Home / Regular Issue / JST Vol. 46 (2) May. 2023 / JTAS-2552-2022

 

Isolation and Characterization of Avian Coronavirus from Diagnostic Cases of Selected Bird Species in Malaysia

Sarenasulastri Awang Besar, Siti Suri Arshad, Siti Zubaidah Ramanoon and Abdul Rahman Omar

Pertanika Journal of Science & Technology, Volume 46, Issue 2, May 2023

DOI: https://doi.org/10.47836/pjtas.46.2.08

Keywords: Avian coronavirus, diagnostic cases, gammacoronavirus, IBV vaccine strain, selected bird species

Published on: 16 May 2023

Infectious bronchitis virus (IBV) in chicken (Gallus gallus) is the most common and well-studied Avian coronavirus (ACoV) in avian species. The study aims to molecularly characterize ACoV isolate of selected bird species other than chicken obtained from the archived samples of field diagnostic cases in the Northern Zone Veterinary Laboratory (MVZU), Malaysia. Twelve archived virus isolates from 2013 to 2019 were amplified using selected primers on the 3’ UTR gene and S1 gene for oligonucleotide sequencing. These sequences were then molecularly characterized and compared with common IBV strains in chicken to determine the genetic diversity of the virus among selected avian species. Subsequent analyses of the nucleotides amplified on 3’ UTR conserved region of 12 selected ACoVs isolates originating from peacocks (Pavo cristatus), turkey (Meleagris), jungle fowl (Gallus gallus spadiceous), guinea fowl (Meleagris gallopavo domesticus), goose (Anser anser domesticus), love bird (Agapornis), macaw (Ara macao), and bird (species unidentified) are classified as belonging to the gammacoronavirus (Gamma-CoV) genus and have a high degree of homology. The S1 complete gene sequence analyses of guinea fowl and jungle fowl showed that both ACoV isolates are Gamma-CoV and under genotype I and GI-13 lineages. Both are identified as having a high similarity of 98% and 99%, respectively, with IBV vaccine strain 4/91 (AF093793). Due attention should be given to ACoVs strains, especially the IBV vaccine strains detected in other bird species, because there is a high probability that other bird species could be the source of pathogenic ACoV infection in general and IBV infection in chickens, as reported in other countries.

  • Adzhar, A., Shaw, K., Britton, P., & Cavanagh, D. (1996). Universal oligonucleotides for the detection of infectious bronchitis virus by the polymerase chain reaction. Avian Pathology, 25(4), 817–36. https://doi.org/10.1080/03079459608419184.

  • Bande, F., Arshad, S. S., Omar, A. R., Bejo, M. H., Abubakar, M. S., & Abba, Y. (2016). Pathogenesis and diagnostic approaches of avian infectious bronchitis. Advances in Virology, 2016, 4621659. https://doi.org/10.1155/2016/4621659

  • Cavanagh, D., Mawditt, K., Sharma, M., Drury, S. E., Ainsworth, H. L., Britton, P., & Gough, R. E. (2001). Detection of a coronavirus from turkey poults in Europe genetically related to infectious bronchitis virus of chickens. Avian Pathology, 30(4), 355-368. https://doi.org/10.1080/03079450120066368

  • Cavanagh, D., Mawditt, K., Welchman, D. D. B., Britton, P., & Gough, R. E. (2002). Coronaviruses from pheasants (Phasianus colchicus) are genetically closely related to coronaviruses of domestic fowl (infectious bronchitis virus) and turkeys. Avian Pathology, 31(1), 81-93. https://doi.org/10.1080/03079450120106651

  • Chamings, A., Nelson, T. M., Vibin, J., Wille, M., Klaassen, M., & Alexandersen, S. (2018). Detection and characterisation of coronaviruses in migratory and non-igratory Australian wild birds. Scientific Report, 8, 5980. https://doi.org/10.1038/s41598-018-24407-x

  • Cook, J. K., Jackwood, M., & Jones, R. C. (2012). The long view: 40 years of infectious bronchitis research. Avian Pathology, 41(3), 239–250. https://doi.org/10.1080/03079457.2012.680432

  • de Wit, J. J., & Cook, J. K. A. (2020). Spotlight on Avian coronaviruses. Avian Pathology, 49(4), 313–316. https://doi.org/10.1080/03079457.2020.1761010

  • Encyclopedia Britannica. (n.d.). Guinea fowl. https://www.britannica.com/animal/guinea-fowl

  • Felippe, P. A. N., da Silva, L. H. A., Santos, M. M. A. B., Spilki, F. R., & Arns, C. W. (2010). Genetic diversity of avian infectious bronchitis virus isolated from domestic chicken flocks and coronaviruses from feral pigeons in Brazil between 2003 and 2009. Avian Diseases, 54(4), 1191-1196. https://doi.org/10.1637/9371-041510-Reg.1

  • Guzmán, M., & Hidalgo, H. (2020). Live attenuated infectious bronchitis virus vaccines in poultry: Modifying local viral populations dynamics. Animals, 10(11), 2058. https://doi.org/10.3390/ani10112058

  • Hughes, L. A., Savage, C., Naylor, C., Bennett, M., Chantrey, J., & Jones, R. (2009). Genetically diverse coronaviruses in wild bird populations of northern England. Emerging Infectious Diseases, 15(7), 1091–1094. https://doi.org/10.3201/eid1507.090067

  • Ismail, M. I. (2019). Molecular characterisation and pathogenicity evaluation of attenuated Malaysian strains of infectious bronchitis virus [Doctoral dissertation, Universiti Putra Malaysia]. Universiti Putra Malaysia Institutional Repository. http://psasir.upm.edu.my/id/eprint/90484/

  • Ismail, M. I., Tan, S. W., Hair-Bejo, M., & Omar, A. R. (2020). Evaluation of the antigen relatedness and efficacy of a single vaccination with different infectious bronchitis virus strains against a challenge with Malaysian variant and QX-like IBV strains. Journal of Veterinary Science, 21(6), e76. https://doi.org/10.4142/jvs.2020.21.e76

  • Khanh, N. P., Tan, S. W., Yeap, S. K., Satharasinghe, D. A., Bejo, M. H., Bich, T. N., & Omar, A. R. (2017). Molecular characterization of QX-like and variant infectious bronchitis virus strains in Malaysia based on partial genomic sequences comprising the S-3a/3b-E-M-intergenic region-5a/5b-N gene order. Avian Diseases, 61(4), 442-452. https://doi.org/10.1637/11637-032817-Reg.1

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096

  • Legnardi, M., Tucciarone, C. M., Franzo, G., & Cecchinato, M. (2020). Infectious bronchitis virus evolution, diagnosis and control. Veterinary Sciences, 7(2), 79. https://doi.org/10.3390/vetsci7020079

  • Leow, B. L., Syamsiah Aini, S., Faizul Fikri, M. Y., Muhammad Redzwan, S., Khoo, C. K., Ong, G. H., Basirah, M. A., Norazura, B., Mazaitul, Z., Mohd Khairil, A., Mohd Jihan, R., Sohayati, A. R., & Chandrawathani, P. (2018). Molecular characterization of avian infectious bronchitis virus isolated in Malaysia during 2014-2016. Tropical Biomedicine, 35(4), 1092–1106.

  • Liu, S., Chen, J., Chen, J., Kong, X., Shao, Y., Han, Z., Feng, L., Cai, X., Gu, S., & Liu, M. (2005). Isolation of avian infectious bronchitis coronavirus from domestic peafowl (Pavo cristatus) and teal (Anas). Journal of General Virology, 86(3), 719-725. https://doi.org/10.1099/vir.0.80546-0

  • Lu, R., Zhao, X., Li, J., Niu, P., Yang, B., Wu, H., Wang, W., Song, H., Huang, B., Zhu, N., Bi, Y., Ma, X., Zhan, F., Wang, L., Hu, T., Zhou, H., Hu, Z., Zhou, W., Zhao, L., …Tan, W. (2020). Genomic characterisation and epidemiology of 2019 novel coronavirus: Implications for virus origins and receptor binding. The Lancet, 395(10224), 565-574. https://doi.org/10.1016/S0140-6736(20)30251-8

  • Muradrasoli, S., Bálint, Á., Wahlgren, J., Waldenström, J., Belák, S., Blomberg, J., & Olsen, B. (2010). Prevalence and phylogeny of coronaviruses in wild birds from the Bering Strait area (Beringia). PLOS One, 5(10), e13640. https://doi.org/10.1371/journal.pone.0013640

  • Okonechnikov, K., Golosova, O., Fursov, M. & the UGENE team (2012). Unipro UGENE: A unified bioinformatics toolkit. Bioinformatics, 28(8), 1166-1167. https://doi.org/10.1093/bioinformatics/bts091

  • Parkhe, P., & Verma, S. (2021). Evolution, interspecies transmission, and zoonotic significance of animal coronaviruses. Frontiers in Veterinary Science, 8, 719834. https://doi.org/10.3389/fvets.2021.719834

  • Promkuntod N. (2016). Dynamics of Avian coronavirus circulation in commercial and non-commercial birds in Asia - A review. The Veterinary Quarterly, 36(1), 30–44. https://doi.org/10.1080/01652176.2015.1126868

  • Sun, L., Zhang, G. H., Jiang, J. W., Fu, J. D., Ren, T., Cao, W. S., Xin, C. A., Liao, M.& Liu, W. J. (2007). A Massachusetts prototype like coronavirus isolated from wild peafowls is pathogenic to chickens. Virus Research, 130(1-2), 121-128. https:/doi.org/10.1016/j.virusres.2007.06.003

  • Suryaman, G. K., Soejoedono, R. D., Setiyono, A., Poetri, O. N., & Handharyani, E. (2019). Isolation and characterization of Avian coronavirus from healthy Eclectus parrots (Eclectus roratus) from Indonesia. Veterinary World, 12(11), 1797-1805. https://doi.org/10.14202/vetworld.2019.1797-1805

  • Syahar, A. A. G., Zakaria, M. H., Zuki, A. B. Z., Lokman, H. I., & Mazlina, M. (2014). The existence of red jungle fowls (Gallus gallus) in oil palm plantation selected states in Malaysia and their morphological characteristics. Malaysian Journal of Veterinary Research, 26(2), 38-40.

  • Valastro, V., Holmes, E. C., Britton, P., Fusaro, A., Jackwood, M. W., Cattoli, G., & Monne, I. (2016). S1 gene-based phylogeny of infectious bronchitis virus: An attempt to harmonize virus classification. Infection, Genetics and Evolution, 39, 349–364. https://doi.org/10.1016/j.meegid.2016.02.015

  • World Organisation for Animal Health. (2018). Manual of diagnostic tests and vaccines for terrestrial animals (Chapter 3.3.2). WOAH.

  • Zhou, Z., Qiu, Y., & Ge, X. (2021). The taxonomy, host range and pathogenicity of coronaviruses and other viruses in the Nidovirales order. Animal Diseases, 1, 5. https://doi.org/10.1186/s44149-021-00005-9

  • Zulperi, Z. M., Omar, A. R., & Arshad, S. S. (2009). Sequence and phylogenetic analysis of S1, S2, M, and N genes of infectious bronchitis virus isolates from Malaysia. Virus Genes, 38, 383–391. https://doi.org/10.1007/s11262-009-0337-2

  • Adzhar, A., Shaw, K., Britton, P., & Cavanagh, D. (1996). Universal oligonucleotides for the detection of infectious bronchitis virus by the polymerase chain reaction. Avian Pathology, 25(4), 817–36. https://doi.org/10.1080/03079459608419184.

  • Bande, F., Arshad, S. S., Omar, A. R., Bejo, M. H., Abubakar, M. S., & Abba, Y. (2016). Pathogenesis and diagnostic approaches of avian infectious bronchitis. Advances in Virology, 2016, 4621659. https://doi.org/10.1155/2016/4621659

  • Cavanagh, D., Mawditt, K., Sharma, M., Drury, S. E., Ainsworth, H. L., Britton, P., & Gough, R. E. (2001). Detection of a coronavirus from turkey poults in Europe genetically related to infectious bronchitis virus of chickens. Avian Pathology, 30(4), 355-368. https://doi.org/10.1080/03079450120066368

  • Cavanagh, D., Mawditt, K., Welchman, D. D. B., Britton, P., & Gough, R. E. (2002). Coronaviruses from pheasants (Phasianus colchicus) are genetically closely related to coronaviruses of domestic fowl (infectious bronchitis virus) and turkeys. Avian Pathology, 31(1), 81-93. https://doi.org/10.1080/03079450120106651

  • Chamings, A., Nelson, T. M., Vibin, J., Wille, M., Klaassen, M., & Alexandersen, S. (2018). Detection and characterisation of coronaviruses in migratory and non-igratory Australian wild birds. Scientific Report, 8, 5980. https://doi.org/10.1038/s41598-018-24407-x

  • Cook, J. K., Jackwood, M., & Jones, R. C. (2012). The long view: 40 years of infectious bronchitis research. Avian Pathology, 41(3), 239–250. https://doi.org/10.1080/03079457.2012.680432

  • de Wit, J. J., & Cook, J. K. A. (2020). Spotlight on Avian coronaviruses. Avian Pathology, 49(4), 313–316. https://doi.org/10.1080/03079457.2020.1761010

  • Encyclopedia Britannica. (n.d.). Guinea fowl. https://www.britannica.com/animal/guinea-fowl

  • Felippe, P. A. N., da Silva, L. H. A., Santos, M. M. A. B., Spilki, F. R., & Arns, C. W. (2010). Genetic diversity of avian infectious bronchitis virus isolated from domestic chicken flocks and coronaviruses from feral pigeons in Brazil between 2003 and 2009. Avian Diseases, 54(4), 1191-1196. https://doi.org/10.1637/9371-041510-Reg.1

  • Guzmán, M., & Hidalgo, H. (2020). Live attenuated infectious bronchitis virus vaccines in poultry: Modifying local viral populations dynamics. Animals, 10(11), 2058. https://doi.org/10.3390/ani10112058

  • Hughes, L. A., Savage, C., Naylor, C., Bennett, M., Chantrey, J., & Jones, R. (2009). Genetically diverse coronaviruses in wild bird populations of northern England. Emerging Infectious Diseases, 15(7), 1091–1094. https://doi.org/10.3201/eid1507.090067

  • Ismail, M. I. (2019). Molecular characterisation and pathogenicity evaluation of attenuated Malaysian strains of infectious bronchitis virus [Doctoral dissertation, Universiti Putra Malaysia]. Universiti Putra Malaysia Institutional Repository. http://psasir.upm.edu.my/id/eprint/90484/

  • Ismail, M. I., Tan, S. W., Hair-Bejo, M., & Omar, A. R. (2020). Evaluation of the antigen relatedness and efficacy of a single vaccination with different infectious bronchitis virus strains against a challenge with Malaysian variant and QX-like IBV strains. Journal of Veterinary Science, 21(6), e76. https://doi.org/10.4142/jvs.2020.21.e76

  • Khanh, N. P., Tan, S. W., Yeap, S. K., Satharasinghe, D. A., Bejo, M. H., Bich, T. N., & Omar, A. R. (2017). Molecular characterization of QX-like and variant infectious bronchitis virus strains in Malaysia based on partial genomic sequences comprising the S-3a/3b-E-M-intergenic region-5a/5b-N gene order. Avian Diseases, 61(4), 442-452. https://doi.org/10.1637/11637-032817-Reg.1

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096

  • Legnardi, M., Tucciarone, C. M., Franzo, G., & Cecchinato, M. (2020). Infectious bronchitis virus evolution, diagnosis and control. Veterinary Sciences, 7(2), 79. https://doi.org/10.3390/vetsci7020079

  • Leow, B. L., Syamsiah Aini, S., Faizul Fikri, M. Y., Muhammad Redzwan, S., Khoo, C. K., Ong, G. H., Basirah, M. A., Norazura, B., Mazaitul, Z., Mohd Khairil, A., Mohd Jihan, R., Sohayati, A. R., & Chandrawathani, P. (2018). Molecular characterization of avian infectious bronchitis virus isolated in Malaysia during 2014-2016. Tropical Biomedicine, 35(4), 1092–1106.

  • Liu, S., Chen, J., Chen, J., Kong, X., Shao, Y., Han, Z., Feng, L., Cai, X., Gu, S., & Liu, M. (2005). Isolation of avian infectious bronchitis coronavirus from domestic peafowl (Pavo cristatus) and teal (Anas). Journal of General Virology, 86(3), 719-725. https://doi.org/10.1099/vir.0.80546-0

  • Lu, R., Zhao, X., Li, J., Niu, P., Yang, B., Wu, H., Wang, W., Song, H., Huang, B., Zhu, N., Bi, Y., Ma, X., Zhan, F., Wang, L., Hu, T., Zhou, H., Hu, Z., Zhou, W., Zhao, L., …Tan, W. (2020). Genomic characterisation and epidemiology of 2019 novel coronavirus: Implications for virus origins and receptor binding. The Lancet, 395(10224), 565-574. https://doi.org/10.1016/S0140-6736(20)30251-8

  • Muradrasoli, S., Bálint, Á., Wahlgren, J., Waldenström, J., Belák, S., Blomberg, J., & Olsen, B. (2010). Prevalence and phylogeny of coronaviruses in wild birds from the Bering Strait area (Beringia). PLOS One, 5(10), e13640. https://doi.org/10.1371/journal.pone.0013640

  • Okonechnikov, K., Golosova, O., Fursov, M. & the UGENE team (2012). Unipro UGENE: A unified bioinformatics toolkit. Bioinformatics, 28(8), 1166-1167. https://doi.org/10.1093/bioinformatics/bts091

  • Parkhe, P., & Verma, S. (2021). Evolution, interspecies transmission, and zoonotic significance of animal coronaviruses. Frontiers in Veterinary Science, 8, 719834. https://doi.org/10.3389/fvets.2021.719834

  • Promkuntod N. (2016). Dynamics of Avian coronavirus circulation in commercial and non-commercial birds in Asia - A review. The Veterinary Quarterly, 36(1), 30–44. https://doi.org/10.1080/01652176.2015.1126868

  • Sun, L., Zhang, G. H., Jiang, J. W., Fu, J. D., Ren, T., Cao, W. S., Xin, C. A., Liao, M.& Liu, W. J. (2007). A Massachusetts prototype like coronavirus isolated from wild peafowls is pathogenic to chickens. Virus Research, 130(1-2), 121-128. https:/doi.org/10.1016/j.virusres.2007.06.003

  • Suryaman, G. K., Soejoedono, R. D., Setiyono, A., Poetri, O. N., & Handharyani, E. (2019). Isolation and characterization of Avian coronavirus from healthy Eclectus parrots (Eclectus roratus) from Indonesia. Veterinary World, 12(11), 1797-1805. https://doi.org/10.14202/vetworld.2019.1797-1805

  • Syahar, A. A. G., Zakaria, M. H., Zuki, A. B. Z., Lokman, H. I., & Mazlina, M. (2014). The existence of red jungle fowls (Gallus gallus) in oil palm plantation selected states in Malaysia and their morphological characteristics. Malaysian Journal of Veterinary Research, 26(2), 38-40.

  • Valastro, V., Holmes, E. C., Britton, P., Fusaro, A., Jackwood, M. W., Cattoli, G., & Monne, I. (2016). S1 gene-based phylogeny of infectious bronchitis virus: An attempt to harmonize virus classification. Infection, Genetics and Evolution, 39, 349–364. https://doi.org/10.1016/j.meegid.2016.02.015

  • World Organisation for Animal Health. (2018). Manual of diagnostic tests and vaccines for terrestrial animals (Chapter 3.3.2). WOAH.

  • Zhou, Z., Qiu, Y., & Ge, X. (2021). The taxonomy, host range and pathogenicity of coronaviruses and other viruses in the Nidovirales order. Animal Diseases, 1, 5. https://doi.org/10.1186/s44149-021-00005-9

  • Zulperi, Z. M., Omar, A. R., & Arshad, S. S. (2009). Sequence and phylogenetic analysis of S1, S2, M, and N genes of infectious bronchitis virus isolates from Malaysia. Virus Genes, 38, 383–391. https://doi.org/10.1007/s11262-009-0337-2