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Evidence for zoonotic transmission of species A rotavirus from goat and cattle in nomadic herds in Morocco, 2012–2014

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Abstract

Species A rotaviruses (RVAs) are a leading cause of diarrhea in children and in the young of a large variety of mammalian and avian host species. The purpose of this study was to identify RVA in nomadic goats and calves during severe diarrhea outbreaks in 2012 and 2014 in Bouaarfa, Morocco, and to characterize the complete genomic constellation of two bovine and caprine strains (S18 and S19) and their genetic relatedness with the human strain ma31 detected in 2011 in Morocco. Partial nucleotide sequencing of VP4 and VP7 genes for the twenty-two positive samples revealed three circulating genotypes: G6P[14], G10P[14], and G10P[5] with predominance of G6P[14] genotype. Full-genome sequencing for both strains S18 and S19 presented, respectively, the following genomic constellations: G6-P[14]-I2-R2-C2-M2-A3-N2-T6-E2-H3 and G10-P[14]-I2-R2-C2-M2-A11-N2-T6-E2-H3. Phylogenetic analyses and the analysis of the VP8* antigenic epitopes for S18, S19 and ma31 revealed a shared similarity with bovine, caprine, ovine and human strains from Morocco and other countries. The VP2 and NSP1 genes of the S19 strain were closely related to those of the cognate genes of the human ma31 strain, while the VP4 gene of S18 strain was closely related to the cogent gene of the ma31 strain. Our findings revealed cases of zoonotic transmission and confirmed the risk of emergence of new genotypes in some environments such as nomadic regions, where close physical proximity between human and livestock is common. The present study is novel in reporting whole-genome analyses of RVA isolates obtained from nomadic livestock in Morocco.

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References

  1. Greenberg HB, Estes MK (2009) Rotaviruses: from pathogenesis to vaccination. Gastroenterology 136(6):1939–1951

    Article  CAS  Google Scholar 

  2. Desselberger U (2014) Rotaviruses. Virus Res 190:75–96

    Article  CAS  Google Scholar 

  3. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD (2012) 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 12(2):136–141

    Article  Google Scholar 

  4. Estes MK (2013) Rotaviruses. In: Knipe DM, et al. (eds) Fields virology. Wolters Kluwer Health, Philadelphia

    Google Scholar 

  5. Estes MK, Kang G, Zeng CQ, Crawford SE, Ciarlet M (2001) Pathogenesis of rotavirus gastroenteritis. Novartis Found Symp 238(82–96):6

    Google Scholar 

  6. Kirkwood CD (2010) Genetic and antigenic diversity of human rotaviruses: potential impact on vaccination programs. J Infect Dis 202(Suppl):S43–48

    Article  CAS  Google Scholar 

  7. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gomara M, Maes P, Patton JT, Rahman M, Van Ranst M (2008) Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82(7):3204–3219

    Article  CAS  Google Scholar 

  8. Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Banyai K, Estes MK, Gentsch JR, Iturriza-Gomara M, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Patton JT, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Desselberger U, Van Ranst M (2008) Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153(8):1621–1629

    Article  CAS  Google Scholar 

  9. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Banyai K, Brister JR, Buesa J, Esona MD, Estes MK, Gentsch JR, Iturriza-Gomara M, Johne R, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Parreno V, Rahman M, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Patton JT, Desselberger U, Van Ranst M (2011) Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156(8):1397–1413

    Article  CAS  Google Scholar 

  10. Trojnar E, Sachsenroder J, Twardziok S, Reetz J, Otto PH, Johne R (2013) Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol 94(1):136–142

    Article  CAS  Google Scholar 

  11. Delogu R, Ianiro G, Morea A, Chironna M, Fiore L, Ruggeri FM (2016) Molecular characterization of two rare human G8P[14] rotavirus strains, detected in Italy in 2012. Infect Genet Evol 44:303–312

    Article  CAS  Google Scholar 

  12. Dennis FE, Fujii Y, Haga K, Damanka S, Lartey B, Agbemabiese CA, Ohta N, Armah GE, Katayama K (2014) Identification of novel Ghanaian G8P[6] human-bovine reassortant rotavirus strain by next generation sequencing. PLoS ONE 9:6

    Google Scholar 

  13. Ghosh S, Kobayashi N (2011) Whole-genomic analysis of rotavirus strains: current status and future prospects. Future Microbiol 6(9):1049–1065

    Article  CAS  Google Scholar 

  14. Doro R, Farkas SL, Martella V, Banyai K (2015) Zoonotic transmission of rotavirus: surveillance and control. Expert Rev Anti Infect Ther 13(11):1337–1350

    Article  CAS  Google Scholar 

  15. Ennima I, Sebbar G, Harif B, Amzazi S, Loutfi C, Touil N (2016) Isolation and identification of group A rotaviruses among neonatal diarrheic calves. Morocco BMC Res Notes 9(1):261

    Article  Google Scholar 

  16. Hassine-Zaafrane M, Ben Salem I, Sdiri-Loulizi K, Kaplon J, Bouslama L, Aouni Z, Sakly N, Pothier P, Aouni M, Ambert-Balay K (2014) Distribution of G (VP7) and P (VP4) genotypes of group A bovine rotaviruses from Tunisian calves with diarrhoea. J Appl Microbiol 116(6):1387–1395

    Article  CAS  Google Scholar 

  17. Ammar SSM, Mokhtaria K, Tahar BB, Amar AA, Redha BA, Yuva B, Mohamed HS, Abdellatif N, Laid B (2014) Prevalence of rotavirus (GARV) and coronavirus (BCoV) associated with neonatal diarrhea in calves in western Algeria. Asian Pac J Trop Biomed 4:S318–S322

    Article  Google Scholar 

  18. Smail NL, Rezali L, Abdelhadi SA (2018) Etude préliminaire sur la mortalité de veaux âgés de 0 à 90 jours en région de Tiaret Algérie Ouest. Livestock Research for Rural Development Volume 30. Article#98. https://www.lrrd.org/lrrd30/6/si_am30098.html

  19. Alaoui Amine S, Melloul M, El Alaoui MA, Touil N, El Fahime E (2019) Full-length genome analysis of the first human G8P[14] rotavirus strain from Morocco suggests evidence of zoonotic transmission. Virus Genes 55(4):465–478

    Article  CAS  Google Scholar 

  20. Iturriza-Gomara M, Kang G, Gray J (2004) Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J Clin Virol 31(4):259–265

    Article  CAS  Google Scholar 

  21. Simmonds MK, Armah G, Asmah R, Banerjee I, Damanka S, Esona M, Gentsch JR, Gray JJ, Kirkwood C, Page N, Iturriza-Gomara M (2008) New oligonucleotide primers for P-typing of rotavirus strains: strategies for typing previously untypeable strains. J Clin Virol 42(4):368–373

    Article  CAS  Google Scholar 

  22. Maes P, Matthijnssens J, Rahman M, Van Ranst M (2009) RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 9(238):1471–2180

    Google Scholar 

  23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  Google Scholar 

  24. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464

    Article  Google Scholar 

  25. Tacharoenmuang R, Komoto S, Guntapong R, Ide T, Haga K, Katayama K, Kato T, Ouchi Y, Kurahashi H, Tsuji T, Sangkitporn S, Taniguchi K (2015) Whole genomic analysis of an unusual human G6P[14] rotavirus strain isolated from a child with diarrhea in Thailand: evidence for bovine-to-human interspecies transmission and reassortment events. PLoS ONE 10(9):e0139381. https://doi.org/10.1371/journal.pone.0139381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. de Beer M, Steele D (2002) Characterization of the VP7 and VP4 genes of a South African group A caprine rotavirus. GenBank record. https://www.ncbi.nlm.nih.gov/nuccore/AY128709.1/andhttps://www.ncbi.nlm.nih.gov/nuccore/AY128708.1. Accessed Feb 2020

  27. Valiakos GA, Chatzopoulos DCA, Tsokana CN (2017) Interspecies transmission of Rotaviruses among ruminants, dogs and humans: current facts and remarks. J Hellen Veterin Med Soc 68(2):123–130

    Article  Google Scholar 

  28. Matthijnssens J, Van Ranst M (2012) Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol 2(4):426–433

    Article  CAS  Google Scholar 

  29. Matthijnssens J, Potgieter CA, Ciarlet M, Parreno V, Martella V, Banyai K, Garaicoechea L, Palombo EA, Novo L, Zeller M, Arista S, Gerna G, Rahman M, Van Ranst M (2009) Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J Virol 83(7):2917–2929

    Article  CAS  Google Scholar 

  30. Jere KC, Mlera L, Page NA, van Dijk AA, O'Neill HG (2011) Whole genome analysis of multiple rotavirus strains from a single stool specimen using sequence-independent amplification and 454(R) pyrosequencing reveals evidence of intergenotype genome segment recombination. Infect Genet Evol 11(8):2072–2082

    Article  CAS  Google Scholar 

  31. Bwogi J, Jere KC, Karamagi C, Byarugaba DK, Namuwulya P, Baliraine FN, Desselberger U, Iturriza-Gomara M (2017) Whole genome analysis of selected human and animal rotaviruses identified in Uganda from 2012 to 2014 reveals complex genome reassortment events between human, bovine, caprine and porcine strains. PLoS ONE 12(6):e0178855

    Article  Google Scholar 

  32. Gabbay YB, Borges AA, Oliveira DS, Linhares AC, Mascarenhas JD, Barardi CR, Simoes CM, Wang Y, Glass RI, Jiang B (2008) Evidence for zoonotic transmission of group C rotaviruses among children in Belem. Braz J Med Virol 80(9):1666–1674

    Article  CAS  Google Scholar 

  33. Luchs A, Cilli A, Morillo SG, de Carmona R et al (2012) Rare G3P[3] rotavirus strain detected in Brazil: possible human-canine interspecies transmission. J Clin Virol 54(1):89–92

    Article  CAS  Google Scholar 

  34. Martella V, Banyai K, Matthijnssens J, Buonavoglia C, Ciarlet M (2010) Zoonotic aspects of rotaviruses. Vet Microbiol 140(3–4):246–255

    Article  CAS  Google Scholar 

  35. Midgley SE, Hjulsager CK, Larsen LE, Falkenhorst G, Bottiger B (2012) Suspected zoonotic transmission of rotavirus group A in Danish adults. Epidemiol Infect 140(6):1013–1017

    Article  CAS  Google Scholar 

  36. Sieg M, Rückner A, Köhler C, Burgener I, Vahlenkamp T (2014) A bovine G8P[1] group A rotavirus isolated from an asymptomatically infected dog. J Gen Virol. https://doi.org/10.1099/vir.0.069120-0

    Article  PubMed  Google Scholar 

  37. Benhafid M, Elomari N, Azzouzi Idrissi M, Rguig A, Gentsch JR, Parashar U, Elaouad R (2014) Effect of monovalent rotavirus vaccine on rotavirus disease burden and circulating rotavirus strains among children in Morocco. J Med Virol 87(6):944–953

    Article  Google Scholar 

  38. Benhafid M, Elomari N, Elqazoui M, Meryem AI, Rguig A, Filali-Maltouf A, Elaouad R (2013) Diversity of rotavirus strains circulating in children under 5 years of age admitted to hospital for acute gastroenteritis in Morocco, June 2006 to May 2009. J Med Virol 85(2):354–362

    Article  Google Scholar 

  39. Benhafid M, Youbi M, Klena JD, Gentsch JR, Teleb N, Widdowson MA, Elaouad R (2009) Epidemiology of rotavirus gastroenteritis among children <5 years of age in Morocco during 1 year of sentinel hospital surveillance, June 2006-May 2007. J Infect Dis 1(200):605048

    Google Scholar 

  40. El Qazoui M, Oumzil H, Baassi L, El Omari N, Sadki K, Amzazi S, Benhafid M, El Aouad R (2014) Rotavirus and norovirus infections among acute gastroenteritis children in Morocco. BMC Infect Dis 14:300–300

    Article  Google Scholar 

  41. Donato CM, Manuelpillai NM, Cowley D, Roczo-Farkas S, Buttery JP, Crawford NW, Kirkwood CD (2014) Genetic characterization of a novel G3P[14] rotavirus strain causing gastroenteritis in 12 year old Australian child. Infect Genet Evol 25:97–109

    Article  CAS  Google Scholar 

  42. Mullick S, Mukherjee A, Ghosh S, Pazhani GP, Sur D, Manna B, Nataro JP, Levine MM, Ramamurthy T, Chawla-Sarkar M (2013) Genomic analysis of human rotavirus strains G6P[14] and G11P[25] isolated from Kolkata in 2009 reveals interspecies transmission and complex reassortment events. Infect Genet Evol 14:15–21

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Center for Scientific and Technical Research (CNRST) and the virology department. There was no involvement of the funding sources in carrying out this work from its conception to the data analysis, article writing and its submission for publication.

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Authors and Affiliations

  1. Genomic Center for Human Pathologies (GENOPATH), Faculty of Medicine and Pharmacy, University Mohammed V in Rabat, Av. Mohamed Belarbi El Alaoui, 6203, Rabat, Morocco

    Sanaâ Alaoui Amine, Marouane Melloul, Hassan Boulahyaoui, Nadia Touil & Elmostafa El Fahime

  2. Molecular Biology and Functional Genomics Platform, National Center for Scientific and Technical Research, CNRST, Angle Avenue Allal El Fassi, Avenue des FAR, Quartier Er-Ryad, 8027, Rabat, Morocco

    Sanaâ Alaoui Amine, Marouane Melloul, Moulay Abdelaziz El Alaoui & Elmostafa El Fahime

  3. Virology Laboratory, Research Team in Molecular Virology and Onco Biology (ERVMOB), Faculty of Medicine and Pharmacy, University Mohammed V in Rabat, Av. Mohamed Belarbi El Alaoui, 6203, Rabat, Morocco

    Moulay Abdelaziz El Alaoui

  4. Département de Virologie, Société de Productions Biologiques et Pharmaceutiques Vétérinaires, Km 2, Route de Casablanca, B.P. 4569, Rabat, Morocco

    Chafiqa Loutfi

  5. Research and Biosafety Laboratory, Med V Military Teaching Hospital in Rabat, 10045, Hay Ryad, Morocco

    Nadia Touil

Authors
  1. Sanaâ Alaoui Amine
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  2. Marouane Melloul
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  3. Moulay Abdelaziz El Alaoui
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  4. Hassan Boulahyaoui
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  6. Nadia Touil
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  7. Elmostafa El Fahime
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Contributions

NT, CL and EE conceived and designed the study. SA, HB and MM carried out the experiments. SA, MM and ME performed the data analysis. SA wrote the draft. NT, EE, MM, CL, HB and ME reviewed the manuscript. All the authors read the final version of the manuscript and approved it for publication.

Corresponding author

Correspondence to Sanaâ Alaoui Amine.

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The authors declare that they have no conflict of interest.

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All fecal samples were collected from different nomadic farmers after authorization and in accordance with the Vet responsible, Dr. S. Fellahi.

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Edited by Juergen A Richt.

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Alaoui Amine, S., Melloul, M., El Alaoui, M.A. et al. Evidence for zoonotic transmission of species A rotavirus from goat and cattle in nomadic herds in Morocco, 2012–2014. Virus Genes 56, 582–593 (2020). https://doi.org/10.1007/s11262-020-01778-w

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