Abstract
An unusual group A rotavirus (RVA) strain MAR/ma31/2011/G8P[14] was detected for the first time in Morocco in a stool sample from hospitalized child aged 18 months suffering from acute gastroenteritis and fever in 2011. Complete genome sequencing of the ma31 strain was done using the capillary sequencing technology. The analysis revealed the G8-P[14]-I2-R2-C2-M2-A11-N2-T6-E2-H3 constellation and the backbone genes: I2-R2-C2-M2-A11-N2-T6-E2-H3 are commonly found in RVA strains from artiodactyls such as cattle. The constellation was shared with another Italian zoonotic G8P[14] strains (BA01 and BA02), two Hungarian human strains (182-02 and BP1062) and a sheep RVA strain OVR762. Phylogenetic analysis of each genome segment of ma31 revealed a mixed gene configuration originated from animals and human. Comparison of the antigenic regions of VP7 and VP4 amino acid sequences between ma31 strain and selected animal and human strains bearing G8 and or P[14], showed a high level of conservation, while many substitutions was observed in comparison with RotaTeq™ and Rotarix™ vaccine strains. In contrast, alignment analysis of the four antigenic sites of VP6 revealed a high degree of conservation. These findings reveal a typical zoonotic origin of the strain and confirm a high potential for RVA zoonotic transmission between bovine and humans, allowing the generation of novel rotavirus genotypes.
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References
Estes MK, Greenberg HB (2013) Rotaviruses. In: Knipe PMHDM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (eds) Fields Virology. Williams and Wilkins, Philadelphia, pp 1347–1401
Martella V, Banyai K, Matthijnssens J, Buonavoglia C, Ciarlet M (2010) Zoonotic aspects of rotaviruses. Vet Microbiol 140(3–4):246–255
Parashar UD, Gibson CJ, Bresee JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12(2):304–306
Tate JE, Burton AH, Boschi-Pinto C, Parashar UD (2016) Global, regional, and nationa estimates of rotavirus mortality in children < 5 years of age, 2000–2013. Clin Infect Dis 1(62):S96–S105
Estes MK, Kapikian AZ (2006) Rotaviruses. In: Knipe D, Griffin D, Lamb R, Martin M, Roizman B, Straus S (eds) Fields Virology. Wolters Kluwer Health; Lippincott Williams and Wilkins, Philadelphia, pp 1917–1974
Iturriza-Gomara M, Dallman T, Banyai K, Bottiger B, Buesa J, Diedrich S, Fiore L, Johansen K, Koopmans M, Korsun N, Koukou D, Kroneman A, Laszlo B, Lappalainen M, Maunula L, Marques AM, Matthijnssens J, Midgley S, Mladenova Z, Nawaz S, Poljsak-Prijatelj M, Pothier P, Ruggeri FM, Sanchez-Fauquier A, Steyer A, Sidaraviciute-Ivaskeviciene I, Syriopoulou V, Tran AN, Usonis V, Van Ranst M, Rougemont A, Gray J (2011) Rotavirus genotypes co-circulating in Europe between 2006 and 2009 as determined by EuroRotaNet, a pan-European collaborative strain surveillance network. Epidemiol Infect 139(6):895–909
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
Rojas Miguel A, Gonçalves Jorge Luiz S, Dias Helver G, Manchego A, Santos N (2017) Identification of two novel rotavirus A genotypes, G35 and P[50], from Peruvian alpaca faeces. Infect Genet Evol 55:71–74
Degiuseppe JI, Beltramino JC, Millan A, Stupka JA, Parra GI (2013) Complete genome analyses of G4P[6] rotavirus detected in Argentinean children with diarrhoea provides evidence of interspecies transmission from swine. Clin Microbiol Infect. https://doi.org/10.1111/1469-0691.12216
Banyai K, Gentsch JR, Griffin DD, Holmes JL, Glass RI, Szucs G (2003) Genetic variability among serotype G6 human rotaviruses: identification of a novel lineage isolated in Hungary. J Med Virol 71(1):124–134
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
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
Medici MC, Tummolo F, Bonica MB, Heylen E, Zeller M, Calderaro A, Matthijnssens J (2015) Genetic diversity in three bovine-like human G8P[14] and G10P[14] rotaviruses suggests independent interspecies transmission events. J Gen Virol 96(Pt 5):1161–1168
Page N, Esona M, Seheri M, Nyangao J, Bos P, Mwenda J, Steele D (2010) Characterization of genotype G8 strains from Malawi, Kenya, and South Africa. J Med Virol 82(12):2073–2081
Armah GE, Steele AD, Esona MD, Akran VA, Nimzing L, Pennap G (2010) Diversity of rotavirus strains circulating in west Africa from 1996 to 2000. J Infect Dis 1(202):653571
Todd S, Page NA, Duncan Steele A, Peenze I, Cunliffe NA (2010) Rotavirus strain types circulating in Africa: review of studies published during 1997-2006. J Infect Dis 1(202):653555
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):e100699
Ghosh S, Gatheru Z, Nyangao J, Adachi N, Urushibara N, Kobayashi N (2011) Full genomic analysis of a G8P[1] rotavirus strain isolated from an asymptomatic infant in Kenya provides evidence for an artiodactyl-to-human interspecies transmission event. J Med Virol 83(2):367–376
Nakagomi T, Doan YH, Dove W, Ngwira B, Iturriza-Gomara M, Nakagomi O, Cunliffe NA (2013) G8 rotaviruses with conserved genotype constellations detected in Malawi over 10 years (1997-2007) display frequent gene reassortment among strains co-circulating in humans. J Gen Virol 94(Pt 6):1273–1295
Gautam R, Mijatovic-Rustempasic S, Roy S, Esona MD, Lopez B, Mencos Y, Rey-Benito G, Bowen MD (2015) Full genomic characterization and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain detected in a sample from Guatemala. Infect Genet Evol 33:206–211
Ianiro G, Delogu R, Bonomo P, Castiglia P, Ruggeri FM, Fiore L (2014) Molecular characterization of human G8P[4] rotavirus strains in Italy: proposal of a more complete subclassification of the G8 genotype in three major lineages. Infect Genet Evol 21:129–133
Doblali T, Touil N, Kaplon J, Ambert-Balay K, Agdar A, El hamzaoui S, Pothier P (2015) Clinical and molecular descriptions of rotavirus in Morocco 2 years after Rotarix® introduction. In 6th European Rotavirus Biology Meeting (ERBM), Dijon, France, 17–20 May
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
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
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
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
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
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464
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
Holmes JL, Kirkwood CD, Gerna G, Clemens JD, Rao MR, Naficy AB, Abu-Elyazeed R, Savarino SJ, Glass RI, Gentsch JR (1999) Characterization of unusual G8 rotavirus strains isolated from Egyptian children. Arch Virol 144(7):1381–1396
Benhafid M, Elomari N, Azzouzi Idrissi M, Rguig A, Gentsch JR, Parashar U, Elaouad R (2015) Effect of monovalent rotavirus vaccine on rotavirus disease burden and circulating rotavirus strains among children in Morocco. J Med Virol 87(6):944–953
Benhafid M, Rguig A, Trivedi T, Elqazoui M, Teleb N, Mouane N, Filali-Maltouf A, Parashar U, Patel M, Elaouad R (2012) Monitoring of rotavirus vaccination in Morocco: establishing the baseline burden of rotavirus disease. Vaccine 30:6515–6520
Gerna G, Steele AD, Hoshino Y, Sereno M, Garcia D, Sarasini A, Flores J (1994) A comparison of the VP7 gene sequences of human and bovine rotaviruses. J Gen Virol 75(Pt 7):1781–1784
Mijatovic-Rustempasic S, Roy S, Sturgeon M, Rungsrisuriyachai K, Reisdorf E, Cortese MM, Bowen MD (2015) Full-genome sequence of the first G8P[14] rotavirus strain detected in the United States. Genome Announc 3(3):00677-15
Matthijnssens J, Van Ranst M (2012) Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol 2(4):426–433
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
Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF, Le Pendu J, Estes MK, Prasad BV (2012) Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485(7397):256–259
Liu Y, Huang P, Tan M, Biesiada J, Meller J, Castello AA, Jiang B, Jiang X (2012) Rotavirus VP8*: phylogeny, host range, and interaction with histo-blood group antigens. J Virol 86(18):9899–9910
Fukai K, Sakai T, Hirose M, Itou T (1999) Prevalence of calf diarrhea caused by bovine group: a rotavirus carrying G serotype 8 specificity. Vet Microbiol 66:301–311
Fodha I, Boumaiza A, Chouikha A, Dewar J, Armah G, Geyer A, Trabelsi A, Steele AD (2005) Detection of group A rotavirus strains circulating in calves in Tunisia. J Vet Med 52:49–50
Matthijnssens J, Rahman M, Yang X, Delbeke T, Arijs I, Kabue JP, Muyembe JT, Van Ranst M (2006) G8 rotavirus strains isolated in the democratic Republic of Congo belong to the DS-1- like genogroup. J Clin Microbiol 44(5):1801–1809
Esona M, Steele D, Kerin T, Armah G, Peenze I, Geyer A, Page N, Nyangao J, Akran Agbaya V, Trabelsi A, Tsion B, Aminu M, Sebunya T, Dewar J, Glass R, Gentsch J (2010) Determination of the G and P types of previously nontypeable rotavirus strains from the African rotavirus network, 1996–2004: identification of unusual G types. J Infect Dis 202:S49–S54
Benmessaoud R, Jroundi I, Mouane N, Moraleda C, Tligui H, Seffar M, Alvarez- Martínez MJ, Pons MJ, Chaacho S, Hayes EB, Vila J, Alonso PL, Bassat Q, Ruiz J (2015) Aetiology, epidemiology and clinical characteristics of acute moderate-to-severe diarrhoea in children under 5 years of age hospitalized in a referral paediatric hospital in Rabat, Morocco. J Med Microbiol 64(1):84–92
Patel M, Steele D, Gentsch J, Wecker J, Glass R, Parashar U (2011) Real-world impact of rotavirus vaccination. Pediatr Infect Dis J 30(1 Suppl):S1–S5
Heylen E, Zeller M, Ciarlet M, Lawrence J, Steele D, Van Ranst M, Matthijnssens J (2015) Comparative analysis of pentavalent rotavirus vaccine strains and G8 rotaviruses identified during vaccine trial in Africa. Sci Rep 5:14658
Dormitzer PR, Sun ZY, Wagner G, Harrison SC (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21(5):885–897
Buragohain M, Cherian SS, Prabhakar G, Chitambar SD (2008) VP6 capsid protein of chicken rotavirus strain CH2: sequence, phylogeny and in silico antigenic analyses. Virus Res 137(2):173–178
Desselberger U, Huppertz HI (2011) Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 203(2):188–195
Franco MA, Angel J, Greenberg HB (2006) Immunity and correlates of protection for rotavirus vaccines. Vaccine 24(15):2718–2731
Delogu R, Ianiro G, Camilloni B, Fiore L, Ruggeri FM (2015) Unexpected spreading of G12P[8] rotavirus strains among young children in a small area of central Italy. J Med Virol 87(8):1292–1302
Kirkwood CD (2010) Genetic and antigenic diversity of human rotaviruses: potential impact on vaccination programs. J Infect Dis 202:S43–S48
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This study was supported by the National Center for Scientific and Technical Research (CNRST) and the Military Health Service. 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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NT and EE conceived and designed the study. SA and MM carried out the experiments. SA, MM and ME performed the data analysis. SA wrote the draft. NT, EE, MM and ME reviewed the manuscript. All the authors read the final version of the manuscript and approved it for publication.
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Ethical approval for this study was obtained from the Biomedical Research Ethics Committee of the Faculty of Medicine and Pharmacy of Rabat, Mohamed V University, Morocco following the guidelines set by the Declaration of Helsinki.
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Alaoui Amine, S., Melloul, M., El Alaoui, M. et al. Full-length genome analysis of the first human G8P[14] rotavirus strain from Morocco suggests evidence of zoonotic transmission. Virus Genes 55, 465–478 (2019). https://doi.org/10.1007/s11262-019-01677-9
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DOI: https://doi.org/10.1007/s11262-019-01677-9