First Detection of an Enterovirus C99 in a Captive Chimpanzee With
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First Detection of an Enterovirus C99 in a Captive Chimpanzee with Acute Flaccid Paralysis, from the Tchimpounga Chimpanzee Rehabilitation Center, Republic of Congo Illich Manfred Mombo, Nicolas Berthet, Alexander Lukashev, Tobias Bleicker, Sebastian Brünink, Lucas Léger, Rebeca Atencia, Debby Cox, Christiane Bouchier, Durand Patrick, et al. To cite this version: Illich Manfred Mombo, Nicolas Berthet, Alexander Lukashev, Tobias Bleicker, Sebastian Brünink, et al.. First Detection of an Enterovirus C99 in a Captive Chimpanzee with Acute Flaccid Paralysis, from the Tchimpounga Chimpanzee Rehabilitation Center, Republic of Congo. PLoS ONE, Public Library of Science, 2015, 10 (8), pp.e0136700. 10.1371/journal.pone.0136700. hal-02074621 HAL Id: hal-02074621 https://hal.archives-ouvertes.fr/hal-02074621 Submitted on 8 Mar 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. RESEARCH ARTICLE First Detection of an Enterovirus C99 in a Captive Chimpanzee with Acute Flaccid Paralysis, from the Tchimpounga Chimpanzee Rehabilitation Center, Republic of Congo Illich Manfred Mombo1,2*, Nicolas Berthet1,3, Alexander N. Lukashev4, Tobias Bleicker5, Sebastian Brünink5, Lucas Léger2, Rebeca Atencia6, Debby Cox6, Christiane Bouchier7, Patrick Durand2, Céline Arnathau2, Lionel Brazier2, Joseph N. Fair8, Bradley S. Schneider8, Jan Felix Drexler5, Franck Prugnolle1,2, Christian Drosten5, François Renaud2,9, Eric M. Leroy1,2‡, Virginie Rougeron1,2‡ 1 Centre International de Recherche Médicale de Franceville, BP769, Franceville, Gabon, 2 Laboratoire MIVEGEC UMR 224–5290 CNRS-IRD-UM1-UM2, IRD, Montpellier, France, 3 Centre National de la Recherche Scientifique, UMR3569, 25 rue du docteur Roux, 75724, Paris, France, 4 Chumakov Institute of Poliomyelitis and Viral Encephalities, Moscow, Russia, 5 Institute of Virology, University of Bonn Medical Centre, Bonn, Germany, 6 The Jane Goodall Institute, Suite 550, 1595 Spring Hill Rd, Vienna, Virginia, OPEN ACCESS 22182, United States of America, 7 Institut Pasteur, Genomic platform, 28, rue du Docteur Roux, F-75724, Paris, France, 8 Metabiota, Inc., 1 Sutter Street, Suite 600, San Francisco, California, 94104, United States Citation: Mombo IM, Berthet N, Lukashev AN, of America, 9 CHRU de Montpellier, Montpellier, France Bleicker T, Brünink S, Léger L, et al. (2015) First ‡ Detection of an Enterovirus C99 in a Captive These authors co-managed this work. * Chimpanzee with Acute Flaccid Paralysis, from the [email protected] Tchimpounga Chimpanzee Rehabilitation Center, Republic of Congo. PLoS ONE 10(8): e0136700. doi:10.1371/journal.pone.0136700 Abstract Editor: Juan C. de la Torre, The Scripps Research Institute, UNITED STATES Enteroviruses, members of the Picornaviridae family, are ubiquitous viruses responsible for Received: May 22, 2015 mild to severe infections in human populations around the world. In 2010 Pointe-Noire, Republic of Congo recorded an outbreak of acute flaccid paralysis (AFP) in the humans, Accepted: August 6, 2015 caused by wild poliovirus type 1 (WPV1). One month later, in the Tchimpounga sanctuary Published: August 24, 2015 near Pointe-Noire, a chimpanzee developed signs similar to AFP, with paralysis of the Copyright: © 2015 Mombo et al. This is an open lower limbs. In the present work, we sought to identify the pathogen, including viral and bac- access article distributed under the terms of the terial agents, responsible for this illness. In order to identify the causative agent, we evalu- Creative Commons Attribution License, which permits C unrestricted use, distribution, and reproduction in any ated a fecal specimen by PCR and sequencing. A Human enterovirus , specifically of the medium, provided the original author and source are EV-C99 type was potentially responsible for the illness in this chimpanzee. To rule out other credited. possible causative agents, we also investigated the bacteriome and the virome using next Data Availability Statement: The EV-C99 isolate generation sequencing. The majority of bacterial reads obtained belonged to commensal IJC04 sequence files are available from the GenBank bacteria (95%), and the mammalian virus reads matched mainly with viruses of the Picorna- database (accession number KP793035). viridae family (99%), in which enteroviruses were the most abundant (99.6%). This study Funding: This work was supported by the Gabonese thus reports the first identification of a chimpanzee presenting AFP most likely caused by an Government, Total Gabon and the ‘Institut National enterovirus and demonstrates once again the cross-species transmission of a human path- d’Ecologie et d’Evolution’ of CNRS (France). The work was also supported by a fellowship BSTD of the ogen to an ape. Institut de Recherche pour le Développement (IRD), France, as well as the generous support of the American people through the United States Agency for International Development (USAID) Emerging PLOS ONE | DOI:10.1371/journal.pone.0136700 August 24, 2015 1/11 Enterovirus C99 Infected a Chimpanzee with Paralytic Illness Pandemic Threats PREDICT. The funders had no Introduction role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. In the last few years, many pathogens capable of infecting humans, such as Ebola virus [1, 2], The contents are the responsibility of the authors and simian immunodeficiency viruses [3], respiratory viruses [4, 5], anthrax [6], herpes viruses [7] do not necessarily reflect the views of USAID or the as well as enteroviruses [8, 9] have been identified in great apes. Contacts between human pop- United States Government. Metabiota, Inc. provided ulations and great apes as well as monkeys are frequent and increasing, due to commercial support in the form of salaries for authors BSS and poaching, deforestation, and monitoring [10–13]. The direct consequence is the increased like- JNF, but did not have any additional role in the study – design, data collection and analysis, decision to lihood of pathogens exchanges and thus of emerging zoonoses and antropozoonoses [10 13]. publish, or preparation of the manuscript. The specific Enteroviruses (EVs) are small non-enveloped viruses with positive single strand RNA roles of these authors are articulated in the ‘author genomes that belong to the Picornaviridae family. Their genome, about 7.5 kb in length, contributions’ section. encodes four structural proteins (VP1-VP4) and seven non-structural proteins (2A to 2C and Competing Interests: The authors have the 3A to 3D). EVs consist of more than 300 serotypes and, based on the VP1 sequence, are classi- following interests. This work was partly supported by fied into nine species EV-A to EV-H and EV-J [14]. EVs infecting humans belong to species Total Gabon. Joseph N. Fair and Bradley S. EV-A to EV-D, formerly termed Human Enterovirus A-D, while the other species contain Schneider are employed by Metabiota, Inc. There are viruses infecting bovines (EV-E and EV-F), porcines (EV-G) and monkeys (EV-H and EV-J) no patents, products in development or marketed products to declare. This does not alter the authors' [14]. EV-C is associated with various human illnesses, such as the common cold, acute hemor- adherence to all the PLOS ONE policies on sharing rhagic conjunctivitis, aseptic meningitis and acute flaccid paralysis (AFP). Human EV A-D data and materials, as detailed online in the guide for have been detected in non-human primates, captive or wild Old World monkeys (such as authors. Macaca sp, Cercopithecus sp, Cercocebus and Papio sp) and wild African great apes (Gorilla gorilla and Pan troglodytes)[8, 15–17]. Importantly, both known and novel types of human enteroviruses could be found in primates, indicating common cross-species transmission [18]. In mid-October 2010, a poliomyelitis outbreak occurred in the human population of Point- Noire and surrounded areas and villages in the Republic of Congo (RC). The causative agent of this outbreak was identified as the type 1 wild poliovirus (WPV1), while a novel enterovirus 105 (EV-C105) was detected in one patient. Both PV1 and EV-C105 are members of the EV-C species [19, 20]. In November 2010, one month after the start of this outbreak, a chimpanzee (Pan troglodytes troglodytes) from the Tchimpounga Chimpanzee Rehabilitation Center devel- oped a syndrome compatible with AFP. The main objective of this study was to identify the pathogen responsible of this syndrome. We identified EV-C99 as a possible causative agent of this chimpanzee’s illness. This is the first identification and characterization of non-polio EV-C in a chimpanzee displaying AFP. Materials and Methods Case report and specimen collection In November 2010, in the Tchimpounga Chimpanzee Rehabilitation Center located 50 km from Pointe-Noire, a juvenile female chimpanzee presented signs of AFP. This chimpanzee first developed a 38.8°C fever and four days after, she lost the ability of her lower limbs and became quadriplegic. The first clinical examination revealed absence of the osteotendinous reflex, a myasthenia