Abstract
The association of colorectal neoplasia (CRN) with Streptococcus bovis biotype I (SBI) infection is well recognized. However, this is not the case for Streptococcus bovis biotype II (SBII). We conducted this study in order to analyze the relationship between SBII and CRN. We analyzed all cases of bacteremia due to SBI (n = 99) and SBII (n = 36) diagnosed in our hospital (during the period 1988–2011) that were followed up with colonoscopy. In addition, we reviewed the literature (during the period 1982–2011) to select all cases of infection of SB that had undergone colonoscopy or other adequate form of colorectal examination. A multivariate analysis was performed to detect CRN risk factors in patients infected with SB. From the 223 cases of SB infection included in the analysis (135 from our institution and 88 from the literature review), 159 were due to SBI and 64 were caused by SBII. As compared with SBI, the SBII cases had a lower frequency of CRN (27 % vs. 67 %, p <0.001), advanced adenomas (8 % vs. 29 %, p <0.01), and carcinomas (6 % vs. 21 %, p <0.01). In a multivariate analysis, and after adjusting for age, sex, type of infection, and biotype, SBII infection was not associated with CRN: odds ratio (OR) = 0.17; 95 % confidence interval (CI) = 0.09 to 0.33. The only factor independently associated with CRN was SBI infection: OR = 5.7; 95 % CI = 3.0 to 10.9. The prevalence of CRN in patients infected with SBII is significantly lower than patients with SBI and does not appear to be higher than the CRN prevalence among the general population.
Similar content being viewed by others
References
Klein RS, Catalano MT, Edberg SC, Casey JI, Steigbigel NH (1979) Streptococcus bovis septicemia and carcinoma of the colon. Ann Intern Med 91:560–562
Gupta A, Madani R, Mukhtar H (2010) Streptococcus bovis endocarditis, a silent sign for colonic tumour. Colorectal Dis 12:164–171
Gold JS, Bayar S, Salem RR (2004) Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch Surg 139:760–765
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
Tjalsma H, Boleij A (2012) Subtyping of Streptococcus bovis group bacteria is needed to fully understand the clinical value of Streptococcus gallolyticus (S. bovis biotype I) infection as early sign of colonic malignancy. Int J Clin Pract 66:326
Beeching NJ, Christmas TI, Ellis-Pegler RB, Nicholson GI (1985) Streptococcus bovis bacteraemia requires rigorous exclusion of colonic neoplasia and endocarditis. Q J Med 56:439–450
Ruoff KL, Miller SI, Garner CV, Ferraro MJ, Calderwood SB (1989) Bacteremia with Streptococcus bovis and Streptococcus salivarius: clinical correlates of more accurate identification of isolates. J Clin Microbiol 27:305–308
Corredoira-Sánchez J, García-Garrote F, Rabuñal R et al (2012) Association between bacteremia due to Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis I) and colorectal neoplasia: a case–control study. Clin Infect Dis 55:491–496
Boleij A, van Gelder MM, Swinkels DW, Tjalsma H (2011) Clinical importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin Infect Dis 53:870–878
Clarridge JE 3rd, Attorri SM, Zhang Q, Bartell J (2001) 16S ribosomal DNA sequence analysis distinguishes biotypes of Streptococcus bovis: Streptococcus bovis biotype II/2 is a separate genospecies and the predominant clinical isolate in adult males. J Clin Microbiol 39:1549–1552
Herrero IA, Rouse MS, Piper KE, Alyaseen SA, Steckelberg JM, Patel R (2002) Reevaluation of Streptococcus bovis endocarditis cases from 1975 to 1985 by 16S ribosomal DNA sequence analysis. J Clin Microbiol 40:3848–3850
Lee RA, Woo PC, To AP, Lau SK, Wong SS, Yuen KY (2003) Geographical difference of disease association in Streptococcus bovis bacteraemia. J Med Microbiol 52:903–908
Jean SS, Teng LJ, Hsueh PR, Ho SW, Luh KT (2004) Bacteremic Streptococcus bovis infections at a university hospital, 1992–2001. J Formos Med Assoc 103:118–123
Tripodi MF, Fortunato R, Utili R, Triassi M, Zarrilli R (2005) Molecular epidemiology of Streptococcus bovis causing endocarditis and bacteraemia in Italian patients. Clin Microbiol Infect 11:814–819
Corredoira JC, Alonso MP, García JF et al (2005) Clinical characteristics and significance of Streptococcus salivarius bacteremia and Streptococcus bovis bacteremia: a prospective 16-year study. Eur J Clin Microbiol Infect Dis 24:250–255
Beck M, Frodl R, Funke G (2008) Comprehensive study of strains previously designated Streptococcus bovis consecutively isolated from human blood cultures and emended description of Streptococcus gallolyticus and Streptococcus infantarius subsp. coli. J Clin Microbiol 46:2966–2972
Vaska VL, Faoagali JL (2009) Streptococcus bovis bacteraemia: identification within organism complex and association with endocarditis and colonic malignancy. Pathology 41:183–186
Romero B, Morosini MI, Loza E et al (2011) Reidentification of Streptococcus bovis isolates causing bacteremia according to the new taxonomy criteria: still an issue? J Clin Microbiol 49:3228–3233
Lieberman DA, Weiss DG, Bond JH, Ahnen DJ, Garewal H, Chejfec G (2000) Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N Engl J Med 343:162–168
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
Vilaichone RK, Mahachai V, Kullavanijaya P, Nunthapisud P (2002) Spontaneous bacterial peritonitis caused by Streptococcus bovis: case series and review of the literature. Am J Gastroenterol 97:1476–1479
Kim SY, Joo SI, Yi J, Kim EC (2010) A case of Streptococcus gallolyticus subsp. gallolyticus infective endocarditis with colon cancer: identification by 16S ribosomal DNA sequencing. Korean J Lab Med 30:160–165
Liddle AD, Abram S, Iyer S, Andrade AJ (2012) Streptococcus gallolyticus prosthetic joint infection associated with undiagnosed colonic malignancy. Knee Surg Sports Traumatol Arthrosc 20:1069–1070
Bleibel W, D’Silva K, Elhorr A, Bleibel S, Dhanjal U (2007) Streptococcus bovis endophthalmitis: a unique presentation of colon cancer. Dig Dis Sci 52:2336–2339
Nobillot R, Grasland-Guillemet A, Nicolas MH, Le Parc JM (1992) Spondylodiscite au cours d’une septicemia á Streptococcus bovis tolerant á la peniciline G chez un malade cirrhotique. Presse Méd 21:1175
Nobile CB, Figueroa ML (2003) Ovarian abscess due to Streptococcus bovis in a patient with unnoticed colonic cancer. Rev Chil Infectol 20:133–135
Marín E, Navas C, Martín-Vivaldi J, García-Tapia A, Martín-Herrera L (2003) Septic arthritis due to Streptococcus bovis in a patient with cirrhosis of enolic etiology. Rev Esp Enferm Dig 95:503–505
Emerton ME, Crook DW, Cooke PH (1995) Streptococcus bovis-infected total hip arthroplasty. J Arthroplasty 10:554–555
Maurya SP (2011) Streptococcus bovis bacteremia and colorectal carcinoma. Indian J Cancer 48:375–376
Angel-Moreno A, Bolaños M, Buceta E, Hernández M, Frances A, Pérez-Arellano J (2002) Streptococcus bovis bacteremia from a venous access port in a patient with AIDS. Scand J Infect Dis 34:764–766
Barragán-Casas JM, Arroyo-Burguillo P, Sanz-Rojas P, Serrano-Heranz R, Sánchez-Fuentes D (2002) Meningitis por Streptococcus bovis biotipo II. Caso clínico y revisión de la literatura. Enferm Infecc Microbiol Clin 20:537–538
Vilarrasa N, Prats A, Pujol M, Gason A, Viladrich PF (2002) Streptococcus bovis meningitis in a healthy adult patient. Scand J Infect Dis 34:61–62
Cohen LF, Dunbar SA, Sirbasku DM, Clarridge JE 3rd (1997) Streptococcus bovis infection of the central nervous system: report of two cases and review. Clin Infect Dis 25:819–823
Coret Ferrer F, Vilchez Padilla JJ, Igual Adell R, Ferrando Ginestar J (1993) Streptococcus bovis meningitis: no association with colonic malignancy. Clin Infect Dis 17:527–528
Smith AH, Sra HK, Bawa S, Stevens R (2010) Streptococcus bovis meningitis and hemorrhoids. J Clin Microbiol 48:2654–2655
Sturt AS, Yang L, Sandhu K, Pei Z, Cassai N, Blaser MJ (2010) Streptococcus gallolyticus subspecies pasteurianus (biotype II/2), a newly reported cause of adult meningitis. J Clin Microbiol 48:2247–2249
Ben-Ami A, Gandelman G, Ergaz D, Shtoeger Z (1999) Meningitis due to Streptococcus bovis type II. Harefuah 136:105–108
Ackerman Z, Eliakim R, Stalnikowicz R (1995) Spontaneous peritonitis caused by Streptococcus bovis: search for colonic neoplasia. J Clin Gastroenterol 21:263
Lossos IS, Schwaber MJ, Levin T, Ackerman Z (1994) Spontaneous peritonitis caused by Streptococcus bovis. J Clin Gastroenterol 19:346
Tanna MS, Akerman S, Ibrahim CB (2011) Spontaneous bacterial peritonitis secondary to Streptococcus bovis in a patient with chronic chylous ascites. Eur J Gastroenterol Hepatol 23:741–742
Eledrisi MS, Zuckerman MJ, Ho H (2000) Spontaneous bacterial peritonitis caused by Streptococcus bovis. Am J Gastroenterol 95:1110–1111
Medina L, Mora L, García V, Santos J (2011) Acute cholecystitis and bacteraemia due to Streptococcus bovis biotype II. Enferm Infecc Microbiol Clin 29:70–71
Grant RJ, Shang WY, Whitehead TR (1997) Isolated septic arthritis due to Streptococcus bovis. Clin Infect Dis 24:1021
Beadsworth M, Waitt C, Jenkins N, Amadi A, Nye F, Beeching N (2005) A retained intravascular medical device and Streptococcus bovis infection, providing early diagnosis of an occult malignancy. J Infect 50:165–167
Hossenbux K, Dale BA, Walls AD, Lawrence JR (1983) Streptococcus bovis endocarditis and colonic carcinoma: a neglected association. Br Med J (Clin Res Ed) 287:21
Menezo V, Yeo TK, Liyanage S, Lynn W, Lightman S (2004) Ocular symptoms and signs as presenting features of endocarditis caused by Streptococcus bovis II. Hosp Med 65:694–695
Namiduru M, Karaoglan I, Aktaran S, Dikensoy O, Baydar I (2003) A case of septicaemia, meningitis and pneumonia caused by Streptococcus bovis type II. Int J Clin Pract 57:735–736
Heitman SJ, Ronksley PE, Hilsden RJ, Manns BJ, Rostom A, Hemmelgarn BR (2009) Prevalence of adenomas and colorectal cancer in average risk individuals: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 7:1272–1278
Arminski TC, McLean DW (1964) Incidence and distribution of adenomatous polyps of the colon and rectum based on 1,000 autopsy examinations. Dis Colon Rectum 7:249–261
Boleij A, Muytjens CM, 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
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. doi:10-1186/1476-4598-9-249
Ferlitsch M, Reinhart K, Pramhas S et al (2011) Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy. JAMA 306:1352–1358
Strul H, Kariv R, Leshno M et al (2006) The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40–80 years. Am J Gastroenterol 101:255–262
Betés M, Muñoz-Navas MA, Duque JM et al (2003) Use of colonoscopy as a primary screening test for colorectal cancer in average risk people. Am J Gastroenterol 98:2648–2654
Johnson DA, Gurney MS, Volpe RJ et al (1990) A prospective study of the prevalence of colonic neoplasms in asymptomatic patients with an age-related risk. Am J Gastroenterol 85:969–974
Di Sario JA, Foutch PG, Mai HD, Pardy K, Manne RK (1991) Prevalence and malignant potential of colorectal polyps in asymptomatic, average-risk men. Am J Gastroenterol 86:941–945
Rex DK, Lehman GA, Ulbright TM et al (1993) Colonic neoplasia in asymptomatic persons with negative fecal occult blood tests: influence of age, gender, and family history. Am J Gastroenterol 88:825–831
Corredoira J, Alonso MP, Coira A, Varela J (2008) Association between Streptococcus infantarius (formerly S. bovis II/1) bacteremia and noncolonic cancer. J Clin Microbiol 46:1570
Schlegel L, Grimont F, Collins MD, Régnault B, Grimont PA, Bouvet A (2000) Streptococcus infantarius sp. nov., Streptococcus infantarius subsp. infantarius subsp. nov. and Streptococcus infantarius subsp. coli subsp. nov., isolated from humans and food. Int J Syst Evol Microbiol 50:1425–1434
Poyart C, Quesne G, Trieu-Cuot P (2002) Taxonomic dissection of the Streptococcus bovis group by analysis of manganese-dependent superoxide dismutase gene (soda) sequences: reclassification of “Streptococcus infantarius subsp. coli” as Streptococcus lutetiensis sp. nov. and of Streptococcus bovis biotype II.2 as Streptococcus pasteurianus sp. nov. Int J Syst Evol Microbiol 52:1247–1255
Schlegel L, Grimont F, Ageron E, Grimont PA, Bouvet A (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
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Corredoira, J.C., Alonso, M.P., García-País, M.J. et al. Is colonoscopy necessary in cases of infection by Streptococcus bovis biotype II?. Eur J Clin Microbiol Infect Dis 33, 171–177 (2014). https://doi.org/10.1007/s10096-013-1940-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-013-1940-7