, Volume 13, Issue 3, pp 499–510 | Cite as

Codetection of Respiratory Syncytial Virus in Habituated Wild Western Lowland Gorillas and Humans During a Respiratory Disease Outbreak

  • Kim S. Grützmacher
  • Sophie Köndgen
  • Verena Keil
  • Angelique Todd
  • Anna Feistner
  • Ilka Herbinger
  • Klara Petrzelkova
  • Terrence Fuh
  • Siv Aina Leendertz
  • Sébastien Calvignac-Spencer
  • Fabian H. LeendertzEmail author
Original Contribution


Pneumoviruses have been identified as causative agents in several respiratory disease outbreaks in habituated wild great apes. Based on phylogenetic evidence, transmission from humans is likely. However, the pathogens have never been detected in the local human population prior to or at the same time as an outbreak. Here, we report the first simultaneous detection of a human respiratory syncytial virus (HRSV) infection in western lowland gorillas (Gorilla gorilla gorilla) and in the local human population at a field program in the Central African Republic. A total of 15 gorilla and 15 human fecal samples and 80 human throat swabs were tested for HRSV, human metapneumovirus, and other respiratory viruses. We were able to obtain identical sequences for HRSV A from four gorillas and four humans. In contrast, we did not detect HRSV or any other classic human respiratory virus in gorilla fecal samples in two other outbreaks in the same field program. Enterovirus sequences were detected but the implication of these viruses in the etiology of these outbreaks remains speculative. Our findings of HRSV in wild but human-habituated gorillas underline, once again, the risk of interspecies transmission from humans to endangered great apes.


respiratory disease respiratory syncytial virus enterovirus western lowland gorillas great apes noninvasive detection 



We would like to thank the government of the Central African Republic for long-term support, especially the Ministère d’Eaux et Fôret, Chasse et Peche and the Ministère de l’Education Nationale, de l’Alphabetisation, de l’Enseignement Superieur, et de la Recherche. In particular, we thank Jean-Baptiste Mamang-Kanga, Guian Zokoe, and Christian Ndadet. We thank the staff of DSPA and especially of the Primate Habituation Programme, for logistical support in the field, and WWF for their support at DSPA and in Bangui. We would also like to thank the Hans Böckler Stiftung, the EAZA Ape Conservation Fund, Zoo Leipzig, and WWF Germany for support and funding. KJP worked under institutional support of the Institute of Vertebrate Biology Academy of Sciences of the Czech Republic (RVO: 68081766).

Informed Consent

Informed consent was obtained from all individual participants included in the study.


  1. Bennett BT, Abee CR, Henrickson, R (1998) Nonhuman primates in biomedical research: diseases. Academic Press, CambridgeGoogle Scholar
  2. Buitendijk H, Fagrouch Z, Niphuis H, Bogers WM, Warren KS, Verschoor EJ (2014) Retrospective serology study of respiratory virus infections in captive great apes. Viruses 6.3:1442-1453PubMedPubMedCentralCrossRefGoogle Scholar
  3. Campbell G, Kuehl H, Diarrassouba A, N’Goran PK, Boesch C (2011) Long-term research sites as refugia for threatened and over-harvested species. Biology Letters rsbl20110155Google Scholar
  4. Chi F, Leider M, Leendertz F, Bergmann C, Boesch C, Schenk S, Pauli G, Ellerbrok H, Hakenbeck R (2007) New Streptococcus pneumoniae clones in deceased wild chimpanzees. Journal of Bacteriology 189:6085–6088PubMedPubMedCentralCrossRefGoogle Scholar
  5. Chmielewicz B, Nitsche A, Schweiger B, Ellerbrok H (2005) Development of a PCR-based assay for detection, quantification, and genotyping of human adenoviruses. Clinical Chemistry 51:1365–1373PubMedCrossRefGoogle Scholar
  6. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9.8, 772PubMedPubMedCentralCrossRefGoogle Scholar
  7. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7 Molecular Biology and Evolution 29:1969-1973PubMedPubMedCentralCrossRefGoogle Scholar
  8. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32.5:1792-97PubMedPubMedCentralCrossRefGoogle Scholar
  9. Gilardi KV, Gillespie TR, Leendertz FH, Macfie EJ, Travis DA, Whittier CA, Williamson EA (2015) Best Practice Guidelines for Health Monitoring and Disease Control in Great Ape Populations. Gland: IUCN SSC Primate Specialist Group. 56 pp.Google Scholar
  10. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4 : a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27.2:221-224PubMedCrossRefGoogle Scholar
  11. Guindon S and Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52:696-704PubMedCrossRefGoogle Scholar
  12. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Systematic Biology 59.3:307-21PubMedCrossRefGoogle Scholar
  13. Gruen L, Fultz A, Pruetz, J (2013) Ethical issues in African great ape field studies. Institute for Laboratory Animal Research Journal 54.1:24-32CrossRefGoogle Scholar
  14. Harvala H, Sharp CP, Ngole EM, Delaporte E, Peeters M, Simmonds P (2011) Detection and genetic characterization of enteroviruses circulating among wild populations of chimpanzees in Cameroon: relationship with human and simian enteroviruses. Journal of Virology 85.9:4480-4486PubMedPubMedCentralCrossRefGoogle Scholar
  15. Harvala H, Van Nguyen D, McIntyre C, Ahuka-Mundeke S, Ngole EM, Delaporte E, Peeters M, Simmonds P (2014) Co-circulation of enteroviruses between apes and humans. Journal of General Virology 95.2:403-407PubMedPubMedCentralCrossRefGoogle Scholar
  16. Hoppe E, Pauly M, Gillespie TR, Akoua-Koffi C, Hohmann G, Fruth B, Karhemere S, Madinda NF, Mugisha L, Muyembe JJ, Todd A, Petrzelkova KJ, Gray M, Robbins M, Bergl RA, Wittig RM, Zuberbühler K, Boesch C, Schubert G, Leendertz FH, Ehlers B, Calvignac-Spencer S (2015) Multiple cross-species transmission events of human adenoviruses (HAdV) during hominine evolution. Molecular Biology and Evolution, msv090Google Scholar
  17. Jang YJ, Lee SH, Kwon HJ, Chung YS, Lee BJ (2005) Development of rhinovirus study model using organ culture of turbinate mucosa. Journal of Virological Methods 125:41–47PubMedCrossRefGoogle Scholar
  18. Johnson DF, Druce JD, Birch C, Grayson ML (2009) A quantitative assessment of the efficacy of surgical and N95 masks to filter influenza virus in patients with acute influenza infection. Clinical Infectious Diseases 49:275–277PubMedCrossRefGoogle Scholar
  19. Kalter SS, Heberling RL, Cooke AW, Barry JD, Tian PY, Northam WJ (1997) Viral infections of nonhuman primates. Comparative Medicine 47.5:461-467Google Scholar
  20. Kaur T, Singh J, Tong S, Humphrey C, Clevenger D, Tan W, Szekely B, Wang Y, Li Y, Muse EA, Kiyono M, Hanamura S, Inoue E, Nakamura M, Huffman MA, Jiang B, Nishida T (2008) Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. American Journal of Primatology 70:755–765PubMedCrossRefGoogle Scholar
  21. Kelly ME, Soike K, Ahmed K, Iatropoulos MJ (1977) Coxsackievirus in an infant chimpanzee. Journal of Medical Primatology, 7.2:119-121Google Scholar
  22. Köndgen S, Kühl H, N’Goran P, Walsh P, Schenk S, Ernst N, Biek R, Formenty P, Mätz-Rensing K, Schweiger B, Junglen S, Ellerbrok H, Nitsche A, Briese T, Lipkin I, Pauli G, Boesch C, Leendertz F (2008) Pandemic human viruses cause decline of endangered great apes. Current Biology 18:1–5CrossRefGoogle Scholar
  23. Köndgen S, Schenk S, Pauli G, Boesch C, Leendertz FH (2010) Noninvasive monitoring of respiratory viruses in wild chimpanzees. Ecohealth 7.3:332-341PubMedCrossRefGoogle Scholar
  24. Köndgen S, Leider M, Lankester F, Bethe A, Lübke-Becker A, Leendertz FH, Ewers C (2011) Pasteurella multocida involved in respiratory disease of wild chimpanzees. PloS one 6.9 e24236-e24236PubMedPubMedCentralCrossRefGoogle Scholar
  25. Kooriyama T, Okamoto M, Yoshida T, Nishida T, Tsubota T, Saito A, Tomonaga M, Matsuzawa T, Akari H, Nishimura H, Miyabe-Nishiwaki T (2013) Epidemiological study of zoonoses derived from humans in captive chimpanzees. Primates 54.1:89-98PubMedCrossRefGoogle Scholar
  26. Lonsdorf EV, Travis D, Pusey AE, Goodall J (2006) Using retrospective health data from the Gombe chimpanzee study to inform future monitoring efforts. Journal of Medical Primatology 68:897–908CrossRefGoogle Scholar
  27. Macfie EJ and Williamson EA (2010) Best Practice Guidelines for Great Ape Tourism. Gland: IUCN/SSC Primate Specialist Group (PSG). 78 ppGoogle Scholar
  28. Mackay IM, Bialasiewicz S, Waliuzzaman Z, Chidlow GR, Fegredo DC, Laingam S, Adamson P, Harnett GB, Rawlinson W, Nissen MD, Sloots TP (2004) Use of the P gene to genotype human metapneumovirus identifies 4 viral subtypes. The Journal of Infectious Diseases 190:1913–1918PubMedCrossRefGoogle Scholar
  29. McAvin JC, Reilly PA, Roudabush RM, Barnes WJ, Salmen A, Jackson GW, Beninga KK, Astorga A, McCleskey FK, Huff WB, Niemeyer D, Lohman KL (2001) Sensitive and specific method for rapid identification of Streptococcus pneumoniae using real-time fluorescence PCR. Journal of Clinical Microbiology 39:3446-3451PubMedPubMedCentralCrossRefGoogle Scholar
  30. Milton DK, Fabian MP, Cowling BJ, Grantham ML, McDevitt JJ (2013) Influenza Virus Aerosols in Human Exhaled Breath: Particle Size, Culturability, and Effect of Surgical Masks. PLoS Pathogens 9(3):e1003205. doi: 10.1371/journal.ppat.1003205 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O’Brien KL, Roca A, Wright PF, Bruce N, Chandran A, Theodoratou E, Sutanto A, Sedyaningsih ER, Ngama M, Munywoki PK, Kartasasmita C, Simões EAF, Rudan I, Weber MW, Campbell H (2010) Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. The Lancet 375.9725:1545-1555CrossRefGoogle Scholar
  32. Nielsen SCA, Mourier T, Baandrup U, Søland TM, Bertelsen MF, Gilbert MTP, Nielsen LP (2012) Probable transmission of coxsackie B3 virus from human to chimpanzee, Denmark. Emerging Infectious Diseases 18.7:1163PubMedCrossRefGoogle Scholar
  33. Nunn CL, Thrall PH, Stewart K, Harcourt AH (2008) Emerging infectious diseases and animal social systems. Evolutionary Ecology 22.4:519-543CrossRefGoogle Scholar
  34. Palacios G, Oberste MS (2005) Enteroviruses as agents of emerging infectious diseases. Journal of Neurovirology 11.5:424-433PubMedCrossRefGoogle Scholar
  35. Palacios G, Lowenstine LJ, Cranfield MR, Gilardi KV, Spelman L, Lukasik-Braum M, Kinani JF, Mudakikwa A, Nyirakaragire E, Bussetti AV, Savji N, Hutchison S, Egholm M, Lipkin WI (2011) Human metapneumovirus infection in wild mountain gorillas, Rwanda. Emerging Infectious Diseases 17.4:711PubMedCrossRefGoogle Scholar
  36. Pusch D, Oh DY, Wolf S, Dumke R, Schröter-Bobsin U, Höhne M, Röske I, Schreier E (2005) Detection of enteric viruses and bacterial indicators in German environmental waters. Archives of Virology 150: 929-947PubMedCrossRefGoogle Scholar
  37. Pusey AE, Pintea L, Wilson ML, Kamenya S, Goodall J (2007) The contribution of long‐term research at Gombe National Park to chimpanzee conservation. Conservation Biology 21.3:623-634PubMedCrossRefGoogle Scholar
  38. Radonovich Jr LJ, Cheng J, Shenal BV, Hodgson M, Bender BS (2009) Respirator tolerance in health care workers. Journal of the American Medical Association 301:36–38PubMedCrossRefGoogle Scholar
  39. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. Available from
  40. Reiche J, Schweiger B (2009) Genetic variability of group A human respiratory syncytial virus strains circulating in Germany from 1998 to 2007. Journal of Clinical Microbiology 47:1800–1810PubMedPubMedCentralCrossRefGoogle Scholar
  41. Reiche J, Jacobsen S, Neubauer K, Hafemann S, Nitsche A, Milde J, Wolff T, Schweiger B (2014) Human Metapneumovirus: insights from a ten-year molecular and epidemiological analysis in Germany. PloS One 9.2Google Scholar
  42. Sadeuh-Mba SA, Bessaud M, Joffret ML, Endegue Zanga MC, Balanant J, Mpoudi Ngole E, Njouom R, Reynes JM, Delpeyroux F, Rousset D (2014) Characterization of Enteroviruses from Non-Human Primates in Cameroon Revealed Virus Types Widespread in Humans along with Candidate New Types and Species. PLoS Neglected Tropical Diseases 8(7):e3052. doi: 10.1371/journal.pntd.0003052 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Schulze M, Nitsche A, Schweiger B, Biere B (2010) Diagnostic approach for the differentiation of the pandemic influenza A (H1N1) v virus from recent human influenza viruses by real-time PCR. PloS one 5.4:e9966PubMedPubMedCentralCrossRefGoogle Scholar
  44. Sato M, Saito R, Sakai T, Sano Y, Nishikawa M, Sasaki A, Sano Y, Nishikawa M, Sasaki A, Shobugawa Y, Gejyo F, Suzuki H (2005) Molecular epidemiology of respiratory syncytial virus infections among children with acute respiratory symptoms in a community over three seasons. Journal of Clinical Microbiology 43:36–40PubMedPubMedCentralCrossRefGoogle Scholar
  45. Slater OM, Terio KA, Zhang Y, Erdman DD, Schneider E, Kuypers, JM, Wolinsky SM, Kunstman KJ, Kunstman J, Kinsel MJ, Gamble KC (2014) Human Metapneumovirus Infection in Chimpanzees, United States. Emerging Infectious Diseases 20.12:2115PubMedCrossRefGoogle Scholar
  46. Szentiks CA, Köndgen S, Silinski S, Speck S, Leendertz FH (2009) Lethal pneumonia in a captive juvenile chimpanzee (Pan troglodytes) due to human‐transmitted human respiratory syncytial virus (HRSV) and infection with Streptococcus pneumoniae. Journal of Medical Primatology 38.4:236-240PubMedCrossRefGoogle Scholar
  47. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56:564-577PubMedCrossRefGoogle Scholar
  48. Tong S, Chern SWW, Li Y, Pallansch MA, Anderson LJ (2008) Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. Journal of Clinical Microbiology 46.8:2652-2658PubMedPubMedCentralCrossRefGoogle Scholar
  49. Unwin S, Chatterton J, Chantrey J (2013) Management of severe respiratory tract disease caused by human respiratory syncytial virus and Streptococcus pneumoniae in captive chimpanzees (Pan troglodytes). Journal of Zoo and Wildlife Medicine 44.1:105-115PubMedCrossRefGoogle Scholar
  50. Weber MW, Mulholland EK, Greenwood BM (1998) Respiratory syncytial virus infection in tropical and developing countries. Tropical Medicine & International Health 3:268–280CrossRefGoogle Scholar
  51. Wevers D, Leendertz FH, Scuda N, Boesch C, Robbins MM, Head J, Ludwig C, Kühn J, Ehlers B (2010) A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla). Virology Journal 7.1:303PubMedPubMedCentralCrossRefGoogle Scholar
  52. Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C, Cameron K, Couacy-Hymann E, Cranfield M, Gray M, Harris LA, Head J, Jeffery K, Knauf S, Lankester F, Leendertz SAJ, Lonsdorf E, Mugisha L, Nitsche A, Reed P, Robbins M, Travis DA, Zommers Z, Fabian H. Leendertz Ehlers B (2011) Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. Journal of Virology 85.20:10774-10784PubMedPubMedCentralCrossRefGoogle Scholar
  53. Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36.02:153-160CrossRefGoogle Scholar
  54. Zhang Y, Cui W, Liu L, Wang J, Zhao H, Liao Y, Na R, Dong C, Wang L, Xie Z, Gao J, Cui P, Zhang X, Li Q (2011) Pathogenesis study of enterovirus 71 infection in rhesus monkeys. Laboratory Investigation 91.9:1337-1350PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2016

Authors and Affiliations

  • Kim S. Grützmacher
    • 1
  • Sophie Köndgen
    • 1
  • Verena Keil
    • 1
  • Angelique Todd
    • 3
  • Anna Feistner
    • 3
  • Ilka Herbinger
    • 2
  • Klara Petrzelkova
    • 4
    • 5
  • Terrence Fuh
    • 3
  • Siv Aina Leendertz
    • 1
  • Sébastien Calvignac-Spencer
    • 1
  • Fabian H. Leendertz
    • 1
    Email author
  1. 1.Project group Epidemiology of Highly Pathogenic MicroorganismsRobert Koch-InstituteBerlinGermany
  2. 2.World Wildlife Fund (WWF) GermanyBerlinGermany
  3. 3.World Wildlife Fund (WWF)BayangaCentral African Republic
  4. 4.Institute of Vertebrate BiologyAcademy of SciencesBrnoCzech Republic
  5. 5.Biology Centre, Institute of ParasitologyAcademy of Sciences of the Czech RepublicCeske BudejoviceCzech Republic

Personalised recommendations