Investigation of Risk Factors for Introduction of Highly Pathogenic Avian Influenza H5N1 Infection Among Commercial Turkey Operations in the United States, 2022: a Case-control Study

Overview

Journal Front Vet Sci

Specialty Veterinary Medicine

Date 2023 Sep 15

PMID 37711433

Authors

Kelly A Patyk

Victoria L Fields

Andrea L Beam

Matthew A Branan

Rachel E McGuigan

Alice Green

Mia K Torchetti

Kristina Lantz

Alexis Freifeld

Katherine Marshall

Amy H Delgado

Affiliations

Soon will be listed here.

Abstract

Introduction: The 2022-2023 highly pathogenic avian influenza (HPAI) H5N1 outbreak in the United States (U.S.) is the largest and most costly animal health event in U.S. history. Approximately 70% of commercial farms affected during this outbreak have been turkey farms.

Methods: We conducted a case-control study to identify potential risk factors for introduction of HPAI virus onto commercial meat turkey operations. Data were collected from 66 case farms and 59 control farms in 12 states. Univariate and multivariable analyses were conducted to compare management and biosecurity factors on case and control farms.

Results: Factors associated with increased risk of infection included being in an existing control zone, having both brooders and growers, having toms, seeing wild waterfowl or shorebirds in the closest field, and using rendering for dead bird disposal. Protective factors included having a restroom facility, including portable, available to crews that visit the farm and workers having access and using a shower at least some of the time when entering a specified barn.

Discussion: Study results provide a better understanding of risk factors for HPAI infection and can be used to inform prevention and control measures for HPAI on U.S. turkey farms.

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References

Nishiguchi A, Kobayashi S, Yamamoto T, Ouchi Y, Sugizaki T, Tsutsui T . Risk factors for the introduction of avian influenza virus into commercial layer chicken farms during the outbreaks caused by a low-pathogenic H5N2 virus in Japan in 2005. Zoonoses Public Health. 2007; 54(9-10):337-43. DOI: 10.1111/j.1863-2378.2007.01074.x. View

Galletti G, Santi A, Guberti V, Paternoster G, Licata E, Loli Piccolomini L . A method to identify the areas at risk for the introduction of avian influenza virus into poultry flocks through direct contact with wild ducks. Transbound Emerg Dis. 2018; 65(4):1033-1038. DOI: 10.1111/tbed.12838. View

Bouwstra R, Gonzales J, de Wit S, Stahl J, Fouchier R, Elbers A . Risk for Low Pathogenicity Avian Influenza Virus on Poultry Farms, the Netherlands, 2007-2013. Emerg Infect Dis. 2017; 23(9):1510-1516. PMC: 5572893. DOI: 10.3201/eid2309.170276. View

Gonzales J, Stegeman J, Koch G, de Wit S, Elbers A . Rate of introduction of a low pathogenic avian influenza virus infection in different poultry production sectors in the Netherlands. Influenza Other Respir Viruses. 2012; 7(1):6-10. PMC: 5780726. DOI: 10.1111/j.1750-2659.2012.00348.x. View

Garber L, Bjork K, Patyk K, Rawdon T, Antognoli M, Delgado A . Factors Associated with Highly Pathogenic Avian Influenza H5N2 Infection on Table-Egg Layer Farms in the Midwestern United States, 2015. Avian Dis. 2016; 60(2):460-6. DOI: 10.1637/11351-121715-Reg. View

Ramey A, DeLiberto T, Berhane Y, Swayne D, Stallknecht D . Lessons learned from research and surveillance directed at highly pathogenic influenza A viruses in wild birds inhabiting North America. Virology. 2018; 518:55-63. DOI: 10.1016/j.virol.2018.02.002. View

Caliendo V, Lewis N, Pohlmann A, Baillie S, Banyard A, Beer M . Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci Rep. 2022; 12(1):11729. PMC: 9276711. DOI: 10.1038/s41598-022-13447-z. View

Elbers A, Holtslag J, Bouma A, Koch G . Within-flock mortality during the high-pathogenicity avian influenza (H7N7) epidemic in The Netherlands in 2003: implications for an early detection system. Avian Dis. 2007; 51(1 Suppl):304-8. DOI: 10.1637/7579-040106R.1. View

Webster R, BEAN W, Gorman O, Chambers T, Kawaoka Y . Evolution and ecology of influenza A viruses. Microbiol Rev. 1992; 56(1):152-79. PMC: 372859. DOI: 10.1128/mr.56.1.152-179.1992. View

10.

Grant M, Brojer C, Zohari S, Noremark M, Uhlhorn H, Jansson D . Highly Pathogenic Avian Influenza (HPAI H5Nx, Clade 2.3.4.4.b) in Poultry and Wild Birds in Sweden: Synopsis of the 2020-2021 Season. Vet Sci. 2022; 9(7). PMC: 9318561. DOI: 10.3390/vetsci9070344. View

11.

Si Y, de Boer W, Gong P . Different environmental drivers of highly pathogenic avian influenza H5N1 outbreaks in poultry and wild birds. PLoS One. 2013; 8(1):e53362. PMC: 3538778. DOI: 10.1371/journal.pone.0053362. View

12.

Bevins S, Shriner S, Cumbee Jr J, Dilione K, Douglass K, Ellis J . Intercontinental Movement of Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4 Virus to the United States, 2021. Emerg Infect Dis. 2022; 28(5):1006-1011. PMC: 9045435. DOI: 10.3201/eid2805.220318. View

13.

Lycett S, Pohlmann A, Staubach C, Caliendo V, Woolhouse M, Beer M . Genesis and spread of multiple reassortants during the 2016/2017 H5 avian influenza epidemic in Eurasia. Proc Natl Acad Sci U S A. 2020; 117(34):20814-20825. PMC: 7456104. DOI: 10.1073/pnas.2001813117. View

14.

Easterday B, Trainer D, Tumova B, Pereira H . Evidence of infection with influenza viruses in migratory waterfowl. Nature. 1968; 219(5153):523-4. DOI: 10.1038/219523a0. View

15.

Li L, Bowman A, DeLiberto T, Killian M, Krauss S, Nolting J . Genetic Evidence Supports Sporadic and Independent Introductions of Subtype H5 Low-Pathogenic Avian Influenza A Viruses from Wild Birds to Domestic Poultry in North America. J Virol. 2018; 92(19). PMC: 6146819. DOI: 10.1128/JVI.00913-18. View

16.

Grear D, Hall J, Dusek R, Ip H . Inferring epidemiologic dynamics from viral evolution: 2014-2015 Eurasian/North American highly pathogenic avian influenza viruses exceed transmission threshold, = 1, in wild birds and poultry in North America. Evol Appl. 2018; 11(4):547-557. PMC: 5891053. DOI: 10.1111/eva.12576. View

17.

Lewis N, Banyard A, Whittard E, Karibayev T, Al Kafagi T, Chvala I . Emergence and spread of novel H5N8, H5N5 and H5N1 clade 2.3.4.4 highly pathogenic avian influenza in 2020. Emerg Microbes Infect. 2021; 10(1):148-151. PMC: 7832535. DOI: 10.1080/22221751.2021.1872355. View

18.

Wells S, Kromm M, VanBeusekom E, Sorley E, Sundaram M, VanderWaal K . Epidemiologic Investigation of Highly Pathogenic H5N2 Avian Influenza Among Upper Midwest U.S. Turkey Farms, 2015. Avian Dis. 2017; 61(2):198-204. DOI: 10.1637/11543-112816-Reg.1. View

19.

Lee D, Torchetti M, Hicks J, Killian M, Bahl J, Pantin-Jackwood M . Transmission Dynamics of Highly Pathogenic Avian Influenza Virus A(H5Nx) Clade 2.3.4.4, North America, 2014-2015. Emerg Infect Dis. 2018; 24(10):1840-1848. PMC: 6154162. DOI: 10.3201/eid2410.171891. View

20.

Yoo D, Lee K, Chun B, Lee H, Park H, Kim J . Preventive effect of on-farm biosecurity practices against highly pathogenic avian influenza (HPAI) H5N6 infection on commercial layer farms in the Republic of Korea during the 2016-17 epidemic: A case-control study. Prev Vet Med. 2021; 199:105556. DOI: 10.1016/j.prevetmed.2021.105556. View