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Adenovirus in Rural Côte D`Ivoire: High Diversity and Cross-Species Detection

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Abstract

The Taï region in Western Côte d`Ivoire is characterized by extensive overlap of human and animal habitats. This could influence patterns of adenovirus transmission between humans and domestic animals. Fecal samples from humans and various domestic animals were tested for the presence of adenoviruses by PCR. Phylogenetic and species delineation analyses were performed to further characterize the adenoviruses circulating in the region and to identify potential cross-species transmission events. Among domestic animals, adenovirus shedding was frequent (21.6% of domestic mammals and 41.5% of chickens) and the detected strains were highly diverse, several of them representing novel types. Although no evidence for zoonotic transmission of animal adenovirus was obtained, the present study provides concordant evidence in favor of common cross-species transmission of adenoviruses between different animal species and first indications for adenovirus transmission from humans to animals. These findings underline the thus far underestimated importance of reverse zoonotic transmission of viruses and of the role of domestic animals as pathogen reservoirs, “bridge species,” or intermediate hosts.

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References

  • Barbezange C, Benko M, Dán Á, and Harrach B (2000). DNA sequencing and phylogenetic analysis of the protease gene of ovine adenovirus 3 suggest that adenoviruses of sheep belong to two different genera. Virus Research 66:79-85.

    Article  CAS  PubMed  Google Scholar 

  • Belák, and Pálfi (1974). An adenovirus isolated from sheep and its relationship to type 2 bovine adenovirus. Archiv für die gesamte Virusforschung 46:366-369.

    Article  PubMed  Google Scholar 

  • Benkö M, and Harrach B (2003). Molecular evolution of adenoviruses. Current Topics in Microbiology and Immunology 272:3-35.

    PubMed  Google Scholar 

  • Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, et al. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS computational biology 10:e1003537.

    Article  PubMed Central  PubMed  Google Scholar 

  • Brister JR, Chodosh J, Curiel DT, Heim A, Jones MS, Kajon A, et al. (2009) Human adenovirus genotype classification. Available: http://hadvwg.gmu.edu/. Accessed on June 15, 2014.

  • Castresana J (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular biology and evolution 17:540-552.

    Article  CAS  PubMed  Google Scholar 

  • Chan EH, Brewer TF, Madoff LC, Pollack MP, Sonricker AL, Keller M, et al. (2010). Global capacity for emerging infectious disease detection. Proceedings of the National Academy of Sciences of the United States of America 107:21701-21706.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen EC, Yagi S, Kelly KR, Mendoza SP, Tarara RP, Canfield DR, et al. (2011). Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a new world monkey colony. PLoS pathogens 7:e1002155.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chiu CY, Yagi S, Lu X, Yu G, Chen EC, Liu M, et al. (2013). A novel adenovirus species associated with an acute respiratory outbreak in a baboon colony and evidence of coincident human infection. MBio 4:e00084.

    Article  PubMed Central  PubMed  Google Scholar 

  • Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, Lam SK, et al. (2000). Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432-1435.

    Article  CAS  PubMed  Google Scholar 

  • Cleaveland S, Laurenson MK, and Taylor LH (2001). Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society B: Biological Sciences 356:991-999.

    Article  CAS  Google Scholar 

  • Cleaveland S, Meslin FX, and Breiman R (2006). Dogs can play useful role as sentinel hosts for disease. Nature 440:605.

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, and Posada D (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature methods 9:772.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Daszak P, Cunningham AA, and Hyatt AD (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287:443-449.

    Article  CAS  PubMed  Google Scholar 

  • Davison AJ, Benkö M, and Harrach B (2003). Genetic content and evolution of adenoviruses. J Gen Virol 84:2895-2908.

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, and Rambaut A (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular biology and evolution 29:1969-1973.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duffy G, and Moriarty EM (2003). Cryptosporidium and its potential as a food-borne pathogen. Animal health research reviews 4:95-107.

    Article  PubMed  Google Scholar 

  • Echavarria M (2008). Adenoviruses in immunocompromised hosts. Clinical Microbiology Reviews 21:704-715.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fujisawa T, and Barraclough TG (2013). Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic biology 62:707-724.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gouy M, Guindon S, and Gascuel O (2010). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular biology and evolution 27:221-224.

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, and Gascuel O (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology 52:696-704.

    Article  PubMed  Google Scholar 

  • Halliday J, Daborn C, Auty H, Mtema Z, Lembo T, Bronsvoort BM, et al. (2012). Bringing together emerging and endemic zoonoses surveillance: shared challenges and a common solution. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 367:2872-2880.

    Article  PubMed Central  PubMed  Google Scholar 

  • Harrach B, Benkö M, Both GW, Brown M, Davison AJ, Echavarría M, et al. (2011). Virus Taxonomy. Elsevier, Oxford.

    Google Scholar 

  • Harrach B, Turnell AS, Leppard KN, and Benkö M (2008). Adenoviruses. in Encyclopedia of Virology B. W. J. Mahy and M. H. V. van Regenmortel, editors. Academic Press, London, Pp 1-24.

    Chapter  Google Scholar 

  • Horwitz M., Wold W. (2007) Adenoviruses. in Fields Virology. Knipe D. M. and P. M. Howley, editors. Lippincott William Wilkins, Philadelphia. pp. 2395-2436.

    Google Scholar 

  • Intisar KS, Ali YH, Khalafalla AI, Taha KM, and Rahman MEA (2010). Adenovirus type 3 infections in camels in Sudan. African Journal of Microbiology Research Vol. 4:1356-1358.

    Google Scholar 

  • Jones BA, Grace D, Kock R, Alonso S, Rushton J, Said MY, et al. (2013). Zoonosis emergence linked to agricultural intensification and environmental change. Proceedings of the National Academy of Sciences of the United States of America 110:8399-8404.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. (2008). Global trends in emerging infectious diseases. Nature 451:990-993.

    Article  CAS  PubMed  Google Scholar 

  • Kajan GL, Kecskemeti S, Harrach B, and Benko M (2013). Molecular typing of fowl adenoviruses, isolated in Hungary recently, reveals high diversity. Veterinary Microbiology 167:357-363.

    Article  CAS  PubMed  Google Scholar 

  • Kojaoghlanian T, Flomenberg P, and Horwitz MS (2003). The impact of adenovirus infection on the immunocompromised host. Reviews in Medical Virology 13:155-171.

    Article  PubMed  Google Scholar 

  • Lehmkuhl HD, and Hobbs LA (2008). Serologic and hexon phylogenetic analysis of ruminant adenoviruses. Archives of virology 153:891-897.

    Article  CAS  PubMed  Google Scholar 

  • Lim TH, Lee HJ, Lee DH, Lee YN, Park JK, Youn HN, et al. (2011). Identification and virulence characterization of fowl adenoviruses in Korea. Avian diseases 55:554-560.

    Article  PubMed  Google Scholar 

  • Marek A, Gunes A, Schulz E, and Hess M (2010). Classification of fowl adenoviruses by use of phylogenetic analysis and high-resolution melting-curve analysis of the hexon L1 gene region. Journal of virological methods 170:147-154.

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Lemey P, Lott M, Moulton V, Posada D, and Lefeuvre P (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462-2463.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin DP, Williamson C, and Posada D (2005). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260-262.

    Article  CAS  PubMed  Google Scholar 

  • Mase M, Chuujou M, Inoue T, Nakamura K, Yamaguchi S, and Imada T (2009). Genetic characterization of fowl adenoviruses isolated from chickens with hydropericardium syndrome in Japan. The Journal of veterinary medical science 71:1455-1458.

    Article  CAS  PubMed  Google Scholar 

  • Messenger AM, Barnes AN, and Gray GC (2014). Reverse zoonotic disease transmission (zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLoS One 9:e89055.

    Article  PubMed Central  PubMed  Google Scholar 

  • Meulemans G, Boschmans M, Berg TP, and Decaesstecker M (2001). Polymerase chain reaction combined with restriction enzyme analysis for detection and differentiation of fowl adenoviruses. Avian Pathology 30:655-660.

    Article  CAS  PubMed  Google Scholar 

  • Ojkic D, Martin E, Swinton J, Vaillancourt JP, Boulianne M, and Gomis S (2008). Genotyping of Canadian isolates of fowl adenoviruses. Avian Pathology 37:95-100.

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Hoppe E, Mugisha L, Petrzelkova K, Akoua-Koffi C, Couacy-Hymann E, et al. (2014). High prevalence and diversity of species D adenoviruses (HAdV-D) in human populations of four Sub-Saharan countries. Virology Journal 11:25.

    Article  PubMed Central  PubMed  Google Scholar 

  • Pearce-Duvet JM (2006). The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease. Biological reviews of the Cambridge Philosophical Society 81:369-382.

    Article  PubMed  Google Scholar 

  • Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, et al. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic biology 55:595-609.

    Article  PubMed  Google Scholar 

  • R-Core-Team (2014). A Language and Environment for Statistical Computing. R F S Computing, Vienna.

    Google Scholar 

  • Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RA, et al. (2006). Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. The American Journal of Pathology 168:176-183.

    Article  PubMed Central  PubMed  Google Scholar 

  • Robinson CM, Zhou X, Rajaiya J, Yousuf MA, Singh G, DeSerres JJ, et al. (2013). Predicting the next eye pathogen: analysis of a novel adenovirus. MBio 4:e00595-00612.

    Article  PubMed Central  PubMed  Google Scholar 

  • Roy S, Sandhu A, Medina A, Clawson DS, and Wilson JM (2012). Adenoviruses in fecal samples from asymptomatic rhesus macaques, United States. Emerging infectious diseases 18:1081-1088.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sibley SD, Goldberg TL, and Pedersen JA (2011). Detection of known and novel adenoviruses in cattle wastes via broad-spectrum primers. Applied and environmental microbiology 77:5001-5008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steer PA, Kirkpatrick NC, O’Rourke D, and Noormohammadi AH (2009). Classification of fowl adenovirus serotypes by use of high-resolution melting-curve analysis of the hexon gene region. Journal of clinical microbiology 47:311-321.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Talavera G, and Castresana J (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic biology 56:564-577.

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, and Gibson TJ (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids research 22:4673-4680.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vestheim H, and Jarman SN (2008). Blocking primers to enhance PCR amplification of rare sequences in mixed samples - a case study on prey DNA in Antarctic krill stomachs. Frontiers in zoology 5:12.

    Article  PubMed Central  PubMed  Google Scholar 

  • Walsh MP, Seto J, Jones MS, Chodosh J, Xu W, and Seto D (2010). Computational analysis identifies human adenovirus type 55 as a re-emergent acute respiratory disease pathogen. Journal of clinical microbiology 48:991-993.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C, Cameron K, et al. (2011). Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. Journal of virology 85:10774-10784.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wood JL, Leach M, Waldman L, Macgregor H, Fooks AR, Jones KE, et al. (2012). A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 367:2881-2892.

    Article  PubMed Central  PubMed  Google Scholar 

  • Yu G, Yagi S, Carrion R, Jr., Chen EC, Liu M, Brasky KM, et al. (2013). Experimental cross-species infection of common marmosets by titi monkey adenovirus. PLoS One 8:e68558.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank all the people who volunteered to participate in this study as study participant or by providing the animals for sample collection. Special thanks go also to the sampling team during the field missions (among others Bozua, Ange Hermann Gnoukpoho, Eric Goueu, Joel Semporé and Dan Driscoll). Moreover, we are grateful to Sonja Liebmann, Ulla Thiesen, and Nezlisah Yasmum for their support and assistance. We also thank the national and local health authorities in Côte d’Ivoire, as well as the according ethics commission for granting permission for this work. This work was partly supported by the “Deutsche Forschungsgemeinschaft” (DFG) Grant LE1813/4-1.

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Authors and Affiliations

  1. Project Group “Epidemiology of highly pathogenic microorganisms”, Robert Koch Institute, Nordufer 20, 13353, Berlin, Germany

    Maude Pauly, Grit Schubert, Sabrina Weiss, Sébastien Calvignac-Spencer, Siv Aina Leendertz & Fabian H. Leendertz

  2. Division 12 “Measles, Mumps, Rubella and Viruses affecting immunocompromised patients”, Robert Koch Institute, Seestr. 10, 13353, Berlin, Germany

    Maude Pauly, Nanina Buchwald & Bernhard Ehlers

  3. Department of Immunology, Luxembourg Institute of Health, 20A Rue Auguste Lumière, 1950, Luxembourg, Luxembourg

    Maude Pauly

  4. Centre de Recherche pour le Développement, Université Alassane Ouattara of Bouake, BP V18, Bouake 01, Côte d’Ivoire

    Chantal Akoua-Koffi, Augustin Etile Anoh & Arsène Mossoun

  5. Laboratoire National d`Aide au Développement Agricole/Laboratoire Central de Pathologie Animale, 206, Bingerville, Côte d’Ivoire

    Emmanuel Couacy-Hymann, Augustin Etile Anoh & Arsène Mossoun

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  1. Maude Pauly
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  2. Chantal Akoua-Koffi
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Correspondence to Fabian H. Leendertz or Bernhard Ehlers.

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Pauly, M., Akoua-Koffi, C., Buchwald, N. et al. Adenovirus in Rural Côte D`Ivoire: High Diversity and Cross-Species Detection. EcoHealth 12, 441–452 (2015). https://doi.org/10.1007/s10393-015-1032-5

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  • DOI: https://doi.org/10.1007/s10393-015-1032-5

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