Histopathological and cytopathological findings in minipigs infected with Streptococcus suis serotype 2

Xie, Chun; Hou, Yi-Xuan; Zhao, Yu-Ting; Cai, Xue-Hui; Li, Cai-Ying; Li, Pei-Feng; Li, Yun-Zhang; Su, Xue; Yue, Xiu-Wei; Wang, Shu-Jie; Liu, Yong-Gang; Yang, Wei-Jun; Yuan, Cong-Li; Cu, Li; Hua, Xiu-Guo; Yang, Zhi-Biao

doi:10.2478/bvip-2014-0030

Abstract

Five pathogen-free miniature pigs (minipigs) were infected with the virulent strain SH08 of Streptococcus suis 2 (SS2) by intramuscular injection. The pigs died consecutively within 72 h after the challenge. An additional five non-infected pigs were euthanised and used as controls. Microstructural observations showed that degeneration, bleeding, congestion, cellular necrosis, and an increase in inflammatory cells were present in all organs and tissues except the brain. Ultrastructural observations revealed mitochondrial vacuolation and malformed or missing cristae, indicating that infection of minipigs with strain SH08 of SS2 can lead to extensive lesions in major internal organs and tissues. The findings also demonstrated that the minipig is a useful model for the study of SS2 infection.

References

1. Arends J.P., Zanen H.C.: Meningitis caused by Streptococcus suis in humans. Rev Infect Dis 1988, 10, 131-137.10.1093/clinids/10.1.131
Search in Google Scholar
2. Beineke A., Bennecke K., Neis C., Schröder C., Waldmann K.H., Baumgärtner W., Valentin-Weigand P., Baums C.G.: Comparative evaluation of virulence and pathology of Streptococcus suis serotypes 2 and 9 in experimentally infected growers. Vet Microbiol 2008, 128, 423-430.10.1016/j.vetmic.2007.10.028
Search in Google Scholar
3. Berthelot-Hérault F., Gottschalk M., Labbé A., Cariolet R., Kobisch M.: Experimental airborne transmission of Streptococcus suis capsular type 2 in pigs. Vet Microbiol 2001, 82, 69-80.10.1016/S0378-1135(01)00376-5
Search in Google Scholar
4. Domínguez-Punaro M.C., Segura M., Plante M.M., Lacouture S., Rivest S., Gottschalk M.: Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J Immunol 2007, 179, 1842-1854.10.4049/jimmunol.179.3.184217641051
Search in Google Scholar
5. Feng W., Laster S.M., Tompkins M., Brown T., Xu J.S., Altier C., Gomez W., Benfield D., McCaw M.B.: In utero infection by porcine reproductive and respiratory syndrome virus is sufficient to increase susceptibility of piglets to challenge by Streptococcus suis type II. J Virol 2001, 75, 4889-4895.10.1128/JVI.75.10.4889-4895.200111424311312360
Search in Google Scholar
6. Fittipaldi N., Sekizaki T., Takamatsu D., de la Cruz Domínguez- Punaro M., Harel J., Bui N.K., Vollmer W., Gottschalk M.: Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol Microbiol 2008, 70, 1120-1135.10.1111/j.1365-2958.2008.06463.x18990186
Search in Google Scholar
7. Glass-Kaastra S.K., Pearl D.L., Reid-Smith R., McEwen B., Slavic D., Fairles J., McEwen S.A.: Multiple-class antimicrobial resistance surveillance in swine Escherichia coli F4, Pasteurella multocida and Streptococcus suis isolates from Ontario and the impact of the 2004-2006 porcine circovirus type-2 associated disease outbreak. Prev Vet Med 2014, 113, 59-64.10.1016/j.prevetmed.2013.11.00824309129
Search in Google Scholar
8. Johannson L.M.: Meningitis and septicemia in a 7-week-old piglet caused by dual streptococcal infection. Can Vet J 2006, 47, 796-798.
Search in Google Scholar
9. Kimball J.W.: Cell biology. Addison-Wesley Publishing Company, Inc. USA and Canada, 1984. p. 62.
Search in Google Scholar
10. Lun S., Willson P.J.: Expression of green fluorescent protein and its application in pathogenesis studies of serotype 2 Streptococcus suis. J Microbiol Meth 2004, 56, 401-412.10.1016/j.mimet.2003.11.01214967232
Search in Google Scholar
11. Madsen L.W., Nielsen B., Aalbaek B., Jensen H.E., Nielsen J.P., Riising H.J.: Experimental infection of conventional pigs with Streptococcus suis serotype 2 by aerosolic exposure. Acta Vet Scand 2001, 42, 303-306.10.1186/1751-0147-42-303220231411503376
Search in Google Scholar
12. Manzin A., Palmieri C., Serra C., Saddi B., Princivalli M.S., Loi G., Angioni G., Tiddia F., Varaldo P.E. Facinelli B.: Streptococcus suis meningitis without history of animal contact, Italy. Emerg Infect Dis 2008, 14, 1946-1948.10.3201/eid1412.080679263463119046529
Search in Google Scholar
13. Nagel A., Manias V., Busquets N., Sniadowsky S., Anzardi J., Méndez Ede L.: Streptococcus suis meningitis in an immunocompetent patient. Rev Argent Microbiol 2008, 40, 158-160.
Search in Google Scholar
14. Okwumabua O., O'Connor M., Shull E.: A polymerase chain reaction (PCR) assay specific for Streptococcus suis based on the gene encoding the glutamate dehydrogenase. FEMS Microbiol Lett 2003, 218, 79-84.10.1111/j.1574-6968.2003.tb11501.x
Search in Google Scholar
15. Pallarés F.J., Halbur P.G., Schmitt C.S., Roth J.A., Opriessnig T., Thomas P.J., Kinyon J.M., Murphy D., Frank D.E., Hoffman L.J.: Comparison of experimental models for Streptococcus suis infection of conventional pigs. Canad J Vet Res 2003, 67, 225-228.
Search in Google Scholar
16. Reams R.Y., Glickman L.T., Harrington D.D., Thacker H.L., Bowersock T.L.: Streptococcus suis infection in swine: a retrospective study of 256 cases. Part II. Clinical signs, gross and microscopic lesions, and coexisting microorganisms. J Vet Diagn Invest 1994, 6, 326-34.10.1177/104063879400600308
Search in Google Scholar
17. Reams R.Y., Harrington D.D., Glickman L.T., Thacker H.L., Bowersock T.B.: Fibrinohemorrhagic pneumonia in pigs naturally infected with Streptococcus suis. J Vet Diagn Invest 1995, 7, 406-408.10.1177/104063879500700323
Search in Google Scholar
18. Salles M.W., Perez-Casal J., Willson P., Middleton D.M.: Changes in the leukocyte subpopulations of the palatine tonsillar crypt epithelium of pigs in response to Streptococcus suis type 2 infection. Vet Immunol Immunopathol 2002, 87, 51-63.10.1016/S0165-2427(02)00040-5
Search in Google Scholar
19. Sanford S.E.: Gross and histopathological findings in unusual lesions caused by Streptococcus suis in pigs. II. Central nervous system lesions. Canad J Vet Res 1987, 51, 486-489.
Search in Google Scholar
20. Si Y., Yuan F., Chang H., Liu X., Li H., Cai K., Xu Z., Huang Q., Bei W., Chen H.: Contribution of glutamine synthetase to the virulence of Streptococcus suis serotype 2. Vet Microbiol 2009, 139, 80-88.10.1016/j.vetmic.2009.04.02419447571
Search in Google Scholar
21. Sun L.Y., Fan H.J., Lu C.P.: Determination of fibronectinbinding region of FBPS of Streptococcus suis type 2. Wei Sheng Wu Xue Bao 2005, 45, 753-756.
Search in Google Scholar
22. Swildens B., Stockhofe-Zurwieden N., van der Meulen J., Wisselink H.J., Nielen M., Niewold T.A.: Intestinal translocation of Streptococcus suis type 2 EF+ in pigs. Vet Microbiol 2004, 103, 29-33.10.1016/j.vetmic.2004.06.01015381263
Search in Google Scholar
23. Tang F., Bossers A., Harders F., Lu C., Smith H.: Comparative genomic analysis of twelve Streptococcus suis (pro)phages. Genomics 2013, 101, 336-344.10.1016/j.ygeno.2013.04.00523587535
Search in Google Scholar
24. Vadeboncoeur N., Segura M., Al-Numani D., Vanier G., Gottschalk M.: Pro-inflammatory cytokine and chemokine release by human brain microvascular endothelial cells stimulated by Streptococcus suis serotype 2. FEMS Immunol Med Microbiol 2003, 35, 49-58.10.1111/j.1574-695X.2003.tb00648.x12589957
Search in Google Scholar
25. Vanier G., Fittipaldi N., Slater J.D., de la Cruz Domínguez- Punaro M., Rycroft A.N., Segura M., Maskell D.J., Gottschalk M.: New putative virulence factors of Streptococcus suis involved in invasion of porcine brain microvascular endothelial cells. Microb Pathog 2009, 46, 13-20.10.1016/j.micpath.2008.10.00318984036
Search in Google Scholar
26. Vasconcelos D., Middleton D.M., Chirino-Trejo J.M.: Lesions caused by natural infection with Streptococcus suis type 9 in weaned pigs. J Vet Diagn Invest 1994, 6, 335-341.10.1177/1040638794006003097948203
Search in Google Scholar
27. Wang J.C., He K.W., He J.Z., Ni Y.X., Hou J.B., Lu L.X., Liu D.X.: Pathogenicity test on Streptococcus suis 2 in animals. Chinese Veterinary Technology 2001, 31, 23-25.
Search in Google Scholar
28. Wang H.R., Wang C.J., Lu C.P., Pan X.Z., Tao K.H., Tang J.Q.: Detection of virulence-associated factors of Streptococcus suis by multiplex PCR assay. Zhonghua Liu Xing Bing Xue Za Zhi 2005, 26, 640-644.
Search in Google Scholar
29. Wang S.Y., Hua X.G., Zhu J.G., Cui L., Yang Z.B.: Dynamic distribution of Streptococcus suis type 2 in mini-swine model. J Shanghai Jiao Tong Univ (Agricult Sci) 2007, 25, 337-341.
Search in Google Scholar
30. Wang Y., Zhang W., Wu Z., Lu C.: Reduced virulence is an important characteristics of biofilm infection of Streptococcus suis. FEMS Microbiol Lett 2011, 316, 36-43.10.1111/j.1574-6968.2010.02189.x21204925
Search in Google Scholar
31. Wertheim H.F., Nghia H.D., Taylor W., Schultsz C.: Streptococcus suis: an emerging human pathogen. Clin Infect Dis 2009, 48, 617-625.10.1086/59676319191650
Search in Google Scholar
32. Wu F.C., Wei H., Gan S.X., Wang A.D.: Analysis on genetic diversity to Bama miniature pig and Guangxi miniature pigs by RAPD. Acta Biol Exp Sinica 2001, 34, 115-120.
Search in Google Scholar
33. Wu Q.Z., Tian Y., Lu C.P.: Guinea-pig model of Streptococcus suis type 2 induced meningitis and septicaemia. Chinese J Vet Sci 2002, 5, 228-230.
Search in Google Scholar
34. Wu Z., Wang W., Tang M., Shao J., Dai C., Zhang W., Fan H., Yao H., Zong J., Chen D., Wang J., Lu C.: Comparative genomic analysis shows that Streptococcus suis meningitis isolate SC070731 contains a unique 105K genomic island. Gene 2014, 535, 156-164.10.1016/j.gene.2013.11.04424316490
Search in Google Scholar
35. Xu J., Fu S., Liu M., Xu Q., Bei W., Chen H., Tan C.: The two- component system NisK/NisR contributes to the virulence of Streptococcus suis serotype 2. Microbiol Res 2013, (in print).10.1016/j.micres.2013.11.00224342108
Search in Google Scholar
36. Yang W., Cai X., Hao Y., Liu Y., Wang S., Xing R., Gu J., Li C., Yue X., Yuan C., Zhang M., Cui L., Hua X., Yang Z.: Characterization of Streptococcus suis serotype 2 blood infections using RT-qPCR to quantify glutamate dehydrogenase copy numbers. J Microbiol Meth 2010, 83, 326-329.10.1016/j.mimet.2010.09.01320869401
Search in Google Scholar
37. 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 groups, human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis 2006, 12, 914-920.10.3201/eid1206.051194337305216707046
Search in Google Scholar
38. Zhang A., Chen B., Yuan Z., Li R., Liu C., Zhou H., Chen H., Jin M.: HP0197 contributes to CPS synthesis and the virulence of Streptococcus suis via CcpA. PLoS One 2012, 7, e50987.10.1371/journal.pone.0050987351144223226442
Search in Google Scholar
39. Zheng F., Ji H., Cao M., Wang C., Feng Y., Li M., Pan X., Wang J., Qin Y., Hu F., Tang J.: Contribution of the Rgg transcription regulator to metabolism and virulence of Streptococcus suis serotype 2. Infect Immun 2011, 79, 1319-1328.10.1128/IAI.00193-10306750621149588
Search in Google Scholar

Histopathological and cytopathological findings in minipigs infected with Streptococcus suis serotype 2

Abstract

Paradigm

My account