Epidemiology of Streptococcus suis in pork meat, pig’s organs, and samples from pigs collected from farms in Khon Kaen Province: Molecular serotyping and antibiotic susceptibility

Main Article Content

Kochakorn Direksin
Nusara Suwannachote
Chuleeporn Saksangawong

Abstract

Objective: To survey, classify serotypes, and test for antimicrobial susceptibility of Streptococcus suis in edible pig meat and organs and in pigs on farms.


Materials and methods: The study was conducted in Khon Kaen Province between June 2019 and December 2020. A total of 417 samples were collected, including pig meat sold at markets (n = 200), edible pig organs (n = 120), oral swabs of piglets (n = 15), oral swabs of nursery pigs (n = 13), vaginal swabs of sows (n = 11), and stillborn pigs (n = 58). Bacterial culture was performed on the samples, followed by molecular identification, molecular serotyping, and antibiotic disc diffusion tests against 14 drugs (7 antibiotic groups).


Results: S. suis was found in pork (6/200; 3%), edible pig organs (14/120; 11.7%), oral cavity of piglets (1/15; 6.7%), oral cavity of nursery pigs (1/13; 7.7%), and stillborn pigs (8/58; 13.6%), but the bacterium was not found in samples from the sow's vagina. The most common strain was serotype 2 (n = 16), followed by serotype 7 (n = 6), serotype 9 (n = 6), and other serotypes (n = 2) that were not classified in this study. Among the 30 isolates, most were susceptible to Penicillins, Cephalosporins, and Fluoroquinolones but resistant to Erythromycin, Kanamycin, and Oxytetracycline.


Conclusion: Consumption of pork sold in Khon Kaen has a relatively low risk of S. suis infection because of low contamination rates. S. suis detection in pigs’ organs and live pigs, on the other hand, indicates S. suis infections in the pigs. In addition, the presence of S. suis in the oral cavity of live pigs suggests an oronasal transmission route, which can easily occur in intensive pig production systems. The dominant serotype 2 (or 1/2) found in this study indicates widespread infection among pigs and consequent pork contamination by this strain.

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References

Bi Y, Li J, Yang L, Zhang S, Li Y, Jia X, Liu W, 2014. Assessment of the pathogenesis of Streptococcus suis type 2 infection in piglets for understanding streptococcal toxic shock-like syndrome, meningitis, and sequelae. Vet Microbiol 173, 299–309. https://doi.org/10.1016/j.vetmic.2014.08.010

Boonyong N, Kaewmongkol S, Khunbutsri D, Satchasataporn K, Meekhanon N, 2019. Contamination of Streptococcus suis in pork and edible pig organs in central Thailand. Vet World 12, 165–169. https://doi.org/10.14202/vetworld.2019.165-169

Chuzeville S, Auger JP, Dumesnil A, Roy D, Lacouture S, Fittipaldi N, Grenier D, Gottschalk M, 2017. Serotype-specific role of antigen I/II in the initial steps of the pathogenesis of the infection caused by Streptococcus suis. Vet Res 48. https://doi.org/10.1186/s13567-017-0443-4

Correa-Fiz F, Neila-Ibáñez C, López-Soria S, Napp S, Martinez B, Sobrevia L, Tibble S, Aragon V, Migura-Garcia L, 2020. Feed additives for the control of post-weaning Streptococcus suis disease and the effect on the faecal and nasal microbiota. Sci Rep 10, 20354. https://doi.org/10.1038/s41598-020-77313-6

Direksin K, Liu D, 2020. Chinese Consumers' opinion about safe and premium quality pork: Survey at Beibei District, Chongqing, People's Republic of China. J Appl Anim Sci 13(1), 9-18.

Dolinsky AL, CLSI, Clinical and Laboratory Standards Institute (CLSI), 2018. M100 performance standards for antimicrobial susceptibility testing. J Serv Mark. https://doi.org/10.1108/08876049410065598

Dutkiewicz J, Zając V, Sroka J, Wasiński B, Cisak E, Sawczyn A, Kloc A, Wójcik-Fatla A, 2018. Streptococcus suis: A re-emerging pathogen associated with occupational exposure to pigs or pork products. Part II – pathogenesis. Ann Agric Environ Med 25, 186–203. https://doi.org/10.26444/aaem/85651

Gottschalk M. 2015. Emergence of Streptococcus suis serotype 9 infection in humans. J Microbiol Immunol Infect 16, 10–11. https://doi.org/10.1016/j.jmii.2015.06.011

Hatrongjit R, Kerdsin A, Gottschalk M, Takeuchi D, Hamada S, Oishi K, 2015. First human case report of sepsis due to infection with Streptococcus suis serotype 31 in Thailand. BMC Infect Dis 15, 1–7. https://doi.org/10.1186/s12879-015-1136-0

Hoa NT, Chieu TTB, Nga TTT, Dung NV, Campbell J, Anh PH, Huu Tho H, Van Vinh Chau N, Bryant JE, Hien TT, Farrar J, Schultsz C, 2011. slaughterhouse pigs are a major reservoir of Streptococcus suis serotype 2 capable of causing human infection in Southern Vietnam. PLoS One 6, e17943. https://doi.org/10.1371/journal.pone.0017943

Huan H, Jiang L, Tang L, Wang Y, Guo S, 2020. Isolation and characterization of Streptococcus suis strains from swine in Jiangsu province, China. J Appl Microbiol 128. https://doi.org/10.1111/jam.14591

Huong VTL, Long HB, Kinh NV, Ngan TTD, Dung VTV, Nadjm B, van Doorn HR, Hoa NT, Horby P, Wertheim HFL, 2018. Long-term outcomes of patients with Streptococcus suis infection in Viet Nam: A case-control study. J Infect 76. https://doi.org/10.1016/j.jinf.2017.09.019

Ishida S, Hong L, Tien T, Osawa R, Tohya M, Nomoto R, Kawamura Y, Takahashi T, Kikuchi N, Kikuchi K, Sekizaki T, 2014. Development of an appropriate PCR system for the reclassification of Streptococcus suis. J Microbiol Methods 107, 66–70. https://doi.org/10.1016/j.mimet.2014.09.003

Kerdsin A, Akeda Y, Hatrongjit R, Detchawna U, Sekizaki T, Hamada S, Gottschalk M, Oishi K, 2016. Streptococcus suis serotyping by a new multiplex PCR. J Med Microbiol 63, 824–830. https://doi.org/10.1099/jmm.0.069757-0

Kerdsin A, Akeda Y, Takeuchi D, Dejsirilert S, Gottschalk M, Oishi K, 2018. Genotypic diversity of Streptococcus suis strains isolated from humans in Thailand. Eur J Clin Microbiol Infect Dis 37, 917–925. https://doi.org/10.1007/s10096-018-3208-8

Kerdsin A, Dejsirilert S, Akeda Y, Sekizaki T, Hamada S, Gottschalk M, Oishi K, 2012. Fifteen Streptococcus suis serotypes identified by multiplex PCR. J Med Microbiol 61, 1669–1672. https://doi.org/10.1099/jmm.0.048587-0

Mancini F, Adamo F, Creti R, Monaco M, Alfarone G, Pantosti A, Ciervo A, 2016. A fatal case of streptococcal toxic shock syndrome caused by Streptococcus suis carrying tet (40) and tet (O/W/32/O), Italy. J Infect Chemother 22, 774–776. https://doi.org/10.1016/j.jiac.2016.05.011

Matiasovic J, Zouharova M, Nedbalcova K, Kralova N, Matiaskova K, Simek B, Kucharovicova I, Gottschalk M, 2020. Resolution of Streptococcus suis Serotypes 1/2 versus 2 and 1 versus 14 by PCR-Restriction Fragment Length Polymorphism Method. J Clin Microbiol 58. https://doi.org/10.1128/JCM.00480-20

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. J Med Microbiol 66, 662–669. https://doi.org/10.1099/jmm.0.000483

Murase K, Watanabe T, Arai S, Kim H, Tohya M, Ishida-Kuroki K, Võ TH, Nguyễn TPB, Nakagawa I, Osawa R, Nguyễn NH, Sekizaki T, 2019. Characterization of pig saliva as the major natural habitat of Streptococcus suis by analyzing oral, fecal, vaginal, and environmental microbiota. PLoS One 14, e0215983. https://doi.org/10.1371/journal.pone.0215983

Nakaranurack C, Puttilerpong C, Suwanpimolkul G, 2017. A decennium of etiology and antimicrobial susceptibility patterns in patients with infective endocarditis at a university hospital, Thailand. Jpn J Infect Dis 70, 295–300. https://doi.org/10.7883/yoken.JJID.2016.294

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. Anim Microbiome 4. https://doi.org/10.1186/s42523-022-00162-3

Nutravong T, Angkititrakul S, Jiwakanon N, Wongchanthong W, Dejsirilerts S, Nawa Y. 2014. Identification of major Streptococcus suis serotypes 2, 7, 8 and 9 isolated from pigs and humans in upper northeastern Thailand. Southeast Asian J Trop Med Public Health 45.

Okura M, Osaki M, Nomoto R, Arai S, Osawa R, Sekizaki T, Takamatsu D, 2016. Current Taxonomical Situation of Streptococcus suis. Pathogens 5, 45. https://doi.org/10.3390/pathogens5030045

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 J Trop Med Public Health 41, 1454–1461.

Pappas G, 2013. Socio-economic, industrial, and cultural parameters of pig-borne infections. Clin Microbiol Infect. https://doi.org/10.1111/1469-0691.12262

Rayanakorn A, Katip W, Goh BH, Oberdorfer P, Lee LH, 2019. Clinical manifestations and risk factors of Streptococcus suis mortality among Northern Thai population: Retrospective 13-year cohort study. Infect Drug Resist 12. https://doi.org/10.2147/IDR.S233326

Rieckmann K, Müller K, Moter A, Baums CG, Seydel A, 2017. Streptococcus suis serotype 9 endocarditis and subsequent severe meningitis in a growing pig despite specific bactericidal humoral immunity. JMM Case Reports 4. https://doi.org/10.1099/jmmcr.0.005093

Seitz M, Valentin-Weigand P, Willenborg J, 2016. Use of antibiotics and antimicrobial resistance in veterinary medicine as exemplified by the swine pathogen Streptococcus suis. Curr Top Microbiol Immunol 398, 103–121. https://doi.org/10.1007/82_2016_506

Soares TCS, Paes AC, Megid J, Ribolla PEM, Paduan KS, Gottschalk M, 2014. Antimicrobial susceptibility of Streptococcus suis isolated from clinically healthy swine in Brazil. Can J Vet Res 78.

Takeuchi D, Kerdsin A, Pienpringam A, Loetthong P, Samerchea S, 2012. Population-Based Study of Streptococcus suis Infection in Humans in Phayao Province in Northern Thailand. PLoS One 7. https://doi.org/10.1371/journal.pone.0031265

Thongkamkoon P, Kiatyingangsulee T, Gottschalk M, 2017. Serotypes of Streptococcus suis isolated from healthy pigs in Phayao Province, Thailand. BMC Res Notes 10. https://doi.org/10.1186/s13104-016-2354-2

Waack U, Nicholson TL, 2018. Subinhibitory concentrations of amoxicillin, lincomycin, and oxytetracycline commonly used to treat swine increase Streptococcus suis biofilm formation. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.02707

Wangkaew S, Chaiwarith R, Tharavichitkul P, 2006. Streptococcus suis infection: a series of 41 cases from Chiang Mai University Hospital.J infect 52(6), 455–460. https://doi.org/10.1016/j.jinf.2005.02.012

Wiwanitkit V, 2017. Streptococcus suis meningitis in Thailand: A summary of case 101 reports. J Neuroinfectious Dis 08. https://doi.org/10.4172/2314-7326.1000264

Wongjittraporn S, Teerasukjinda O, Yee M, Chung HH, 2014. Streptococcus suis meningoencephalitis with seizure from raw pork ingestion: a case report. Hawaii J Med Public Health 73, 13–14.

Wongnak P, Wiratsudakul A, Nuanualsuwan S, 2020. A risk assessment of pathogenic Streptococcus suis in pork supply chains and markets in Thailand. Food Control 118, 107432. https://doi.org/10.1016/j.foodcont.2020.107432

Xu X, Tang Q, Luo R, 2021. Purulent meningitis caused by Streptococcus suis: a case report. Chinese J Neurol 54. https://doi.org/10.3760/cma.j.cn113694-20200512-00347

Zhou Y, Dong X, Li Z, Zou G, Lin L, Wang X, Chen H, Gasser RB, Li J, 2017. Predominance of Streptococcus suis ST1 and ST7 in human cases in China, and detection of a novel sequence type, st658. Virulence 8. https://doi.org/10.1080/21505594.2016.1243193