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Prevalence and predictors of small intestinal bacterial overgrowth in irritable bowel syndrome: a systematic review and meta-analysis

Abstract

Background

The reported prevalence of small intestinal bacterial overgrowth (SIBO) among individuals with irritable bowel syndrome (IBS) is highly variable. The aim of the study is to estimate the prevalence and identify predictors of SIBO in IBS.

Methods

PubMed, Cochrane Library, and EMBASE through July 2017 were searched to identify studies evaluating the prevalence of SIBO in IBS. The pooled prevalence of SIBO among individuals with IBS and the pooled odds ratio (OR) of SIBO among those with IBS compared with healthy controls were calculated. Predictors of SIBO among IBS patients were also evaluated.

Results

Fifty studies (8398 IBS, 1432 controls) met the inclusion criteria. Overall pooled prevalence of SIBO in IBS was 38% (95% CI 32–44) and was higher among individuals with IBS (OR 4.7, 95% CI 3.1–7.2) compared with controls. The pooled prevalence of SIBO in IBS was higher in studies diagnosed by breath tests (40%, 95% CI 33–46) compared with cultures (19%, 95% CI 8–30). Among those with IBS, female gender (OR 1.5, 95% CI 1.0–2.1), older age (standard mean difference 3.1 years, 95% CI 0.9–5.4), and IBS-diarrhea (OR 1.7, 95% CI 1.3–2.3) compared with other IBS subtypes increased the odds of SIBO; proton pump inhibitor (PPI) use (OR 1.1, 95% CI 0.7–1.7) was not associated with SIBO.

Conclusions

More than one-third of IBS patients tested positive for SIBO, and the odds of SIBO in IBS were increased by nearly fivefold. The prevalence of SIBO varied according to the diagnostic modality performed. Female gender, older age, and IBS-diarrhea, but not PPI use, were associated with SIBO among individuals with IBS.

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References

  1. Rodriguez-Fandino O, Hernandez-Ruiz J, Schmulson M. From cytokines to toll-like receptors and beyond—current knowledge and future research needs in irritable bowel syndrome. J Neurogastroenterol Motil. 2010;16(4):363–73.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Lovell RM, Ford AC. Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis. Clin Gastroenterol Hepatol. 2012;10(7):712–721.e714.

    Article  PubMed  Google Scholar 

  3. Ghoshal UC, Shukla R, Ghoshal U, et al. The gut microbiota and irritable bowel syndrome: friend or foe? Int J Inflam. 2012;2012:151085.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Reddymasu SC, Sostarich S, McCallum RW. Small intestinal bacterial overgrowth in irritable bowel syndrome: are there any predictors? BMC Gastroenterol. 2010;10:23.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Chu H, Fox M, Zheng X, et al. Small intestinal bacterial overgrowth in patients with irritable bowel syndrome: clinical characteristics, psychological factors, and peripheral cytokines. Gastroenterol Res Pract. 2016;2016:3230859.

    PubMed  PubMed Central  Google Scholar 

  6. Ford AC, Spiegel BM, Talley NJ, et al. Small intestinal bacterial overgrowth in irritable bowel syndrome: systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2009;7(12):1279–86.

    Article  PubMed  Google Scholar 

  7. Posserud I, Stotzer PO, Bjornsson ES, et al. Small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Gut. 2007;56(6):802–8.

    Article  PubMed  Google Scholar 

  8. Pimentel M. Review of rifaximin as treatment for SIBO and IBS. Expert Opin Investig Drugs. 2009;18(3):349–58.

    Article  PubMed  CAS  Google Scholar 

  9. Bures J, Cyrany J, Kohoutova D, et al. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol. 2010;16(24):2978–90.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Ghoshal UC. How to interpret hydrogen breath tests. J Neurogastroenterol Motil. 2011;17(3):312–7.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Pimentel M, Wallace D, Hallegua D, et al. A link between irritable bowel syndrome and fibromyalgia may be related to findings on lactulose breath testing. Ann Rheum Dis. 2004;63(4):450–2.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Ghoshal UC, Srivastava D. Irritable bowel syndrome and small intestinal bacterial overgrowth: meaningful association or unnecessary hype. World J Gastroenterol. 2014;20(10):2482–91.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Sachdeva S, Rawat AK, Reddy RS, et al. Small intestinal bacterial overgrowth (SIBO) in irritable bowel syndrome: frequency and predictors. J Gastroenterol Hepatol. 2011;26(Suppl 3):135–8.

    Article  PubMed  Google Scholar 

  14. Krajicek EJ, Almazar AE, Zinsmeister AR, et al. Clinical predictors of small intestinal bacterial overgrowth (SIBO) by duodenal aspirate culture. Neurogastroenterol Motil. 2016;28:26–7.

    Article  CAS  Google Scholar 

  15. Wells GA, Shea B, O’Connell D et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Hospital Research Institute, Ottawa. 2017.http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed 25 Aug 2017.

  16. Quality Assessment Tool for Case Series Studies (QATCSS). NIH Institute. 2016. https://www.nhlbi.nih.gov/health-pro/guidelines/in-develop/cardiovascular-risk-reducton/tools/case_series. Accessed 2 Sept 2016.

  17. Mitsui T, Shimaoka K, Goto Y, et al. Small bowel bacterial overgrowth is not seen in healthy adults but is in disabled older adults. Hepatogastroenterology. 2006;53(67):82–5.

    PubMed  Google Scholar 

  18. Elphick DA, Chew TS, Higham SE, et al. Small bowel bacterial overgrowth in symptomatic older people: can it be diagnosed earlier? Gerontology. 2005;51(6):396–401.

    Article  PubMed  CAS  Google Scholar 

  19. Su T, Lai S, Lee A, et al. Meta-analysis: proton pump inhibitors moderately increase the risk of small intestinal bacterial overgrowth. J Gastroenterol. 2018;53(1):27–36.

    Article  PubMed  CAS  Google Scholar 

  20. Smith A, Contreras C, Ko KH, et al. Gender-specific protection of estrogen against gastric acid-induced duodenal injury: stimulation of duodenal mucosal bicarbonate secretion. Endocrinology. 2008;149(9):4554–66.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Lupascu A, Gabrielli M, Lauritano EC, et al. Hydrogen glucose breath test to detect small intestinal bacterial overgrowth: a prevalence case–control study in irritable bowel syndrome. Aliment Pharmacol Ther. 2005;22(11–12):1157–60.

    Article  PubMed  CAS  Google Scholar 

  22. Grover M, Kanazawa M, Palsson OS, et al. Small intestinal bacterial overgrowth in irritable bowel syndrome: association with colon motility, bowel symptoms, and psychological distress. Neurogastroenterol Motil. 2008;20(9):998–1008.

    Article  PubMed  CAS  Google Scholar 

  23. Rana SV, Sinha SK, Sikander A, et al. Study of small intestinal bacterial overgrowth in North Indian patients with irritable bowel syndrome: a case control study. Trop Gastroenterol. 2008;29(1):23–5.

    PubMed  CAS  Google Scholar 

  24. Park JH, Park DI, Kim HJ, et al. The relationship between small-intestinal bacterial overgrowth and intestinal permeability in patients with irritable bowel syndrome. Gut Liver. 2009;3(3):174–9.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Parodi A, Dulbecco P, Savarino E, et al. Positive glucose breath testing is more prevalent in patients with IBS-like symptoms compared with controls of similar age and gender distribution. J Clin Gastroenterol. 2009;43(10):962–6.

    Article  PubMed  Google Scholar 

  26. Park JS, Yu JH, Lim HC, et al. Usefulness of lactulose breath test for the prediction of small intestinal bacterial overgrowth in irritable bowel syndrome. Korean J Gastroenterol. 2010;56(4):242–8.

    Article  PubMed  Google Scholar 

  27. Sachdeva S, Rawat AK, Reddy RS, et al. Small intestinal bacterial overgrowth (SIBO) in irritable bowel syndrome (IBS): frequency and predictors. Indian J Gastroenterol. 2010;29(1):A28.

    Article  Google Scholar 

  28. Pyleris M, Giamarellos-Bourboulis EJ, Koussoulas B, et al. Small bowel culture confirms the presence of small intestinal bacterial overgrowth in a subset of IBS subjects. Gastroenterology. 2011;140(5):S152.

    Article  Google Scholar 

  29. Bertelè A, Papadia C, Bosi S, et al. Bacterial overgrowth in irritable bowel syndrome: a cohort study. Dig Liver Dis. 2012;44:S132.

    Article  Google Scholar 

  30. Philip A, Joseph V, Mukunda M, et al. Prevalence of small intestinal bacterial overgrowth in patients with irritable bowel syndrome using lactulose hydrogen breath test. Indian J Gastroenterol. 2013;32(1):A31.

    Google Scholar 

  31. Qing Y. Relationship between the irritable bowel syndrome and small intestinal bacterial. J Gastroenterol Hepatol. 2013;28:375.

    Google Scholar 

  32. Zhao J, Zheng X, Chu H, et al. A study of the methodological and clinical validity of the combined lactulose hydrogen breath test with scintigraphic oro-cecal transit test for diagnosing small intestinal bacterial overgrowth in IBS patients. Neurogastroenterol Motil. 2014;26(6):794–802.

    Article  PubMed  CAS  Google Scholar 

  33. Li N, Wang Z, Fei G, et al. Measurement of methane and hydrogen on lactulose breath test detects small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Neurogastroenterol Motil. 2014;26:46.

    Article  CAS  Google Scholar 

  34. Moraru IG, Moraru AG, Andrei M, et al. Small intestinal bacterial overgrowth is associated to symptoms in irritable bowel syndrome. Evidence from a multicentre study in Romania. Rom J Intern Med. 2014;52(3):143–50.

    PubMed  Google Scholar 

  35. Lombardo L, Foti M, Ruggia O, et al. Increased incidence of small intestinal bacterial overgrowth during proton pump inhibitor therapy. Clin Gastroenterol Hepatol. 2010;8(6):504–8.

    Article  PubMed  Google Scholar 

  36. Evans K, Lunn E, Raza S, et al. Does small intestine bacterial overgrowth cause neurodysmotility in IBS and coeliac disease? Gut. 2012;61:A317.

    Google Scholar 

  37. Abbasi MH, Zahedi M, Darvish Moghadam S, et al. Small bowel bacterial overgrowth in patients with irritable bowel syndrome: the first study in Iran. Middle East J Dig Dis. 2015;7(1):36–40.

    PubMed  PubMed Central  Google Scholar 

  38. Bratten JR, Spanier J, Jones MP. Lactulose breath testing does not discriminate patients with irritable bowel syndrome from healthy controls. Am J Gastroenterol. 2008;103(4):958–63.

    Article  PubMed  CAS  Google Scholar 

  39. Ghoshal UC, Kumar S, Mehrotra M, et al. Frequency of small intestinal bacterial overgrowth in patients with irritable bowel syndrome and chronic non-specific diarrhea. J Neurogastroenterol Motil. 2010;16(1):40–6.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Scarpellini E, Giorgio V, Gabrielli M, et al. Prevalence of small intestinal bacterial overgrowth in children with irritable bowel syndrome: a case–control study. J Pediatr. 2009;155(3):416–20.

    Article  PubMed  CAS  Google Scholar 

  41. Rana SV, Sharma S, Kaur J, et al. Comparison of lactulose and glucose breath test for diagnosis of small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Digestion. 2012;85(3):243–7.

    Article  PubMed  CAS  Google Scholar 

  42. Pimentel M, Chow EJ, Lin HC. Eradication of small intestinal bacterial overgrowth reduces symptoms of irritable bowel syndrome. Am J Gastroenterol. 2000;95(12):3503–6.

    Article  PubMed  CAS  Google Scholar 

  43. Cuoco L, Salvagnini M. Small intestine bacterial overgrowth in irritable bowel syndrome: a retrospective study with rifaximin. Minerva Gastroenterol Dietol. 2006;52(1):89–95.

    PubMed  CAS  Google Scholar 

  44. Majewski M, McCallum RW. Results of small intestinal bacterial overgrowth testing in irritable bowel syndrome patients: clinical profiles and effects of antibiotic trial. Adv Med Sci. 2007;52:139–42.

    PubMed  CAS  Google Scholar 

  45. Madrid SAM, Defilippi CC, Defilippi GC, et al. Small intestinal bacterial overgrowth in patients with functional gastrointestinal diseases. Rev Med Chile. 2007;135(10):1245–52.

    Article  PubMed  Google Scholar 

  46. Law D, Pimentel M. Proton pump inhibitor therapy does not affect hydrogen production on lactulose breath test in subjects with IBS. Dig Dis Sci. 2010;55(8):2302–8.

    Article  PubMed  CAS  Google Scholar 

  47. Mann NS, Logan IJ. Diarrhea dominant irritable bowel patients with small intestinal bacterial overgrowth produce more hydrogen after oral lactulose compared to constipation dominant irritable bowel patients. Gastroenterology. 2010;138(5):S382.

    Google Scholar 

  48. Chodos A, Gandhi D, Kaswala D, et al. Demographic characteristics of patients with irritable bowel syndrome (IBS) and positive lactulose breath test (LBT) and the role of antibiotics. Am J Gastroenterol. 2011;106:S508.

    Article  CAS  Google Scholar 

  49. Dumitrascu DL, Liliana D. Intestinal inflammation detected by fecal calprotectine test is more frequent in postinfectious IBS than in non-postinfectious IBS. Gastroenterology. 2011;140(5):S611.

    Article  Google Scholar 

  50. Yakoob J, Abbas Z, Khan R, et al. Small intestinal bacterial overgrowth and lactose intolerance contribute to irritable bowel syndrome symptomatology in Pakistan. Saudi J Gastroenterol. 2011;17(6):371–5.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Meyrat P, Safroneeva E, Schoepfer AM. Rifaximin treatment for the irritable bowel syndrome with a positive lactulose hydrogen breath test improves symptoms for at least 3 months. Aliment Pharmacol Ther. 2012;36(11–12):1084–93.

    Article  PubMed  CAS  Google Scholar 

  52. Stoicescu A, Andrei M, Becheanu G, et al. Microscopic colitis and small intestinal bacterial overgrowth-diagnosis behind the irritable bowel syndrome? Rev Med Chir Soc Med Nat Iasi. 2012;116(3):766–72.

    PubMed  Google Scholar 

  53. Desai L, Simon EG, Chowdhury SD, et al. Small intestinal bacterial overgrowth and oro-cecal transit time in irritable bowel syndrome patients. Indian J Gastroenterol. 2013;32(1):A28–9.

    Article  Google Scholar 

  54. Ghoshal U, Srivastava D, Ghoshal U, et al. Randomized double-blind placebo-controlled trial of antibiotic treatment in patients with IBS directed to SIBO. J Gastroenterol Hepatol. 2013;28:523.

    Article  CAS  Google Scholar 

  55. Jahng AW, Ou S, Lee RH. PPI use and small intestinal bacterial overgrowth detected on lactulose breath testing: Results of a prospective cross sectional study among U.S. Veterans with irritable bowel syndrome. Gastroenterology. 2013;144(5):S535.

    Article  Google Scholar 

  56. Man F, Bustos Fernandez L, Bolino C. Prevalence of abnormal hydrogen excretion in non constipated irritable bowel syndrome patients. J Gastroenterol Hepatol. 2013;28:124.

    Google Scholar 

  57. Hayman JR, Pickering G, Sanders DS. Is there a relationship between irritable bowel syndrome symptoms and small bowel bacterial overgrowth? Gut. 2014;63:A198–9.

    Article  Google Scholar 

  58. David L, Babin A, Picos A, et al. Small intestinal bacterial overgrowth is associated with intestinal inflammation in the irritable bowel syndrome. Clujul Med. 2014;87(3):163–5.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Srivastava D, Ghoshal U, Mittal RD, et al. Associations between IL-1RA polymorphisms and small intestinal bacterial overgrowth among patients with irritable bowel syndrome from India. Neurogastroenterol Motil. 2014;26(10):1408–16.

    Article  PubMed  CAS  Google Scholar 

  60. Giamarellos-Bourboulis EJ, Pyleris E, Barbatzas C, et al. Small intestinal bacterial overgrowth is associated with irritable bowel syndrome and is independent of proton pump inhibitor usage. BMC Gastroenterol. 2016;16(1):67.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Kim KN, Joo NS, Jung SE, et al. Abdominal obesity is inversely associated with small intestinal bacterial overgrowth in irritable bowel syndrome. Obes Rev. 2016;17:31–2.

    Article  Google Scholar 

  62. Liu ZJ, Wei H, Duan LP, et al. Clinical features of irritable bowel syndrome with small intestinal bacterial overgrowth and a preliminary study of effectiveness of Rifaximin. Zhonghua Yi Xue Za Zhi. 2016;96(24):1896–902.

    PubMed  CAS  Google Scholar 

  63. Jung SE, Joo NS. Obesity is inversely related to hydrogen-producing small intestinal bacterial overgrowth in non-constipation irritable bowel syndrome. J Korean Med Sci. 2017;32(6):948–53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Lasa JS, Senderovsky MT, Fanjul I, et al. Proton-pump inhibitors’ influence on lactulose breath tests and irritable bowel syndrome symptom severity. Gastroenterology. 2014;146(5):S-537.

    Article  Google Scholar 

  65. Nucera G, Gabrielli M, Lupascu A, et al. Abnormal breath tests to lactose, fructose and sorbitol in irritable bowel syndrome may be explained by small intestinal bacterial overgrowth. Aliment Pharmacol Ther. 2005;21(11):1391–5.

    Article  PubMed  CAS  Google Scholar 

  66. Carrara M, Desideri S, Azzurro M, et al. Small intestine bacterial overgrowth in patients with irritable bowel syndrome. Eur Rev Med Pharmacol Sci. 2008;12(3):197–202.

    PubMed  CAS  Google Scholar 

  67. McCallum R, Schultz C, Sostarich S. Evaluating the role of small intestinal bacterial overgrowth (SIBO) in diarrhea predominant irritable bowel syndrome (IBS-D) patients utilizing the glucose breath test (GBT). Gastroenterology. 2005;128(4):A460.

    Google Scholar 

  68. Stoicescu A, Becheanu G, Dumbrava M, et al. Microscopic colitis—a missed diagnosis in diarrhea-predominant irritable bowel syndrome. Maedica (Buchar). 2012;7(1):3–9.

    Google Scholar 

  69. Khoshini R, Dai SC, Lezcano S, et al. A systematic review of diagnostic tests for small intestinal bacterial overgrowth. Dig Dis Sci. 2008;53(6):1443–54.

    Article  PubMed  Google Scholar 

  70. Saad RJ, Chey WD. Breath testing for small intestinal bacterial overgrowth: maximizing test accuracy. Clin Gastroenterol Hepatol. 2014;12(12):1964–72 (quiz e1119-1920).

    Article  PubMed  Google Scholar 

  71. Boyce PM, Koloski NA, Talley NJ. Irritable bowel syndrome according to varying diagnostic criteria: are the new Rome II criteria unnecessarily restrictive for research and practice? Am J Gastroenterol. 2000;95(11):3176–83.

    Article  PubMed  CAS  Google Scholar 

  72. Ravella K, Al-Hendy A, Sharan C, et al. Chronic estrogen deficiency causes gastroparesis by altering neuronal nitric oxide synthase function. Dig Dis Sci. 2013;58(6):1507–15.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Choung RS, Locke GR, Schleck CD, et al. Associations between medication use and functional gastrointestinal disorders: a population-based study. Neurogastroenterol Motil. 2013;25(5):413–9 (e298).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Fujiwara Y, Watanabe T, Muraki M, et al. Association between chronic use of proton pump inhibitors and small-intestinal bacterial overgrowth assessed using lactulose hydrogen breath tests. Hepatogastroenterology. 2015;62(138):268–72.

    PubMed  CAS  Google Scholar 

  75. Spiegel BM, Chey WD, Chang L. Bacterial overgrowth and irritable bowel syndrome: unifying hypothesis or a spurious consequence of proton pump inhibitors? Am J Gastroenterol. 2008;103(12):2972–6.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Lo W, Chan WW. Proton pump inhibitor use and the risk of small intestinal bacterial overgrowth: a meta-analysis. Clin Gastroenterol Hepatol. 2013;11(5):483–90.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC 81670487).

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Chen, B., Kim, J.JW., Zhang, Y. et al. Prevalence and predictors of small intestinal bacterial overgrowth in irritable bowel syndrome: a systematic review and meta-analysis. J Gastroenterol 53, 807–818 (2018). https://doi.org/10.1007/s00535-018-1476-9

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Keywords

  • Small intestinal bacterial overgrowth
  • Irritable bowel syndrome
  • Culture
  • Breath test