e-ISSN 2231-8542
ISSN 1511-3701
Bahiyah Azli, Nur Farhana Salim, Abdul Rahman Omar, Mohd Hair-Bejo, Norfitriah Mohamed Sohaimi and Nurulfiza Mat Isa
Pertanika Journal of Tropical Agricultural Science, Volume 46, Issue 3, August 2023
DOI: https://doi.org/10.47836/pjtas.46.3.15
Keywords: Adenovirus, FAdV, fibre, fowl adenovirus, hexon, inclusion body hepatitis, phylogenetic analysis, serotype
Published on: 30 August 2023
Fowl adenovirus (FAdV) is reported to pose a severe risk to the poultry industry, affecting food and nutrient security nationally and globally. FAdV is identified as the primary pathogen for inclusion body hepatitis (IBH) disease in avians during outbreaks in farms. Numerous interventions have been employed to reduce the chicken’s mortality rate in future outbreaks, such as local autogenous vaccine production that has yet to be successfully commercialised. Fibre and hexon protein are two out of the three major components of the adenoviral capsid, identified to contribute towards FAdV virulence. Hence, this study aims to determine the fibre and hexon gene molecular changes of a local isolate, FAdV UPMT1901, in Malaysia’s recent IBH outbreak and identify the evolutionary relationship with known FAdV strains. Propagation of FAdV UPMT1901 was performed in specific pathogen-free embryonated chicken prior to genomic extraction. The genes were amplified, and the retrieved nucleotide sequences were aligned with the published FAdV sequences. The phylogenetic tree analysis showed that UPMT1901 partial fibre and hexon genes are 99% similar to other known FAdV serotype 8b (FAdV-8b) species, especially the published Malaysian FAdV-8b isolates. Interestingly, the amino acid residue analysis further supported consistent residues amongst Malaysian isolates at fibre positions T176A, Q195H, D213E, S243T, A258V, F335Y, and F353V and hexon position T422M. These findings elucidate the structural proteins’ functional capacity and molecular diversity, specifically amongst Malaysian FAdV isolates and FAdV-8b, while contributing to global initiatives to establish biosecurity, such as a vaccine or antiviral production against future outbreaks.
Absalón, A. E., Morales-Garzón, A., Vera-Hernández, P. F., Cortés-Espinosa, D. V., Uribe-Ochoa, S. M., García, L. J., & Lucio-Decanini, E. (2017). Complete genome sequence of a non-pathogenic strain of Fowl Adenovirus serotype 11: Minimal genomic differences between pathogenic and non-pathogenic viruses. Virology, 501, 63–69. https://doi.org/10.1016/j.virol.2016.11.006
Ahmed, S. (2020). Development of a live attenuated vaccine against fowl adenovirus by mutating fiber gene using CRISPR-Cas9 technology [Doctoral thesis, Universiti Putra Malaysia]. Universiti Putra Malaysia Institutional Repository. http://psasir.upm.edu.my/id/eprint/92705/
Ahmed, S., Mariatulqabtiah, A. R., Bejo, M. H., Omar, A. R., Ideris, A., & Mat Isa, N. (2021). Molecular markers and phylogenetic analysis of UPMT27, a field isolate of the Malaysian fowl adenovirus associated with inclusion body hepatitis. Pertanika Journal of Science and Technology, 29(1), 547-563. https://doi.org/10.47836/pjst.29.1.29
Alzohairy, A. M. (2011). BioEdit: An important software for molecular biology. GERF Bulletin of Biosciences, 2(1), 60–61.
Butterworth, A., & Weeks, C. (2010). The impact of disease on welfare. In I. Duncan & P. Hawkins (Eds.), The welfare of domestic fowl and other captive birds (Vol. 9, pp. 189–218). Springer. https://doi.org/10.1007/978-90-481-3650-6_8
Cizmecigil, U. Y., Umar, S., Yilmaz, A., Bayraktar, E., Turan, N., Tali, B., Aydin, O., Tali, H. E., Yaramanoglu, M., Yilmaz, S. G., Kolukisa, A., Sadeyen, J.-R., Iqbal, M., & Yilmaz, H. (2020). Characterisation of fowl adenovirus (FAdV-8b) strain concerning the geographic analysis and pathological lesions associated with inclusion body hepatitis in broiler flocks in Turkey. Journal of Veterinary Research, 64(2), 231–237. https://doi.org/10.2478/jvetres-2020-0026
Conesa, A., Götz, S., García-Gómez, J. M., Terol, J., Talón, M., & Robles, M. (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18), 3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Crawford-Miksza, L., & Schnurr, D. P. (1996). Analysis of 15 adenovirus hexon proteins reveals the location and structure of seven hypervariable regions containing serotype-specific residues. Journal of Virology, 70(3), 1836–1844. https://doi.org/10.1128/jvi.70.3.1836-1844.1996
Davison, A. J., Benkő, M., & Harrach, B. (2003). Genetic content and evolution of adenoviruses. Journal of General Virology, 84(11), 2895–2908. https://doi.org/10.1099/vir.0.19497-0
De Luca, C., Schachner, A., Mitra, T., Heidl, S., Liebhart, D., & Hess, M. (2020). Fowl adenovirus (FAdV) fiber-based vaccine against inclusion body hepatitis (IBH) provides type-specific protection guided by humoral immunity and regulation of B and T cell response. Veterinary Research, 51, 143. https://doi.org/10.1186/s13567-020-00869-8
Department of Statistics Malaysia. (2022a). Selected agricultural indicators, Malaysia, 2022. DOSM. https://dosm.gov.my/site/downloadrelease?id=selected-agricultural-indicators-malaysia-2022&lang=English
Department of Statistics. (2022b). Supply and utilization accounts selected agricultural commodities, Malaysia 2017-2021. DOSM. https://v2.dosm.gov.my/portal-main/release-content/supply-and-utilization-accounts-selected-agricultural-commodities-malaysia-2017-2021
Fu, G., Chen, H., Huang, Y., Cheng, L., Fu, Q., Shi, S., Wan, C., Chen, C., & Lin, J. (2013). Full genome sequence of egg drop syndrome virus strain FJ12025 isolated from muscovy duckling. Genome Announcements, 1(4), e00623-13. https://doi.org/10.1128/genomeA.00623-13
Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., & Bairoch, A. (2003). ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research, 31(13), 3784–3788. https://doi.org/10.1093/nar/gkg563
Grgić, H., Krell, P. J., & Nagy, É. (2014). Comparison of fiber gene sequences of inclusion body hepatitis (IBH) and non-IBH strains of serotype 8 and 11 fowl adenoviruses. Virus Genes, 48, 74–80. https://doi.org/10.1007/s11262-013-0995-y
Grgić, H., Poljak, Z., Sharif, S., & Nagy, É. (2013). Pathogenicity and cytokine gene expression pattern of a serotype 4 fowl adenovirus isolate. PLOS One, 8(10), e77601. https://doi.org/10.1371/journal.pone.0077601
Grgić, H., Yang, D.-H., & Nagy, É. (2011). Pathogenicity and complete genome sequence of a fowl adenovirus serotype 8 isolate. Virus Research, 156(1–2), 91–97. https://doi.org/10.1016/j.virusres.2011.01.002
Gupta, A., Popowich, S., Ojkic, D., Kurukulasuriya, S., Chow-Lockerbie, B., Gunawardana, T., Goonewardene, K., Karunarathna, R., Ayalew, L. E., Ahmed, K. A., Tikoo, S. K., Willson, P., & Gomis, S. (2018). Inactivated and live bivalent fowl adenovirus (FAdV8b + FAdV11) breeder vaccines provide broad-spectrum protection in chicks against inclusion body hepatitis (IBH). Vaccine, 36(5), 744–750. https://doi.org/10.1016/j.vaccine.2017.12.047
Hafez, M. H. (2011). Avian adenovirus infections with special attention to inclusion body hepatitis/hydropericardium syndrome and egg drop syndrome. Pakistan Veterinary Journal, 31(2), 85–92.
Hair-Bejo, M. (2005). Inclusion body hepatitis in a flock of a commercial broilers chickens. Journal of Veterinary Malaysia, 17(1), 23–26.
Islam, M. N., Rahman, M. M., Rahman, M. K., & Alam, J. (2023). First evidence of fowl adenovirus induced inclusion body hepatitis in chicken in Bangladesh. Canadian Journal of Infectious Diseases and Medical Microbiology, 2023, 7253433. https://doi.org/10.1155/2023/7253433
Jordan, A. B., Blake, L., Bisnath, J., Ramgattie, C., Carrington, C. V., & Oura, C. A. L. (2019). Identification of four serotypes of fowl adenovirus in clinically affected commercial poultry co-infected with chicken infectious anaemia virus in Trinidad and Tobago. Transboundary and Emerging Diseases, 66(3), 1341–1348. https://doi.org/10.1111/tbed.13162
Jørgensen, P. H., Otte, L., Nielsen, O. L., & Bisgaard, M. (1995). Influence of subclinical virus infections and other factors on broiler flock performance. British Poultry Science, 36(3), 455–463. https://doi.org/10.1080/00071669508417791
Juliana, M. A., Nurulfiza, M. I., Hair-Bejo, M., Abdul Rahman, O., & Aini, I. (2014). Molecular characterization of fowl adenoviruses isolated from inclusion body hepatitis outbreaks in commercial broiler chickens in Malaysia. Pertanika Journal of Tropical Agriculture Science, 37(4), 483–497.
Kaján, G. L., Affranio, I., Tóthné Bistyák, A., Kecskeméti, S., & Benkő, M. (2019). An emerging new fowl adenovirus genotype. Heliyon, 5(5), e01732. https://doi.org/10.1016/j.heliyon.2019.e01732
Kinsley, N. (2020, July 20). Popularity of poultry continues globally. Poultry World. https://www.poultryworld.net/poultry/popularity-of-poultry-continues-globally/
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platform. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
Li, S., Zhao, R., Yang, Q., Wu, M., Ma, J., Wei, Y., Pang, Z., Wu, C., Liu, Y., Gu, Y., Liao, M., & Sun, H. (2022). Phylogenetic and pathogenic characterization of current fowl adenoviruses in China. Infection, Genetics and Evolution, 105, 105366. https://doi.org/10.1016/j.meegid.2022.105366
Liu, Y., Wan, W., Gao, D., Li, Y., Yang, X., Liu, H., Yao, H., Chen, L., Wang, C., & Zhao, J. (2016). Genetic characterization of novel fowl aviadenovirus 4 isolates from outbreaks of hepatitis-hydropericardium syndrome in broiler chickens in China. Emerging Microbes and Infections, 5(1), 1-8. https://doi.org/10.1038/emi.2016.115
Majdi, A., & Bejo, M. H. (2015). Pathogenecity of Malaysian fowl adenovirus isolates in specific pathogen free chickens. In R. Abdullah, M. A. Omar, A. R. M. A. R. Bahaman, S. A. Aziz, S. S. Arshad, G. T. Selvarajah, & W. M. S. M. Mossadeq (Eds.), 10th Proceeding of the Seminar of Veterinary Sciences (pp. 15–19). Universiti Putra Malaysia Press. https://vet.upm.edu.my/upload/dokumen/2021090610331010th_Proceedings_of_the_Seminar_on_Veterinary_Sciences.pdf
Marek, A., Kaján, G. L., Kosiol, C., Benkő, M., Schachner, A., & Hess, M. (2016). Genetic diversity of species Fowl aviadenovirus D and Fowl aviadenovirus E. Journal of General Virology, 97(9), 2323–2332. https://doi.org/10.1099/jgv.0.000519
Marek, A., Kosiol, C., Harrach, B., Kaján, G. L., Schlötterer, C., & Hess, M. (2013). The first whole genome sequence of a fowl adenovirus B strain enables interspecies comparisons within the genus Aviadenovirus. Veterinary Microbiology, 166(1–2), 250–256. https://doi.org/10.1016/j.vetmic.2013.05.017
Marek, A., Nolte, V., Schachner, A., Berger, E., Schlötterer, C., & Hess, M. (2012). Two fiber genes of nearly equal lengths are a common and distinctive feature of Fowl adenovirus C members. Veterinary Microbiology, 156(3–4), 411–417. https://doi.org/10.1016/j.vetmic.2011.11.003
Mat Isa, N., Mohd Ayob, J., Ravi, S., Mustapha, N. A., Ashari, K. S., Bejo, M. H., Omar, A. R., & Ideris, A. (2019). Complete genome sequence of fowl adenovirus-8b UPM04217 isolate associated with the inclusion body hepatitis disease in commercial broiler chickens in Malaysia reveals intermediate evolution. VirusDisease, 30, 426–432. https://doi.org/10.1007/s13337-019-00530-9
McFerran, J. B., & Smyth, J. A. (2000). Avian adenoviruses. Revue Scientifique et Technique, 19(2), 589–601. https://doi.org/10.20506/rst.19.2.1238
Meulemans, G., Boschmans, M., van den Berg, T. P., & Decaesstecker, M. (2001). Polymerase chain reaction combined with restriction enzyme analysis for detection and differentiation of fowl adenoviruses. Avian Pathology, 30(6), 655–660. https://doi.org/10.1080/03079450120092143
Nakamura, K., Mase, M., Yamamoto, Y., Takizawa, K., Kabeya, M., Wakuda, T., Matsuda, M., Chikuba, T., Yamamoto, Y., Ohyama, T., Takahashi, K., Sato, N., Akiyama, N., Honma, H., & Imai, K. (2011). Inclusion body hepatitis caused by fowl adenovirus in broiler chickens in Japan, 2009–2010. Avian Diseases, 55(4), 719–723. https://doi.org/10.1637/9813-052511-Case.1
Niczyporuk, J. S. (2018). Deep analysis of loop L1 HVRs1-4 region of the hexon gene of adenovirus field strains isolated in Poland. PLOS One, 13(11), e0207668. https://doi.org/10.1371/journal.pone.0207668
Niu, D., Feng, J., Duan, B., Shi, Q., Li, Y., Chen, Z., Ma, L., Liu, H., & Wang, Y. (2022). Epidemiological survey of avian adenovirus in China from 2015 to 2021 and the genetic variability of highly pathogenic Fadv-4 isolates. Infection, Genetics and Evolution, 101, 105277. https://doi.org/10.1016/j.meegid.2022.105277
Ojkic, D., & Nagy, É. (2000). The complete nucleotide sequence of fowl adenovirus type 8. Microbiology, 81(7), 1833–1837. https://doi.org/10.1099/0022-1317-81-7-1833
Pallister, J., Wright, P. J., & Sheppard, M. (1996). A single gene encoding the fiber is responsible for variations in virulence in the fowl adenoviruses. Journal of Virology, 70(8), 5115–5122. https://doi.org/10.1128/JVI.70.8.5115-5122.1996
Pan, Q., Liu, L., Gao, Y., Liu, C., Qi, X., Zhang, Y., Wang, Y., Li, K., Gao, L., Wang, X., & Cui, H. (2017). Characterization of a hypervirulent fowl adenovirus 4 with the novel genotype newly prevalent in China and establishment of reproduction infection model of hydropericardium syndrome in chickens. Poultry Science, 96(6), 1581–1588. https://doi.org/10.3382/ps/pew431
Qinghua, H., Xinxin, M., Xiaoying, H., Yanyan, H., Shaohua, Y., Lin, Z., Ning, C., & Chuantian, X. (2019). Pathogenicity and complete genome sequence of a fowl adenovirus serotype 8b isolate from China. Poultry Science, 98(2), 573–580. https://doi.org/10.3382/ps/pey425
Rux, J. J., Kuser, P. R., & Burnett, R. M. (2003). Structural and phylogenetic analysis of adenovirus hexons by use of high-resolution x-ray crystallographic, molecular modeling, and sequence-based methods. Journal of Virology, 77(17), 9553–9566. https://doi.org/10.1128/JVI.77.17.9553-9566.2003
Sabarudin, N. S., Tan, S. W., Phang, Y. F., & Omar, A. R. (2021). Molecular characterization of Malaysian fowl adenovirus (FAdV) serotype 8b species E and pathogenicity of the virus in specific-pathogen-free chicken. Journal of Veterinary Science, 22(4), e42. https://doi.org/10.4142/jvs.2021.22.e42
Schachner, A., Gonzalez, G., Endler, L., Ito, K., & Hess, M. (2019). Fowl adenovirus (FAdV) recombination with intertypic crossovers in genomes of FAdV-D and FAdV-E, displaying hybrid serological phenotypes. Viruses, 11(12), 1094. https://doi.org/10.3390/v11121094
Schachner, A., Grafl, B., & Hess, M. (2021). Spotlight on avian pathology: Fowl adenovirus (FAdV) in chickens and beyond – an unresolved host-pathogen interplay. Avian Pathology, 50(1), 2–5. https://doi.org/10.1080/03079457.2020.1810629
Schachner, A., Marek, A., Jaskulska, B., Bilic, I., & Hess, M. (2014). Recombinant FAdV-4 fiber-2 protein protects chickens against hepatitis–hydropericardium syndrome (HHS). Vaccine, 32(9), 1086–1092. https://doi.org/10.1016/j.vaccine.2013.12.056
Schonewille, E., Jaspers, R., Paul, G., & Hess, M. (2010). Specific-pathogen-free chickens vaccinated with a live FAdV-4 vaccine are fully protected against a severe challenge even in the absence of neutralizing antibodies. Avian Diseases, 54(2), 905–910. https://doi.org/10.1637/8999-072309-Reg.1
Shah, M. S., Ashraf, A., Khan, M. I., Rahman, M., Habib, M., Chughtai, M. I., & Qureshi, J. A. (2017). Fowl adenovirus: History, emergence, biology and development of a vaccine against hydropericardium syndrome. Archives of Virology, 162, 1833–1843. https://doi.org/10.1007/s00705-017-3313-5
Slaine, P. D., Ackford, J. G., Kropinski, A. M., Kozak, R. A., Krell, P. J., & Nagy, É. (2016). Molecular characterization of pathogenic and nonpathogenic fowl aviadenovirus serotype 11 isolates. Canadian Journal of Microbiology, 62(12), 993–1002. https://doi.org/10.1139/cjm-2016-0297
Sohaimi, N. M. (2018). Development of live attenuated fowl adenovirus isolate of Malaysia for vaccine production [Doctoral thesis, Universiti Putra Malaysia]. Universiti Putra Malaysia Institutional Repository. http://psasir.upm.edu.my/id/eprint/76334/1/FPV 2018 26 IR.pdf
Sohaimi, N. M., & Clifford, U. C. (2021). Fowl adenovirus in chickens: Diseases, epidemiology, impact, and control strategies to the Malaysian poultry industry - A review. Journal of World’s Poultry Research, 11(3), 387–396. https://doi.org/10.36380/jwpr.2021.46
Sohaimi, N. M., Bejo, M. H., Omar, A. R., Ideris, A., & Isa, N. M. (2018). Hexon and fiber gene changes in an attenuated fowl adenovirus isolate from Malaysia in embryonated chicken eggs and its infectivity in chickens. Journal of Veterinary Science, 19(6), 759–770. https://doi.org/10.4142/jvs.2018.19.6.759
Sohaimi, N. M., Omar, A. R., & Ideris, A. (2018). Molecular detection and pathogenicity of fowl adenovirus. International Journal of Agricultural Sciences and Veterinary Medicine, 6(1), 73-84.
Steer, P. A., Kirkpatrick, N. C., O’Rourke, D., & Noormohammadi, A. H. (2009). Classification of fowl adenovirus serotypes by use of high-resolution melting-curve analysis of the hexon gene region. Journal of Clinical Microbiology, 47(2), 311–321. https://doi.org/10.1128/JCM.01567-08
Steer, P. A., O’Rourke, D., Ghorashi, S., & Noormohammadi, A. (2011). Application of high-resolution melting curve analysis for typing of fowl adenoviruses in field cases of inclusion body hepatitis. Australian Veterinary Journal, 89(5), 184–192. https://doi.org/10.1111/j.1751-0813.2011.00695.x
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673–4680. https://doi.org/10.1093/nar/22.22.4673
Wang, Z., & Zhao, J. (2019). Pathogenesis of hypervirulent fowl adenovirus serotype 4: The contributions of viral and host factors. Viruses, 11(8), 741. https://doi.org/10.3390/v11080741
Wei, Z., Liu, H., Diao, Y., Li, X., Zhang, S., Gao, B., Tang, Y., Hu, J., & Diao, Y. (2019). Pathogenicity of fowl adenovirus (FAdV) serotype 4 strain SDJN in Taizhou geese. Avian Pathology, 48(5), 477–485. https://doi.org/10.1080/03079457.2019.1625305
Yin, D., He, L., Zhu, E., Fang, T., Yue, J., Wen, M., Wang, K., & Cheng, Z. (2021). A fowl adenovirus serotype 4 (FAdV-4) Fiber2 subunit vaccine candidate provides complete protection against challenge with virulent FAdV-4 strain in chickens. Veterinary Microbiology, 263, 109250. https://doi.org/10.1016/j.vetmic.2021.109250
Zhang, Y., Liu, R., Tian, K., Wang, Z., Yang, X., Gao, D., Zhang, Y., Fu, J., Wang, H., & Zhao, J. (2018). Fiber2 and hexon genes are closely associated with the virulence of the emerging and highly pathogenic fowl adenovirus 4. Emerging Microbes & Infections, 7(1), 1–10. https://doi.org/10.1038/s41426-018-0203-1
Zhao, J., Zhong, Q., Zhao, Y., Hu, Y., & Zhang, G. (2015). Pathogenicity and complete genome characterization of fowl adenoviruses isolated from chickens associated with inclusion body hepatitis and hydropericardium syndrome in China. PLOS One, 10(7), e0133073. https://doi.org/10.1371/journal.pone.0133073
ISSN 1511-3701
e-ISSN 2231-8542