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Streptococcus bovis/Streptococcus equinus complex fecal carriage, colorectal carcinoma, and infective endocarditis: a new appraisal of a complex connection

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Abstract

The proportion of group D streptococcal infective endocarditis (IE) (predominantly due to Streptococcus gallolyticus) and the incidence of colorectal cancer are higher in France than in most European countries. We assumed that this could be explained by a high group D streptococci (GDS) fecal carriage rate. The aims of this study were to re-assess the GDS fecal carriage rate in France and its relationship with colorectal cancer. Consecutive adult subjects who were to undergo a complete colonoscopy were invited to participate. GDS were searched in subjects’ stools before their colonoscopy using biomolecular techniques. Colonoscopic findings were sorted into four subgroups: normal colonoscopy, non-tumoral lesions, benign tumors, and premalignant/malignant tumors. GDS fecal carriages were calculated overall and in each subgroup and compared. The data from 259 subjects were analyzed. GDS were identified in the feces of 12 subjects, with the following distribution: S. lutetiensis (n = 9), S. pasteurianus (n = 2), and S. gallolyticus (n = 1). This accounted for an overall GDS fecal carriage rate of 4.6 %. The GDS fecal carriage rate was 6 % in case of normal colonoscopy, 1.3 % in case of non-tumoral lesions, 3.2 % in case of benign tumors, and 11 % in case of premalignant/malignant tumors. These four percentages were not statistically different. The GDS fecal carriage rate was lower than expected, which did not confirm our working hypothesis. Most strains belonged to S. bovis biotype II, while S. gallolyticus was found only once. These findings suggest that different GDS play different roles in the etiopathogenesis of IE and colorectal cancer.

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References

  1. Klein RS, Recco RA, Catalano MT et al (1977) Association of Streptococcus bovis with carcinoma of the colon. N Engl J Med 297:800–802

    Article  PubMed  CAS  Google Scholar 

  2. Klein RS, Catalano MT, Edberg SC et al (1979) Streptococcus bovis septicemia and carcinoma of the colon. Ann Intern Med 91:560–562

    Article  PubMed  CAS  Google Scholar 

  3. Hoen B, Briançon S, Delahaye F et al (1994) Tumors of the colon increase the risk of developing Streptococcus bovis endocarditis: case–control study. Clin Infect Dis 19:361–362

    Article  PubMed  CAS  Google Scholar 

  4. Schlegel L, Grimont F, Ageron E et al (2003) Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int J Syst Evol Microbiol 53:631–645

    Article  PubMed  CAS  Google Scholar 

  5. Leclercq R, Huet C, Picherot M et al (2005) Genetic basis of antibiotic resistance in clinical isolates of Streptococcus gallolyticus (Streptococcus bovis). Antimicrob Agents Chemother 49:1646–1648

    Article  PubMed  CAS  Google Scholar 

  6. Habib G, Hoen B, Tornos P et al (2009) Guidelines on the prevention, diagnosis, and treatment of infective endocarditis (new version 2009): the Task Force on the Prevention, Diagnosis, and Treatment of Infective Endocarditis of the European Society of Cardiology (ESC). Endorsed by the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and the International Society of Chemotherapy (ISC) for Infection and Cancer. Eur Heart J 30:2369–2413

    Article  PubMed  Google Scholar 

  7. Burns CA, McCaughey R, Lauter CB (1985) The association of Streptococcus bovis fecal carriage and colon neoplasia: possible relationship with polyps and their premalignant potential. Am J Gastroenterol 80:42–46

    PubMed  CAS  Google Scholar 

  8. Gold JS, Bayar S, Salem RR (2004) Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch Surg 139:760–765

    Article  PubMed  Google Scholar 

  9. Abdulamir AS, Hafidh RR, Mahdi LK et al (2009) Investigation into the controversial association of Streptococcus gallolyticus with colorectal cancer and adenoma. BMC Cancer 9:403

    Article  PubMed  Google Scholar 

  10. Al-Jashamy K, Murad A, Zeehaida M et al (2010) Prevalence of colorectal cancer associated with Streptococcus bovis among inflammatory bowel and chronic gastrointestinal tract disease patients. Asian Pac J Cancer Prev 11:1765–1768

    PubMed  Google Scholar 

  11. Abdulamir AS, Hafidh RR, Bakar FA (2010) Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8. Mol Cancer 9:249

    Article  PubMed  Google Scholar 

  12. Garza-González E, Ríos M, Bosques-Padilla FJ et al (2012) Immune response against Streptococcus gallolyticus in patients with adenomatous polyps in colon. Int J Cancer 131:2294–2299

    Article  PubMed  Google Scholar 

  13. Dubrow R, Edberg S, Wikfors E et al (1991) Fecal carriage of Streptococcus bovis and colorectal adenomas. Gastroenterology 101:721–725

    PubMed  CAS  Google Scholar 

  14. Potter MA, Cunliffe NA, Smith M et al (1998) A prospective controlled study of the association of Streptococcus bovis with colorectal carcinoma. J Clin Pathol 51:473–474

    Article  PubMed  CAS  Google Scholar 

  15. Huang C-C, Chang S-C, Shen M-H et al (2008) Streptococcus bovis fecal carriage is not associated with an increased risk of colorectal neoplasm. J Soc Colon Rectal Surgeon 19:71–77

    Google Scholar 

  16. Delahaye F, Goulet V, Lacassin F et al (1995) Characteristics of infective endocarditis in France in 1991. A 1-year survey. Eur Heart J 16:394–401

    PubMed  CAS  Google Scholar 

  17. Hoen B, Alla F, Selton-Suty C et al (2002) Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA 288:75–81

    Article  PubMed  Google Scholar 

  18. Selton-Suty C, Célard M, Le Moing V et al (2012) Preeminence of Staphylococcus aureus in infective endocarditis: a 1-year population-based survey. Clin Infect Dis 54:1230–1239

    Article  PubMed  Google Scholar 

  19. Tripodi MF, Adinolfi LE, Ragone E et al (2004) Streptococcus bovis endocarditis and its association with chronic liver disease: an underestimated risk factor. Clin Infect Dis 38:1394–1400

    Article  PubMed  CAS  Google Scholar 

  20. Hoen B, Chirouze C, Cabell CH et al (2005) Emergence of endocarditis due to group D streptococci: findings derived from the merged database of the International Collaboration on Endocarditis. Eur J Clin Microbiol Infect Dis 24:12–16

    Article  PubMed  CAS  Google Scholar 

  21. Tripodi MF, Fortunato R, Utili R et al (2005) Molecular epidemiology of Streptococcus bovis causing endocarditis and bacteraemia in Italian patients. Clin Microbial Infect 11:814–819

    Article  CAS  Google Scholar 

  22. Giannitsioti E, Chirouze C, Bouvet A et al (2007) Characteristics and regional variations of group D streptococcal endocarditis in France. Clin Microbiol Infect 13:770–776

    Article  PubMed  CAS  Google Scholar 

  23. Corredoira J, Alonso MP, Coira A et al (2008) Characteristics of Streptococcus bovis endocarditis and its differences with Streptococcus viridans endocarditis. Eur J Clin Microbiol Infect Dis 27:285–291

    Article  PubMed  CAS  Google Scholar 

  24. Institut National du Cancer. Epidémiologie des cancers en France métropolitaine—incidence et mortalité. Available online at: http://www.lesdonnees.e-cancer.fr. Accessed 26 November 2012

  25. Institut de Veille Sanitaire. Bulletin épidémiologique hebdomadaire numéro thématique—dépistage organisé du cancer colorectal en France. Available online at: http://www.invs.sante.fr/beh/. Accessed 26 November 2012

  26. Chauvenet M, Cottet V, Lepage C et al (2011) Trends in colorectal cancer incidence: a period and birth-cohort analysis in a well-defined French population. BMC Cancer 11:282

    Article  PubMed  Google Scholar 

  27. Ferlay J, Autier P, Boniol M et al (2007) Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 18:581–592

    Article  PubMed  CAS  Google Scholar 

  28. Weisburg WG, Barns SM, Pelletier DA et al (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  29. Devulder G, Perrière G, Baty F et al (2003) BIBI, a bioinformatics bacterial identification tool. J Clin Microbiol 41:1785–1787

    Article  PubMed  CAS  Google Scholar 

  30. Norfleet RG, Mitchell PD (1993) Streptococcus bovis does not selectively colonize colorectal cancer and polyps. J Clin Gastroenterol 17:25–28

    Article  PubMed  CAS  Google Scholar 

  31. Shanan S, Gumaa SA, Sandström G et al (2011) Significant association of Streptococcus bovis with malignant gastrointestinal diseases. Int J Microbiol 2011:792019

    PubMed  Google Scholar 

  32. Boleij A, Van Gelder MMHJ, Swinkels DW et al (2011) Clinical importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin Infect Dis 53:870–878

    Article  PubMed  CAS  Google Scholar 

  33. Koenig JE, Spor A, Scalfone N et al (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108:4578–4585

    Article  PubMed  CAS  Google Scholar 

  34. Woodmansey EJ, McMurdo MET, Macfarlane GT et al (2004) Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects. Appl Environ Microbiol 70:6113–6122

    Article  PubMed  CAS  Google Scholar 

  35. Nam Y-D, Jung M-J, Roh SW et al (2011) Comparative analysis of Korean Human gut microbiota by barcoded pyrosequencing. PLoS One 6:e22109

    Article  PubMed  CAS  Google Scholar 

  36. De Filippo C, Cavalieri D, Di Paola M et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107:14691–14696

    Article  PubMed  Google Scholar 

  37. Fédération Nationale des Observatoires Régionaux de la Santé. Le cancer dans les régions de France. Available online at: http://www.fnors.org/fnors/ors/travaux/synthesekcer.pdf. Accessed 26 November 2012

  38. Boleij A, Muytjens CMJ, Bukhari SI et al (2011) Novel clues on the specific association of Streptococcus gallolyticus subsp gallolyticus with colorectal cancer. J Infect Dis 203:1101–1109

    Article  PubMed  CAS  Google Scholar 

  39. Ellmerich S, Schöller M, Duranton B et al (2000) Promotion of intestinal carcinogenesis by Streptococcus bovis. Carcinogenesis 21:753–756

    Article  PubMed  CAS  Google Scholar 

  40. Biarc J, Nguyen IS, Pini A et al (2004) Carcinogenic properties of proteins with pro-inflammatory activity from Streptococcus infantarius (formerly S.bovis). Carcinogenesis 25:1477–1484

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge Mathilde Choux who performed the bacteriological analyses.

Funding

This work was supported by a research grant from the French Ministry of Health Program (Programme Hospitalier de Recherche Clinique, PHRC).

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All authors do not have any commercial or other association that might pose a conflict of interest.

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Correspondence to C. Chirouze.

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Chirouze, C., Patry, I., Duval, X. et al. Streptococcus bovis/Streptococcus equinus complex fecal carriage, colorectal carcinoma, and infective endocarditis: a new appraisal of a complex connection. Eur J Clin Microbiol Infect Dis 32, 1171–1176 (2013). https://doi.org/10.1007/s10096-013-1863-3

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  • DOI: https://doi.org/10.1007/s10096-013-1863-3

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