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Volume 23, Number 12—December 2017
Synopsis

Fatal Outbreak in Tonkean Macaques Caused by Possibly Novel Orthopoxvirus, Italy, January 20151

Giusy Cardeti2Comments to Author , Cesare Ernesto Maria Gruber2, Claudia Eleni, Fabrizio Carletti, Concetta Castilletti, Giuseppe Manna, Francesca Rosone, Emanuela Giombini, Marina Selleri, Daniele Lapa, Vincenzo Puro, Antonino Di Caro, Raniero Lorenzetti, Maria Teresa Scicluna, Goffredo Grifoni, Annapaola Rizzoli, Valentina Tagliapietra, Lorenzo De Marco, Maria Rosaria Capobianchi, and Gian Luca Autorino
Author affiliations: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Rome, Italy (G. Cardeti, C. Eleni, G. Manna, F. Rosone, R. Lorenzetti, M.T. Scicluna, G. Grifoni, G.L. Autorino); L, Spallanzani National Institute of Infectious Diseases, Rome (C.E.M. Gruber, F. Carletti, C. Castilletti, E. Giombini, M. Selleri, D. Lapa, V. Puro, A. Di Caro, M.R. Capobianchi); Fondazione Edmund Mach di San Michele all’Adige, Trento, Italy (A. Rizzoli, V. Tagliapietra); Parco Faunistico Piano dell'Abatino, Poggio San Lorenzo, Italy (L. De Marco)

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Figure 6

Phylogenetic analysis of OPV Abatino obtained from skin lesion of Tonkean macaque during outbreak at animal sanctuary, Italy, January 2015. Nine conserved genes (GenBank accession nos. KY100107–KY100115) obtained with next-generation sequencing were concatenated and aligned with the homologous concatenated sequences from representative OPV strains (GenBank accession no.): TATV-Dahomey-1968 (DQ437594.1), VARV-Bangladesh-1975 (L22579.1), CMLV-M96 (AF438165.1), CPXV-HumAac09–1 (KC813508.1), CPXV-Ge

Figure 6. Phylogenetic analysis of OPV Abatino obtained from skin lesion of Tonkean macaque during outbreak at animal sanctuary, Italy, January 2015. Nine conserved genes (GenBank accession nos. KY100107–KY100115) obtained with next-generation sequencing were concatenated and aligned with the homologous concatenated sequences from representative OPV strains (GenBank accession no.): TATV-Dahomey-1968 (DQ437594.1), VARV-Bangladesh-1975 (L22579.1), CMLV-M96 (AF438165.1), CPXV-HumAac09–1 (KC813508.1), CPXV-Germany2002-MKY (HQ420898.1), CPXV-Germany1998–2 (HQ420897.1), CPXV-MarLei07–1 (KC813499.1), MPXV-Congo2003–358 (DQ011154.1), CPXV-Finland2000 (HQ420893.1), VACV-Lister (KX061501.1), ECTV-Moscow (AF012825.2), OPV GCP2013 Akhmeta (KM046934–42), and OPV Tena Dona AK2015 (KX914668–76). New World strain RACV-MD19 (GenBank accession no. FJ807746–54) was added to the analysis as an outgroup. We generated multiple alignments with MUSCLE version 3.8.31 (30) and built the phylogenetic tree by using the Bayesian Markov chain Monte Carlo model with MRBAYES version 3.2.5 (31) using the general time-reversible plus gamma model with 1 million generations, retaining a minimum of 10,000 posterior probabilities, and maximum-likelihood model RaxML version 8.1.24 (32) using the general time-reversible plus gamma with 1,000 pseudoreplicates. Numbers represent the reliability of the nodes with the minimum probability of 75% and minimum bootstrap value of 75. Scale bar indicates nucleotide substitutions per site. CMLV, camelpox virus; CPXV, cowpox virus; ECTV, ectromelia virus; MPXV, monkeypox virus; OPV, orthopoxvirus; RACV, raccoonpox virus; TATV, taterapox virus; VACV, vaccinia virus; VARV, variola virus.

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References
  1. McFadden  G. Poxvirus tropism. Nat Rev Microbiol. 2005;3:201–13. DOIPubMedGoogle Scholar
  2. Fenner  F. Mousepox (infectious ectromelia): past, present, and future. Lab Anim Sci. 1981;31:553–9.PubMedGoogle Scholar
  3. Esteban  DJ, Buller  RM. Ectromelia virus: the causative agent of mousepox. J Gen Virol. 2005;86:2645–59. DOIPubMedGoogle Scholar
  4. Hoffmann  D, Franke  A, Jenckel  M, Tamošiūnaitė  A, Schluckebier  J, Granzow  H, et al. Out of the reservoir: phenotypic and genotypic characterization of a novel cowpox virus isolated from a common vole. J Virol. 2015;89:10959–69. DOIPubMedGoogle Scholar
  5. Smithson  C, Tang  N, Sammons  S, Frace  M, Batra  D, Li  Y, et al. The genomes of three North American orthopoxviruses. Virus Genes. 2017;53:21–34. DOIPubMedGoogle Scholar
  6. Carroll  DS, Emerson  GL, Li  Y, Sammons  S, Olson  V, Frace  M, et al. Chasing Jenner’s vaccine: revisiting cowpox virus classification. PLoS One. 2011;6:e23086. DOIPubMedGoogle Scholar
  7. Dabrowski  PW, Radonić  A, Kurth  A, Nitsche  A. Genome-wide comparison of cowpox viruses reveals a new clade related to Variola virus. PLoS One. 2013;8:e79953. DOIPubMedGoogle Scholar
  8. Vora  NM, Li  Y, Geleishvili  M, Emerson  GL, Khmaladze  E, Maghlakelidze  G, et al. Human infection with a zoonotic orthopoxvirus in the country of Georgia. N Engl J Med. 2015;372:1223–30. DOIPubMedGoogle Scholar
  9. Springer  YP, Hsu  CH, Werle  ZR, Olson  LE, Cooper  MP, Castrodale  LJ, et al. Novel orthopoxvirus infection in an Alaska resident. Clin Infect Dis. 2017;64:1737–41. DOIPubMedGoogle Scholar
  10. Chantrey  J, Meyer  H, Baxby  D, Begon  M, Bown  KJ, Hazel  SM, et al. Cowpox: reservoir hosts and geographic range. Epidemiol Infect. 1999;122:455–60. DOIPubMedGoogle Scholar
  11. Kurth  A, Wibbelt  G, Gerber  HP, Petschaelis  A, Pauli  G, Nitsche  A. Rat-to-elephant-to-human transmission of cowpox virus. Emerg Infect Dis. 2008;14:670–1. DOIPubMedGoogle Scholar
  12. Schmiedeknecht  G, Eickmann  M, Köhler  K, Herden  CE, Kolesnikova  L, Förster  C, et al. Fatal cowpox virus infection in captive banded mongooses (Mungos mungo). Vet Pathol. 2010;47:547–52. DOIPubMedGoogle Scholar
  13. Martina  BEE, van Doornum  G, Dorrestein  GM, Niesters  HGM, Stittelaar  KJ, Wolters  MABI, et al. Cowpox virus transmission from rats to monkeys, the Netherlands. Emerg Infect Dis. 2006;12:1005–7. DOIPubMedGoogle Scholar
  14. Kalthoff  D, Bock  WI, Hühn  F, Beer  M, Hoffmann  B. Fatal cowpox virus infection in cotton-top tamarins (Saguinus oedipus) in Germany. Vector Borne Zoonotic Dis. 2014;14:303–5. DOIPubMedGoogle Scholar
  15. Kurth  A, Straube  M, Kuczka  A, Dunsche  AJ, Meyer  H, Nitsche  A. Cowpox virus outbreak in banded mongooses (Mungos mungo) and jaguarundis (Herpailurus yagouaroundi) with a time-delayed infection to humans. PLoS One. 2009;4:e6883. DOIPubMedGoogle Scholar
  16. Mätz-Rensing  K, Ellerbrok  H, Ehlers  B, Pauli  G, Floto  A, Alex  M, et al. Fatal poxvirus outbreak in a colony of New World monkeys. Vet Pathol. 2006;43:212–8. DOIPubMedGoogle Scholar
  17. Girling  SJ, Pizzi  R, Cox  A, Beard  PM. Fatal cowpox virus infection in two squirrel monkeys (Saimiri sciureus). Vet Rec. 2011;169:156. DOIPubMedGoogle Scholar
  18. iNaturalist.org. Tonkean macaque. (Macaca tonkeana) [cited 2017 May 5]. http://www.inaturalist.org/taxa/43453-Macaca-tonkeana
  19. Scagliarini  A, Casà  G, Trentin  B, Gallina  L, Savini  F, Morent  M, et al. Evidence of zoonotic Poxviridae coinfections in clinically diagnosed papillomas using a newly developed mini-array test. J Vet Diagn Invest. 2016;28:59–64. DOIPubMedGoogle Scholar
  20. Cardeti  G, Brozzi  A, Eleni  C, Polici  N, D’Alterio  G, Carletti  F, et al. Cowpox virus in llama, Italy. Emerg Infect Dis. 2011;17:1513–5. DOIPubMedGoogle Scholar
  21. Carletti  F, Bordi  L, Castilletti  C, Di Caro  A, Falasca  L, Gioia  C, et al. Cat-to-human orthopoxvirus transmission, northeastern Italy. Emerg Infect Dis. 2009;15:499–500. DOIPubMedGoogle Scholar
  22. Biel  SS, Gelderblom  HR. Electron microscopy of viruses. In: Cann AJ, editor. Virus culture—a practical approach. New York: Oxford University Press; 1999. p. 11–47.
  23. Carletti  F, Di Caro  A, Calcaterra  S, Grolla  A, Czub  M, Ippolito  G, et al. Rapid, differential diagnosis of orthopox- and herpesviruses based upon real-time PCR product melting temperature and restriction enzyme analysis of amplicons. J Virol Methods. 2005;129:97–100. DOIPubMedGoogle Scholar
  24. Darling  AE, Mau  B, Perna  NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5:e11147. DOIPubMedGoogle Scholar
  25. Tagliapietra  V, Rosà  R, Hauffe  HC, Laakkonen  J, Voutilainen  L, Vapalahti  O, et al. Spatial and temporal dynamics of lymphocytic choriomeningitis virus in wild rodents, northern Italy. Emerg Infect Dis. 2009;15:1019–25. DOIPubMedGoogle Scholar
  26. Meyer  H, Ropp  SL, Esposito  JJ. Gene for A-type inclusion body protein is useful for a polymerase chain reaction assay to differentiate orthopoxviruses. J Virol Methods. 1997;64:217–21. DOIPubMedGoogle Scholar
  27. Ryabinin  VA, Shundrin  LA, Kostina  EB, Laassri  M, Chizhikov  V, Shchelkunov  SN, et al. Microarray assay for detection and discrimination of Orthopoxvirus species. J Med Virol. 2006;78:1325–40. DOIPubMedGoogle Scholar
  28. Emerson  GL, Li  Y, Frace  MA, Olsen-Rasmussen  MA, Khristova  ML, Govil  D, et al. The phylogenetics and ecology of the orthopoxviruses endemic to North America. PLoS One. 2009;4:e7666. DOIPubMedGoogle Scholar
  29. Lakis  NS, Li  Y, Abraham  JL, Upton  C, Blair  DC, Smith  S, et al. Novel poxvirus infection in an immune suppressed patient. Clin Infect Dis. 2015;61:1543–8. DOIPubMedGoogle Scholar
  30. Edgar  RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7. DOIPubMedGoogle Scholar
  31. Huelsenbeck  JP, Ronquist  F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–5. DOIPubMedGoogle Scholar
  32. Stamatakis  A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3. DOIPubMedGoogle Scholar
  33. Product leaflet for IMVANEX. Annex I. Summary of product characteristics. Kvistgaard, Denmark: Bavarian Nordic A/S; 2013 [cited Sep 2016]. http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Product_Information/human/002596/WC500147896.pdf
  34. Silva-Fernandes  AT, Travassos  CE, Ferreira  JM, Abrahão  JS, Rocha  ES, Viana-Ferreira  F, et al. Natural human infections with Vaccinia virus during bovine vaccinia outbreaks. J Clin Virol. 2009;44:308–13. DOIPubMedGoogle Scholar

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1Preliminary results from this study were presented at the Xth International Congress of the European Society for Veterinary Virology; August 31–September 3, 2015; Montpellier, France.

2These first authors were co–principal investigators who contributed equally to this article.

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