western gorillas in Central African Republic–Bai Hokou. Gorilla Gazette 21, 31–34.Google Scholar
Masi, S., Cipolletta, C. and Robbins, M. M. (2009). Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory. American Journal of Primatology 71, 91–100.CrossRefGoogle ScholarPubMed
Morton, F. B., Todd, A. F., Lee, P. and Masi, S. (2013). Observational monitoring of clinical signs during the last stage of habituation in a wild western gorilla group at Bai Hokou, Central African Republic. Folia Primatology (Basel) 84, 118–133.CrossRefGoogle Scholar
Mueller, I., Zimmerman, P. A. and Reeder, J. C. (2007). Plasmodium malariae and Plasmodium ovale – the ‘bashful’ malaria parasites. Trends in Parasitology 23, 278–283.CrossRefGoogle ScholarPubMed
Müller-Graf, C. D. M., Collins, D. A. and Woolhouse, M. E. J. (1996). Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112: 489–497.Google Scholar
Newcombe, R. G. (1998). Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics in Medicine 17, 857–872.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Ollomo, B., Durand, P., Prugnolle, F., Douzery, E., Arnathau, C., Nkoghe, D., Leroy, E. and Renaud, F. (2009). A new malaria agent in African hominids. PLoS Pathogens 5, e1000446.Google Scholar
Pacheco, M. A., Cranfield, M., Cameron, K. and Escalante, A. A. (2013). Malarial parasites diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malaria Journal 12, 328.Google Scholar
Pathak, S., Rege, M., Gogtay, N. J., Aigal, U., Sharma, S. K., Valecha, N., Bhanot, G., Kshirsagar, N. A. and Sharma, S. (2012). Age-dependent sex bias in clinical malarial disease in hypoendemic regions. PLoS ONE 7, e35592.Google Scholar
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. (2010). African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum . Proceedings of the National Academy of Sciences 107, 1458–1463.Google Scholar
Prugnolle, F., Durand, P., Ollomo, B., Duval, L., Ariey, F., Arnathau, C., Gonzalez, J.-P., Leroy, E. and Renaud, F. (2011 a). A fresh look at the origin of Plasmodium falciparum, the most malignant malaria agent. PLoS Pathogens 7, e1001283.Google Scholar
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. (2011 b). African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. Proceedings of the National Academy of Sciences 108, 11948–11953.Google Scholar
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. (2013). Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proceedings of the National Academy of Sciences 110, 8123–8128.Google Scholar
Rayner, J. C., Liu, W., Peeters, M., Sharp, P. M. and Hahn, B. H. (2011). A plethora of Plasmodium species in wild apes: a source of human infection? Trends in Parasitology 27, 222–229.CrossRefGoogle ScholarPubMed
R Development Core Team (2011), R: A Language and Environment for Statistical Computing. Vienna, Austria: the R Foundation for Statistical Computing. ISBN: 3-900051-07-0.Google Scholar
Reid, M. J., Ursic, R., Cooper, D., Nazzari, H., Griffiths, M., Galdikas, B. M., Garriga, R. M., Skinner, M. and Lowenberger, C. (2006). Transmission of human and macaque Plasmodium spp. to ex-captive orangutans in Kalimantan, Indonesia. Emerging Infectious Diseases 12, 1902–1908.Google Scholar
Remis, M. J. and Jost Robinson, C. A. (2012). Reductions in primate abundance and diversity in a multiuse protected area: synergistic impacts of hunting and logging in a Congo Basin forest. American Journal of Primatology 74, 602–612.Google Scholar
Rodhain, J. (1939). Les plasmodiums des anthropoides de I'Afrique centrale et leurs relations avec les plasmodiums humains. Annales de la Societe Belge de Medecine Tropicale 19, 563–572.Google Scholar
Rothman, J. M., Dierenfeld, E. S., Hintz, H. F. and Pell, A. N. (2008). Nutritional quality of gorilla diets: consequences of age, sex, and season. Oecologia 155, 111–122.Google Scholar
Sak, B., Petrzelkova, K. J., Kvetonova, D., Mynarova, A., Shutt, K. A., Pomajbikova, K., Kalousova, B., Modry, D., Benavides, J., Todd, A. and Kvac, M. (2013). Long-term monitoring of microsporidia, cryptosporidium and giardia infections in western lowland gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. PLoS ONE 8, e71840.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. and Koella, J. (1994). Variability and its implications for host–parasite interactions. Parasitology Today 10, 98–102.Google Scholar
Shutt, K., Heistermann, M., Kasim, A., Todd, A., Kalousova, B., Profosouva, I., Petrzelkova, K., Fuh, T., Dicky, J.-F., Bopalanzognako, J.-B. and Setchell, J. M. (2014). Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: implications for conservation management. Biological Conservation 172, 72–79.CrossRefGoogle Scholar
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. (2013). Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proceedings of the National Academy of Sciences 110, 7020–7025.Google Scholar
Sutherland, C., Tanomsing, N., Nolder, D., Oguike, M., Jennison, C., Pukrittayakamee, S., Dolecek, C., Hien, T. T., do Rosário, V. E., Arez, A. P., Pinto, J., Michon, P., Escalante, A., Nosten, F., Burke, M., Lee, R., Blaze, M., Otto, T. D., Barnwell, J., Pain, A., Williams, J., White, N. J., Day, N. P. J., Snounou, G., Lockhart, P. J., Chiodini, P. L., Imwong, M. and Polley, S.D. (2010). Two non-recombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally. The Journal of Infectious Disease. 201, 1544–1550.CrossRefGoogle Scholar
Verhulst, N. O., Smallegange, R. C. and Takken, W. (2012). Mosquitoes as potential bridge vectors of malaria parasites from non-human primates to humans. Frontiers in Physiology 3, 197.CrossRefGoogle ScholarPubMed
Wildling, E., Winkler, S., Kremsner, P., Brandts, C., Jenne, L. and Wernsdorfer, W. (1995). Malaria epidemiology in the province of Moyen Ogoov, Gabon. Tropical Medicine and Parasitology 46, 77–82.Google Scholar
Win, T. T., Jalloh, A., Tantular, I. S., Tsuboi, T., Ferreira, M. U., Kimura, M. and Kawamoto, F. (2004). Molecular analysis of Plasmodium ovale variants. Emerging Infectious Diseases 10, 1235–1240.CrossRefGoogle ScholarPubMed