Skip to main content
Log in

Genomic comparison of Newcastle disease viruses isolated in Nigeria between 2002 and 2015 reveals circulation of highly diverse genotypes and spillover into wild birds

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Newcastle disease virus (NDV) has a wide avian host range and a high degree of genetic variability, and virulent strains cause Newcastle disease (ND), a worldwide concern for poultry health. Although NDV has been studied in Nigeria, genetic information about the viruses involved in the endemicity of the disease and the transmission that likely occurs at the poultry-wildlife interface is still largely incomplete. Next-generation and Sanger sequencing was performed to provide complete (n = 73) and partial genomic sequence data (n = 38) for NDV isolates collected from domestic and wild birds in Nigeria during 2002-2015, including the first complete genome sequences of genotype IV and subgenotype VIh from the African continent. Phylogenetic analysis revealed that viruses of seven different genotypes circulated in that period, demonstrating high genetic diversity of NDV for a single country. In addition, a high degree of similarity between NDV isolates from domestic and wild birds was observed, suggesting that spillovers had occurred, including to three species that had not previously been shown to be susceptible to NDV infection. Furthermore, the first spillover of a mesogenic Komarov vaccine virus is documented, suggesting a previous spillover and evolution of this virus. The similarities between viruses from poultry and multiple bird species and the lack of evidence for host adaptation in codon usage suggest that transmission of NDV between poultry and non-poultry birds occurred recently. This is especially significant when considering that some viruses were isolated from species of conservation concern. The high diversity of NDV observed in both domestic and wild birds in Nigeria emphasizes the need for active surveillance and epidemiology of NDV in all bird species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Amarasinghe GK et al (2018) Taxonomy of the order Mononegavirales: update 2018. Arch Virol 163(8):2283–2294

    Article  CAS  Google Scholar 

  2. Alexander DJ, Aldous EW, Fuller CM (2012) The long view: a selective review of 40 years of Newcastle disease research. Avian Pathol 41(4):329–335

    Article  Google Scholar 

  3. OIE (2012) Newcastle disease. In: Manual of diagnostic tests and vaccines for terrestrial animals, pp 555–574 http://www.oie.int/standard-setting/terrestrial-manual/access-online/. Accessed 10 Feb 2019

  4. Czeglédi A, Ujvári D, Somogyi E, Wehmann E, Werner O, Lomniczi B (2006) Third genome size category of avian paramyxovirus serotype 1 (Newcastle disease virus) and evolutionary implications. Virus Res 120(1–2):36–48

    Article  Google Scholar 

  5. Dimitrov KM, Ramey AM, Qiu X, Bahl J, Afonso CL (2016) Temporal, geographic, and host distribution of avian paramyxovirus 1 (Newcastle disease virus). Infect Genet Evol 39:22–34

    Article  Google Scholar 

  6. Hill DH, Davis OS, Wilde JKH (1953) Newcastle disease in Nigeria. Br Vet J 109(9):381–385

    Article  Google Scholar 

  7. Snoeck CJ, Ducatez MF, Owoade AA, Faleke OO, Alkali BR, Tahita MC, Tarnagda Z, Ouedraogo JB, Maikano I, Mbah PO, Kremer JR, Muller CP (2007) Newcastle disease virus in West Africa: new virulent strains identified in non-commercial farms. Arch Virol 154(1):47–54

    Article  Google Scholar 

  8. Bello MB, Yusoff KM, Ideris A, Hair-Bejo M, Peeters BP, Jibril AH, Tambuwal FM, Omar AR (2018) Genotype diversity of Newcastle disease virus in Nigeria: disease control challenges and future outlook. Adv Virol. https://doi.org/10.1155/2018/6097291

    Article  PubMed  PubMed Central  Google Scholar 

  9. Shittu I, Joannis TM, Odaibo GN, Olaleye OD (2016) Newcastle disease in Nigeria: epizootiology and current knowledge of circulating genotypes. Virus Dis 27(4):329–339

    Article  Google Scholar 

  10. Snoeck CJ, Owoade AA, Couacy-Hymann E, Alkali BR, Okwen MP, Adeyanju AT, Komoyo GF, Nakoune E, Le Faou A, Muller CP (2013) High genetic diversity of Newcastle disease virus in poultry in West and Central Africa: co-circulation of genotypes XIV and newly defined genotypes XVII and XVIII. J Clin Microbiol 51:2250–2260

    Article  Google Scholar 

  11. Snoeck CJ, Adeyanju AT, Owoade AA, Couacy-Hymann E, Alkali BR, Ottosson U, Muller CP (2013) Genetic diversity of Newcastle disease virus in wild birds and pigeons in West Africa. Appl Environ Microbiol 79:7867–7874

    Article  CAS  Google Scholar 

  12. Kaleta EF, Baldauf C (1988) Newcastle disease in free-living and pet birds. Newcastle disease. Springer, Boston, pp 197–246

    Chapter  Google Scholar 

  13. Miller PJ, Koch G (2013) Newcastle disease. Dis Poult 13:89–138

    Google Scholar 

  14. Cardenas-Garcia S, Lopez RN, Morales R, Olvera MA, Marquez MA, Merino R, Miller PJ, Afonso CL (2013) Molecular epidemiology of Newcastle disease in Mexico: potential spillover of viruses from poultry into wild bird species. Appl Environ Microbiol 79:4985–4992

    Article  Google Scholar 

  15. Ayala AJ, Dimitrov KM, Becker CR, Goraichuk IV, Arns CW, Bolotin VI, Ferreira HL, Gerilovych AP, Goujgoulova GV, Martini MC, Muzyka DV, Orsi MA, Scagion GP, Silva RK, Solodiankin OS, Stegniy BT, Miller PJ, Afonso CL (2016) Presence of vaccine-derived Newcastle disease viruses in wild birds. PLoS One 11(9):e0162484

    Article  Google Scholar 

  16. Dimitrov KM, Lee DH, Williams-Coplin D, Olivier TL, Miller PJ, Afonso CL (2016) Newcastle disease viruses causing recent outbreaks worldwide show unexpectedly high genetic similarity with historical virulent isolates from the 1940’s. J Clin Microbiol 54:1228–1235

    Article  CAS  Google Scholar 

  17. Vidanović D, Šekler M, Ašanin R, Milić N, Nišavić J, Petrović T, Savić V (2011) Characterization of velogenic Newcastle disease viruses isolated from dead wild birds in Serbia during 2007. J Wildl Dis 47(2):433–441

    Article  Google Scholar 

  18. Carrasco ADOT, Seki MC, de Freitas Raso T, Paulillo AC, Pinto AA (2008) Experimental infection of Newcastle disease virus in pigeons (Columba livia): Humoral antibody response, contact transmission and viral genome shedding. Vet Microbiol 129(1–2):89–96

    Article  CAS  Google Scholar 

  19. Kapczynski DR, Wise MG, King DJ (2006) Susceptibility and protection of naive and vaccinated racing pigeons (Columbia livia) against exotic Newcastle disease virus from the California 2002–2003 outbreak. Avian Dis 50(3):336–341

    Article  Google Scholar 

  20. Ramey AM, Reeves AB, Ogawa H, Ip HS, Imai K, Bui VN, Yamaguchi E, Silko NY, Afonso CL (2013) Genetic diversity and mutation of avian paramyxovirus serotype 1 (Newcastle disease virus) in wild birds and evidence for intercontinental spread. Arch Virol 158(12):2495–2503

    Article  CAS  Google Scholar 

  21. Stanislawek WL, Wilks CR, Meers J, Horner GW, Alexander DJ, Manvell RJ, Kattenbelt JA, Gould AR (2002) Avian paramyxoviruses and influenza viruses isolated from mallard ducks (Anas platyrhynchos) in New Zealand. Arch Virol 147(7):1287–1302

    Article  CAS  Google Scholar 

  22. Banerjee M, Reed WM, Fitzgerald SD, Panigrahy B (1994) Neurotropic velogenic Newcastle disease in cormorants in Michigan: pathology and virus characterization. Avian Dis 38(4):873–878

    Article  CAS  Google Scholar 

  23. Ducatez MF, Olinger CM, Owoade AA, Tarnagda Z, Tahita MC, Sow A, De Landtsheer S, Ammerlaan W, Oudraogo JB, Osterhaus ADME, Fouchier RAM, Muller CP (2007) Molecular and antigenic evolution and geographical spread of H5N1 highly pathogenic avian influenza viruses in western Africa. J General Virol 88(8):2297–2306

    Article  CAS  Google Scholar 

  24. Musa U, Abdu PA, Dafwang II, Umoh JU, Saidu L, Mera UM, Edache JA (2009) Seroprevalence, seasonal occurrence and clinical manifestation of Newcastle disease in rural household chickens in Plateau State, Nigeria. Int J Poult Sci 8(2):200–204

    Article  Google Scholar 

  25. Sa’idu L, Abdu PA (2008) Outbreak of Viscerotropic Velogenic form of Newcastle dis-ease in vaccinated six weeks old pullets. Sokoto J Vet Sci 7(1):37–40

    Google Scholar 

  26. Barre J, Delor V (2004) Newcastle disease in wildlife (unpublished document)

  27. Heckert FLR (2007) Newcastle disease and related avian paramyxoviruses. In: Thomas NJ, Hunterand DB, Atkinson CT (eds) Infectious diseases of wild birds. Blackwell Publishing, Oxford, pp 3–16

    Google Scholar 

  28. Cappelle J, Caron A, De Almeida RS, Gil P, Pedrono M, Mundava J, Fofana B, Balanca G, Dakouo M, Ould El Mamy AB, Abolnik C, Maminiaina OF, Cumming GS, De Visscher MN, Albina E, Chevalier V, Gaidet N (2015) Empirical analysis suggests continuous and homogeneous circulation of Newcastle disease virus in a wide range of wild bird species in Africa. Epidemiol Infect 143(6):1292–1303

    Article  CAS  Google Scholar 

  29. Miguel E, Grosbois V, Berthouly-Salazar C, Caron A, Cappelle J, Roger F (2013) A meta-analysis of observational epidemiological studies of Newcastle disease in African agro-systems, 1980–2009. Epidemiol Infect 141(6):1117–1133

    Article  CAS  Google Scholar 

  30. Spackman E, Senne DA, Myers TJ, Bulaga LL, Garber LP, Perdue ML, Lohman K, Daum LT, Suarez DL (2002) Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol 40(9):3256–3260

    Article  CAS  Google Scholar 

  31. Ibu OJ, Okoye JOA, Adulugba EP, Chah KF, Shoyinka SVO, Salihu E, Chukwuedo AA, Baba SS (2009) Prevalence of Newcastle disease virus in wild and captive birds in Central Nigeria. Int J Poult Sci 8(6):574–578

    Article  Google Scholar 

  32. Dimitrov KM, Sharma P, Volkening JD, Goraichuk IV, Wajid A, Rehmani SF, Basharat A, Shittu I, Joannis T, Miller PJ, Afonso CL (2017) A robust and cost-effective approach to sequence and analyze complete genomes of small RNA viruses. Virol J 14(1):72

    Article  Google Scholar 

  33. Dimitrov KM, Bolotin V, Muzyka D, Goraichuk IV, Solodiankin O, Gerilovych A, Stegniy B, Goujgoulova GV, Silko NY, Pantin-Jackwood MJ, Miller PJ, Afonso CL (2016) Repeated isolation of virulent Newcastle disease viruses of sub-genotype VIId from backyard chickens in Bulgaria and Ukraine between 2002 and 2013. Arch Virol 161(12):3345–3353

    Article  CAS  Google Scholar 

  34. Miller PJ, Dimitrov KM, Williams-Coplin D, Peterson MP, Pantin-Jackwood MJ, Swayne DE, Suarez DL, Afonso CL (2015) International biological engagement programs facilitate Newcastle disease epidemiological studies. Front Public Health 3:235

    Article  Google Scholar 

  35. Abolnik C, de Castro M, Rees J (2012) Full genomic sequence of an African Avian Paramyxovirus Type 4 strain isolated from a wild duck. Virus Genes 45:537–541

    CAS  PubMed  Google Scholar 

  36. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2017) GenBank. Nucleic Acids Res 45:D37–D42

    Article  CAS  Google Scholar 

  37. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  Google Scholar 

  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0

  39. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    Article  CAS  Google Scholar 

  40. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313

    Article  CAS  Google Scholar 

  41. Rambaut A, Drummond A (2012) FigTree: tree figure drawing tool, v1. 4.2. Institute of Evolutionary Biology, University of Edinburgh

  42. Diel DG, da Silva LH, Liu H, Wang Z, Miller PJ, Afonso CL (2012) Genetic diversity of avian paramyxovirus type 1: proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12(8):1770–1779

    Article  Google Scholar 

  43. Taylor TL, Dimitrov KM, Afonso CL (2017) Genome-wide analysis reveals class and gene specific codon usage adaptation in avian paramyxoviruses 1. Infect Genet Evol 50:28–37

    Article  CAS  Google Scholar 

  44. Xia X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30(7):1720–1728

    Article  CAS  Google Scholar 

  45. Xia X (2007) An improved implementation of codon adaptation index. Evolut Bioinform 3:117693430700300028

    Google Scholar 

  46. Sharp PM, Li WH (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295

    Article  CAS  Google Scholar 

  47. Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87(1):23–29

    Article  CAS  Google Scholar 

  48. Alexander DJ, Swayne DE (1998) Newcastle disease virus and other avian paramyxoviruses. In: Swayne DE, Glisson JR, Jackwood MW, Pearson JE, Reed WM (eds) A Laboratory Manual for the Isolation and Identification of Avian Pathogens. The American Association of Avian Pathologists, Kennett Square, pp 156–163

    Google Scholar 

  49. BirdLife International (2018) Gyps africanus. The IUCN red list of threatened species 2018: http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22695189A126667006.en. Accessed 30 Jan 2019

  50. Snoeck CJ, Adeyanju AT, Owoade AA, Couacy-Hymann E, Alkali BR, Ottosson U, Muller CP (2013) Genetic diversity of Newcastle disease virus in wild birds and pigeons in West Africa. Appl Environ Microbiol 79:7867–7874

    Article  CAS  Google Scholar 

  51. Sabra M, Dimitrov KM, Goraichuk IV, Wajid A, Sharma P, Williams-Coplin D, Basharat A, Rehmani SF, Muzyka DV, Miller PJ, Afonso CL (2017) Phylogenetic assessment reveals continuous evolution and circulation of pigeon-derived virulent avian avulaviruses 1 in Eastern Europe, Asia, and Africa. BMC Vet Res 13(1):291

    Article  Google Scholar 

  52. Schelling E, Thur B, Griot C, Audige L (1999) Epidemiological study of Newcastle disease in backyard poultry and wild bird populations in Switzerland. Avian Pathol 28(3):263–272

    Article  CAS  Google Scholar 

  53. Ameji ON, Saidu L, Abdu PA (2015) Newcastle disease antibodies in apparently healthy wild birds in Kogi State, Nigeria. Res J Vet Sci 8:52–60

    Article  CAS  Google Scholar 

  54. Khalafalla AI, Hajer I, Nimir AH (1990) Role of some Passeriformes birds in transmission of Newcastle disease II Pathogenesis of Newcastle disease virus in Sudan house sparrows (Passer domesticus arborius). Bull Animal Health Prod Africa 38(1):51–54

    Google Scholar 

  55. Zhu W, Dong J, Xie Z, Liu Q, Khan MI (2010) Phylogenetic and pathogenic analysis of Newcastle disease virus isolated from house sparrow (Passer domesticus) living around poultry farm in southern China. Virus Genes 40(2):231–235

    Article  Google Scholar 

  56. Wehmann E, Czegledi A, Werner O, Kaleta EF, Lomniczi B (2003) Occurrence of genotypes IV, V, VI and VIIa in Newcastle disease outbreaks in Germany between 1939 and 1995. Avian Pathol 32:157–163

    Article  Google Scholar 

  57. Adene DF (2004) An integrated rural poultry improvement scheme. Poultry health and production, principles and practices. Stirling Horden Publishers, Ibadan, pp 280–284

    Google Scholar 

  58. Soos C, Padilla L, Iglesias A, Gottdenker N, Bédon MC, Rios A, Parker PG (2008) Comparison of pathogens in broiler and backyard chickens on the Galapagos Islands: implications for transmission to wildlife. Auk 125(2):445–455

    Article  Google Scholar 

  59. Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK, Swayne DE (2008) Diseases of Poultry, 12th edn. Blackwell Publishing, Iowa

    Google Scholar 

Download references

Acknowledgements

We want to thank the staff of the Central Diagnostic Laboratory /Regional Laboratory NVRI Vom and surveillance officers in the State and Federal Ministries of Agriculture, Nigeria. This research was supported by the Agricultural Research Service (ARS) and supported by the USDA Current Research Information System (CRIS) (number 6612-32000-072-00D) and partially funded by The Defense Threat Reduction Agency (DTRA) (FRCALL12-6-2-0015).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudio L. Afonso.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by William G Dundon.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Maximum composite likelihood tree with no collapsed branches, constructed using complete fusion gene coding sequences. Genotypes and subgenotypes of viruses are presented with Roman numerals and lowercase letters in each taxon name. (PDF 134 kb)

Online Resource 2

Maximum composite likelihood tree constructed using complete genome coding sequences. Genotypes and subgenotypes of viruses are presented with Roman numerals and lowercase letters in each taxon name. Red lettering indicates viruses sequenced for this study. (PDF 60 kb)

Online Resource 3

List of sequences used for the maximum composite likelihood tree constructed using complete fusion gene coding sequences (Fig. 2, Online Resource 1). Isolates indicated in bold were sequenced for this study. (PDF 164 kb)

Online Resource 4

List of sequences used for the maximum composite likelihood tree constructed using complete gene coding sequences (Online Resource 2). Isolates indicated in bold were sequenced for this study. (PDF 74 kb)

Online Resource 5

Complete genome relative synonymous codon usage (RSCU) values among poultry and wild bird viruses. (PDF 101 kb)

Online Resource 6

Number of codons used in the reference Gallus gallus dataset as implemented in DAMBE. (PDF 9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Welch, C.N., Shittu, I., Abolnik, C. et al. Genomic comparison of Newcastle disease viruses isolated in Nigeria between 2002 and 2015 reveals circulation of highly diverse genotypes and spillover into wild birds. Arch Virol 164, 2031–2047 (2019). https://doi.org/10.1007/s00705-019-04288-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-019-04288-9

Navigation