Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-29T02:44:25.215Z Has data issue: false hasContentIssue false
  • English
  • Français

Swine influenza surveillance in East and Southeast Asia: a systematic review

Published online by Cambridge University Press:  29 November 2011

Karen Trevennec ,
Benjamin J. Cowling ,
Marisa Peyre ,
Eugénie Baudon ,
Guy-Pierre Martineau  and
François Roger
Karen Trevennec*
Affiliation:
French Agricultural Research Center for International Development (CIRAD), Animal and Integrated Risk Management Research Unit (AGIRs), Montpellier, France Ecole National Vétérinaire de Toulouse (ENVT), INP, Toulouse, France
Benjamin J. Cowling
Affiliation:
University of Hong Kong, Hong Kong Special Administrative Region, People's Republic of China
Marisa Peyre
Affiliation:
French Agricultural Research Center for International Development (CIRAD), Animal and Integrated Risk Management Research Unit (AGIRs), Montpellier, France
Eugénie Baudon
Affiliation:
HKU-Pasteur Research Centre, Hong Kong Special Administrative Region, People's Republic of China
Guy-Pierre Martineau
Affiliation:
Ecole National Vétérinaire de Toulouse (ENVT), INP, Toulouse, France
François Roger
Affiliation:
French Agricultural Research Center for International Development (CIRAD), Animal and Integrated Risk Management Research Unit (AGIRs), Montpellier, France
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

East and Southeast Asia are important pig- and poultry-producing areas, where the majority of production takes place on small-scale farms with low biosecurity levels. This systematic review synthesizes data on swine influenza virology, serology and epidemiology in East and Southeast Asia. A total of 77 research articles, literature reviews and conference papers were selected and analyzed from 510 references retrieved from PubMed and ISI Web of KnowledgeSM. The number of published articles increased in the last 3 years, which may be attributed to improvement in monitoring and/or a better promotion of surveillance data. Nevertheless, large inequalities in surveillance and research among countries are underlined. Virological results represent the largest part of published data, while the serological and epidemiological features of swine influenza in East and Southeast Asia remain poorly described. The literature shows that there have been several emergences of swine influenza in the region, and also considerable evidence of multiple introductions of North American and avian-like European strains. Furthermore, several avian-origin strains are isolated from pigs, including H5 and H9 subtypes. However, their low seroprevalence in swine also shows that pigs remain poorly infected by these subtypes. We conclude that sero-epidemioligical investigations have been neglected, and that they may help to improve virological surveillance. Inter- and intra-continental surveillance of gene flows will benefit the region. Greater investment is needed in swine influenza surveillance, to improve our knowledge of circulating strains as well as the epidemiology and disease burden in the region.

Keywords

swine influenzaSoutheast Asiasurveillancecross-species transmissionemergence
Type
Review Article
Information
Animal Health Research Reviews , Volume 12 , Issue 2 , December 2011 , pp. 213 - 223
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ACIAR (2002). Priorities for Pig Research in Southeast Asia and the Pacific to 2010. Canberra, Australia: Australian Centre for International Agricultural Research.Google Scholar
Bastianelli, D, Derail, L and Klotz, S (2007). Traditional Pig Breeding. CIRAD. Available from http://pigtrop.cirad.fr/content/view/full/1089/(accessed 4 November 2011).Google Scholar
Bi, Y, Fu, G, Chen, J, Peng, J, Sun, Y, Wang, J, Pu, J, Zhang, Y, Gao, H, Ma, G, Tian, F, Brown, IH and Liu, J (2010). Novel swine influenza virus reassortants in pigs, China. Emerging Infectious Diseases 16: 1162–1164.CrossRefGoogle ScholarPubMed
Brown, IH (2000). The epidemiology and evolution of influenza viruses in pigs. Veterinary Microbiology 74: 29–46.CrossRefGoogle ScholarPubMed
Choi, YK, Nguyen, TD, Ozaki, H, Webby, RJ, Puthavathana, P, Buranathal, C, Chaisingh, A, Auewarakul, P, Hanh, NT, Ma, SK, Hui, PY, Guan, Y, Peiris, JS and Webster, RG (2005). Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam and Thailand in 2004. Journal of Virology 79: 10821–10825.CrossRefGoogle ScholarPubMed
Chutinimitkul, S, Thippamom, N, Damrongwatanapokin, S, Payungporn, S, Thanawongnuwech, R, Amonsin, A, Boonsuk, P, Sreta, D, Bunpong, N, Tantilertcharoen, R, Chamnanpood, P, Parchariyanon, S, Theamboonlers, A and Poovorawan, Y (2008). Genetic characterization of H1N1, H1N2 and H3N2 swine influenza virus in Thailand. Archives of Virology 153: 1049–1056.CrossRefGoogle ScholarPubMed
Cocks, P, Abila, R, Bouchot, A, Benigno, C, Morzaria, S, Inthavong, P, Long, NV, Bourgeois-Luthi, N, Scoizet, A and Sieng, S (2009). Cross-Border movement and market chains of large ruminants and pigs in the Greater Mekong SubRegion, Bangkok. Available from http://ulm.animalhealthresearch.asia/newsletters/FAO_ADB_OIE_Cross-Border%20movement%20study_Final%20Report.pdf (accessed 4 November 2011).Google Scholar
Cong, Y, Wang, G, Guan, Z, Chang, S, Zhang, Q, Yang, G, Wang, W, Meng, Q, Ren, W, Wang, C and Ding, Z (2010). Reassortant between human-Like H3N2 and avian H5 subtype influenza A viruses in pigs: a potential public health risk. PLoS ONE 5: e12591.CrossRefGoogle ScholarPubMed
Cong, YL, Wang, CF, Yan, CM, Peng, JS, Jiang, ZL and Liu, JH (2008). Swine infection with H9N2 influenza viruses in China in 2004. Virus Genes 36: 461–469.CrossRefGoogle Scholar
Damrongwatanapokin, S, Parchariyanon, S and Pinyochon, W (2003). Serological study of swine influenza virus H1N1 infection in pigs of Thailand. In: Fourth International Symposium on Emerging and Re-emerging Pig Diseases – June 29–July 2, Rome. Available from http://www.unipr.it/arpa/facvet/dip/dipsa/ric/prrs2003/262-262.pdf (accessed 4 November 2011).Google Scholar
Garten, RJ, Davis, CT, Russell, CA, Shu, B, Lindstrom, S, Balish, A, Sessions, WM, Xu, X, Skepner, E, Deyde, V, Okomo-Adhiambo, M, Gubareva, L, Barnes, J, Smith, CB, Emery, SL, Hillman, MJ, Rivailler, P, Smagala, J, de Graaf, M, Burke, DF, Fouchier, RA, Pappas, C, Alpuche-Aranda, CM, Lopez-Gatell, H, Olivera, H, Lopez, I, Myers, CA, Faix, D, Blair, PJ, Yu, C, Keene, KM, Dotson, PD Jr, Boxrud, D, Sambol, AR, Abid, SH, St George, K, Bannerman, T, Moore, AL, Stringer, DJ, Blevins, P, Demmler-Harrison, GJ, Ginsberg, M, Kriner, P, Waterman, S, Smole, S, Guevara, HF, Belongia, EA, Clark, PA, Beatrice, ST, Donis, R, Katz, J, Finelli, L, Bridges, CB, Shaw, M, Jernigan, DB, Uyeki, TM, Smith, DJ, Klimov, AI and Cox, NJ (2009). Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197–201.CrossRefGoogle ScholarPubMed
Guan, Y, Shortridge, KF, Krauss, S, Li, PH, Kawaoka, Y and Webster, RG (1996). Emergence of avian H1N1 influenza viruses in pigs in China. Journal of Virology 70: 8041–8046.CrossRefGoogle ScholarPubMed
Inui, K (2009). South East Asia Sub-Regional Laboratory Network, Technical Meeting, ed.FAO, Bangkok, Thailand.Google Scholar
Kitikoon, P, Sreta, D, Tuanudom, R, Amonsin, A, Suradhat, S, Oraveerakul, K, Poovorawan, Y and Thanawongnuwech, R (2011). Serological evidence of pig-to-human influenza virus transmission on Thai swine farms. Veterinary Microbiology 148: 413–418.CrossRefGoogle Scholar
Kundin, WD (1970). Hong Kong A-2 influenza virus infection among swine during a human epidemic in Taiwan. Nature 228: 857.CrossRefGoogle ScholarPubMed
Kuntz-Simon, G and Madec, F (2009). Genetic and antigenic evolution of swine influenza viruses in Europe and evaluation of their zoonotic potential. Zoonoses and Public Health 56: 310–325.CrossRefGoogle ScholarPubMed
Kupradinun, S, Peanpijit, P, Bhodhikosoom, C, Yoshioka, Y, Endo, A and Nerome, K (1991). The first isolation of swine H1N1 influenza viruses from pigs in Thailand. Archives of Virology 118: 289–297.CrossRefGoogle ScholarPubMed
Lekcharoensuk, P, Nanakorn, J, Wajjwalku, W, Webby, R and Chumsing, W (2010). First whole genome characterization of swine influenza virus subtype H3N2 in Thailand. Vet Microbiol 145 (3-4): 230–244.CrossRefGoogle ScholarPubMed
Li, H, Xin, X, Yang, H, Li, Y, Qin, Y, Xuehui, C, Chen, H, Yu, K, Bi, Y and Tong, G (2003). Serological and virologic surveillance for swine influenza virus infections among pigs over large areas in China in 1998–2002, paper presented to the 4th International Symposium on Emerging and Re-emerging Pig Diseases, Rome, June 29–July 2, 2003.Google Scholar
Li, H, Yu, K, Xin, X, Yang, H, Li, Y, Qin, Y, Bi, Y, Tong, G and Chen, H (2004). Serological and virologic surveillance of swine influenza in China from 2000 to 2003. International Congress Series 1263: 754–757.CrossRefGoogle Scholar
Liu, W, Wei, MT, Tong, Y, Tang, F, Zhang, L, Fang, L, Yang, H and Cao, WC (2011). Seroprevalence and genetic characteristics of five subtypes of influenza A viruses in the Chinese pig population: a pooled data analysis. Veterinary Journal 187: 200–206.CrossRefGoogle ScholarPubMed
Nakharuthai, C, Boonsoongnern, A, Poolperm, P, Wajjwalku, W, Urairong, K, Chumsing, W, Lertwitcharasarakul, P and Lekcharoensuk, P (2008). Occurrence of swine influenza virus infection in swine with porcine respiratory disease complex. Southeast Asian Journal of Tropical Medicine and Public Health 39: 1045–1053.Google ScholarPubMed
Ngo, LT, Hiromoto, Y, Pham, VP, Le, HT, Nguyen, HT, Le, VT, Takemae, N and Saito, T (2011). Isolation of novel triple-reassortant swine H3N2 influenza viruses possessing the hemagglutinin and neuraminidase genes of a seasonal influenza virus in Vietnam in 2010. Influenza and Other Respiratory Viruses doi: 10.1111/j.1750-2659.2011.00267.x [Epublication ahead of print].Google ScholarPubMed
Nidom, CA, Takano, R, Yamada, S, Sakai-Tagawa, Y, Daulay, S, Aswadi, D, Suzuki, T, Suzuki, Y, Shinya, K, Iwatsuki-Horimoto, K, Muramoto, Y and Kawaoka, Y (2010). Influenza A (H5N1) viruses from pigs. Indonesia. Emerging Infectious Diseases 16: 1515–1523.CrossRefGoogle ScholarPubMed
Ninomiya, A, Takada, A, Okazaki, K, Shortridge, KF and Kida, H (2002). Seroepidemiological evidence of avian H4, H5, and H9 influenza A virus transmission to pigs in southeastern China. Veterinary Microbiology 88: 107–114.CrossRefGoogle ScholarPubMed
OFFLU (2010). Strategy Document for Surveillance and Monitoring of Influenzas in Animals. OIE-FAO Network of Expertise on Influenza. Available from http://www.offlu.net/(accessed 20 January 2010).Google Scholar
OFFLU (2011). Technical Meeting – Coordinating worldwide surveillance for influenza in pigs, OIE, FAO, Paris, France, 6–7 April 2011. Available at http://www.offlu.net/fileadmin/home/en/news/pdf/SIV-Summary_final.pdf (accessed 4 November 2011).Google Scholar
Olsen, C, Brown, I, Easterday, B and Van Reeth, K (2006). Swine influenza. Diseases of Swine. 9th edn.Ames, IA: Blackwell Publishing, pp. 469–482.Google Scholar
Parchariyanon, S (2006). Investigation of influenza A virus infection in pigs from 5 reported AIV outbreak provinces in 2004. Journal of the Thai Veterinary Medical Association 57: 16–25.Google Scholar
Peiris, JS, Guan, Y, Markwell, D, Ghose, P, Webster, RG and Shortridge, KF (2001). Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? Journal of Virology 75: 9679–9686.CrossRefGoogle ScholarPubMed
Qi, X, Pang, B and Lu, CP (2009). Genetic characterization of H1N1 swine influenza A viruses isolated in eastern China. Virus Genes 39(2): 193–199.CrossRefGoogle ScholarPubMed
Santhia, K, Ramy, A, Jayaningsih, P, Samaan, G, Putra, AA, Dibia, N, Sulaimin, C, Joni, G, Leung, CY, Sriyal, J, Peiris, M, Wandra, T and Kandun, N (2009). Avian influenza A H5N1 infections in Bali Province, Indonesia: a behavioral, virological and seroepidemiological study. Influenza and Other Respiratory Viruses 3: 81–89.CrossRefGoogle ScholarPubMed
Shi, W, Lei, F, Zhu, C, Sievers, F and Higgins, DG (2010). A complete analysis of HA and NA genes of influenza A viruses. PLoS ONE 5: e14454.CrossRefGoogle ScholarPubMed
Shieh, HK, Chang, PC, Chen, TH, Li, KP and Chan, CH (2008). Surveillance of avian and swine influenza in the swine population in Taiwan, 2004. Journal of Microbiology Immunology Infection 41: 231–42.Google ScholarPubMed
Shortridge, K and Stuart-Harris, C (1982). An influenza epicentre? Lancet 320: 812–813.CrossRefGoogle Scholar
Shu, LL, Zhou, NN, Sharp, GB, He, SQ, Zhang, TJ, Zou, WW and Webster, RG (1996). An epidemiological study of influenza viruses among Chinese farm families with household ducks and pigs. Epidemiology and Infection 117: 179–188.CrossRefGoogle ScholarPubMed
Smith, GJ, Vijaykrishna, D, Bahl, J, Lycett, SJ, Worobey, M, Pybus, OG, Ma, SK, Cheung, CL, Raghwani, J, Bhatt, S, Peiris, JS, Guan, Y and Rambaut, A (2009). Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122–1125.CrossRefGoogle ScholarPubMed
Song, XH, Xiao, H, Huang, Y, Fu, G, Jiang, B, Kitamura, Y, Liu, W, Liu, D and Gao, GF (2010). Serological surveillance of influenza A virus infection in swine populations in Fujian province, China: no evidence of naturally occurring H5N1 infection in pigs. Zoonoses and Public Health 57: 291–298.CrossRefGoogle ScholarPubMed
Sreta, D, Tantawet, S, Na Ayudhya, SN, Thontiravong, A, Wongphatcharachai, M, Lapkuntod, J, Bunpapong, N, Tuanudom, R, Suradhat, S, Vimolket, L, Poovorawan, Y, Thanawongnuwech, R, Amonsin, A and Kitikoon, P (2010). Pandemic (H1N1) 2009 virus on commercial swine farm, Thailand. Emerg Infect Dis 16(10): 1587–1590.CrossRefGoogle ScholarPubMed
Suriya, R, Hassan, L, Omar, AR, Aini, I, Tan, CG, Lim, YS and Kamaruddin, MI (2008). Seroprevalence and risk factors for influenza a viruses in pigs in peninsular Malaysia. Zoonoses and Public Health 55: 342–351.CrossRefGoogle ScholarPubMed
Takano, R, Nidom, CA, Kiso, M, Muramoto, Y, Yamada, S, Shinya, K, Sakai-Tagawa, Y and Kawaoka, Y (2009). A comparison of the pathogenicity of avian and swine H5N1 influenza viruses in Indonesia. Archives of Virology 154: 677–681.CrossRefGoogle ScholarPubMed
Takemae, N, Parchariyanon, S, Damrongwatanapokin, S, Uchida, Y, Ruttanapumma, R, Watanabe, C, Yamaguchi, S and Saito, T (2008). Genetic diversity of swine influenza viruses isolated from pigs during 2000 to 2005 in Thailand. Influenza and Other Respiratory Viruses 2: 181–189.CrossRefGoogle ScholarPubMed
Thawatsupha, P, Waicharoen, S, Maneewong, P, Prasittikhet, K, Chittaganapitch, M and Sawanpanyalert, P (2003). Isolation and identification of influenza virus strains circulating in Thailand in 2001. Southeast Asian J Trop Med Public Health 34(1): 94–97.Google ScholarPubMed
Trevennec, K, Mortier, F, Lyazrhi, F, Huong, HT, Chevalier, V and Roger, F (2011). Swine influenza in Vietnam: preliminary results of epidemiological studies. Influenza and Other Respiratory Viruses 5: 71–73.Google Scholar
Tu, J, Zhou, H, Jiang, T, Li, C, Zhang, A, Guo, X, Zou, W, Chen, H and Jin, M (2009). Isolation and molecular characterization of equine H3N8 influenza viruses from pigs in China. Archives of Virology 154: 887–890.CrossRefGoogle ScholarPubMed
Van Reeth, K and Nicoll, A (2009). A human case of swine influenza virus infection in Europe–implications for human health and research. European Surveillance 14: 19124.Google ScholarPubMed
Vijaykrishna, D, Poon, LLM, Zhu, HC, Ma, SK, Li, OTW, Cheung, CL, Smith, GJD, Peiris, JSM and Guan, Y (2010). Reassortment of pandemic H1N1/2009 influenza A Virus in swine. Science 328: 1529.CrossRefGoogle ScholarPubMed
Vijaykrishna, D, Smith, GJD, Pybus, OG, Zhu, H, Bhatt, S, Poon, LLM, Riley, S, Bahl, J, Ma, SK and Cheung, CL (2011). Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473: 519–522.CrossRefGoogle ScholarPubMed
Vincent, AL, Ma, W, Lager, KM, Janke, BH and Richt, JA (2008). Swine influenza viruses a North American perspective. Advances in Virus Research 72: 127–154.CrossRefGoogle ScholarPubMed
Webby, RJ and Webster, RG (2001). Emergence of influenza A viruses. Philosophical Transactions of the Royal Society London B: Biological Sciences 356: 1817–1828.CrossRefGoogle ScholarPubMed
Webster, RG, Bean, WJ, Gorman, OT, Chambers, TM and Kawaoka, Y (1992). Evolution and ecology of influenza A viruses. Microbiological Reviews 56: 152–179.CrossRefGoogle ScholarPubMed
Xu, C, Zhu, Q, Yang, H, Zhang, X, Qiao, C, Chen, Y, Xin, X and Chen, H (2009). Two genotypes of H1N2 swine influenza viruses appeared among pigs in China. Journal of Clinical Virology 46: 192–195.CrossRefGoogle ScholarPubMed
Yu, H, Hua, RH, Wei, TC, Zhou, YJ, Tian, ZJ, Li, GX, Liu, TQ and Tong, GZ (2008). Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. Veterinary Microbiology 131: 82–92.CrossRefGoogle ScholarPubMed
Yu, H, Zhang, GH, Hua, RH, Zhang, Q, Liu, TQ, Liao, M and Tong, GZ (2007). Isolation and genetic analysis of human origin H1N1 and H3N2 influenza viruses from pigs in China. Biochemical and Biophysical Research Communications 356: 91–96.CrossRefGoogle ScholarPubMed
Yu, H, Zhang, PC, Zhou, YJ, Li, GX, Pan, J, Yan, LP, Shi, XX, Liu, HL and Tong, GZ (2009). Isolation and genetic characterization of avian-like H1N1 and novel ressortant H1N2 influenza viruses from pigs in China. Biochemical and Biophysical Research Communications 386: 278–283.CrossRefGoogle ScholarPubMed
Yu, H, Zhou, Y-J, Li, G-X, Ma, J-H, Yan, L-P, Wang, B, Yang, F-R, Huang, M & Tong, G-Z (2011). Genetic diversity of H9N2 influenza viruses from pigs in China: a potential threat to human health? Veterinary Microbiology 149: 254–261.CrossRefGoogle Scholar
Zhang, G, Kong, W, Qi, W, Long, LP, Cao, Z, Huang, L, Qi, H, Cao, N, Wang, W, Zhao, F, Ning, Z, Liao, M and Wan, XF (2011). Identification of an H6N6 swine influenza virus in southern China. Infection, Genetics and Evolution 11: 1174–1177.CrossRefGoogle ScholarPubMed
Zhu, Q, Yang, H, Chen, W, Cao, W, Zhong, G, Jiao, P, Deng, G, Yu, K, Yang, C, Bu, Z, Kawaoka, Y and Chen, H (2008). A naturally occurring deletion in its NS gene contributes to the attenuation of an H5N1 swine influenza virus in chickens. Journal of Virology 82: 220–228.CrossRefGoogle Scholar