Influenza A(H1N1)pdm09 Virus in Pigs, Réunion Island

Eric Cardinale¹

, Hervé Pascalis¹, Sarah Temmam², Séverine Hervé², Aure Saulnier, Magali Turpin, Nicolas Barbier, Johny Hoarau, Stéphane Quéguiner, Stéphane Gorin, Coralie Foray, Matthieu Roger, Vincent Porphyre, Paul André, Thierry Thomas, Xavier de Lamballerie, Koussay Dellagi, and Gaëlle Simon

Author affiliations: Le Centre de Recherche et de Veille sur les Maladies Emergentes dans l’Océan Indien, Sainte-Clotilde, Ile de la Réunion, France (E. Cardinale, H. Pascalis, S. Temmam, M. Turpin, J. Hoarau, C. Foray, M. Roger, K. Dellagi); Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Montpellier, France (E. Cardinale, J. Hoarau, C. Foray, M. Roger, V. Porphyre); Institut de Recherche pour le Développement, Sainte-Clotilde (H. Pascalis, M. Turpin, K. Dellagi); Centre National de la Recherche Scientifique–Université de Lyon, Lyon, France (S. Temmam); Agence Nationale de Sécurité Sanitaire, de l’alimentation, de l’Environnement, et du Travail (ANSES), National Reference Laboratory for Swine Influenza, Ploufragan, France (S. Hervé, A. Saulnier, N. Barbier, S. Quéguiner, S. Gorin, G. Simon); Clinique Vétérinaire, Saint-Louis, Ile de la Réunion (P. André); Coopérative des Producteurs de Porcs de la Réunion, Saint-Pierre, Ile de la Réunion (T. Thomas); and Université de la Méditerranée, Marseille, France (X. de Lamballerie)

Abstract

During 2009, pandemic influenza A(H1N1)pdm09 virus affected humans on Réunion Island. Since then, the virus has sustained circulation among local swine herds, raising concerns about the potential for genetic evolution of the virus and possible retransmission back to humans of variants with increased virulence. Continuous surveillance of A(H1N1)pdm09 infection in pigs is recommended.

Influenza A(H1N1)pdm09 virus, which caused the last influenza pandemic among humans, is a unique reassortant derived from swine influenza viruses of the triple reassortant swine North American lineage and the avian-like swine Eurasian lineage (1). Réunion Island, a tropical French overseas department in the southwestern Indian Ocean, was struck by the influenza pandemic during July–August 2009. The epidemic had a high attack rate in humans (estimated clinically at 12.5% and serologically at 40.0%) (2,3). A(H1N1)pdm09 virus was reported to cause a reverse zoonosis in pigs (4); thus, a long-term (2009–2011) serologic and virologic survey was designed to check for transmission of the virus to pigs on Réunion Island, where the pork industry is a key economic activity and no live pigs have been imported since 1978. At 6-month intervals, a local veterinary surveillance system conducts serologic surveillance for pathogenic swine influenza viruses (H1N1, H1N2, and H3N2) among local herds, and during the last 20 years, none have been detected.

The Study

Figure

Thumbnail of Location of farms tested for antibodies against influenza A(H1N1)pdm09 virus in serologic surveys, Réunion Island, 2009–2011. Blue dots, seronegative farms; red dots, seropositive farms.

Figure. . Location of farms tested for antibodies against influenza A(H1N1)pdm09 virus in serologic surveys, Réunion Island, 2009–2011. Blue dots, seronegative farms; red dots, seropositive farms.

During a first step (November 2009–February 2010), seroprevalence rates for A(H1N1)pdm09 virus were assessed in 120 breeding pigs (>4 years old) from 57 farms. Blood was obtained from randomly selected pigs at the only slaughterhouse on the island, where pigs are held for <3 hours. We screened the samples for antibodies to influenza A viruses by using the ID Screen Antibody Influenza A kit (ID.vet, Montpellier, France), and titers were determined by using hemagglutination-inhibition (HI) assays (5) against all classical swine influenza viruses and A(H1N1)pdm09 virus (Table 1). Ninety-eight (81.7%; 95% CI 74.7%–88.5%) of the 120 serum samples were positive for A(H1N1)pdm09 virus (HI titers >20); the range of positive titers was 40–640, and 54.2% of the samples expressed high HI titers (160–640). Of the 98 serum samples, 5 reacted at low titer and with only 1 European A (H1N1) swine virus (titer <20), i.e., >4 dilutions lower than for A(H1N1)pdm09 virus, indicating cross reactivity (6). Thus, pigs from 47 (82.4%) of 57 tested farms had been infected by A(H1N1)pdm09 virus; the seroprevalence rate was 81%–100% for pigs on 79.0% of the farms. Farms with affected pigs were located throughout the island (Figure).