Prevalence of virulence markers and pHS-2-like plasmids among Shigella sonnei and Shigella flexneri isolates originating from shigellosis cases in Romania

Open access

Abstract

The surveillance of shigellosis is carried out under the auspice of the European Centre for Disease Prevention and Control which requires a reliable laboratory-based surveillance at national level. To date, little information is published about the members of Shigella spp. responsible for Romanian cases of shigellosis which hinders the understanding of the current epidemiology of shigellosis. Consequently, this retrospective study aimed to assess the diversity of virulence profiles displayed by the strains circulating in our region, by using key chromosome- and plasmid-associated markers, and to document the prevalence of pHS-2-like plasmid previously proposed as a potential marker for reactive arthritis.

The study focused on 65 Shigella sonnei and 49 Shigella flexneri clinical isolates, originated from local patients, recovered through the national surveillance system in 2009 - 2013. PCR assays were performed for the detection of ipaH, ipaBCD, ial, sen, set1A, set1B, sat, and pic genes, and a PCR-sequencing approach on plasmid preparations was used for identifying pHS-2-specific sequences.

Overall, the virulence markers ranged in prevalence from 21% (set1A, set1B, pic) to 100% (ipaH). S. flexneri isolates displayed a higher content of virulence markers than S. sonnei, the most common genotype, detected exclusively in S. flexneri serotype 2a isolates, being defined by the association ipaH+ipaBCD+ial+sen+sat+set1A+ set1B+pic. pHS-2-like plasmids were found in S. flexneri isolates of various serotypes suggesting the potential to trigger postinfection complications in specific subjects.

This study provided baseline data regarding the molecular characteristics of the Shigella strains from Romania, useful for defining the picture of shigellosis in our region.

1. Nicolas X, Granier H, Le Guen P. Shigellosis or bacillary dysentery. Presse Med. 2007 Nov;36(11 Pt 2):1606-18. DOI: 10.1016/j.lpm.2007.03.001

2. Pfeiffer ML, DuPont HL, Ochoa TJ. The patient presenting with acute dysentery-a systematic review. J Infect. 2012 Apr;64(4):374-86. DOI: 10.1016/j.jinf.2012.01.006

3. Schroeder GN, Hilbi H. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev. 2008 Jan;21(1):134-56. DOI: 10.1128/CMR.00032-07

4. Hodges K, Gill R. Infectious diarrhea: Cellular and molecular mechanisms. Gut Microbes. 2010 Jan;1(1):4-21. DOI: 10.4161/gmic.1.1.11036

5. Parsot C. Shigella spp. and enteroinvasive Escherichia coli pathogenicity factors. FEMS Microbiol Lett. 2005 Nov 1;252(1):11-8. DOI: 10.1016/j.femsle.2005.08.046

6. Hannu T, Mattila L, Siitonen A, Leirisalo-Repo M. Reactive arthritis attributable to Shigella infection: a clinical and epidemiological nationwide study. Ann Rheum Dis. 2005 Apr;64(4):594-8. DOI: 10.1136/ard.2004.027524

7. Martin DJ, White BK, Rossman MG. Reactive arthritis after Shigella gastroenteritis in American military in Afghanistan. J Clin Rheumatol. 2012 Aug;18(5):257-8. DOI: 10.1097/RHU.0b013e3182614bde

8. Tilanus A, Mertens R, Seyler L, Lacor P, Velkeniers B. Reactive arthritis due to Shigella infection after a visit to Egypt: A Late Complication of an Intestinal Infection. Case Rep Gastrointest Med. 2012;2012:972517.

9. Ajene AN, Fischer Walker CL, Black RE. Enteric pathogens and reactive arthritis: a systematic review of Campylobacter, salmonella and Shigella-associated reactive arthritis. J Health Popul Nutr. 2013 Sep;31(3):299-307. DOI: 10.3329/jhpn.v31i3.16515

10. Keat A. Reiter’s syndrome and reactive arthritis in perspective. N Engl J Med. 1983 Dec 29;309(26):1606–15. DOI: 10.1056/NEJM198312293092604

11. Stieglitz H, Fosmire S, Lipsky P. Identification of a 2-Md plasmid from Shigella flexneri associated with reactive arthritis. Arthritis Rheum. 1989 Aug;32(8):937-46. DOI: 10.1002/anr.1780320802

12. Stieglitz H, Lipsky P. Association between reactive arthritis and antecedent infection with Shigella flexneri carrying a 2-Md plasmid and encoding an HLA-B27 mimetic epitope. Arthritis Rheum. 1993 Oct;36(10):1387-91. DOI: 10.1002/art.1780361010

13. Tornieporth NG, John J, Salgado K, de Jesus P, Latham E, Melo MC, et al. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J Clin Microbiol. 1995 May;33(5):1371-4.

14. Farshad S, Sheikhi R, Japoni A, Basiri E, Alborzi A. Characterization of Shigella strains in Iran by plasmid profile analysis and PCR amplification of ipa genes. J Clin Microbiol. 2006 Aug;44(8):2879-83. DOI: 10.1128/JCM.00310-06

15. Vargas M, Gascon J, Jimenez De Anta MT, Vila J. Prevalence of Shigella enterotoxins 1 and 2 among Shigella strains isolated from patients with traveler’s diarrhea. J Clin Microbiol. 1999 Nov;37(11):3608-11.

16. Boisen N, Ruiz-Perez F, Scheutz F, Krogfelt KA, Nataro JP. Short report: high prevalence of serine protease autotransporter cytotoxins among strains of enteroaggregative Escherichia coli. Am J Trop Med Hyg. 2009 Feb;80(2):294-301.

17. Frankel G, Riley L, Giron JA, Valmassoi J, Friedmann A, Strockbine N, et al. Detection of Shigella in feces using DNA amplification. J Infect Dis. 1990 Jun;161(6):1252-6. DOI: 10.1093/infdis/161.6.1252

18. Sansonetti PJ, Tran Van Nhieu G, Egile C. Rupture of the intestinal epithelial barrier and mucosal invasion by Shigella flexneri. Clin Infect Dis. 1999 Mar;28(3):466-75. DOI: 10.1086/515150

19. Farfán MJ, Toro CS, Barry EM, Nataro JP. Shigella enterotoxin-2 is a type III effector that participates in Shigella-induced interleukin 8 secretion by epithelial cells. FEMS Immunol Med Microbiol. 2011 Apr;61(3):332-9. DOI: 10.1111/j.1574-695X.2011.00778.x

20. Sasakawa C, Kamata K, Sakai T, Murayama SY, Makino S, Yoshikawa M. Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and Congo red binding activity in Shigella flexneri. Infect Immun. 1986 Feb;51(2):470-5.

21. Venkatesan MM, Buysse JM, Kopecko DJ. Use of Shigella flexneri ipaC and ipaH gene sequences for the general identification of Shigella spp. and enteroinvasive Escherichia coli. J Clin Microbiol. 1989 Dec;27(12):2687-91.

22. Qu M, Zhang X, Liu G, Huang Y, Jia L, Liang W, et al. An eight-year study of Shigella species in Beijing, China: serodiversity, virulence genes, and antimicrobial resistance. J Infect Dev Ctries. 2014 Jul 14;8(7):904-8. DOI: 10.3855/jidc.3692

23. Roy S, Thanasekaran K, Dutta Roy AR, Sehgal SC. Distribution of Shigella enterotoxin genes and secreted autotransporter toxin gene among diverse species and serotypes of shigella isolated from Andaman Islands, India. Trop Med Int Health. 2006 Nov;11(11):1694-8. DOI: 10.1111/j.1365-3156.2006.01723.x

24. Al-Hasani K, Rajakumar K, Bulach D, Robins-Browne R, Adler B, Sakellaris H. Genetic organization of the she pathogenicity island in Shigella flexneri 2a. Microb Pathog. 2001 Jan;30(1):1-8. DOI: 10.1006/mpat.2000.0404

25. Lluque A, Mosquito S, Gomes C, Riveros M, Durand D, Tilley DH, et al. Virulence factors and mechanisms of antimicrobial resistance in Shigella strains from periurban areas of Lima (Peru). Int J Med Microbiol. 2015 Jun-Aug;305(4-5):480-90. DOI: 10.1016/j.ijmm.2015.04.005

26. Schaumburg F, Alabi AS, Kaba H, Lell B, Becker K, Grobusch MP, et al. Molecular characterization of Shigella spp. from patients in Gabon 2011-2013. Trans R Soc Trop Med Hyg. 2015 Apr;109(4):275-9. DOI: 10.1093/trstmh/tru175

27. Adam T, Siewerdt R, Offermann I, Lang J, Tschäpe H, Sieper J, et al. Prevalence and molecular diversity of pHS-2 plasmids, marker for arthritogenicity, among clinical Escherichia coli Shigella isolates. Microbes Infect. 2003 Jun;5(7):579-92. DOI: 10.1016/S1286-4579(03)00093-5

Revista Romana de Medicina de Laborator

Romanian Journal of Laboratory Medicine

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