Antimicrobial Susceptibility, Serotypes, and Genetic Diversity of Streptococcus suis in Diseased and Healthy Pigs in Southern China

In the study, the characteristics of 81 Streptococcus suis isolates recovered from healthy and diseased pigs in Southern China were analyzed. These isolates showed differential resistance rates of over 40% to 22 and over 80% to 11 antibiotics out of 42 tested drugs. These isolates belonged to 6 serotypes (2, 3, 7, 9, 19, and 28), 9.9% of which were characterised as non-typable (NT), and were classified into 15 sequence types (STs), 8 of which were new (ST812-ST815, ST821-823, and ST832). Additionally, 6 virulence-associated gene patterns (VAGPs) and 10 random amplified polymorphic DNA (RAPD) patterns were found among the 81 strains. Among the 4 genotyping methods used in this study, multilocus sequence typing (MLST) provided the highest resolution for identification of S. suis strains. Significant differences in STs, RAPD patterns, and VAGPs were observed between strains isolated from healthy pigs and those isolated from diseased pigs. This study did not find any statistically significant correlations between antimicrobial resistance and serotypes, STs, RAPD patterns, VAGPs, or strain sources. Serotype 2 strains were predominant (44.4%) in the study and all of these strains showed the molecular characteristics of highly pathogenic strains in VAGP, GDH sequence types, and MLST. Our results showed that S. suis strains in Southern China are continually evolving, and therefore increased surveillance of S. suis in piggeries must be considered.

Güney Çin’de Hastalıklı ve Sağlıklı Domuzlarda Streptococcus suis’in Antimikrobiyal Direnci, Serotipleri ve Genetik Çeşitliliği

Bu çalışmada Güney Çin’de sağlıklı ve hasta domuzlardan elde edilen 81 Streptococcus suis izolatının özellikleri incelendi. İzolatlar, test edilen 42 antibiyotikten 22’sine %40’ın üzerinde ve 11’ine %80’in üzerinde değişen direnç gösterdi. Bu izolatlar 6 serotipe (2, 3, 7, 9, 19 ve 28) ait olup %9.9’u tiplendirilemeyen olarak karakterize edildi ve 8’i yeni (ST812-ST815, ST821-823 ve ST832) olmak üzere 15 sekans tipine (ST) sınıflandırıldı. Ayrıca, 81 suşta 6 adet virulans ile ilişkili gen şeması (VAGP) ve 10 adet rastgele amplifiye polimorfik DNA (RAPD) şeması bulundu. Çalışmada kullanılan 4 genotiplendirme metodu arasında multilokus sekans tiplendirme (MLST) S. suis suşlarının tespitinde en yüksek rezolusyonu sağladı. Sağlıklı ve hasta domuzlardan izole edilen suşlar arasında sekans tiplerinde, RAPD şemasında ve VAGP’lerde anlamlı farklılıklar gözlemlendi. Çalışmada antimikrobiyal direnç ile serotipler, ST, RAPD şeması, VAGP’ler veya suş kaynakları arasında istatistiksel olarak bir ilişki tespit edilmedi. Serotip 2 suşu çalışmadaki predominant olandı ve tüm bu suşlar VAGP, GDH sekans tipi ve MIST’de oldukça patojenik suşların moleküler özelliklerini göstermekteydi. Elde edilen sonuçlar Güney Çin’de S. suis suşlarının sürekli olarak değiştiğini ve bu yüzden domuzlarda S.suis takibinin gerekli olduğunu göstermiştir.

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1. Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ: Streptococcus suis: An emerging zoonotic. Lancet Infect Dis, 7 (3): 201-209, 2007. DOI: 10.1016/ S1473-3099(07)70001-4

2. Windsor RS, Elliott SD: Streptococcal infection in young pigs: IV An outbreak of streptococcal meningitis in weaned pigs. J Hyg (Lond), 75 (1): 69-78, 1975. DOI: 10.1017/S0022172400047070

3. Staats JJ, Feder I, Okwumabua O, Chengappa MM: Streptococcus suis: Past and present. Vet Res Commun, 21, 381-407, 1997. DOI: 10.1023/ a:1005870317757

4. Kerdsin A, Akeda Y, Hatrongjit R, Detchawna U, Sekizaki T, Hamada S, Gottschalk M, Oishi K: Streptococcus suis serotyping by a new multiplex PCR. J Med Microbiol, 63 (6): 824-830, 2014. DOI: 10.1099/jmm.0.069757-0

5. Pan Z, Ma J, Dong W, Song W, Wang K, Lu C, Yao H: Novel variant serotype of Streptococcus suis isolated from piglets with meningitis. Appl Environ Microbiol, 81 (3): 976-985, 2015. DOI: 10.1128/AEM.02962-14

6. Baums CG, Valentin-Weigand P: Surface-associated and secreted factors of Streptococcus suis in epidemiology pathogenesisand vaccine development. Anim Health Res Rev, 10 (1): 65-83, 2009. DOI: 10.1017/ S146625230999003X

7. Fitipaldi N, Segura M, Grenier D, Gottschalk M: Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol, 7 (2): 259-279, 2012. DOI: 10.2217/fmb.11.149

8. Oh SI, Jeon AB, Jung BY, Byun JW, Gottschalk M, Kim A, Kim JW, Kim HY: Capsular serotypes, virulence-associated genes and antimicrobial susceptibility of Streptococcus suis isolates from pigs in Korea. J Vet Med Sci, 79 (4): 780-787, 2017. DOI: 10.1292/jvms.16-0514

9. Calderaro FF, Moreno LZ, Doto DS, Matajira CEC, Gomes VTM, Ferreira TSP, Mesquita RE, Moreno AM: Characterization of Streptococcus suis through serotyping, SE-AFLP and virulence profile. Pesq Vet Bras, 36 (8): 701-704, 2016. DOI: 10.1590/S0100-736X2016000800004

10. Dong W, Ma J, Zhu Y, Zhu J, Yuan L, Wang Y, Xu J, Pan Z, Wu Z, Zhang W, Lu C1, Yao H: Virulence genotyping and population analysis of Streptococcus suis serotype 2 isolates from China. Infect Genet Evol, 36 (12): 483-489, 2015. DOI: 10.1016/j.meegid.2015.08.021

11. Yongkiettrakul S, Maneerat K, Arechanajan B, Malila Y, Srimanote P, Gottschalk M, Visessanguan W: Antimicrobial susceptibility of Streptococcus suis isolated from diseased pigs, asymptomatic pigs, and human patients in Thailand. BMC Vet Res, 15:5, 2019. DOI: 10.1186/ s12917-018-1732-5

12. Van Hout J, Heuvelink A, Gonggrijp M: Monitoring of antimicrobial susceptibility of Streptococcus suis in the Netherlands, 2013-2015. Vet Microbiol, 194, 5-10, 2016. DOI: 10.1016/j.vetmic.2016.03.014

13. Seitz M, Valentinweigand P, Willenborg J: Use of antibiotics and antimicrobial resistance in veterinary medicine as exemplified by the swine pathogen Streptococcus suis. Curr Top Microbiol Immunol, 398, 103121, 2016. DOI: 10.1007/82_2016_506

14. Zhang CP, Zhang ZQ, Song L, Fan XZ, Wen F, Xu SX, Ning YB: Antimicrobial resistance profile and genotypic characteristics of Streptococcus suis capsular type 2 isolated from clinical carrier sows and diseased pigs in China. Biomed Res Int, 2015:284303, 2015. DOI: 10.1155/ 2015/284303

15. Gurung M, Tamang MD, Moon DC, Kim SR, Jeong JH, Jang GC, Jung SC, Park YH, Lim SK: Molecular basis of resistance to selected antimicrobial agents in the emerging zoonotic pathogen streptococcus suis. J Clin Microbiol, 53 (7): 2332-2336, 2015. DOI: 10.1128/JCM.00123-15

16. Kerdsin A, Akeda Y, Takeuchi D, Dejsirilert S, Gottschalk M, Oishi K: Genotypic diversity of Streptococcus suis strains isolated from humans in Thailand. Eur J Clin Microbiol Infect Dis, 37 (5): 917-925, 2018. DOI: 10.1007/s10096-018-3208-8

17. Doto DS, Moreno LZ, Calderaro FF, Matajira CE, de Moura Gomes VT, Ferreira TS, Mesquita RE, Timenetsky J, Gottschalk M, Moreno AM: Genetic diversity of Streptococcus suis serotype 2 isolated from pigs in Brazil. Can J Vet Res, 80 (2): 106-111, 2016.

18. Wang S, Gao M, An T, Liu Y, Jin J1, Wang G, Jiang C, Tu Y, Hu S, Li J, Wang J, Zhou D, Cai X: Genetic diversity and virulence of novel sequence types of Streptococcus suis from diseased and healthy pigs in China. Front Microbiol, 6:173, 2015. DOI: 10.3389/fmicb.2015.00173

19. Okura M, Lachanc C, Osaki M, Sekiza T, Maruyam F, Nozawa T, Nakagawa I, Hamada S, Rossigno C, Gottschalk M, Takamats D: Development of a two-step multiplex PCR assay for typing of capsular polysaccharide synthesis gene clusters of Streptococcus suis. J Clin Microbiol, 52 (5): 1714-1719, 2014. DOI: 10.1128/JCM.03411-13

20. Soares TC, Gottschalk M, Lacouture S, Megid J, Ribolla PEM, Figueiredo-Pantoja JC, Paes AC: Streptococcus suis in employees and the environment of swine slaughterhouses in São Paulo Brazil: Occurrence risk factors serotype distribution and antimicrobial susceptibility. Can J Vet Res, 79 (4): 279-284, 2015.

21. Silva LMG, Baum CG, Rehm T, Wisselink HJ, Goethe R, ValentinWeigand P: Virulence-associated gene profiling of Streptococcus suis isolates by PCR. Vet Microbiol, 115 (1-3): 117–127, 2006. DOI: 10.1016/j. vetmic.2005.12.013

22. Kim D, Han K, Oh Y, Kim CH, Kang I, Lee J, Gottschalk M, Chae C: Distribution of capsular serotypes and virulence markers of Streptococcus suis isolated frompigs with polyserositis in Korea. Can J Vet Res, 74 (4): 314316, 2010.

23. King SJ, Allen AG, Maskell DJ, Dowson CJ, Whatmore AM: Distribution genetic diversity and variable expression of the gene encoding hyaluronatelyase within the Streptococcus suis population. J Bacteriol, 186 (14): 4740-4747, 2004. DOI: 10.1128/JB.186.14.4740-4747.2004

24. Okwumabua O, Chinnapapakkagari S: Identification of the gene encoding a 38-kilodalton immunogenic and protective antigen of Streptococcus suis. Clin Diagn Lab Immunol, 12 (4): 484-490, 2005. DOI: 10.1128/CDLI.12.4.484-490.2005

25. Rui P, Zhang ZZ, Ma ZJ, Fang H, Yang WJ, Zhang XZ, Chen J, Jia QH: Detection of virulence-associated factors of Streptococcus suis serotype 2 by PCR assay in Hebei Province of China. Afr J Microbiol Res, 6 (5): 10611064, 2012.

26. Okwumabua O, Persaud JS, Reddy PG: Cloning and characterization of the gene encoding the glutamate dehydrogenase of Streptococcus suis serotype 2. Clin Diagn Lab Immunol, 8 (2): 251-257, 2001. DOI: 10.1128/ CDLI.8.2.251-257.2001

27. Kutz R, Okwumabua O: Differentiation of highly virulent strains of Streptococcus suis Serotype 2 according to glutamate dehydrogenase electrophoretic and sequence type. J Clin Microbiol, 46 (10): 3201-3207, 2008. DOI: 10.1128/JCM.02309-07

28. Kidchana A, Meekhanon N, Hatrongjit R, Gottschalk M, Kerdsin A: Application of random amplified polymorphism DNA and 16S-23S rDNA intergenic spacer polymerase chain reaction-restriction fragment length polymorphism to predict major Streptococcus suis clonal complexes isolated from humans and pigs. Mol Cell Probes, 43 (2): 34-39, 2019. DOI: 10.1016/j.mcp.2018.12.002

29. Maneerat K, Yongkiettrakul S, Kramomtong I, Tongtawe P, Tapchaisri P, Luangsuk P, Chaicumpa W, Gottschalk M, Srimanote P: Virulence genes and genetic diversity of Streptococcus suis serotype 2 isolates from Thailand. Transboun Emerg Dis, 60 (Suppl. 2): 69-79, 2013. DOI: 10.1111/tbed.12157

30. Cloutier G, D’Allaire S, Martinez G, Surprenant C, Lacouture S, Gottschalk M: Epidemiology of streptococcus suis serotype 5 infection in a pig herd with and without clinical disease.  Vet Microbiol, 97 (1-2): 135151, 2003. DOI: 10.1016/j.vetmic.2003.09.018

31. King SJ, Leigh JA, Heath PJ, Luque I, Tarradas C, Dowson CG, Whatmore AM: Development of a multilocus sequence typing scheme for the pig pathogen Streptococcus suis: Identification of virulent clones and potential  capsularserotype  exchange. J Clin Microbiol,  40 (10): 36713688, 2002. DOI: 10.1128/JCM.40.10.3671-3680.2002

32. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood evolutionary distance and maximum parsimony methods. Mol Biol Evol, 28 (10): 2731-2739, 2011. DOI: 10.1093/molbev/msr121

33. Jolley KA, Maiden MCJ: BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics, 11: 595, 2010. DOI: 10.1186/1471-2105-11-595

34. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG: eBURST: Inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typingdata. J Bacteriol, 186 (5): 1518-1530, 2004. DOI: 10.1128/JB.186.5.1518-1530.2004

35. Bischoff KM, White DG, McDermott PF, Zhao S, Gaines S, Maurer JJ, Nisbet DJ: Characterization of chloramphenicol resistance in betahemolytic Escherichia coli associated with diarrhea in neonatal swine. J Clin Microbiol, 40 (2): 389-394, 2002. DOI: 10.1128/JCM.40.2.389-394.2002

36. Wisselink HJ, Veldman KT, Van den Eede C, Salmon SA, Mevius DJ: Quantitative susceptibility of Streptococcus suis strains isolated from diseased pigs in seven European countries to antimicrobial agents licenced in veterinary medicine. Vet Microbiol, 113 (1-2): 73-82, 2006. DOI: 10.1016/j.vetmic.2005.10.035

37. Ye C, Bai X, Zhang J, Jing H, Zheng H, Du H, Cui Z, Zhang S, Jin D, Xu Y, Xiong Y, Zhao A, Luo X, Sun Q, Gottschalk M, Xu Y: Spread of Streptococcus suis sequence type 7, China. Emerg Infect Dis, 14 (5): 787791, 2008. DOI: 10.3201/eid1405.070437

38. Chu YW, Cheung TKM, Chu MY, Tsang VYM, Fung JTL, Kam KM, Lo JYC: Resistance to tetracycline, erythromycin and clindamycin in Streptococcus suis serotype 2 in Hong Kong. Int J Antimicrob Agents, 34 (2): 181-182, 2009. DOI: 10.1016/j.ijantimicag.2009.01.007

39. Wang K, Zhang W, Li X, Lu C, Chen J, Fan W, Huang B: Characterization of Streptococcus suis isolates from slaughter swine. Curr Microbiol, 66 (4): 344-349, 2013. DOI: 10.1007/s00284-012-0275-4

40. Feng Y, Zhang H, Wu Z, Wang S, Cao M, Hu D, Wang C: Streptococcus  suis  infection:an emerging/reemerging  challenge  of bacterial infectious diseases? Virulence, 5 (4): 477–497, 2014. DOI: 10.4161/viru.28595

41. Ye C, Zhu X, Jing H, Du H, Segura M, Zheng H, Kan B, Wang L, Bai X, Zhou Y, Cui Z, Zhang S, Jin D, Sun N, Luo X, Zhang J, Gong Z, Wang X, Wang L, Sun H, Li Z, Sun Q, Liu H, Dong B, Ke C, Yuan H, Wang H, Tian K, Wang Y, Gottschalk M, Xu J: Streptococcus suis sequence type 7 outbreak, Sichuan, China. Emerg Infect Dis, 12 (8): 1203-1208, 2006. DOI: 10.3201/eid1208.060232
Kafkas Üniversitesi Veteriner Fakültesi Dergisi-Cover
  • ISSN: 1300-6045
  • Yayın Aralığı: 6
  • Başlangıç: 1995
  • Yayıncı: Kafkas Üniv. Veteriner Fak.
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