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Co-infection of Newcastle disease virus genotype XIII with low pathogenic avian influenza exacerbates clinical outcome of Newcastle disease in vaccinated layer poultry flocks

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Abstract

Newcastle disease (ND) and avian influenza (AI) are economically important infectious diseases of poultry. Sometime, concomitant secondary viral/or bacterial infections significantly alters the pathobiology of ND and AI in poultry. As of now, the disease patterns and dynamics of co-infections caused by ND virus (NDV, genotype XIII) and Low Pathogenic AI viruses (LPAI, H9N2) are explicitly elusive. Thus, we examined the clinicopathological disease conditions due to these two economically important viruses to understand the complex disease outcomes by virus–virus interactions in vaccinated flocks. The findings of clinicopathological and molecular investigations carried on 37 commercial ND vaccinated poultry flocks revealed simultaneous circulation of NDV and AIV in same flock/bird. Further, molecular characterization of hemagglutinin (HA) and neuraminidase (NA) genes confirmed that all the identified AIVs were of low pathogenicity H9N2 subtype and fusion (F) gene analysis of detected NDVs belong to NDV class II, genotype XIII, a virulent type. The NDV and H9N2 alone or co-infected flocks (NDV + LPAI) exhibit clinical signs and lesions similar to that of virulent NDV except the degree of severity, which was higher in H9N2–NDV co-infected flocks. Additionally, avian pathogenic E. coli and mycoplasma infections were detected in majority of the ailing/dead birds from the co-infected flocks during progression of the clinical disease. Overall, the findings highlight the multi-factorial disease complexity in commercial poultry and suggest the importance of NDV genotype XIII in intensifying the clinical disease in vaccinated birds.

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Availability of data and materials

All reported data has been submitted to the public domain of NCBI and are accessible under accession numbers; HG 780865, HG 780863, HG 780864, HG 780866, HG 780860, HG780862, HG780869,HG 780867,HG 780868,CY 099356, CY 099357, CY 099363 and CY 099347.

References

  1. Ahmed Z, Pandurang G, Acharya RS, Parihar NS. A report on outbreaks of respiratory disease in chicken in andhra pradesh with particular reference to infectious laryngotracheitis. Indian Vet J. 1969;46:646–50.

    CAS  PubMed  Google Scholar 

  2. Akhtar S, Muneer M, Muhammad K, Tibu M, Anees M, Rasid I, Rehman R, Hussain I. Molecular characterization and epitope mapping of fusion (F) and hemagglutinin (HN) genes of avian paramyxovirus serotype I from peacocks in Pakistan. Pak J Zool. 2017;49:755–9.

    Article  CAS  Google Scholar 

  3. Al-Mohana A, Kadhimv H, Al-Charrakh A, Al-Habubi Z, Nasir F, Al-Hilali A, Hadi Z. Molecular diagnosis of avian respiratory diseases in commercial broiler chicken flocks in province of Najaf, Iraq. Sci Res Essays. 2013;8:1191–5.

    Google Scholar 

  4. Bano S, Naeem K, Malik SA. Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens. Avian Dis. 2003;47:817–22.

    Article  CAS  PubMed  Google Scholar 

  5. Bradbury JM. Avian mycoplasma infections: prototype of mixed infections with mycoplasmas, bacteria and viruses. Ann Microbiol (Paris). 1984;135A:83–9.

    CAS  Google Scholar 

  6. Capua I, Alexander DJ. Avian influenza: recent developments. Avian Pathol J WVPA. 2004;33:393–404.

    Article  Google Scholar 

  7. Costa-Hurtado M, Afonso CL, Miller PJ, Spackman E, Kapczynski DR, Swayne DE, Shepherd E, Smith D, Zsak A, Pantin-Jackwood M. Virus interference between H7N2 low pathogenic avian influenza virus and lentogenic Newcastle disease virus in experimental co-infections in chickens and turkeys. Vet Res. 2014;45:1.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Diel G, da Silva LHA, Liu H, Wang Z, Miller PJ, Afonso CL. Genetic diversity of avian paramyxovirus type 1: proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2012;12:1770–9.

    Google Scholar 

  9. Dormitorio TV, Giambrone JJ, Guo K, Hepp GR. Detection and characterization of avian influenza and other avian paramyxoviruses from wild waterfowl in parts of the southeastern United States. Poult Sci. 2009;88:851–5.

    Article  CAS  PubMed  Google Scholar 

  10. El Zowalaty ME, Chander Y, Redig PT, Abd El Latif HK, El Sayed MA, Goyal SM. Selective isolation of avian influenza virus (AIV) from cloacal samples containing AIV and Newcastle disease virus. J Vet Diagn Investig. 2011;23:330–2.

    Article  Google Scholar 

  11. França M, Howerth EW, Carter D, Byas A, Poulson R, Afonso CL, Stallknecht DE. Co-infection of mallards with low-virulence Newcastle disease virus and low-pathogenic avian influenza virus. Avian Pathol J WVPA. 2014;43:96–104.

    Article  Google Scholar 

  12. Glisson J, Jackwood M, Pearson J, Reed W, Swayne D, Woolcock P. Isolation, identification, and characterization of avian pathogens. 5th ed. Jacksonville: American Association of Avian Pathologists; 2008.

    Google Scholar 

  13. Goekjian VH, Smith JT, Howell DL, Senne DA, Swayne DE, Stallknecht DE. Avian influenza viruses and avian paramyxoviruses in wintering and breeding waterfowl populations in North Carolina, USA. J Wildl Dis. 2011;47:240–5.

    Article  PubMed  Google Scholar 

  14. Gowthaman V. 2011. Etio-pathology and differential diagnosis of low pathogenic avian influenza (LPAI) in poultry. Ph.D. thesis, Indian Veterinary Research Institute.

  15. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.

    Article  CAS  PubMed  Google Scholar 

  16. Haghighat-Jahromi M, Asasi K, Nili H, Dadras H, Shooshtari AH. Coinfection of avian influenza virus (H9N2 subtype) with infectious bronchitis live vaccine. Arch Virol. 2008;153:651–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol. 2001;146:2275–89.

    Article  CAS  PubMed  Google Scholar 

  18. Jakhesara SJ, Prasad VVSP, Pal JK, Jhala MK, Prajapati KS, Joshi CG. Pathotypic and sequence characterization of Newcastle disease viruses from vaccinated chickens reveals circulation of genotype II, IV and XIII and in India. Transbound Emerg Dis. 2014;63:523.

    Article  PubMed  CAS  Google Scholar 

  19. Jeong J, Kim Y, An I, Wang S-J, Kim Y, Lee H-J, Choi K-S, Im S-P, Min W, Oem J-K, Jheong W. Complete genome sequence of a novel avian paramyxovirus isolated from wild birds in South Korea. Arch Virol. 2018;163:223–7.

    Article  CAS  PubMed  Google Scholar 

  20. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol. 2006;6:29.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Khorajiya JH, Pandey S, Ghodasara PD, Joshi BP, Prajapati KS, Ghodasara DJ, Mathakiya RA. Patho-epidemiological study on Genotype-XIII Newcastle disease virus infection in commercial vaccinated layer farms. Vet World. 2015;8:372–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kishida N, Sakoda Y, Eto M, Sunaga Y, Kida H. Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens. Arch Virol. 2004;149:2095–104.

    Article  CAS  PubMed  Google Scholar 

  23. Kotani T, Odagiri Y, Nakamura J, Horiuchi T. Pathological changes of tracheal mucosa in chickens infected with lentogenic Newcastle disease virus. Avian Dis. 1987;31:491–7.

    Article  CAS  PubMed  Google Scholar 

  24. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lee D-H, Park J-K, Yuk S-S, Erdene-Ochir T-O, Kwon J-H, Lee J-B, Park S-Y, Choi I-S, Lee S-W, Song C-S. Complete genome sequence of a natural reassortant H9N2 avian influenza virus found in bean goose (Anser fabalis): direct evidence for virus exchange between Korea and China via wild birds. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2014;26:250–4.

    CAS  Google Scholar 

  26. Luna L. Manual on histologic staining methods of the armed force institute of pathology. 3rd ed. New York City: McGraw-Hill Book Co; 1968. p. 32–46.

    Google Scholar 

  27. Malik BS, Verma KC. Coexistence of antibodies against chronic respiratory disease, infectious laryngotracheitis, and infectious bronchitis on poultry farms of Uttar Pradesh, Andhra Pradesh, and Madras. Avian Dis. 1969;13:695–9.

    Article  CAS  PubMed  Google Scholar 

  28. Mast J, Nanbru C, van den Berg T, Meulemans G. Ultrastructural changes of the tracheal epithelium after vaccination of day-old chickens with the La Sota strain of Newcastle disease virus. Vet Pathol. 2005;42:559–65.

    Article  CAS  PubMed  Google Scholar 

  29. Mendoza-Espinoza A, Koga Y, Zavaleta AI. Amplified 16S ribosomal DNA restriction analysis for identification of Avibacterium paragallinarum. Avian Dis. 2008;52:54–8.

    Article  PubMed  Google Scholar 

  30. Miller PJ, Haddas R, Simanov L, Lublin A, Rehmani SF, Wajid A, Bibi T, Khan TA, Yaqub T, Setiyaningsih S, Afonso CL. Identification of new sub-genotypes of virulent Newcastle disease virus with potential panzootic features. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2015;29:216–29.

    Google Scholar 

  31. Mo IP, Brugh M, Fletcher OJ, Rowland GN, Swayne DE. Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity. Avian Dis. 1997;41:125–36.

    Article  CAS  PubMed  Google Scholar 

  32. Nath B, Kumar S. Emerging variant of genotype XIII Newcastle disease virus from Northeast India. Acta Trop. 2017;172:64–9.

    Article  PubMed  Google Scholar 

  33. Nili H, Asasi K. Avian influenza (H9N2) outbreak in Iran. Avian Dis. 2003;47:828–31.

    Article  CAS  PubMed  Google Scholar 

  34. OIE. Avian mycoplasmosis. Manual of diagnostic tests and vaccines for terrestrial animals; 2008. pp. 482–496.

  35. OIE. Newcastle disease. Manual of diagnostic tests and vaccines for terrestrial animals, chapter 2314; 2012.

  36. Ottiger H-P. Development, standardization and assessment of PCR systems for purity testing of avian viral vaccines. Biol J Int Assoc Biol Stand. 2010;38:381–8.

    CAS  Google Scholar 

  37. Pan Q, Liu A, Zhang F, Ling Y, Ou C, Hou N, He C. Co-infection of broilers with Ornithobacterium rhinotracheale and H9N2 avian influenza virus. BMC Vet Res. 2012;8:104.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Roussan DA, Haddad R, Khawaldeh G. Molecular survey of avian respiratory pathogens in commercial broiler chicken flocks with respiratory diseases in Jordan. Poult Sci. 2008;87:444–8.

    Article  CAS  PubMed  Google Scholar 

  39. Seififi S, Asasi K, Mohammadi Ali. Natural co-infection caused by avian influenza H9 subtype and infectious bronchitis viruses in broiler chicken farms. Vet Arh. 2010;80:269–81.

    Google Scholar 

  40. Shalaby AA, Slemons RD, Swayne DE. Pathological studies of A/chicken/Alabama/7395/75 (H4N8) influenza virus in specific-pathogen-free laying hens. Avian Dis. 1994;38:22–32.

    Article  CAS  PubMed  Google Scholar 

  41. Siddique N, Naeem K, Abbas MA, Ali Malik A, Rashid F, Rafique S, Ghafar A, Rehman A. Sequence and phylogenetic analysis of virulent Newcastle disease virus isolates from Pakistan during 2009–2013 reveals circulation of new sub genotype. Virology. 2013;444:37–40.

    Article  CAS  PubMed  Google Scholar 

  42. Smietanka K, Minta Z, Swiętoń E, Olszewska M, Jóźwiak M, Domańska-Blicharz K, Wyrostek K, Tomczyk G, Pikuła A. Avian influenza H9N2 subtype in Poland–characterization of the isolates and evidence of concomitant infections. Avian Pathol J WVPA. 2014;43:427–36.

    Article  CAS  Google Scholar 

  43. Spickler A, Roth J. Emerging and exotic diseases of animals. Ames: CFSPH Iowa State University; 2008. p. 203–4.

    Google Scholar 

  44. Susta L, Jones MEB, Cattoli G, Cardenas-Garcia S, Miller PJ, Brown CC, Afonso CL. Pathologic characterization of genotypes XIV and XVII Newcastle disease viruses and efficacy of classical vaccination on specific pathogen-free birds. Vet Pathol. 2015;52:120–31.

    Article  CAS  PubMed  Google Scholar 

  45. Tashiro M, Ciborowski P, Klenk HD, Pulverer G, Rott R. Role of Staphylococcus protease in the development of influenza pneumonia. Nature. 1987;325:536–7.

    Article  CAS  PubMed  Google Scholar 

  46. Terregino C, Aldous EW, Heidari A, Fuller CM, De Nardi R, Manvell RJ, Beato MS, Shell WM, Monne I, Brown IH, Alexander DJ, Capua I. Antigenic and genetic analyses of isolate APMV/wigeon/Italy/3920-1/2005 indicate that it represents a new avian paramyxovirus (APMV-12). Arch Virol. 2013;158:2233–43.

    Article  CAS  PubMed  Google Scholar 

  47. Toyoda T, Sakaguchi T, Hirota H, Gotoh B, Kuma K, Miyata T, Nagai Y. Newcastle disease virus evolution. II. Lack of gene recombination in generating virulent and avirulent strains. Virology. 1989;169:273–82.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Authors are thankful to Indian Veterinary Research Institute and Indian Council of Agricultural Research for providing facilities and funds for carrying out the study.

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Correspondence to V. Gowthaman.

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Gowthaman, V., Singh, S.D., Dhama, K. et al. Co-infection of Newcastle disease virus genotype XIII with low pathogenic avian influenza exacerbates clinical outcome of Newcastle disease in vaccinated layer poultry flocks. VirusDis. 30, 441–452 (2019). https://doi.org/10.1007/s13337-019-00533-6

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