Tierarztl Prax Ausg G Grosstiere Nutztiere 2024; 52(05): 296-303
DOI: 10.1055/a-2410-1530
Case Report

Reverse zoonotic transmission of human seasonal influenza to a pig herd in Sweden

Reverse zoonotische Übertragung der saisonalen humanen Influenza in einem Schweinebetrieb in Schweden
Kaisa Ryytty Sylvén
1   Farm & Animal Health, Uppsala, Sweden
,
Magdalena Jacobson
2   Department of Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden
,
Lukas Schwarz
3   Clinical Centre for Population Medicine in Fish, Pig and Poultry, Clinical Department for Farm Animals and Food System Science, University of Veterinary Medicine Vienna, Austria
,
Siamak Zohari
4   Department of Microbiology, Swedish Veterinary Agency (SVA), Uppsala, Sweden
› Author Affiliations

Abstract

In January 2023, a Swedish piglet-producing farm with 2800 sows in production (SIP) was diagnosed with IAV (Influenza A virus) and the isolates were shown to cluster with the human seasonal influenza (2022/2023). In December 2022, employees with flu like symptoms tended to the pigs and a few weeks later, respiratory signs appeared in different age groups; sows in farrowing units were anorectic and pyrectic. Lung and nasal swabs were tested positive for IAV and other respiratory infectious agents. Blanket vaccination against H1N1pdm09 of sows and gilts was initiated but discontinued for sows after 2 treatments. Biosecurity measures aiming to reduce the spread of virus were implemented. However, the compliance to follow the protocol was moderate.

Combining immunity and strict sanitary measures is crucial to control virus circulation. As the farmer discontinued sow vaccination and just partly increased biosecurity, this may have contributed to ongoing virus circulation and clinical signs in pigs, even 5 months post-diagnosis. Although H1N1pdm09 already had been found in the herd in 2017, there were no clinical signs or diagnostic results indicating continuous circulation of this or other IAV strains afterwards. However, this cannot be entirely excluded. Swine IAVs pose a risk of reintroduction into the human population, highlighting the importance of vaccination of farm workers against seasonal influenza.

Zusammenfassung

Im Januar 2023 wurde auf einem schwedischen Ferkelerzeugerbetrieb mit 2800 produktiven Sauen Influenza A Virus (IAV) nachgewiesen. Es konnte gezeigt werden, dass diese Virusisolate mit saisonalen humanen Influenza A Viren (2022/2023) clusterten. Im Dezember 2022 arbeiteten Mitarbeiter, die an grippeähnlichen Symptomen litten, in dem Betrieb und einige Wochen später traten Atemwegssymptome in Schweinen verschiedener Altersgruppen auf; Sauen in der Abferkelung waren anorektisch und hatten eine erhöhte innere Körpertemperatur. Lungen und Nasentupfer waren positiv auf IAV und andere respiratorische Erreger. Eine flächendeckende Impfung gegen H1N1pdm09 von Sauen und Jungsauen wurde eingeleitet, aber nach 2 Behandlungen bei den Sauen eingestellt. Biosicherheitsmaßnahmen zur Unterbrechung der Infektketten wurden eingeführt. Diese wurden jedoch durch den Landwirt nicht konsequent umgesetzt.

Die Kombination von Immunität und strengen hygienischen Maßnahmen ist entscheidend, um die Viruszirkulation zu kontrollieren. Da der Landwirt die Impfung der Sauen eingestellt und die Biosicherheit nur teilweise angepasst hat, könnte dies zur selbst 5 Monate nach der Diagnose anhaltenden Viruszirkulation und klinischen Symptomatik bei den Schweinen beigetragen haben. Obwohl in 2017 H1N1pdm09 in dem Betrieb nachgewiesen wurde, gab es in den Jahren danach keine klinischen Anzeichen oder auch diagnostische Nachweise die eine kontinuierliche Zirkulation dieses oder anderer IAV Stämme vermuten lassen. Dies kann jedoch nicht vollständig ausgeschlossen werden. Porzine IAVs stellen ein Risiko für den Wiedereintrag in die menschliche Bevölkerung dar, was die Bedeutung der Impfung von Arbeitskräften in Schweineställen gegen saisonale Influenza unterstreicht.

Zusätzliches Material



Publication History

Received: 05 March 2024

Accepted: 20 June 2024

Article published online:
24 October 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Salvesen HA, Whitelaw CBA. Current and prospective control strategies of influenza A virus in swine. Porcine Health Manag 2021; 7: 23
  • 2 Janke BH. Influenza A. Virus Infections in Swine. Vet Pathol 2014; 51: 410-426
  • 3 Webster RG, Bean WJ, Gorman OT. et al. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56: 152-179
  • 4 Chauhan RP, Gordon ML. A Systematic Review Analyzing the Prevalence and Circulation of Influenza Viruses in Swine Population Worldwide. Pathogens 2020; 9: 355
  • 5 Janke BH. Clinicopathological Features of Swine Influenza. Curr Top Microbiol Immunol 2013; 370: 69-83
  • 6 Holyoake P, Kirkland P, Davis R. et al. The First Identified Case of Pandemic H1N1 Influenza in Pigs in Australia: PRODUCTION ANIMALS. Australian Veterinary Journal 2011; 89: 427-431
  • 7 Gumbert S, Froehlich S, Rieger A. et al. Reproductive performance of pandemic influenza A virus infected sow herds before and after implementation of a vaccine against the influenza A (H1N1 ) pdm09 virus. Porcine Health Manag 2020; 6: 4
  • 8 Grøntvedt CA, Er C, Gjerset B. et al. Clinical Impact of Infection with Pandemic Influenza (H1N1) 2009 Virus in Naïve Nucleus and Multiplier Pig Herds in Norway. Influenza Research and Treatment 2011; 2011: 1-6
  • 9 Fablet C, Marois-Créhan C, Simon G. et al. Infectious agents associated with respiratory diseases in 125 farrow-to-finish pig herds: A cross-sectional study. Vet Microbiol 2012; 157: 152-163
  • 10 Deblanc C, Robert F, Pinard T. et al. Pre-infection of pigs with Mycoplasma hyopneumoniae induces oxidative stress that influences outcomes of a subsequent infection with a swine influenza virus of H1N1 subtype. Vet Microbiol 2013; 162: 643-651
  • 11 Maes D, Deluyker H, Verdonck M. et al. Herd factors associated with the seroprevalences of four major respiratory pathogens in slaughter pigs from farrow-to-finish pig herds. Vet Res 2000; 31: 313-327
  • 12 Osbjer K, Berg M, Seng S. et al. Influenza A Virus in Backyard Pigs and Poultry in Rural Cambodia. Transboundary and Emerging Diseases 2016; 64
  • 13 Wei K, Lin Y, Xie D. Evolutionary and ecological dynamics of transboundary disease caused by H5N1 virus in Southeast Asia. Transbound Emerg Dis 2015; 62: 315-327
  • 14 van der Kolk JH. Role for migratory domestic poultry and/or wild birds in the global spread of avian influenza?. Vet Q 2019; 39: 161-167
  • 15 Rajao DS, Vincent AL, Perez DR. Adaptation of Human Influenza Viruses to Swine. Front Vet Sci 2019; 5: 347
  • 16 Gambaryan AS, Karasin AI, Tuzikov AB. et al. Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Res 2005; 114: 15-22
  • 17 Trebbien R, Larsen LE, Viuff BM. Distribution of sialic acid receptors and influenza A virus of avian and swine origin in experimentally infected pigs. Virol J 2011; 8: 434
  • 18 Neumann G, Noda T, Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 2009; 459: 931-939
  • 19 Bhatt S, Lam TT, Lycett SJ. et al. The evolutionary dynamics of influenza A virus adaptation to mammalian hosts. Philos Trans R Soc B Biol Sci 2013; 368: 20120382
  • 20 López-Valinas A, Valle M, Wang M. et al Vaccination against swine influenza in pigs causes different drift evolutionary patterns upon swine influenza virus experimental infection and reduces the likelihood of genomic reassortments. Front Cell Infect Microbiol 2023; Sec Virus and Host
  • 21 Taylor KY, Agu I, José I. et al. Influenza A Virus Reassortment Is Strain Dependent. PLoS Pathog 2023; 19: e1011155
  • 22 Hennig C, Graaf A, Petric PP. et al. Are pigs overestimated as a source of zoonotic influenza viruses?. Porcine Health Manag 2022; 8: 30
  • 23 Brookes SM, Núñez A, Choudhury B. et al. Replication, pathogenesis and transmission of pandemic (H1N1) 2009 virus in non-immune pigs. PLoS One 2010; 5: e9068
  • 24 Lange E, Kalthoff D, Blohm U. et al. Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J Gen Virol 2009; 90: 2119-2123
  • 25 Tellier R. Review of aerosol transmission of influenza A virus. Emerg Infect Dis 2006; 12: 1657-1662
  • 26 Lopez-Moreno G, Culhane MR, Davies P. et al. Farm management practices associated with influenza A virus contamination of people working in Midwestern United States swine farms. Porcine Health Manag 2023; 9: 13
  • 27 Pereda A, Cappuccio J, Quiroga MA. et al. Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerging Infectious Diseases 2010; 16: 304-307
  • 28 Van Reeth K, Vincent AL. Influenza Viruses. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, Zhang J, editors. Diseases of swine. 11th ed. Ames: Wiley; 2019: 576-588
  • 29 Ewald C, Heer A, Havenith U. Factors associated with the occurrence of influenza A virus infections in fattening swine. Berl Munch Tierarztl Wochenschr 1994; 107: 256-262
  • 30 Suriya R, Hassan L, Omar AR. et al. Seroprevalence and risk factors for influenza A viruses in pigs in Peninsular Malaysia. Zoonoses Public Health 2008; 55: 342-351
  • 31 Poljak Z, Dewey CE, Martin SW. et al. Prevalence of and risk factors for influenza in southern Ontario swine herds in 2001 and 2003. Can J Vet Res 2008; 72: 7-17
  • 32 Fablet C, Simon G, Dorenlor V. et al. Different herd level factors associated with H1N1 or H1N2 influenza virus infections in fattening pigs. Prev Vet Med 2013; 112: 257-265
  • 33 Chauhan RP, Gordon ML. A systematic review of influenza A virus prevalence and transmission dynamics in backyard swine populations globally. Porcine Health Manag 2022; 8: 10
  • 34 Chastagner A, Enouf V, Peroz D. et al. Bidirectional human-swine transmission of seasonal influenza A(H1N1)pdm09 virus in Pig Herd, France, 2018. Emerg Infect Dis 2019; 25: 1940-1943
  • 35 Chastagner A, Bonin E, Fablet C. et al. Virus persistence in pig herds led to successive reassortment events between swine and human influenza A viruses, resulting in the emergence of a novel triple-reassortant swine influenza virus. Vet Res 2019; 50: 77
  • 36 Gray GC, Kayali G. Facing pandemic influenza threats: The importance of including poultry and swine workers in preparedness plans. Poult Sci 2009; 88: 880-884
  • 37 Mancera Gracia JC, Pearce DS, Masic A. et al. Influenza A Virus in Swine: Epidemiology, Challenges and Vaccination Strategies. Front Vet Sci 2020; 7: 647 PMID: 33195504; PMCID: PMC7536279
  • 38 Anjorin A-AA, Sausy A, Muller CP. et al. Human Seasonal Influenza Viruses in Swine Workers in Lagos, Nigeria: Consequences for Animal and Public Health. Viruses 2023; 15: 1219
  • 39 Tawfik SA, Azab MM, Ahmed AAA. et al. Illumina MiSeq Sequencing for Preliminary Analysis of Microbiome Causing Primary Endodontic Infections in Egypt. International Journal of Microbiology 2018; 2018: 2837328
  • 40 Zhou H, Wu S, Joo JY. et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009; 4: 381-384
  • 41 Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33: 1870-1874 Epub 2016 Mar 22 PMID: 27004904; PMCID: PMC8210823.
  • 42 Surveillance of infectious diseases in animals and humans in Sweden 2022, National Veterinary Institute (SVA), Uppsala, Sweden. SVA:s rapportserie 89 1654-7098
  • 43 McRebel (by McCaw, M. 1995. PRRS control: whole herd management concepts and research update. Proceedings of the North Carolina Healthy Hogs Seminar, pp. 57-64, Greenville, North Carolina, U.S.A)
  • 44 Deblanc C, Hervé S, Gorin S. et al. Maternally-Derived Antibodies Do Not Inhibit Swine Influenza Virus Replication in Piglets but Decrease Excreted Virus Infectivity and Impair Post-Infectious Immune Responses. Veterinary Microbiology 2018; 216: 142-152
  • 45 Fonville JM, Wilks SH, James SL. et al. Antibody landscapes after influenza virus infection or vaccination. Science 2014; 346: 996-1000
  • 46 Deblanc C, Quéguiner S, Gorin S. et al. Evaluation of the Pathogenicity and the Escape from Vaccine Protection of a New Antigenic Variant Derived from the European Human-Like Reassortant Swine H1N2 Influenza Virus. Viruses 2020; 12: 1155
  • 47 Markowska-Daniel I, Pomorska-Mól M, Pejsak Z. The influence of age and maternal antibodies on the postvaccinal response against swine influenza viruses in pigs. Vet Immunol Immunopathol 2011; 142: 81-86
  • 48 Loeffen WLA, Stockhofe N, Weesendorp E. et al. Efficacy of a Pandemic (H1N1) 2009 Virus Vaccine in Pigs against the Pandemic Influenza Virus Is Superior to Commercially Available Swine Influenza Vaccines. Veterinary Microbiology 2011; 152: 304-314
  • 49 Lopez-Moreno G, Schmitt C, Spronk T. et al. Evaluation of Internal Farm Biosecurity Measures Combined with Sow Vaccination to Prevent Influenza A Virus Infection in Groups of Due-to-Wean Pigs. BMC Vet Res 2022; 18: 393
  • 50 White LA, Torremorell M, Craft ME. Influenza A virus in swine breeding herds: Combination of vaccination and biosecurity practices can reduce likelihood of endemic piglet reservoir. Prev Vet Med 2017; 138: 55-69
  • 51 Rajao DS, Sandbulte MR. et al. Heterologous challenge in the presence of maternally derived antibodies results in vaccine-associated enhanced respiratory disease in weaned piglets. Virology 2016; 491: 79-88
  • 52 Goodell CK, Prickett J, Kittawornrat A. et al Evaluation of Screening Assays for the Detection of Influenza A Virus Serum Antibodies in Swine. Transbound Emerg Dis 2016; 63: 24-35 Epub 2014 Feb 27 24571447
  • 53 Rose N, Hervé S, Eveno E. et al. Dynamics of influenza A virus infections in permanently infected pig farms: evidence of recurrent infections, circulation of several swine influenza viruses and reassortment events. Vet Res 2013; 44: 72
  • 54 WOAH, The World Organisation for Animal Health (2023). Chapter 3.9.7 - Influenza A virus of swine. Manual of Diagnostic Tests and Vaccines for Terristrial Animals 2023 (Terrestrial Manual Online Access) https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.09.07_INF_A_SWINE.pdf [2023-02-10]
  • 55 Pomorska-Mól M, Dors A, Kwit K. et al. Kinetics of Single and Dual Infection of Pigs with Swine Influenza Virus and Actinobacillus Pleuropneumoniae. Veterinary Microbiology 2017; 201: 113-120
  • 56 Pomorska-Mól M, Dors A, Kwit K. et al. Coinfection Modulates Inflammatory Responses, Clinical Outcome and Pathogen Load of H1N1 Swine Influenza Virus and Haemophilus Parasuis Infections in Pigs. BMC Vet Res 2017; 13: 376
  • 57 Vaccination mot säsongs influensa “Vaccination against seasonal influenza” https://www.gardochdjurhalsan.se/ ?s=influensa Accessed 8 February 2024