Codetection of Respiratory Syncytial Virus in Habituated Wild Western Lowland Gorillas and Humans During a Respiratory Disease Outbreak
Language English Country United States Media print-electronic
Document type Journal Article
PubMed
27436109
PubMed Central
PMC7088376
DOI
10.1007/s10393-016-1144-6
PII: 10.1007/s10393-016-1144-6
Knihovny.cz E-resources
- Keywords
- enterovirus, great apes, noninvasive detection, respiratory disease, respiratory syncytial virus, western lowland gorillas,
- MeSH
- Disease Outbreaks * MeSH
- Phylogeny MeSH
- Gorilla gorilla virology MeSH
- Respiratory Syncytial Virus Infections epidemiology veterinary MeSH
- Humans MeSH
- Respiratory Tract Diseases MeSH
- Respiratory Syncytial Viruses * MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
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.
Institute of Vertebrate Biology Academy of Sciences Brno 60365 Czech Republic
World Wildlife Fund Dzanga Sangha Protected Areas Bayanga Central African Republic
See more in PubMed
Bennett BT, Abee CR, Henrickson R. Nonhuman primates in biomedical research: diseases. Cambridge: Academic Press; 1998.
Buitendijk H, Fagrouch Z, Niphuis H, Bogers WM, Warren KS, Verschoor EJ. Retrospective serology study of respiratory virus infections in captive great apes. Viruses. 2014;6(3):1442–1453. doi: 10.3390/v6031442. PubMed DOI PMC
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 rsbl20110155 PubMed PMC
Chi F, Leider M, Leendertz F, Bergmann C, Boesch C, Schenk S, Pauli G, Ellerbrok H, Hakenbeck R. New Streptococcus pneumoniae clones in deceased wild chimpanzees. Journal of Bacteriology. 2007;189:6085–6088. doi: 10.1128/JB.00468-07. PubMed DOI PMC
Chmielewicz B, Nitsche A, Schweiger B, Ellerbrok H. Development of a PCR-based assay for detection, quantification, and genotyping of human adenoviruses. Clinical Chemistry. 2005;51:1365–1373. doi: 10.1373/clinchem.2004.045088. PubMed DOI
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods. 2012;9(8):772. doi: 10.1038/nmeth.2109. PubMed DOI PMC
Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004;32(5):1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Gilardi KV, Gillespie TR, Leendertz FH, Macfie EJ, Travis DA, Whittier CA, Williamson EA. Best Practice Guidelines for Health Monitoring and Disease Control in Great Ape Populations. Gland: IUCN SSC Primate Specialist Group; 2015. p. 56.
Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution. 2010;27(2):221–224. doi: 10.1093/molbev/msp259. PubMed DOI
Guindon S, Gascuel O. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology. 2003;52:696–704. doi: 10.1080/10635150390235520. PubMed DOI
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Systematic Biology. 2010;59(3):307–321. doi: 10.1093/sysbio/syq010. PubMed DOI
Gruen L, Fultz A, Pruetz J. Ethical issues in African great ape field studies. Institute for Laboratory Animal Research Journal. 2013;54(1):24–32. doi: 10.1093/ilar/ilt016. PubMed DOI
Harvala H, Sharp CP, Ngole EM, Delaporte E, Peeters M, Simmonds P. Detection and genetic characterization of enteroviruses circulating among wild populations of chimpanzees in Cameroon: relationship with human and simian enteroviruses. Journal of Virology. 2011;85(9):4480–4486. doi: 10.1128/JVI.02285-10. PubMed DOI PMC
Harvala H, Van Nguyen D, McIntyre C, Ahuka-Mundeke S, Ngole EM, Delaporte E, Peeters M, Simmonds P. Co-circulation of enteroviruses between apes and humans. Journal of General Virology. 2014;95(2):403–407. doi: 10.1099/vir.0.059048-0. PubMed DOI PMC
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, msv090 PubMed PMC
Jang YJ, Lee SH, Kwon HJ, Chung YS, Lee BJ. Development of rhinovirus study model using organ culture of turbinate mucosa. Journal of Virological Methods. 2005;125:41–47. doi: 10.1016/j.jviromet.2004.12.004. PubMed DOI PMC
Johnson DF, Druce JD, Birch C, Grayson ML. A quantitative assessment of the efficacy of surgical and N95 masks to filter influenza virus in patients with acute influenza infection. Clinical Infectious Diseases. 2009;49:275–277. doi: 10.1086/600041. PubMed DOI
Kalter SS, Heberling RL, Cooke AW, Barry JD, Tian PY, Northam WJ. Viral infections of nonhuman primates. Comparative Medicine. 1997;47(5):461–467. PubMed
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. 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. 2008;70:755–765. doi: 10.1002/ajp.20565. PubMed DOI PMC
Kelly ME, Soike K, Ahmed K, Iatropoulos MJ. Coxsackievirus in an infant chimpanzee. Journal of Medical Primatology. 1977;7(2):119–121. PubMed
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. Pandemic human viruses cause decline of endangered great apes. Current Biology. 2008;18:1–5. doi: 10.1016/j.cub.2008.01.012. PubMed DOI
Köndgen S, Schenk S, Pauli G, Boesch C, Leendertz FH. Noninvasive monitoring of respiratory viruses in wild chimpanzees. Ecohealth. 2010;7(3):332–341. doi: 10.1007/s10393-010-0340-z. PubMed DOI
Köndgen S, Leider M, Lankester F, Bethe A, Lübke-Becker A, Leendertz FH, Ewers C. Pasteurella multocida involved in respiratory disease of wild chimpanzees. PloS one. 2011;6(9):e24236–e24236. doi: 10.1371/journal.pone.0024236. PubMed DOI PMC
Kooriyama T, Okamoto M, Yoshida T, Nishida T, Tsubota T, Saito A, Tomonaga M, Matsuzawa T, Akari H, Nishimura H, Miyabe-Nishiwaki T. Epidemiological study of zoonoses derived from humans in captive chimpanzees. Primates. 2013;54(1):89–98. doi: 10.1007/s10329-012-0320-8. PubMed DOI PMC
Lonsdorf EV, Travis D, Pusey AE, Goodall J. Using retrospective health data from the Gombe chimpanzee study to inform future monitoring efforts. Journal of Medical Primatology. 2006;68:897–908. doi: 10.1002/ajp.20296. PubMed DOI
Macfie EJ and Williamson EA (2010) Best Practice Guidelines for Great Ape Tourism. Gland: IUCN/SSC Primate Specialist Group (PSG). 78 pp
Mackay IM, Bialasiewicz S, Waliuzzaman Z, Chidlow GR, Fegredo DC, Laingam S, Adamson P, Harnett GB, Rawlinson W, Nissen MD, Sloots TP. Use of the P gene to genotype human metapneumovirus identifies 4 viral subtypes. The Journal of Infectious Diseases. 2004;190:1913–1918. doi: 10.1086/425013. PubMed DOI
McAvin JC, Reilly PA, Roudabush RM, Barnes WJ, Salmen A, Jackson GW, Beninga KK, Astorga A, McCleskey FK, Huff WB, Niemeyer D, Lohman KL. Sensitive and specific method for rapid identification of Streptococcus pneumoniae using real-time fluorescence PCR. Journal of Clinical Microbiology. 2001;39:3446–3451. doi: 10.1128/JCM.39.10.3446-3451.2001. PubMed DOI PMC
Milton DK, Fabian MP, Cowling BJ, Grantham ML, McDevitt JJ. Influenza Virus Aerosols in Human Exhaled Breath: Particle Size, Culturability, and Effect of Surgical Masks. PLoS Pathogens. 2013;9(3):e1003205. doi: 10.1371/journal.ppat.1003205. PubMed DOI PMC
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. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. The Lancet. 2010;375(9725):1545–1555. doi: 10.1016/S0140-6736(10)60206-1. PubMed DOI PMC
Nielsen SCA, Mourier T, Baandrup U, Søland TM, Bertelsen MF, Gilbert MTP, Nielsen LP. Probable transmission of coxsackie B3 virus from human to chimpanzee. Denmark. Emerging Infectious Diseases. 2012;18(7):1163. doi: 10.3201/eid1807.111689. PubMed DOI PMC
Nunn CL, Thrall PH, Stewart K, Harcourt AH. Emerging infectious diseases and animal social systems. Evolutionary Ecology. 2008;22(4):519–543. doi: 10.1007/s10682-007-9180-x. DOI
Palacios G, Oberste MS. Enteroviruses as agents of emerging infectious diseases. Journal of Neurovirology. 2005;11(5):424–433. doi: 10.1080/13550280591002531. PubMed DOI
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. Human metapneumovirus infection in wild mountain gorillas. Rwanda. Emerging Infectious Diseases. 2011;17(4):711. doi: 10.3201/eid1704.100883. PubMed DOI PMC
Pusch D, Oh DY, Wolf S, Dumke R, Schröter-Bobsin U, Höhne M, Röske I, Schreier E. Detection of enteric viruses and bacterial indicators in German environmental waters. Archives of Virology. 2005;150:929–947. doi: 10.1007/s00705-004-0467-8. PubMed DOI
Pusey AE, Pintea L, Wilson ML, Kamenya S, Goodall J. The contribution of long-term research at Gombe National Park to chimpanzee conservation. Conservation Biology. 2007;21(3):623–634. doi: 10.1111/j.1523-1739.2007.00704.x. PubMed DOI
Radonovich LJ, Jr, Cheng J, Shenal BV, Hodgson M, Bender BS. Respirator tolerance in health care workers. Journal of the American Medical Association. 2009;301:36–38. doi: 10.1001/jama.2008.894. PubMed DOI
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer
Reiche J, Schweiger B. Genetic variability of group A human respiratory syncytial virus strains circulating in Germany from 1998 to 2007. Journal of Clinical Microbiology. 2009;47:1800–1810. doi: 10.1128/JCM.02286-08. PubMed DOI PMC
Reiche J, Jacobsen S, Neubauer K, Hafemann S, Nitsche A, Milde J, Wolff T, Schweiger B. Human Metapneumovirus: insights from a ten-year molecular and epidemiological analysis in Germany. PloS One. 2014;9:2. PubMed PMC
Sadeuh-Mba SA, Bessaud M, Joffret ML, Endegue Zanga MC, Balanant J, Mpoudi Ngole E, Njouom R, Reynes JM, Delpeyroux F, Rousset D. 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. 2014;8(7):e3052. doi: 10.1371/journal.pntd.0003052. PubMed DOI PMC
Schulze M, Nitsche A, Schweiger B, Biere B. Diagnostic approach for the differentiation of the pandemic influenza A (H1N1) v virus from recent human influenza viruses by real-time PCR. PloS one. 2010;5(4):e9966. doi: 10.1371/journal.pone.0009966. PubMed DOI PMC
Sato M, Saito R, Sakai T, Sano Y, Nishikawa M, Sasaki A, Sano Y, Nishikawa M, Sasaki A, Shobugawa Y, Gejyo F, Suzuki H. Molecular epidemiology of respiratory syncytial virus infections among children with acute respiratory symptoms in a community over three seasons. Journal of Clinical Microbiology. 2005;43:36–40. doi: 10.1128/JCM.43.1.36-40.2005. PubMed DOI PMC
Slater OM, Terio KA, Zhang Y, Erdman DD, Schneider E, Kuypers JM, Wolinsky SM, Kunstman KJ, Kunstman J, Kinsel MJ, Gamble KC. Human Metapneumovirus Infection in Chimpanzees. United States. Emerging Infectious Diseases. 2014;20(12):2115. doi: 10.3201/eid2012.140408. PubMed DOI PMC
Szentiks CA, Köndgen S, Silinski S, Speck S, Leendertz FH. 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. 2009;38(4):236–240. doi: 10.1111/j.1600-0684.2009.00346.x. PubMed DOI
Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology. 2007;56:564–577. doi: 10.1080/10635150701472164. PubMed DOI
Tong S, Chern SWW, Li Y, Pallansch MA, Anderson LJ. Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. Journal of Clinical Microbiology. 2008;46(8):2652–2658. doi: 10.1128/JCM.00192-08. PubMed DOI PMC
Unwin S, Chatterton J, Chantrey J. 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. 2013;44(1):105–115. doi: 10.1638/1042-7260-44.1.105. PubMed DOI
Weber MW, Mulholland EK, Greenwood BM. Respiratory syncytial virus infection in tropical and developing countries. Tropical Medicine & International Health. 1998;3:268–280. doi: 10.1046/j.1365-3156.1998.00213.x. PubMed DOI
Wevers D, Leendertz FH, Scuda N, Boesch C, Robbins MM, Head J, Ludwig C, Kühn J, Ehlers B. A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla) Virology Journal. 2010;7(1):303. doi: 10.1186/1743-422X-7-303. PubMed DOI PMC
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, Leendertz Fabian H, Ehlers B. Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. Journal of Virology. 2011;85(20):10774–10784. doi: 10.1128/JVI.00810-11. PubMed DOI PMC
Woodford MH, Butynski TM, Karesh WB. Habituating the great apes: the disease risks. Oryx. 2002;36(02):153–160. doi: 10.1017/S0030605302000224. DOI
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. Pathogenesis study of enterovirus 71 infection in rhesus monkeys. Laboratory Investigation. 2011;91(9):1337–1350. doi: 10.1038/labinvest.2011.82. PubMed DOI