Skip to main content
Top
Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Research

Molecular epidemiology of Avian Rotaviruses Group A and D shed by different bird species in Nigeria

Authors: Maude Pauly, Oluwole O. Oni, Aurélie Sausy, Ademola A. Owoade, Christopher A. O. Adeyefa, Claude P. Muller, Judith M. Hübschen, Chantal J. Snoeck

Published in: Virology Journal | Issue 1/2017

Login to get access

Abstract

Background

Avian rotaviruses (RVs) cause gastrointestinal diseases of birds worldwide. However, prevalence, diversity, epidemiology and phylogeny of RVs remain largely under-investigated in Africa.

Methods

Fecal samples from 349 birds (158 symptomatic, 107 asymptomatic and 84 birds without recorded health status) were screened by reverse transcription PCR to detect RV groups A and D (RVA and RVD). Partial gene sequences of VP4, VP6, VP7 and NSP4 for RVA, and of VP6 and VP7 for RVD were obtained and analyzed to infer phylogenetic relationship. Fisher’s exact test and logistic regression were applied to identify factors potentially influencing virus shedding in chickens.

Results

A high prevalence of RVA (36.1%; 126/349) and RVD (31.8%; 111/349) shedding was revealed in birds. In chickens, RV shedding was age-dependent and highest RVD shedding rates were found in commercial farms. No negative health effect could be shown, and RVA and RVD shedding was significantly more likely in asymptomatic chickens: RVA/RVD were detected in 51.9/48.1% of the asymptomatic chickens, compared to 18.9/29.7% of the symptomatic chickens (p < 0.001/p = 0.01). First RVA sequences were obtained from mallard ducks (Anas platyrhynchos) and guinea fowls (Numida meleagris). Phylogenetic analyses illustrated the high genetic diversity of RVA and RVD in Nigerian birds and suggested cross-species transmission of RVA, especially at live bird markets. Indeed, RVA strains highly similar to a recently published fox rotavirus (RVA/Fox-tc/ITA/288356/2011/G18P[17]) and distantly related to other avian RVs were detected in different bird species, including pigeons, ducks, guinea fowls, quails and chickens.

Conclusion

This study provides new insights into epidemiology, diversity and classification of avian RVA and RVD in Nigeria. We show that cross-species transmission of host permissive RV strains occurs when different bird species are mixed.
Appendix
Available only for authorised users
Literature
1.
go back to reference Estes MK, Kapikian AZ. Rotaviruses. In: Knipe DM, Howley PM, editors. Fields Virology. Volume 2. 5th edition. Philadelphia: Lippincott William & Wilkins; 2007. Estes MK, Kapikian AZ. Rotaviruses. In: Knipe DM, Howley PM, editors. Fields Virology. Volume 2. 5th edition. Philadelphia: Lippincott William & Wilkins; 2007.
2.
go back to reference Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, Steele D, et al. Global mortality associated with rotavirus disease among children in 2004. J Infect Dis. 2009;200(Suppl 1):S9–s15.CrossRefPubMed Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, Steele D, et al. Global mortality associated with rotavirus disease among children in 2004. J Infect Dis. 2009;200(Suppl 1):S9–s15.CrossRefPubMed
4.
go back to reference McNulty MS, Jones RC. Rotaviruses. In: Pattison, McMullin, Bradbury, Alexander, editors. Poultry diseases. 6th edition. Philadelphia: SAUNDERS Elsevier; 2008. McNulty MS, Jones RC. Rotaviruses. In: Pattison, McMullin, Bradbury, Alexander, editors. Poultry diseases. 6th edition. Philadelphia: SAUNDERS Elsevier; 2008.
5.
6.
go back to reference Otto P, Liebler-Tenorio EM, Elschner M, Reetz J, Lohren U, Diller R. Detection of rotaviruses and intestinal lesions in broiler chicks from flocks with runting and stunting syndrome (RSS). Avian Dis. 2006;50:411–8.CrossRefPubMed Otto P, Liebler-Tenorio EM, Elschner M, Reetz J, Lohren U, Diller R. Detection of rotaviruses and intestinal lesions in broiler chicks from flocks with runting and stunting syndrome (RSS). Avian Dis. 2006;50:411–8.CrossRefPubMed
7.
go back to reference Moura-Alvarez J, Chacon JV, Scanavini LS, Nunez LF, Astolfi-Ferreira CS, Jones RC, et al. Enteric viruses in Brazilian turkey flocks: single and multiple virus infection frequency according to age and clinical signs of intestinal disease. Poult Sci. 2013;92:945–55.CrossRefPubMed Moura-Alvarez J, Chacon JV, Scanavini LS, Nunez LF, Astolfi-Ferreira CS, Jones RC, et al. Enteric viruses in Brazilian turkey flocks: single and multiple virus infection frequency according to age and clinical signs of intestinal disease. Poult Sci. 2013;92:945–55.CrossRefPubMed
9.
go back to reference Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M, Johne R. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol. 2012;157:1177–82.CrossRefPubMed Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M, Johne R. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol. 2012;157:1177–82.CrossRefPubMed
10.
go back to reference Mihalov-Kovacs E, Gellert A, Marton S, Farkas SL, Feher E, Oldal M, et al. Candidate new rotavirus species in sheltered dogs, Hungary. Emerg Infect Dis. 2015;21:660–3.CrossRefPubMed Mihalov-Kovacs E, Gellert A, Marton S, Farkas SL, Feher E, Oldal M, et al. Candidate new rotavirus species in sheltered dogs, Hungary. Emerg Infect Dis. 2015;21:660–3.CrossRefPubMed
11.
go back to reference Banyai K, Kemenesi G, Budinski I, Foldes F, Zana B, Marton S, et al. Candidate new rotavirus species in Schreiber's bats, Serbia. Infect Genet Evol. 2017;48:19–26.CrossRefPubMed Banyai K, Kemenesi G, Budinski I, Foldes F, Zana B, Marton S, et al. Candidate new rotavirus species in Schreiber's bats, Serbia. Infect Genet Evol. 2017;48:19–26.CrossRefPubMed
12.
go back to reference Phan TG, Leutenegger CM, Chan R, Delwart E. Rotavirus I in feces of a cat with diarrhea. Virus Genes. 2017;53:487–90.CrossRefPubMed Phan TG, Leutenegger CM, Chan R, Delwart E. Rotavirus I in feces of a cat with diarrhea. Virus Genes. 2017;53:487–90.CrossRefPubMed
13.
go back to reference Otto PH, Ahmed MU, Hotzel H, Machnowska P, Reetz J, Roth B, et al. Detection of avian rotaviruses of groups a, D, F and G in diseased chickens and turkeys from Europe and Bangladesh. Vet Microbiol. 2012;156:8–15.CrossRefPubMed Otto PH, Ahmed MU, Hotzel H, Machnowska P, Reetz J, Roth B, et al. Detection of avian rotaviruses of groups a, D, F and G in diseased chickens and turkeys from Europe and Bangladesh. Vet Microbiol. 2012;156:8–15.CrossRefPubMed
14.
go back to reference Iturriza-Gomara M, Desselberger U, Gray J. Molecular epidemiology of rotaviruses: genetic mechanisms associated with diversity. In: Desselberger U, Gray J, editors. Viral gastroenteritis. Amsterdam: Elsevier Science; 2003. p. 317–44.CrossRef Iturriza-Gomara M, Desselberger U, Gray J. Molecular epidemiology of rotaviruses: genetic mechanisms associated with diversity. In: Desselberger U, Gray J, editors. Viral gastroenteritis. Amsterdam: Elsevier Science; 2003. p. 317–44.CrossRef
15.
go back to reference Martella V, Banyai K, Matthijnssens J, Buonavoglia C, Ciarlet M. Zoonotic aspects of rotaviruses. Vet Microbiol. 2010;140:246–55.CrossRefPubMed Martella V, Banyai K, Matthijnssens J, Buonavoglia C, Ciarlet M. Zoonotic aspects of rotaviruses. Vet Microbiol. 2010;140:246–55.CrossRefPubMed
16.
go back to reference Kattoor JJ, Malik YS, Sasidharan A, Rajan VM, Dhama K, Ghosh S, et al. Analysis of codon usage pattern evolution in avian rotaviruses and their preferred host. Infect Genet Evol. 2015;34:17–25.CrossRefPubMed Kattoor JJ, Malik YS, Sasidharan A, Rajan VM, Dhama K, Ghosh S, et al. Analysis of codon usage pattern evolution in avian rotaviruses and their preferred host. Infect Genet Evol. 2015;34:17–25.CrossRefPubMed
17.
go back to reference Le Pendu J, Nystrom K, Ruvoen-Clouet N. Host-pathogen co-evolution and glycan interactions. Curr Opin Virol. 2014;7:88–94.CrossRefPubMed Le Pendu J, Nystrom K, Ruvoen-Clouet N. Host-pathogen co-evolution and glycan interactions. Curr Opin Virol. 2014;7:88–94.CrossRefPubMed
18.
go back to reference Kindler E, Trojnar E, Heckel G, Otto PH, Johne R. Analysis of rotavirus species diversity and evolution including the newly determined full-length genome sequences of rotavirus F and G. Infect Genet Evol. 2013;14:58–67.CrossRefPubMed Kindler E, Trojnar E, Heckel G, Otto PH, Johne R. Analysis of rotavirus species diversity and evolution including the newly determined full-length genome sequences of rotavirus F and G. Infect Genet Evol. 2013;14:58–67.CrossRefPubMed
19.
go back to reference Schumann T, Hotzel H, Otto P, Johne R. Evidence of interspecies transmission and reassortment among avian group a rotaviruses. Virology. 2009;386:334–43.CrossRefPubMed Schumann T, Hotzel H, Otto P, Johne R. Evidence of interspecies transmission and reassortment among avian group a rotaviruses. Virology. 2009;386:334–43.CrossRefPubMed
20.
go back to reference Trojnar E, Otto P, Roth B, Reetz J, Johne R. The genome segments of a group D rotavirus possess group A-like conserved termini but encode group-specific proteins. J Virol. 2010;84:10254–65.CrossRefPubMedPubMedCentral Trojnar E, Otto P, Roth B, Reetz J, Johne R. The genome segments of a group D rotavirus possess group A-like conserved termini but encode group-specific proteins. J Virol. 2010;84:10254–65.CrossRefPubMedPubMedCentral
21.
go back to reference Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K, Ramachandran M, et al. Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis. 2005;192(Suppl 1):S146–59.CrossRefPubMed Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K, Ramachandran M, et al. Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis. 2005;192(Suppl 1):S146–59.CrossRefPubMed
22.
go back to reference McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L, Wang S, et al. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009;5:e1000634. McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L, Wang S, et al. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009;5:e1000634.
23.
go back to reference Maunula L, Von Bonsdorff CH. Frequent reassortments may explain the genetic heterogeneity of rotaviruses: analysis of Finnish rotavirus strains. J Virol. 2002;76:11793–800.CrossRefPubMedPubMedCentral Maunula L, Von Bonsdorff CH. Frequent reassortments may explain the genetic heterogeneity of rotaviruses: analysis of Finnish rotavirus strains. J Virol. 2002;76:11793–800.CrossRefPubMedPubMedCentral
24.
go back to reference Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Banyai K, Brister JR, et al. Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification Working group (RCWG). Arch Virol. 2011;156:1397–413. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Banyai K, Brister JR, et al. Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification Working group (RCWG). Arch Virol. 2011;156:1397–413.
25.
go back to reference Pantin-Jackwood MJ, Day JM, Jackwood MW, Spackman E. Enteric viruses detected by molecular methods in commercial chicken and turkey flocks in the United States between 2005 and 2006. Avian Dis. 2008;52:235–44.CrossRefPubMed Pantin-Jackwood MJ, Day JM, Jackwood MW, Spackman E. Enteric viruses detected by molecular methods in commercial chicken and turkey flocks in the United States between 2005 and 2006. Avian Dis. 2008;52:235–44.CrossRefPubMed
26.
go back to reference Bezerra DA, da Silva RR, Kaiano JH, de Souza OD, Gabbay YB, Linhares AC, et al. Detection, epidemiology and characterization of VP6 and VP7 genes of group D rotavirus in broiler chickens. Avian Pathol. 2014;43:238–43. Bezerra DA, da Silva RR, Kaiano JH, de Souza OD, Gabbay YB, Linhares AC, et al. Detection, epidemiology and characterization of VP6 and VP7 genes of group D rotavirus in broiler chickens. Avian Pathol. 2014;43:238–43.
27.
go back to reference Koo BS, Lee HR, Jeon EO, Han MS, Min KC, Lee SB, et al. Molecular survey of enteric viruses in commercial chicken farms in Korea with a history of enteritis. Poult Sci. 2013;92:2876–85. Koo BS, Lee HR, Jeon EO, Han MS, Min KC, Lee SB, et al. Molecular survey of enteric viruses in commercial chicken farms in Korea with a history of enteritis. Poult Sci. 2013;92:2876–85.
28.
go back to reference Karim M, Rume F, Alam M, Ahmed M. Molecular epidemiologic study on avian rotavirus prevailing in Bangladesh. Bangl J Vet Med. 2007;5:43–8. Karim M, Rume F, Alam M, Ahmed M. Molecular epidemiologic study on avian rotavirus prevailing in Bangladesh. Bangl J Vet Med. 2007;5:43–8.
29.
go back to reference Oni OO, Owoade AA. Genetic evidence of rotavirus in chicken from two localities in southwestern Nigeria. Animal Res Int. 2010;7:1139–41. Oni OO, Owoade AA. Genetic evidence of rotavirus in chicken from two localities in southwestern Nigeria. Animal Res Int. 2010;7:1139–41.
30.
go back to reference WHO: Collecting, preserving and shipping specimens for the diagnosis of avian influenza a(H5N1) virus infection. Guide for field operations. 2006. WHO: Collecting, preserving and shipping specimens for the diagnosis of avian influenza a(H5N1) virus infection. Guide for field operations. 2006.
31.
go back to reference Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
32.
go back to reference Maes P, Matthijnssens J, Rahman M, Van Ranst M. RotaC: a web-based tool for the complete genome classification of group a rotaviruses. BMC Microbiol. 2009;9:238.CrossRefPubMedPubMedCentral Maes P, Matthijnssens J, Rahman M, Van Ranst M. RotaC: a web-based tool for the complete genome classification of group a rotaviruses. BMC Microbiol. 2009;9:238.CrossRefPubMedPubMedCentral
33.
go back to reference Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.CrossRefPubMed Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.CrossRefPubMed
34.
go back to reference Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–77.CrossRefPubMed Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–77.CrossRefPubMed
35.
go back to reference Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–4.CrossRefPubMed Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–4.CrossRefPubMed
37.
go back to reference Pauly M, Akoua-Koffi C, Buchwald N, Schubert G, Weiss S, Couacy-Hymann E, Anoh AE, Mossoun A, Calvignac-Spencer S, Leendertz SA, et al. Adenovirus in Rural Cote D’Ivoire: High Diversity and Cross-Species Detection. Ecohealth. 2015;12(3):441-52. doi:10.1007/s10393-015-1032-5. Epub 2015 May 20. Pauly M, Akoua-Koffi C, Buchwald N, Schubert G, Weiss S, Couacy-Hymann E, Anoh AE, Mossoun A, Calvignac-Spencer S, Leendertz SA, et al. Adenovirus in Rural Cote D’Ivoire: High Diversity and Cross-Species Detection. Ecohealth. 2015;12(3):441-52. doi:10.​1007/​s10393-015-1032-5. Epub 2015 May 20.
38.
go back to reference R Development Core Team. R: a language and environment for statistical computing. Vienna: Computing RFfS ed; 2008. R Development Core Team. R: a language and environment for statistical computing. Vienna: Computing RFfS ed; 2008.
40.
go back to reference Eddelbuettel D, François R. Rcpp: seamless R and C++ integration. J Stat Softw. 2011;40:1–18. Eddelbuettel D, François R. Rcpp: seamless R and C++ integration. J Stat Softw. 2011;40:1–18.
41.
go back to reference Ducatez MF, Martin AM, Owoade AA, Olatoye IO, Alkali BR, Maikano I, et al. Characterization of a new genotype and serotype of infectious bronchitis virus in western Africa. J Gen Virol. 2009;90:2679–85.CrossRefPubMed Ducatez MF, Martin AM, Owoade AA, Olatoye IO, Alkali BR, Maikano I, et al. Characterization of a new genotype and serotype of infectious bronchitis virus in western Africa. J Gen Virol. 2009;90:2679–85.CrossRefPubMed
42.
go back to reference Snoeck CJ, Owoade AA, Couacy-Hymann E, Alkali BR, Okwen MP, Adeyanju AT, et al. High genetic diversity of Newcastle disease virus in poultry in west and Central Africa: cocirculation of genotype XIV and newly defined genotypes XVII and XVIII. J Clin Microbiol. 2013;51:2250–60. Snoeck CJ, Owoade AA, Couacy-Hymann E, Alkali BR, Okwen MP, Adeyanju AT, et al. High genetic diversity of Newcastle disease virus in poultry in west and Central Africa: cocirculation of genotype XIV and newly defined genotypes XVII and XVIII. J Clin Microbiol. 2013;51:2250–60.
43.
go back to reference Monne I, Meseko C, Joannis T, Shittu I, Ahmed M, Tassoni L, et al. Highly pathogenic avian influenza a(H5N1) virus in poultry, Nigeria, 2015. Emerg Infect Dis. 2015;21:1275–7. Monne I, Meseko C, Joannis T, Shittu I, Ahmed M, Tassoni L, et al. Highly pathogenic avian influenza a(H5N1) virus in poultry, Nigeria, 2015. Emerg Infect Dis. 2015;21:1275–7.
44.
go back to reference Brüssow H, Nakagomi O, Gerna G, Eichhorn W. Isolation of an avianlike group a rotavirus from a calf with diarrhea. J Clin Microbiol. 1992;30:67–73.PubMedPubMedCentral Brüssow H, Nakagomi O, Gerna G, Eichhorn W. Isolation of an avianlike group a rotavirus from a calf with diarrhea. J Clin Microbiol. 1992;30:67–73.PubMedPubMedCentral
45.
go back to reference Brüssow H, Nakagomi O, Minamoto N, Eichhorn W. Rotavirus 993/83, isolated from calf faeces, closely resembles an avian rotavirus. J Gen Virol. 1992;73(Pt 7):1873–5.CrossRefPubMed Brüssow H, Nakagomi O, Minamoto N, Eichhorn W. Rotavirus 993/83, isolated from calf faeces, closely resembles an avian rotavirus. J Gen Virol. 1992;73(Pt 7):1873–5.CrossRefPubMed
46.
go back to reference Rohwedder A, Schutz KI, Minamoto N, Brussow H. Sequence analysis of pigeon, turkey, and chicken rotavirus VP8* identifies rotavirus 993/83, isolated from calf feces, as a pigeon rotavirus. Virology. 1995;210:231–5.CrossRefPubMed Rohwedder A, Schutz KI, Minamoto N, Brussow H. Sequence analysis of pigeon, turkey, and chicken rotavirus VP8* identifies rotavirus 993/83, isolated from calf feces, as a pigeon rotavirus. Virology. 1995;210:231–5.CrossRefPubMed
47.
go back to reference Ito H, Minamoto N, Hiraga S, Sugiyama M. Sequence analysis of the VP6 gene in group a turkey and chicken rotaviruses. Virus Res. 1997;47:79–83.CrossRefPubMed Ito H, Minamoto N, Hiraga S, Sugiyama M. Sequence analysis of the VP6 gene in group a turkey and chicken rotaviruses. Virus Res. 1997;47:79–83.CrossRefPubMed
48.
go back to reference Lin SL, Tian P. Detailed computational analysis of a comprehensive set of group a rotavirus NSP4 proteins. Virus Genes. 2003;26:271–82.CrossRefPubMed Lin SL, Tian P. Detailed computational analysis of a comprehensive set of group a rotavirus NSP4 proteins. Virus Genes. 2003;26:271–82.CrossRefPubMed
49.
go back to reference Trojnar E, Otto P, Johne R. The first complete genome sequence of a chicken group a rotavirus indicates independent evolution of mammalian and avian strains. Virology. 2009;386:325–33.CrossRefPubMed Trojnar E, Otto P, Johne R. The first complete genome sequence of a chicken group a rotavirus indicates independent evolution of mammalian and avian strains. Virology. 2009;386:325–33.CrossRefPubMed
50.
go back to reference Johne R, Reetz J, Kaufer BB, Trojnar E. Generation of an avian-mammalian rotavirus Reassortant by using a helper virus-dependent reverse genetics system. J Virol. 2016;90:1439–43.CrossRefPubMedCentral Johne R, Reetz J, Kaufer BB, Trojnar E. Generation of an avian-mammalian rotavirus Reassortant by using a helper virus-dependent reverse genetics system. J Virol. 2016;90:1439–43.CrossRefPubMedCentral
Metadata
Title
Molecular epidemiology of Avian Rotaviruses Group A and D shed by different bird species in Nigeria
Authors
Maude Pauly
Oluwole O. Oni
Aurélie Sausy
Ademola A. Owoade
Christopher A. O. Adeyefa
Claude P. Muller
Judith M. Hübschen
Chantal J. Snoeck
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0778-5

Other articles of this Issue 1/2017

Virology Journal 1/2017 Go to the issue