Abstract
Avian infectious laryngotracheitis (ILT) is a respiratory disease that causes severe economic losses in the poultry industry, mainly due to high morbidity and mortality and reduced egg production. Molecular characterization was performed on samples collected from flocks in the Brazilian States of São Paulo, Pernambuco, and Minas Gerais during 2015 and 2016 that presented clinical signs of respiratory disease. End-point PCR was used for viral detection, and DNA sequencing was used for differentiation of vaccine and field strains. Molecular analysis based on the infected cell protein (ICP4) gene separated four of the nine samples together with previous Brazilian isolates (São Paulo and Minas Gerais), one sample was grouped on the same branch as Minas Gerais strains (along with another related sample), one sample was separately branched but still related to the tissue culture origin (TCO) vaccine strain, and two samples were grouped on the same branch as the TCO vaccine strain. Molecular analysis of the thymidine kinase (TK) gene showed the existence of strains of both high and low virulence. The characterization of two fragments of the ICP4 gene and a fragment of the TK gene in this study suggested that the virus circulating in Guatapará, as well as those in Barretos and Itanhandu, that is causing respiratory problems in birds is a highly virulent field strain. The clinical signs point to a TCO vaccine strain that most likely underwent some reversal event and is a latent reactivated infection.
Similar content being viewed by others
References
Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch JD, Minson AC et al (2009) The order herpesvirales. Arch Virol 154:171–177. https://doi.org/10.1007/s00705-008-0278-4
Gowthaman V, Singh SD, Dhama K, Barathidasan R, Mathapati BS, Srinivasan P et al (2014) Molecular detection and characterization of infectious laryngotracheitis virus (Gallid herpesvirus-1) from clinical samples of commercial poultry flocks in India. Virusdis 25:345–349. https://doi.org/10.1007/s13337-014-0206-z
García M, Riblet SM (2001) Characterization of infectious laryngotracheitis virus isolates: demonstration of viral subpopulations within vaccine preparations. Avian Dis 45:558–566
Samberg Y, Cuperstein E, Bendheim U, Aronovici I (1971) The development of a vaccine against avian infectious laryngotracheitis. IV. Immunization of chickens with a modified laryngotracheitis vaccine in the drinking water. Avian Dis 15:413–417
Hitchner SB, Fabricant J, Bagust TJ (1977) A fluorescent-antibody study of the pathogenesis of infectious laryngotracheitis. Avian Dis 21:185–194. https://doi.org/10.2307/1589339
Gelenczei EF, Marty EW (1964) Studies on a tissue-culture modified infectious laryngotracheitis virus. Avian Dis 8:105–122
Fulton RM, Schrader DL, Will M (2000) Effect of route of vaccination on the prevention of infectious laryngotracheitis in commercial egg-laying chickens. Avian Dis 44:8–16
Hughes CS, Williams RA, Gaskell RM, Jordan FT, Bradbury JM, Bennett M, Jones RC (1991) Latency reactivation of infectious laryngotracheitis vaccine virus. Arch Virol 121:213–218. https://doi.org/10.1007/bf01316755
Garcia M (2016) Current and future vaccines and vaccination strategies against infectious laryngotracheitis (ILT) respiratory disease of poultry. Vet Microbiol 206:157–162. https://doi.org/10.1016/j.vetmic.2016.12.023
Coppo MJC, Noormohammadi AH, Browning GF, Devlin JM (2013) Challenges and recent advancements in infectious laryngotracheitis virus vaccines. Avian Pathol 42:195–205. https://doi.org/10.1080/03079457.2013.800634
García M, Volkening J, Riblet S, Spatz S (2013) Genomic sequence analysis of the United States infectious laryngotracheitis vaccine strains chicken embryo origin (CEO) and tissue culture origin (TCO). Virology 440:64–74. https://doi.org/10.1016/j.virol.2013.02.007
Bagust TJ, Johnson MA (1995) Avian infectious laryngotracheitis: virus-host interactions in relation to prospects for eradication. Avian Pathol 24:373–391. https://doi.org/10.1080/03079459508419079
Dufour-Zavala L (2008) Epizootiology of infectious laryngotracheitis and presentation of an industry control program. Avian Dis 52:1–7. https://doi.org/10.1637/8018-051007-review
Chacon JL, Mizuma MY, Piantino Ferreira AJ (2010) Characterization by restriction fragment length polymorphism and sequence analysis of field and vaccine strains of infectious laryngotracheitis virus involved in severe outbreaks. Avian Pathol 39:425–433. https://doi.org/10.1080/03079457.2010.516386
Parra SS, Nunez L, Buim MR, Astolfi-Ferreira CS, Piantino Ferreira AJ (2018) Development of a qPCR for the detection of infectious laryngotracheitis virus (ILTV) based on the gE gene. Br Poult Sci 59:402–407. https://doi.org/10.1080/00071668.2018.1479060
Chacon JL, Ferreira AJP (2009) Differentiation of field isolates and vaccine strains of infectious laryngotracheitis virus by DNA sequencing. Vaccine 27:6731–6738. https://doi.org/10.1016/j.vaccine.2009.08.083
Lee SW, Devlin JM, Markham JF, Noormahammadi AH, Browning GF, Ficorilli NP et al (2013) Phylogenetic and molecular epidemiological studies reveal evidence of multiple past recombination events between infectious laryngotracheitis viruses. PLoS One 8:e55121. https://doi.org/10.1371/journal.pone.0055121
Bagust TJ, Jones RC, Guy JS (2000) Avian infectious laryngotracheitis. Rev Sci Tech 19:483–492. https://doi.org/10.20506/rst.19.2.1229
Johnson MA, Tyack SG, Prideaux C, Kongsuwan K, Sheppard M (1995) Nucleotide sequence of infectious laryngotracheitis virus (Gallid herpesvirus 1) ICP4 gene. Virus Res 35:193–204. https://doi.org/10.1016/0168-1702(94)00096-u
Couto RM, Preis IS, Braga JFV, Brasil BSAF, Drummond MG, Martins NRS, Ecco R (2014) Molecular characterization of infectious laryngotracheitis virus in naturally infected egg layer chickens in a multi-age flock in Brazil. Arch Virol 160:241–252. https://doi.org/10.1007/s00705-014-2273-2
Han MG, Kim SJ (2001) Analysis of Korean strains of infectious laryngotracheitis virus by nucleotide sequences and restriction fragment length polymorphism. Vet Microbiol 83:321–331. https://doi.org/10.1016/S0378-1135(01)00423-0
Hipólito O, Soares LA, Pereira OAC, Pinto AA, Bottino JA (1974) Isolamento e identificação do vírus da laringotraqueíte infecciosa das galinhas no Brasil. 10th CBM, Rio de Janeiro, Brazil, proceedings pp. 16.
Chacon JL, Brandao PE, Villareal LYB, Gama NM, Ferreira AJP (2007) Survey of infectious laryngotracheitis outbreak in layer hens and differential diagnosis with other respiratory pathogens. Braz J Poult Sci 9:61–67
Preis IS, Braga JF, Couto RM, Brasil BS, Martins NR, Ecco R (2013) Outbreak of infectious laryngotracheitis in large multi-age egg layer chicken flocks in Minas Gerais. Pesq Vet Bras 33:591–596. https://doi.org/10.1590/S0100-736X2013000500007
Chomczynski PA (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and protein for the cell and tissues samples. Biotechniques 15:532–536
Chacon JL, Ferreira AJP (2008) Development and validation of nested-PCR for the diagnosis of clinical and subclinical infectious laryngotracheitis. J Virol Methods 151:188–193. https://doi.org/10.1016/j.jviromet.2008.05.012
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Huson DH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73
Martin D, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003. https://doi.org/10.1093/ve/vev003
Bruen TC, Philippe H, Bryant DA (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681. https://doi.org/10.1534/genetics.105.048975
Oldoni I, García M (2007) Characterization of infectious laryngotracheitis virus isolates from the US by polymerase chain reaction and restriction fragment length polymorphism of multiple genome regions. Avian Pathol 36:167–176. https://doi.org/10.1080/03079450701216654v
Parra SHS, Nuñez LFN, Astolfi-Ferreira CS, Ferreira AJP (2015) Occurrence of infectious laryngotracheitis virus (ILTV) in 2009–2013 in the State of São Paulo, Brazil. Braz J Poult Sci 17:117–120. https://doi.org/10.1590/1516-635x1701117-120
Chacon JL, Nuñez LFN, Vejarano MP, Parra SHS, Astolfi-Ferreira CS, Ferreira AJP (2015) Persistence and spreading of field and vaccine strains of infectious laryngotracheitis virus (ILTV) in vaccinated and unvaccinated geographic regions, in Brazil. Trop Anim Health Prod 47:1101–1108. https://doi.org/10.1007/s11250-015-0834-3
Luciano RL, Buim MR, Del Fava C, Ikuno AA, Harakava R, Ishizuca MM et al (2011) Detecção e caracterização do vírus de laringotraqueíte infecciosa em um surto em aves de postura no estado de São Paulo, Brasil. Rev Educ Cont Med Vet Zootec 9:41
Chang PC, Lee YL, Shien JH, Shieh HK (1997) Rapid differentiation of vaccine strains and field isolates of infectious laryngotracheitis virus by restriction fragment length polymorphism of PCR products. J Virol Methods 66:179–186. https://doi.org/10.1016/S0166-0934(97)00050-5
Wanasawaeng W, Chansiripornchai N (2010) Molecular classification of infectious laryngotracheitis virus from chick embryo origin vaccine, tissue culture origin vaccine and field isolates. Thai J Vet Med 40:393–398. https://he01.tci-thaijo.org/index.php/tjvm/article/view/35777
Williams RA, Bennett M, Bradbury JM, Gaskell RM, Jones RC, Jordan FTW (1992) Demonstration of sites of latency of infectious laryngotracheitis virus using the polymerase chain reaction. J Gen Virol 73:2415–2420. https://doi.org/10.1099/0022-1317-73-9-2415
Wang LG, Ma J, Xue CY, Wang W, Guo C, Chen F et al (2013) Dynamic distribution and tissue tropism of infectious laryngotracheitis virus in experimentally infected chickens. Arch Virol 158:659–666. https://doi.org/10.1007/s00705-012-1414-8
Parra SHS, Nuñez LFN, Astolfi-Ferreira CS, Ferreira AJP (2015) Persistence of the tissue culture origin vaccine for infectious laryngotracheitis virus in commercial chicken flocks in Brazil. Poult Sci 17:2608–2615. https://doi.org/10.3382/ps/pev213
Hughes CS, Gaskell RM, Jones RC, Bradbury JM, Jordan FT (1989) Effects of certain stress factors on the re-excretion of infectious laryngotracheitis virus from latently infected carrier birds. Res Vet Sci 46:274–276. https://doi.org/10.1016/S0034-5288(18)31158-5
Rodríguez-Avila A, Oldoni I, Riblet S, García M (2007) Replication and transmission of live attenuated infectious laryngotracheitis virus (ILTV) vaccines. Avian Dis 51:905–911. https://doi.org/10.1637/8011-041907-regr.1
Agnew-Crumpton R, Vaz PK, Devlin JM, O’Rourke D, Blacker-Smith HP, Konsak-Ilievski B et al (2016) Spread of the newly emerging infectious laryngotracheitis viruses in Australia. Infect Genet Evol 43:67–73. https://doi.org/10.1016/j.meegid.2016.05.023
Loncoman CA, Vaz PK, Coppo MJC, Hartley C, Morera FJ, Browning GF, Devlin M (2017) Natural recombination in alphaherpesviruses: insights into viral evolution through full genome sequencing and sequence analysis. Infect Genet Evol 49:174–185. https://doi.org/10.1016/j.meegid.2016.12.022
Perez Contreras A, Van der Meer F, Checkley S, Joseph T, King R, Ravi M et al (2020) Analysis of whole-genome sequences of infectious laryngotracheitis virus isolates from poultry flocks in Canada: evidence of recombination. Viruses 11:1302. https://doi.org/10.3390/v12111302
La T, Choin E, Lee J, Park S, Song S, Choi I, Lee S (2019) Comparative genome analysis of Korean field strains of infectious laryngotracheitis virus. PLoS One 14:e0211158. https://doi.org/10.1371/journal.pone.0211158
Acknowledgements
The authors would like to thank the poultry companies in Brazil that generously donated the samples for the development of this study.
Funding
This research was supported by the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) grants number 140744/2014–2 and 306380/2014–5. A. J. Piantino Ferreira is the recipient of a CNPq fellowship grant number 301084/2019–0.
Author information
Authors and Affiliations
Contributions
SHS-P performed the detection ILTV in the clinical samples; LFNN prepared the draft the manuscript; MRB assessed and acquired samples of ILT from chickens; CSA-F revised the manuscript; CAL contributed with molecular analysis; AJPF conceived the study and revised the manuscript. All authors contributed to the analysis and interpretation of the data and revised the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Responsible Editor: Luiz Henrique Rosa
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Santander-Parra, S.H., Nuñez, L.F.N., Buim, M.R. et al. Detection and molecular characterization of infectious laryngotracheitis virus (ILTV) in chicken with respiratory signs in Brazil during 2015 and 2016. Braz J Microbiol 53, 2223–2232 (2022). https://doi.org/10.1007/s42770-022-00833-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-022-00833-y