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Evaluation of ELISA and haemagglutination inhibition as screening tests in serosurveillance for H5/H7 avian influenza in commercial chicken flocks

  • M. E. Arnold (a1), M. J. Slomka (a2) (a3), A. C. Breed (a2) (a4), C. K. Hjulsager (a5), S. Pritz-Verschuren (a6), S. Venema-Kemper (a6), R. J. Bouwstra (a6), R. Trebbien (a5), S. Zohari (a7), V. Ceeraz (a2) (a3), L. E. Larsen (a5), R. J. Manvell (a2) (a3), G. Koch (a6) and I. H. Brown (a2) (a3)...

Abstract

Avian influenza virus (AIV) subtypes H5 and H7 can infect poultry causing low pathogenicity (LP) AI, but these LPAIVs may mutate to highly pathogenic AIV in chickens or turkeys causing high mortality, hence H5/H7 subtypes demand statutory intervention. Serological surveillance in the European Union provides evidence of H5/H7 AIV exposure in apparently healthy poultry. To identify the most sensitive screening method as the first step in an algorithm to provide evidence of H5/H7 AIV infection, the standard approach of H5/H7 antibody testing by haemagglutination inhibition (HI) was compared with an ELISA, which detects antibodies to all subtypes. Sera (n = 1055) from 74 commercial chicken flocks were tested by both methods. A Bayesian approach served to estimate diagnostic test sensitivities and specificities, without assuming any ‘gold standard’. Sensitivity and specificity of the ELISA was 97% and 99.8%, and for H5/H7 HI 43% and 99.8%, respectively, although H5/H7 HI sensitivity varied considerably between infected flocks. ELISA therefore provides superior sensitivity for the screening of chicken flocks as part of an algorithm, which subsequently utilises H5/H7 HI to identify infection by these two subtypes. With the calculated sensitivity and specificity, testing nine sera per flock is sufficient to detect a flock seroprevalence of 30% with 95% probability.

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Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: M. J. Slomka, E-mail: marek.slomka@apha.gsi.gov.uk

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Reprints will not be available from the author.

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Current address: School of Veterinary Science, University of Queensland, Brisbane, Australia.

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References

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1.Alexander, DJ (2007) An overview of the epidemiology of avian influenza. Vaccine 25, 56375644.10.1016/j.vaccine.2006.10.051
2.Suarez, D (2010) Avian influenza: our current understanding. Animal Health Research Reviews 11, 1933.10.1017/S1466252310000095
3.Alexander, DJ and Brown, IH (2009) History of highly pathogenic avian influenza. Revue Scientifique et Technique (Paris) 28, 1938.10.20506/rst.28.1.1856
4.OIE (World Organisation for Animal Health) (2017) Avian influenza. In World Health Organization for Animal Health, Terrestrial Animal Health Code, 2017. Paris: OIE, ch. 10.4. Available at http://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/current/chapitre_avian_influenza_viruses.pdf (Accessed 13 October 2017).
5.EC (European Commission) (2006) Council Directive 2005/94/EC of 20 December 2005 on community measures for the control of avian influenza and repealing Directive 92/40/EEC. Official Journal of the European Union 2006; L10: 20/16. Available at http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32005L0094 (Accessed 13 October 2017).
6.Vapnek, J (2010) Regulatory measures against outbreaks of highly pathogenic avian influenza. FAO Legal Papers Online #82. Available at http://www.fao.org/fileadmin/user_upload/legal/docs/lpo82.pdf (Accessed 13 October 2017).
7.OIE (World Organisation for Animal Health) (2015) Avian influenza (infection with avian influenza viruses). In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Paris: OIE, ch. 2.3.4. Available at http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.03.04_AI.pdf (Accessed 13 October 2017).
8.WHO (World Health Organisation) (2016) Avian and other zoonotic influenza. In Fact Sheet, Updated November 2016. Geneva: WHO. Available at http://www.who.int/mediacentre/factsheets/avian_influenza/en/ (Accessed 13 October 2017).
9.Elbers, ARW, Koch, G and Bouma, A (2005) Performance of clinical signs in poultry for the detection of outbreaks during the avian influenza A (H7N7) epidemic in The Netherlands in 2003. Avian Pathology 34, 181187.10.1080/03079450500096497
10.Brown, IH (2010) Summary of avian influenza activity in Europe, Asia, and Africa, 2006–2009. Avian Diseases 54, 187193.10.1637/8949-053109-Reg.1
11.Pasick, J, Pedersen, J and Hernandez, MS (2012) Avian influenza in North America, 2009–2011. Avian Diseases 56, 845848.10.1637/10206-041512-Reg.1
12.Swayne, DE and Halvorson, DA (2008) Influenza. In Saif, YM, Fadly, AM, Glissom, JR, McDougald, LR, Nolan, LK and Swayne, DE (eds). Diseases of Poultry, 12th edn. Ames, Iowa: Blackwell, pp. 153184.
13.EC (European Commission) (2010) Commission Decision of 25 June 2010 on the implementation by Member States of surveillance programmes for avian influenza in poultry and wild birds. Official Journal of the European Union L166, 2232. Available at http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=uriserv:OJ.L_.2010.166.01.0022.01.ENG&toc=OJ:L:2010:166:TOC (Accessed 13 October 2017).
14.Bean, WJ, et al. (1985) Characterisation of virulent and avirulent A/chicken/Pennsylvania/83 influenza A viruses: potential role of defective interfering RNAs in nature. Journal of Virology 54, 151160.
15.Capua, I, et al. (2008) Avian influenza in Italy 1997–2006. In Klenk, H-D, Matrosovich, MN and Stech, J (eds). Avian Influenza. Monographs in Virology. Basel: Karger, vol. 27, pp. 5970.10.1159/000151608
16.Senne, DA, Holt, TJ and Akey, BL (2005) An overview of the 2002 outbreak of low-pathogenic H7N2 avian influenza in Virginia, West Virginia and North Carolina. In Schrijver, RS and Koch, G (eds). Avian Influenza: Prevention and Control. Wageningen: UR Frontis Series, Springer, ch. 6, pp. 4147.10.1007/1-4020-3441-5_6
17.Gonzales, JL, et al. (2010) Low-pathogenic notifiable avian influenza serosurveillance and the risk of infection in poultry – a critical review of the European Union active surveillance programme (2005–2007). Influenza and Other Respiratory Viruses 4, 9199.10.1111/j.1750-2659.2009.00126.x
18.Breed, AC, et al. (2015) Annual Report on surveillance for avian influenza in poultry and wild birds in Member States of the European Union in 2014. Available at https://ec.europa.eu/food/animals/animal-diseases/control-measures/avian-influenza_en (Accessed 13 October 2017).
19.Breed, AC, et al. (2016) Annual Report on surveillance for avian influenza in poultry and wild birds in Member States of the European Union in 2015. Available at https://ec.europa.eu/food/animals/animal-diseases/control-measures/avian-influenza_en (Accessed 13 October 2017).
20.Spackman, E, Suarez, DL and Senne, DA (2008) Avian influenza diagnostics and surveillance methods. In Swayne, DE (ed.). Avian Influenza, 1st edn. Ames, Iowa: Blackwell, ch. 13, pp. 299308.10.1002/9780813818634.ch13
21.EC (European Commission) (2006) Commission decision of 4 August 2006 approving a Diagnostic Manual for avian influenza. Official Journal of the European Union 2006; L237/1. Available at http://publications.europa.eu/en/publication-detail/-/publication/a5511c6a-d9d7-4507-a9af-3bb5366ba5d9/language-en/format-PDF/source-2188753 (Accessed 13 October 2017).
22.Pedersen, JC (2008) Hemagglutination-inhibition test for avian influenza virus subtype identification and the detection and quantification of serum antibodies to the avian influenza virus. Methods in Molecular Biology 436, 5366. In: Spackman E, ed: Avian Influenza, 1st edition. Totowa, New Jersey: Humana Press, pp. 53–66.
23.Slomka, MJ, et al. (2010) Role of real time RT-PCR platform technology in the diagnosis and management of notifiable avian influenza outbreaks: experiences in Great Britain. Avian Diseases 54, 591596.10.1637/8947-052909-Reg.1
24.OIE (World Organisation for Animal Health) (2017) Principles and methods of validation of diagnostic assays for infectious diseases. In Manual of Diagnostic Tests for Aquatic Animals, 2017. Paris: OIE, ch. 1.1.2. Available at http://www.oie.int/fileadmin/Home/eng/Health_standards/aahm/current/chapitre_validation_diagnostics_assays.pdf (Accessed 13 October 2017).
25.EC (European Commission) (2015) In EU Reference Laboratories for avian influenza and Newcastle disease: Work programmes 2016–2017, 2015. Available at https://ec.europa.eu/food/sites/food/files/safety/docs/oc_eurl_wp_2016_avian_influenza_newcastle_disease_en.pdf (Accessed 13 October 2017).
26.Enøe, C, Georgiadis, MP and Johnson, WO (2000) Estimation of sensitivity and specificity of diagnostic tests and disease prevalence when the true disease state is unknown. Preventive Veterinary Medicine 45, 6181.10.1016/S0167-5877(00)00117-3
27.Branscum, AJ, Gardner, IA and Johnson, WO (2005) Estimation of diagnostic-test sensitivity and specificity through Bayesian modelling. Preventive Veterinary Medicine 68, 145163.10.1016/j.prevetmed.2004.12.005
28.Gelman, AE, et al. (2003) Bayesian Data Analysis, 2nd edn. Boca Raton, FL: Chapman and Hall/CRC Press.
29.Nérette, P, et al. (2008) Using pseudogold standards and latent-class analysis in combination to evaluate the accuracy of three diagnostic tests. Preventative Veterinary Medicine 85, 207225.10.1016/j.prevetmed.2008.01.011
30.Cannon, RM and Roe, RT (1982) Livestock Disease Surveys. A Field Manual for Veterinarians. Bureau of Rural Science, Department of Primary Industry. Canberra: Australian Government Publishing Service.
31.Hirst, GK (1942) The quantitative determination of influenza virus and antibodies by means of red cell agglutination. Journal of Experimental Medicine 75, 4964.10.1084/jem.75.1.49
32.Schulman, JL and Kilbourne, ED (1969) Independent variation in nature of hemagglutinin and neuraminidase antigens of influenza virus: distinctiveness of hemagglutinin antigen of Hong Kong-68 virus. Proceedings of the National Academy of Sciences of the USA 63, 326333.10.1073/pnas.63.2.326
33.Escoria, M, et al. (2010) impact of antigenic and genetic drift on the serologic surveillance of H5N2 avian influenza viruses. BMC Veterinary Research 2010; 6: 57. Available at http://www.biomedcentral.com/1746-6148/6/57 (Accessed 13 October 2017).10.1186/1746-6148-6-57
34.Beato, MS, et al. (2014) Antigenic and genetic evolution of low-pathogenicity avian influenza viruses of subtype H7N3 following heterologous vaccination. Clinical and Vaccine Immunology 21, 603612.10.1128/CVI.00647-13
35.Rawdon, TG, et al. (2010) Surveillance for avian influenza virus subtypes H5 and H7 in chickens and turkeys farmed commercially in New Zealand. New Zealand Veterinary Journal 58, 292298.10.1080/00480169.2010.69756
36.Comin, A, et al. (2013) Serological diagnosis of avian influenza in poultry: is the haemaglutinationm inhibition test really the ‘gold standard’? Influenza and Other Respiratory Viruses 7, 257264.10.1111/j.1750-2659.2012.00391.x
37.Marché, S, Lambrecht, B and van den Berg, T (2010) Evaluation of different serological markers for the early detection of avian influenza infection in chickens. Avian Diseases 54, 690698.10.1637/8907-043009-ResNote.1
38.Lu, H and Castro, AE (2004) Evaluation of the infectivity, length of infection and immune response of a low-pathogenicity H7N2 avian influenza virus in specific-pathogen-free chickens. Avian Diseases 48, 263270.10.1637/7064

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