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Malaria-Like Symptoms Associated with a Natural Plasmodium Reichenowi Infection in a Chimpanzee

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Malaria-Like Symptoms Associated with a Natural Plasmodium Reichenowi Infection in a Chimpanzee Herbert et al. Malaria Journal (2015) 14:220 DOI 10.1186/s12936-015-0743-y CASE REPORT Open Access Malaria-like symptoms associated with a natural Plasmodium reichenowi infection in a chimpanzee Anaïs Herbert1*, Larson Boundenga2,5, Anne Meyer3, Diamella Nancy Moukodoum2, Alain Prince Okouga2, Céline Arnathau4, Patrick Durand4, Julie Magnus2, Barthélémy Ngoubangoye1, Eric Willaume3, Cheikh Tidiane Ba5, Virginie Rougeron2,4, François Renaud4, Benjamin Ollomo2*† and Franck Prugnolle2,4*† Abstract Although Plasmodium infections have never been clearly associated with symptoms in non-human primates, the question of the pathogenicity of Plasmodium parasites in non-human primates still remains unanswered. A young chimpanzee, followed before and after release to a sanctuary, in a semi-free ranging enclosure located in an equatorial forest, showed fever and strong anaemia associated with a high Plasmodium reichenowi infection, shortly after release. The animal recovered from anaemia after several months despite recurrent infection with other Plasmodium species. This may be the first description of malaria-like symptoms in a chimpanzee infected with Plasmodium. Keywords: Plasmodium, Pan troglodytes, Chimpanzee, Symptom, Malaria, Anaemia, Hyperthermia, Fever Background Despite their genetic proximity with human parasite Non-human primates and particularly great apes are species especially P. falciparum, it is still unclear whether natural hosts of various Plasmodium parasites [1, 2], ape Plasmodium are virulent, that is whether great apes including species very closely related to human parasites, express disease or not when they are infected [5]. A case like Plasmodium falciparum (the most virulent agent of of a fatal Plasmodium infection in a chimpanzee was human malaria), Plasmodium malariae, Plasmodium previously described [6], as well as in a gorilla [7], but ovale and Plasmodium vivax (Fig. 1) [3, 4]. Among the theexactnatureoftheparasiteinvolvedwasnever species related to P. falciparum and classified into the determined with molecular tools, thus leaving the possi- subgenus Laverania, three species were shown to infect bility of an infection with a human parasite (P. falcip- only chimpanzees (Plasmodium gaboni, Plasmodium arum in particular). In addition, other pathogens could billcollinsi and Plasmodium reichenowi) and three only have caused these deaths and no special efforts were gorillas (Plasmodium adleri, Plasmodium blacklocki and made to reject these possibilities. In contrast, other Plasmodium praefalciparum). For the species related to authors showed that the presence of Plasmodium in P. malariae, P. ovale and P. vivax and classified in the African great apes was not correlated with any increase subgenus Plasmodium, they were all shown to infect of temperature or any other symptoms [1] or that the both chimpanzees and gorillas. haematologic and biochemical values, as well as the ma- jority of immunologic parameters, remained unaltered in chimpanzees infected with P. falciparum [8]. * Correspondence: [email protected]; [email protected]; franck. Some researchers noticed malaria-like symptoms [email protected] responding to anti-malaria treatment in orangutans † Equal contributors but without clear evidence of the presence of the 1Centre de Primatologie, Centre International de Recherches Médicales de Franceville, BP 769 Franceville, Gabon pathogen [9]. In non-human primates other than great 2Unité de Biodiversité, Ecologie et Evolution des Parasites (UBEEP), Centre apes, studies showed that experimental infections of rhe- International de Recherches Médicales de Franceville, BP 769 Franceville, sus macaques with Plasmodium knowlesi, Plasmodium Gabon Full list of author information is available at the end of the article coatneyi,andlessoftenPlasmodium cynomolgi,maybe © 2015 Herbert et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Herbert et al. Malaria Journal (2015) 14:220 Page 2 of 8 HM235317-P. gaboni FJ895308-P. gaboni 96 HM234979- P. gaboni P. gaboni 95 Wonga day307_day344_day393 JX893151-P. gaboni clone 39C 99 GQ355471-P. billbrayi UGD P. billbrayi 99 GQ355470-P. billbrayi-UGB GU045321-P. adleri P. adleri 100 HM235059-P. adleri Subgenus Laverania KP875468-P. praefalciparum P. praefalciparum 100 100 AY910013-P. falciparum AY588280-P. falciparum P. falciparum 92 AF069605-P. falciparum 3D7 HM234980-P. reichenowi 97 GU045315-P. reichenowi P. reichenowi 99 Wonga day192 78 GQ355477-P. billcollinsi-UGD P. billcollinsi GU045317-P. blacklocki P. blacklocki AB489193-P. malariae 65 99 KF591814-P. vivax JQ345521-P. knowlesi Subgenus Plasmodium (non-Laverania) 96 JF923756-P. sp. DAJ-2004 84 JF923752-P. gonderi AB182496-P. ovale 0.02 Human Gorilla Chimpanzee Fig. 1 Phylogenetic relationships among primate Plasmodium based on cytochrome b sequences (680 bp). Sequences obtained for Wonga at the different checkups are included in red. The sequences reported in this study were deposited in Genbank under the following accession numbers: KR350681 to KR350683 characterized by jaundice, anorexia, listlessness, fever, Franceville (CIRMF) and finally released into semi-free anaemia, and splenomegaly in spleen-intact animals [10]. ranging enclosures in the sanctuary. Wonga was re- Moreover, P. knowlesi-infected baboons expressed either leased into a group of 10 chimpanzees, ranging from 3 acute infection with multiple system organ dysfunctions to 12 year-old, sharing a 7-ha-semi-free ranging enclos- and cerebral involvement, or a chronic infection with ure in dense equatorial forest. The chimpanzees are left spleen enlargement [11]. in the enclosure nights and days, and sleep in the trees. Therefore, no evidence of symptoms was ever clearly Food supplementation is offered every day, around associated with natural Plasmodium infection in non- 10 am and 2 pm, and consists of fruits and protein human primates, especially in great apes. This case cakes. During feeding, keepers monitor animals’ global present what could be the first description of symptoms health on site. Contacts with humans are extremely associated to a clearly identified natural Plasmodium limited, to annual medical check-ups or health-care- infection in a chimpanzee. needed anesthesia. Chimpanzees are not followed dur- ing the day and evolve freely into the enclosure. Case presentation Three and a half months after Wonga’s release into History the group, routine medical annual check-up was per- A 6-year-old female chimpanzee (Pan troglodytes troglo- formed on all the chimpanzees of the group. dytes), named Wonga, was brought to the Centre Inter- All procedures in this study involving animals were national de Recherches Médicales de Franceville (CIRMF) approved by the Government of the Republic of Gabon. after being confiscated from illegal owners in Libreville, This study complied with the relevant national guidelines Gabon. She was captured by the owners after they killed and with the IUCN Policy Statement on Research Involv- her mother and was kept as a pet for most of her life, living ing Species at Risk of Extinction. inside the owners’ house in an urban environment. She spent her quarantine at CIRMF and cleared out after Clinical examinations 90 days. She was then transferred to the sanctuary “Parc de During her quarantine, three clinical check-ups were la Lékédi”, Bakoumba (Haut-Ogooué, Gabon). performed on days 0, 22 and 51, following CIRMF quar- The sanctuary “Parc de la Lékédi”, Bakoumba, holds antine protocol. For every medical check-up, the animal various primates species, including gorillas, chimpanzees was anaesthetized with ketamine (10 mg/kg) via intra- and small monkeys, all bushmeat-poaching-issued or- muscular injection. Once asleep, blood was collected phans, which have been confiscated by the Gabonese from femoral vena into EDTA and dry tubes, on which Government, gone through a quarantine period at pathogen screenings were performed. Wonga expressed the Centre International de Recherches Médicales de no clinical symptoms of any disease or infection. Her Herbert et al. Malaria Journal (2015) 14:220 Page 3 of 8 temperature was stable over these check-ups (mean = results showed no strong abnormalities all along check- 37.1 °C; SD = 0.25166). She constantly gained weight ups (Table 1) [12]. During her quarantine at CIRMF, over the three check-ups, which is expected from an in- Wonga was sampled three times. Her haematologic dividual recently confiscated and poorly nourished upon results were within or slightly below normal ranges for arrival at CIRMF (Fig. 2f). juvenile female chimpanzees (Table 2) [12]. Three and a half months after her transfer to the Parc During her first post-release check-up (day 192), de la Lékédi, on day 192, annual check-up of all chim- correlated with her fever, her haematological results panzees of the group was routinely performed. Four showed anaemia, with low haematocrit, low haemo- chimpanzees (including this animal) were sampled on globin level and low red blood cell count (Table 2 the same day. They were anaesthetized with ketamine and Fig. 2). (10 mg/kg) via intramuscular injection. The veterina- rians noticed
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