Serological and molecular epidemiological study on swine influenza in Zambia.

Publisher: Blackwell Verlag Country of Publication: Germany NLM ID: 101319538 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1865-1682 (Electronic) Linking ISSN: 18651674 NLM ISO Abbreviation: Transbound Emerg Dis Subsets: MEDLINE

Original Publication: Berlin : Blackwell Verlag

Influenza A Virus, H1N1 Subtype*/genetics ; Influenza A virus*/genetics ; Influenza, Human* ; Orthomyxoviridae Infections*/epidemiology ; Orthomyxoviridae Infections*/veterinary ; Swine Diseases*; Animals ; Humans ; Influenza A Virus, H3N2 Subtype/genetics ; Phylogeny ; Swine ; Zambia/epidemiology

Influenza A viruses (IAVs) cause highly contagious respiratory diseases in humans and animals. In 2009, a swine-origin pandemic H1N1 IAV, designated A(H1N1)pdm09 virus, spread worldwide, and has since frequently been introduced into pig populations. Since novel reassortant IAVs with pandemic potential may emerge in pigs, surveillance for IAV in pigs is therefore necessary not only for the pig industry but also for public health. However, epidemiological information on IAV infection of pigs in Africa remains sparse. In this study, we collected 246 serum and 605 nasal swab samples from pigs in Zambia during the years 2011-2018. Serological analyses revealed that 49% and 32% of the sera collected in 2011 were positive for hemagglutination-inhibition (HI) and neutralizing antibodies against A(H1N1)pdm09 virus, respectively, whereas less than 5.3% of sera collected during the following period (2012-2018) were positive in both serological tests. The positive rate and the neutralization titres to A(H1N1)pdm09 virus were higher than those to classical swine H1N1 and H1N2 IAVs. On the other hand, the positive rate for swine H3N2 IAV was very low in the pig population in Zambia in 2011-2018 (5.3% and 0% in HI and neutralization tests, respectively). From nasal swab samples, we isolated one H3N2 and eight H1N1 IAV strains with an isolation rate of 1.5%. Phylogenetic analyses of all eight gene segments revealed that the isolated IAVs were closely related to human IAV strains belonging to A(H1N1)pdm09 and seasonal H3N2 lineages. Our findings indicate that reverse zoonotic transmission from humans to pigs occurred during the study period in Zambia and highlight the need for continued surveillance to monitor the status of IAVs circulating in swine populations in Africa.
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Adeola, O. A., Olugasa, B. O., & Emikpe, B. O. (2016). Antigenic detection of human strain of influenza virus A (H3N2) in swine populations at three locations in Nigeria and Ghana during the dry early months of 2014. Zoonoses Public Health, 63(2), 106-111. https://doi.org/10.1111/zph.12210.
Alexander, D. J., Brown, I. H., Harris, P. A., & Mccauley, J. W. (1998). Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. Journal of General Virology, 79(Pt 12), 2947-2955. https://doi.org/10.1099/0022-1317-79-12-2947.
Brown, I. H. (2000). The epidemiology and evolution of influenza viruses in pigs. Veterinary Microbiology, 74(1-2), 29-46. https://doi.org/10.1016/s0378-1135(00)00164-4.
Cao, N., Zhu, W., Chen, Ye, Tan, L., Zhou, P., Cao, Z., Ke, C., Li, Y., Wu, J., Qi, W., Jiao, P., & Zhang, G. (2013). Avian influenza A (H5N1) virus antibodies in pigs and residents of swine farms, southern China. Journal of Clinical Virology, 58(4), 647-651. https://doi.org/10.1016/j.jcv.2013.09.017.
Castrucci, M. R., Donatelli, I., Sidoli, L., Barigazzi, G., Kawaoka, Y., & Webster, R. G. (1993). Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology, 193(1), 503-506. https://doi.org/10.1006/viro.1993.1155.
Chauhan, R. P., & Gordon, M. L. (2020). A systematic review analyzing the prevalence and circulation of influenza viruses in swine population worldwide. Pathogens, 9(5), 355. https://doi.org/10.3390/pathogens9050355.
Dawood, F. S., Jain, S., Finelli, L., Shaw, M. W., Lindstrom, S., Garten, R. J., … Team, N. S.-O. I. A. H. N. V. I. (2009). Emergence of a novel swine-origin influenza A (H1N1) virus in humans. New England Journal of Medicine, 360(25), 2605-2615. https://doi.org/10.1056/NEJMoa0903810.
Ducatez, M. F., Awoume, F., & Webby, R. J. (2015). Influenza A(H1N1)pdm09 virus in pigs, Togo, 2013. Veterinary Microbiology, 177(1-2), 201-205. https://doi.org/10.1016/j.vetmic.2015.02.028.
Harima, H., Kajihara, M., Simulundu, E., Bwalya, E., Qiu, Y., Isono, M., Okuya, K., Gonzalez, G., Yamagishi, J., Hang'ombe, B. M., Sawa, H., Mweene, A. S., & Takada, A. (2020). Genetic and biological diversity of porcine sapeloviruses prevailing in Zambia. Viruses, 12(2), 180. https://doi.org/10.3390/v12020180.
Hiromoto, Y., Parchariyanon, S., Ketusing, N., Netrabukkana, P., Hayashi, T., Kobayashi, T., Takemae, N., & Saito, T. (2012). Isolation of the pandemic (H1N1) 2009 virus and its reassortant with an H3N2 swine influenza virus from healthy weaning pigs in Thailand in 2011. Virus Research, 169(1), 175-181. https://doi.org/10.1016/j.virusres.2012.07.025.
Hoffmann, E., Stech, J., Guan, Y., Webster, R. G., & Perez, D. R. (2001). Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol, 146(12), 2275-2289. https://doi.org/10.1007/s007050170002.
Ito, T., Couceiro, J. N. S. S., Kelm, S., Baum, L. G., Krauss, S., Castrucci, M. R., Donatelli, I., Kida, H., Paulson, J. C., Webster, R. G., & Kawaoka, Y. (1998). Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. Journal of Virology, 72(9), 7367-7373. https://doi.org/10.1128/JVI.72.9.7367-7373.1998.
Kitikoon, P., Vincent, A. L., Jones, K. R., Nilubol, D., Yu, S., Janke, B. H., Thacker, B. J., & Thacker, E. L. (2009). Vaccine efficacy and immune response to swine influenza virus challenge in pigs infected with porcine reproductive and respiratory syndrome virus at the time of SIV vaccination. Veterinary Microbiology, 139(3-4), 235-244. https://doi.org/10.1016/j.vetmic.2009.06.003.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874. https://doi.org/10.1093/molbev/msw054.
Kyriakis, C. S., Brown, I. H., Foni, E., Kuntz-Simon, G., Maldonado, J., Madec, F., Essen, S. C., Chiapponi, C., & Van Reeth, K. (2011). Virological surveillance and preliminary antigenic characterization of influenza viruses in pigs in five European countries from 2006 to 2008. Zoonoses Public Health, 58(2), 93-101. https://doi.org/10.1111/j.1863-2378.2009.01301.x.
Lee, M.-S., Chang, P.-C., Shien, J.-H., Cheng, M.-C., & Shieh, H. K. (2001). Identification and subtyping of avian influenza viruses by reverse transcription-PCR. Journal of Virological Methods, 97(1-2), 13-22. https://doi.org/10.1016/s0166-0934(01)00301-9.
Ludwig, S., Stitz, L., Planz, O., Van, H., Fitch, W. M., & Scholtissek, C. (1995). European swine virus as a possible source for the next influenza pandemic? Virology, 212(2), 555-561. https://doi.org/10.1006/viro.1995.1513.
Ma, W., Kahn, R. E., & Richt, J. A. (2008). The pig as a mixing vessel for influenza viruses: Human and veterinary implications. Journal of Molecular and Genetic Medicine, 3(1), 158-166.
Meseko, C. A., Heidari, A., Odaibo, G. N., & Olaleye, D. O. (2019). Complete genome sequencing of H1N1pdm09 swine influenza isolates from Nigeria reveals likely reverse zoonotic transmission at the human-animal interface in intensive piggery. Infection Ecology & Epidemiology, 9(1), 1696632. https://doi.org/10.1080/20008686.2019.1696632.
Mine, J., Abe, H., Parchariyanon, S., Boonpornprasert, P., Ubonyaem, N., Nuansrichay, B., Takemae, N., Tanikawa, T., Tsunekuni, R., Uchida, Y., & Saito, T. (2019). Genetic and antigenic dynamics of influenza A viruses of swine on pig farms in Thailand. Archives of Virology, 164(2), 457-472. https://doi.org/10.1007/s00705-018-4091-4.
Mine, J., Uchida, Y., Takemae, N., & Saito, T. (2020). Genetic characterization of influenza A viruses in Japanese Swine in 2015 to 2019. Journal of Virology, 94(14). https://doi.org/10.1128/JVI.02169-19.
Munyua, P., Onyango, C., Mwasi, L., Waiboci, L. W., Arunga, G., Fields, B., Mott, J. A., Cardona, C. J., Kitala, P., Nyaga, P. N., & Njenga, M. K. (2018). Identification and characterization of influenza A viruses in selected domestic animals in Kenya, 2010-2012. PLoS One, 13(2), e0192721. https://doi.org/10.1371/journal.pone.0192721.
Nerome, K., Sakamoto, S., Yano, N., Yamamoto, T., Kobayashi, S., Webster, R. G., & Oya, A. (1983). Antigenic characteristics and genome composition of a naturally occurring recombinant influenza virus isolated from a pig in Japan. Journal of General Virology, 64(Pt 12), 2611-2620. https://doi.org/10.1099/0022-1317-64-12-2611.
Ngo, L. T., Hiromoto, Y., Pham, Vu P., Le, Ha T. H., Nguyen, Ha T., Le, Vu T., Takemae, N., & Saito, T. (2012). 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 Other Respir Viruses, 6(1), 6-10. https://doi.org/10.1111/j.1750-2659.2011.00267.x.
Okamatsu, M., Sakoda, Y., Hiono, T., Yamamoto, N., & Kida, H. (2013). Potency of a vaccine prepared from A/swine/Hokkaido/2/1981 (H1N1) against A/Narita/1/2009 (H1N1) pandemic influenza virus strain. Virology Journal, 10, 47. https://doi.org/10.1186/1743-422X-10-47.
Olaleye, O. D., Omilabu, S. A., Baba, S. S., & Fagbami, A. H. (1990). Haemagglutination-inhibiting (HI) antibodies against strains of influenza A virus in horse and pig sera in Nigeria. Journal of Hygiene, Epidemiology, Microbiology and Immunology, 34(4), 365-370.
Olsen, C. W. (2002). The emergence of novel swine influenza viruses in North America. Virus Research, 85(2), 199-210. https://doi.org/10.1016/s0168-1702(02)00027-8.
Ozawa, M., Matsuu, A., Yonezawa, K., Igarashi, M., Okuya, K., Kawabata, T., Ito, K., Tsukiyama-Kohara, K., Taneno, A., & Deguchi, E. (2015). Efficient isolation of Swine influenza viruses by age-targeted specimen collection. Journal of Clinical Microbiology, 53(4), 1331-1338. https://doi.org/10.1128/JCM.02941-14.
Penrith, M.-L., Vosloo, W., Jori, F., & Bastos, A. D.S. (2013). African swine fever virus eradication in Africa. Virus Research, 173(1), 228-246. https://doi.org/10.1016/j.virusres.2012.10.011.
Pensaert, M., Ottis, K., Vandeputte, J., Kaplan, M. M., & Bachmann, P. A. (1981). Evidence for the natural transmission of influenza A virus from wild ducts to swine and its potential importance for man. Bulletin of the World Health Organization, 59(1), 75-78.
Reed, L. J., & Muench, H. (1938). A simple method of estimating fifty per cent endpoints. American Journal of Epidemiology, 27(3), 493-497.
Shortridge, K. F., Webster, R. G., Butterfield, W. K., & Campbell, C. H. (1977). Persistence of Hong Kong influenza virus variants in pigs. Science, 196(4297), 1454-1455. https://doi.org/10.1126/science.867041.
Simulundu, E., Chambaro, H. M., Sinkala, Y., Kajihara, M., Ogawa, H., Mori, A., Ndebe, J., Dautu, G., Mataa, L., Lubaba, C. H., Simuntala, C., Fandamu, P., Simuunza, M., Pandey, G. S., Samui, K. L., Misinzo, G., Takada, A., & Mweene, A. S. (2018). Co-circulation of multiple genotypes of African swine fever viruses among domestic pigs in Zambia (2013-2015). Transboundary and Emerging Diseases, 65(1), 114-122. https://doi.org/10.1111/tbed.12635.
Snoeck, C. J., Abiola, O. J., Sausy, A., Okwen, M. P., Olubayo, A. G., Owoade, A. A., & Muller, C. P. (2015). Serological evidence of pandemic (H1N1) 2009 virus in pigs, West and Central Africa. Veterinary Microbiology, 176(1-2), 165-171. https://doi.org/10.1016/j.vetmic.2014.12.022.
Stafford, K., Stafford, Y., Paton, D., & Gamble, P. (1992). Antibodies to some swine diseases in commercial piggeries in Central Zambia. Revue D Elevage Et De Medecine Veterinaire Des Pays Tropicaux, 45(3-4), 229-230.
Takemae, N., Nguyen, T., Ngo, L. T., Hiromoto, Y., Uchida, Y., Pham, Vu P., Kageyama, T., Kasuo, S., Shimada, S., Yamashita, Y., Goto, K., Kubo, H., Le, Vu T., Van Vo, H., Do, H. T., Nguyen, D. H., Hayashi, T., Matsuu, A., & Saito, T. (2013). Antigenic variation of H1N1, H1N2 and H3N2 swine influenza viruses in Japan and Vietnam. Archives of Virology, 158(4), 859-876. https://doi.org/10.1007/s00705-013-1616-8.
Takemae, N., Parchariyanon, S., Ruttanapumma, R., Hiromoto, Y., Hayashi, T., Uchida, Y., & Saito, T. (2011). Swine influenza virus infection in different age groups of pigs in farrow-to-finish farms in Thailand. Virology Journal, 8, 537. https://doi.org/10.1186/1743-422X-8-537.
Takemae, N., Shobugawa, Y., Nguyen, P. T., Nguyen, T., Nguyen, T. N., To, T. L., Thai, P. D., Nguyen, T. D., Nguyen, D. T., Nguyen, D. K., Do, H. T., Le, T. Q. A., Hua, P. T., Van Vo, H., Nguyen, D. T., Nguyen, D. H., Uchida, Y., Saito, R., & Saito, T. (2016). Effect of herd size on subclinical infection of swine in Vietnam with influenza A viruses. BMC Veterinary Research, 12(1), 227. https://doi.org/10.1186/s12917-016-0844-z.
Tialla, D., Sausy, A., Cissé, A., Sagna, T., Ilboudo, A. K., Ouédraogo, G. A., Hübschen, J. M., Tarnagda, Z., & Snoeck, C. J. (2020). Serological evidence of swine exposure to pandemic H1N1/2009 influenza A virus in Burkina Faso. Veterinary Microbiology, 241, 108572. https://doi.org/10.1016/j.vetmic.2019.108572.
Van Reeth, K. (2007). Avian and swine influenza viruses: Our current understanding of the zoonotic risk. Veterinary Research, 38(2), 243-260. https://doi.org/10.1051/vetres:2006062.
Vincent, A., Awada, L., Brown, I., Chen, H., Claes, F., Dauphin, G., Donis, R., Culhane, M., Hamilton, K., Lewis, N., Mumford, E., Nguyen, T., Parchariyanon, S., Pasick, J., Pavade, G., Pereda, A., Peiris, M., Saito, T., Swenson, S.…Ciacci-Zanella, J. (2014). Review of influenza A virus in swine worldwide: A call for increased surveillance and research. Zoonoses Public Health, 61(1), 4-17. https://doi.org/10.1111/zph.12049.
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., & Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiological Reviews, 56(1), 152-179.
WHO. (2002). WHO manual on animal influenza diagnosis and surveillance. Retrieved from https://apps.who.int/iris/handle/10665/68026.
Wright, P. F., Neumann, G., & Kawaoka, Y. (2013). Orthomyxoviruses. In: D. M. Knipe, P. M. Howley, J. I. Cohen, D. E. Griffin, R. A. Lamb, M. A. Martin, V. R. Racaniello, & B. Roizman (Eds) Fields Virology (6th ed., vol 2,, pp 1186-1243). Philadelphia, United States: Wolters Kluwer/Lippincott Williams, & Winlkins..
Yazawa, S. (2004). Experimental dual infection of pigs with an H1N1 swine influenza virus (A/Sw/Hok/2/81) and Mycoplasma hyopneumoniae. Veterinary Microbiology, 98(3-4), 221-228. https://doi.org/10.1016/j.vetmic.2003.11.005.
Yu, H., Hua, R.-H., Zhang, Q., Liu, T.-Q., Liu, H.-L., Li, G.-X., & Tong, G.-Z. (2008). Genetic evolution of swine influenza A (H3N2) viruses in China from 1970 to 2006. Journal of Clinical Microbiology, 46(3), 1067-1075. https://doi.org/10.1128/JCM.01257-07.

JP15fm0108008 Japan Initiative for Global Research Network of Infectious Diseases; Japan Agency for Medical Research and Development; JP20wm0125008 Japan Program for Infectious Diseases Research and Infrastructure; Japan International Cooperation Agency; JP21jm0110019 Science and Technology Research Partnership for Sustainable Development

Keywords: Zambia; complete genome; influenza A virus; pig; surveillance

Date Created: 20211101 Date Completed: 20220721 Latest Revision: 20220721

20240829

10.1111/tbed.14373

34724353