Identification of Streptococcus suis carriage in healthy pigs in Chiang Mai, Thailand https://doi.org/10.12982/VIS.2022.027
Article Sidebar
Main Article Content
Abstract
Streptococcus suis (S. suis) belongs to the critical streptococcal swine pathogens affecting financial losses in pig production globally and being concerned as a zoonotic bacterial that causes a severe invasive disease emerging in pigs and humans. Serotype 2 is considered the major serotype and is the most pathogenic S. suis obtained from human cases, and the healthy pigs are known as the major reservoir of S. suis. In this cross-sectional study, S. suis prevalence was conducted in live pigs from 111 farms across Chiang Mai, Thailand. S. suis carriage rate and serotypes were determined from the bacteriological and multiplex PCR method from tonsil swab samples. We found that 18.2% (138/760) of tonsil swab samples and 54.1% (60/111) of pig farms were positive to S. suis, and only one (0.72%) from 138 isolates was identified as serotype 9. Meanwhile, all the remains were identified as non-serotype ½/1/2/7/9/14 strains. In addition, there was an independent relation between age-ranged, farm types, and production systems with S. suis-positive rates at the farm level. The results indicate that both intensive and smallholder production systems can generally be the source of S. suis carriage. Therefore, implementing good husbandry practices and S. suis-infection predisposing factors limiting that appropriate for each farm type is essential to minimize the opportunities of S. suis outbreak in humans.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Arndt, E.R., Farzan, A., Slavic, D., MacInnes, J.I., Friendship, R.M., 2018. An epidemiological study of Streptococcus suis serotypes of pigs in Ontario determined by a multiplex polymerase chain reaction. Can. Vet. J. 59(9), 997-1000.
Beltran-Alcrudo, D., Falco, J.R., Raizman, E., Dietze, K., 2019. Transboundary spread of pig diseases: the role of international trade and travel. BMC Veterinary Research 15, 64.
Correa-Fiz, F., Fraile, L., Aragon, V., 2016. Piglet nasal microbiota at weaning may influence the development of Glässer's disease during the rearing period. BMC Genomics 17, 404.
Djordjevic, S., Stokes, H., Roy Chowdhury, P., 2013. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Frontiers in Microbiology 4, 86.
DLD, 2015. Statistical data on livestock population. Department of Livestock Development, Ministry of Agriculture and Cooperatives, 193 p.
Du, P., Zheng, H., Zhou, J., Lan, R., Ye, C., Jing, H., Jin, D., Cui, Z., Bai, X., Liang, J., Liu, J., Xu, L., Zhang, W., Chen, C., Xu, J., 2017. Detection of Multiple Parallel Transmission Outbreak of Streptococcus suis Human Infection by Use of Genome Epidemiology, China, 2005. Emerg Infect Dis 23, 204-211.
Dutkiewicz, J., Sroka, J., Zając, V., Wasiński, B., Cisak, E., Sawczyn, A., Kloc, A., Wójcik-Fatla, A., 2017. Streptococcus suis: a re-emerging pathogen associated with occupational exposure to pigs or pork products. Part I–Epidemiology. Annals of Agricultural and Environmental Medicine 24, 683-695.
Fittipaldi, N., Segura, M., Grenier, D., Gottschalk, M., 2012. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiology 7, 259-279.
Gottschalk, M., Segura, M., 2019. Streptococcosis. Diseases of Swine, 934-950.
Goyette-Desjardins, G., Auger, J.-P., Xu, J., Segura, M., Gottschalk, M., 2014. Streptococcus suis, an important pig pathogen and emerging zoonotic agent—an update on the worldwide distribution based on serotyping and sequence typing. Emerging microbes & infections 3, 1-20.
Hadjirin, N.F., Miller, E.L., Murray, G.G.R., Yen, P.L.K., Phuc, H.D., Wileman, T.M., Hernandez-Garcia, J., Williamson, S.M., Parkhill, J., Maskell, D.J., Zhou, R., Fittipaldi, N., Gottschalk, M., Tucker, A.W., Hoa, N.T., Welch, J.J., Weinert, L.A., 2021. Large-scale genomic analysis of antimicrobial resistance in the zoonotic pathogen Streptococcus suis. BMC Biology 19, 191.
Hatrongjit, R., Kerdsin, A., Gottschalk, M., Takeuchi, D., Hamada, S., Oishi, K., Akeda, Y., 2015. First human case report of sepsis due to infection with Streptococcus suis serotype 31 in Thailand. BMC Infect Dis 15, 392.
Higgins, R., Gottschalk, M., 1990. An update on Streptococcus suis identification. Journal of Veterinary Diagnostic Investigation 2, 249-252.
Kerdsin, A., Hatrongjit, R., Gottschalk, M., Takeuchi, D., Hamada, S., Akeda, Y., Oishi, K., 2017. Emergence of Streptococcus suis serotype 9 infection in humans. Journal of Microbiology, Immunology and Infection 50, 545-546.
Kerdsin, A., Takeuchi, D., Nuangmek, A., Akeda, Y., Gottschalk, M., Oishi, K., 2020. Genotypic Comparison between Streptococcus suis Isolated from Pigs and Humans in Thailand. Pathogens 9.
Kongkaew, S., Wongsawan, K., Pansumdang, C., Takam, S., Yano, T., Yamsakul, P., Patchanee, P., 2012. Identification and antimicrobial susceptibility of Streptococcus suis isolated from pigs tonsil swabs. Kasetsart Veterinarians 22, 1-13.
Lakkitjaroen, N., Kaewmongkol, S., Metheenukul, P., Karnchanabanthoeng, A., Satchasataporn, K., Abking, N., Rerkamnuaychoke, W., 2011. Prevalence and antimicrobial susceptibility of Streptococcus suis isolated from slaughter pigs in northern Thailand. Agriculture and Natural Resources 45, 78-83.
Luque, I., Blume, V., Borge, C., Vela, A.I., Perea, J.A., Márquez, J.M., Fernández-Garayzábal, J.F., Tarradas, C., 2010. Genetic analysis of Streptococcus suis isolates recovered from diseased and healthy carrier pigs at different stages of production on a pig farm. The Veterinary Journal 186, 396-398.
Marois, C., Bougeard, S., Gottschalk, M., Kobisch, M., 2004. Multiplex PCR assay for detection of Streptococcus suis species and serotypes 2 and 1/2 in tonsils of live and dead pigs. Journal of clinical microbiology 42, 3169-3175.
Meekhanon, N., Kaewmongkol, S., Phimpraphai, W., Okura, M., Osaki, M., Sekizaki, T., Takamatsu, D., 2017. Potentially hazardous Streptococcus suis strains latent in asymptomatic pigs in a major swine production area of Thailand.
Nguyen, N.T.T., Luu, Y.T.H., Hoang, T.D., Nguyen, H.X., Dao, T.D., Bui, V.N., Gray, G.C., 2021. An epidemiological study of Streptococcus suis prevalence among swine at industrial swine farms in Northern Vietnam. One Health 13, 100254.
Nhung, N.T., Yen, N.T.P., Cuong, N., Kiet, B.T., Hien, V.B., Campbell, J., Thwaites, G., Baker, S., Geskus, R., Ashton, P., Carrique-Mas, J., 2020. Carriage of the zoonotic organism Streptococcus suis in chicken flocks in Vietnam. Zoonoses and Public Health 67, 843-848.
Niazy, M., Hill, S., Nadeem, K., Ricker, N., Farzan, A., 2022. Compositional analysis of the tonsil microbiota in relationship to Streptococcus suis disease in nursery pigs in Ontario. Animal Microbiome 4, 10.
Okura, M., Osaki, M., Nomoto, R., Arai, S., Osawa, R., Sekizaki, T., Takamatsu, D., 2016. Current Taxonomical Situation of Streptococcus suis. Pathogens 5.
Okwumabua, O., Peterson, H., Hsu, H.-M., Bochsler, P., Behr, M., 2017. Isolation and partial characterization of Streptococcus suis from clinical cases in cattle. Journal of veterinary diagnostic investigation 29, 160-168.
Opriessnig, T., Giménez-Lirola, L.G., Halbur, P.G., 2011. Polymicrobial respiratory disease in pigs. Animal Health Research Reviews 12, 133-148.
Padungtod, P., Tharavichitkul, P., Junya, S., Chaisowong, W., Kadohira, M., Makino, S., Sthitmatee, N., 2010. Incidence and presence of virulence factors of Streptococcus suis infection in slaughtered pigs from Chiang Mai, Thailand. Southeast Asian journal of tropical medicine and public health 41, 1454.
Pathanasophon, P., Narongsak, W., Worarach, A., Yuwapanichsampan, S., Sagarasaeranee, P., 2009. Prevalence of Streptococcus suis in pigs and pig farmers in 11 provinces in the East and the West of Thailand. Journal of the Thai Veterinary Medical Association 60, 49-62.
Pathanasophon, P., Worarach, A., Narongsak, W., Yuwapanichsampan, S., Nuangmek, A., Sakdasirisathaporn, A., Chuxnum, T., 2013.
Prevalence of Streptococcus suis in Tonsils of Slaughtered Pigs in Lampang and Phayao Provinces, Thailand, 2009-2010. Journal of Tropical Medicine & Parasitology 36, 8-14.
Pena Cortes, L.C., LeVeque, R.M., Funk, J., Marsh, T.L., Mulks, M.H., 2018. Development of the tonsillar microbiome in pigs from newborn through weaning. BMC Microbiology 18, 35.
Rayanakorn, A., Ademi, Z., Liew, D., Lee, L.-H., 2021. Burden of disease and productivity impact of Streptococcus suis infection in Thailand. PLOS Neglected Tropical Diseases 15, e0008985.
Rayanakorn, A., Goh, B.-H., Lee, L.-H., Khan, T.M., Saokaew, S., 2018. Risk factors for Streptococcus suis infection: A systematic review and meta-analysis. Scientific Reports 8, 13358.
Salaneuve, K., Meunier, A., Aubry, K., 2020. Bilateral total deafness after preparation of wild boar meat. European Annals of Otorhinolaryngology, Head and Neck Diseases 137, 419-421.
Segura, M., Aragon, V., Brockmeier, S.L., Gebhart, C., Greeff, A.d., Kerdsin, A., O'Dea, M.A., Okura, M., Saléry, M., Schultsz, C., Valentin-Weigand, P., Weinert, L.A., Wells, J.M., Gottschalk, M., 2020. Update on Streptococcus suis Research and Prevention in the Era of Antimicrobial Restriction: 4th International Workshop on S. suis. Pathogens (Basel, Switzerland) 9, 374.
Smith, H.E., van Bruijnsvoort, L., Buijs, H., Wisselink, H.J., Smits, M.A., 1999. Rapid PCR test for Streptococcus suis serotype 7. FEMS Microbiology Letters 178, 265-270.
Smith Hilde, E., Veenbergen, V., van der Velde, J., Damman, M., Wisselink Henk, J., Smits Mari, A., 1999. The cps Genes of Streptococcus suis Serotypes 1, 2, and 9: Development of Rapid Serotype-Specific PCR Assays. Journal of Clinical Microbiology 37, 3146-3152.
Suzuki, S., Fuchimoto, D., 2019. Fetal and early postnatal development of the porcine tonsils of the soft palate. Experimental animals, 18-0142.
Takeuchi, D., Kerdsin, A., Akeda, Y., Chiranairadul, P., Loetthong, P., Tanburawong, N., Areeratana, P., Puangmali, P., Khamisara, K., Pinyo, W., Anukul, R., Samerchea, S., Lekhalula, P., Nakayama, T., Yamamoto, K., Hirose, M., Hamada, S., Dejsirilert, S., Oishi, K., 2017. Impact of a Food Safety Campaign on Streptococcus suis Infection in Humans in Thailand. The American journal of tropical medicine and hygiene 96, 1370-1377.
Thanapongtharm, W., Linard, C., Chinson, P., Kasemsuwan, S., Visser, M., Gaughan, A.E., Epprech, M., Robinson, T.P., Gilbert, M., 2016. Spatial analysis and characteristics of pig farming in Thailand. BMC Veterinary Research 12, 218.
Thanh Duy, P., Thi Nguyen, T.N., Vu Thuy, D., Chung The, H., Alcock, F., Boinett, C., Dan Thanh, H.N., Thanh Tuyen, H., Thwaites, G.E., Rabaa, M.A., Baker, S., 2020. Commensal Escherichia coli are a reservoir for the transfer of XDR plasmids into epidemic fluoroquinolone-resistant Shigella sonnei. Nature Microbiology 5, 256-264.
Thongkamkoon, P., Kiatyingangsulee, T., Gottschalk, M., 2017. Serotypes of Streptococcus suis isolated from healthy pigs in Phayao Province, Thailand. BMC research notes 10, 53.
Thongsawad, S., 2016. Burden and epidemiological characterisations of Streptococcus suis in Chiang Mai, Thailand, PhD thesis. The University of Edinburgh, Edinburgh.
Wisselink, H.J., Joosten, J.J., Smith, H.E., 2002. Multiplex PCR Assays for Simultaneous Detection of Six Major Serotypes and Two Virulence-Associated Phenotypes of Streptococcus suis in Tonsillar Specimens from Pigs. Journal of Clinical Microbiology 40, 2922-2929.
Wongkumma, A., Hinjoy, S., Choomkhasian, P., 2014. A surveillance report of Streptococcus suis infection in humans, Thailand, 2011–2013. Bureau of Epidemiology, Department of Disease Control, Ministry of Public Health, Nonthaburi.
Yu, H., Jing, H., Chen, Z., Zheng, H., Zhu, X., Wang, H., Wang, S., Liu, L., Zu, R., Luo, L., Xiang, N., Liu, H., Liu, X., Shu, Y., Lee, S.S., Chuang, S.K., Wang, Y., Xu, J., Yang, W., Streptococcus suis study, g., 2006. Human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis 12, 914-920.
Zheng, H., Qiu, X., Roy, D., Segura, M., Du, P., Xu, J., Gottschalk, M., 2017. Genotyping and investigating capsular polysaccharide synthesis gene loci of non-serotypeable Streptococcus suis isolated from diseased pigs in Canada. Veterinary Research 48, 10.
Zou, G., Zhou, J., Xiao, R., Zhang, L., Cheng, Y., Jin, H., Li, L., Zhang, L., Wu, B., Qian, P., Li, S., Ren, L., Wang, J., Oshota, O., Hernandez-Garcia, J., Wileman Thomas, M., Bentley, S., Weinert, L., Maskell Duncan, J., Tucker, A.W., Zhou, R., Drake Harold, L., 2018. Effects of Environmental and Management-Associated Factors on Prevalence and Diversity of Streptococcus suis in Clinically Healthy Pig Herds in China and the United Kingdom. Applied and Environmental Microbiology 84, e02590-02517.