Obesity Surgery

, Volume 29, Issue 11, pp 3457–3464 | Cite as

Lactulose Breath Testing Can Be a Positive Predictor Before Weight Gain in Participants with Obesity Submitted to Roux-en-Y Gastric Bypass

  • Luciano Kowalski Coelho
  • Nayara Salgado Carvalho
  • Tomas Navarro-RodriguezEmail author
  • Fernando Augusto Lima Marson
  • Paulo Jose Pereira Campos Carvalho
Original Contributions



Small intestinal bacterial overgrowth (SIBO) is defined as the colonization of fermentative bacteria in the duodenum and jejunum. The alteration of digestive anatomy promoted by bariatric surgery may be a pre-disposing factor for SIBO. In this context, the prevalence of SIBO in participants undergoing bariatric surgery using Roux-en-Y gastric bypass (BGYR) was evaluated.


Participants, both sexes, older than 18 years, were those who (a) had bariatric surgery by the BGYR technique at least 1 year before the data collection and (b) did not use antibiotics recently. The SIBO diagnosis was established through the hydrogen breath test (H2BT), with intake of lactulose and serial collection of breath samples over 2 h. A test with ≥ 12-point elevation over the basal sample at 60 min after substrate intake was deemed positive.


A total of 18 participants (14 females (77.8%)) were enrolled with a mean age of 50.5 years (range, 23 to 79 years). The interval between surgery and data collection ranged from 5 to 20 years (mean, 11.2 years). The mean preoperative body mass index (BMI) was 44.6 kg/m2 (range, 36.7–56.2 kg/m2). The H2RT with lactulose was positive for SIBO in seven (six female) participants. The participants with negative test measured trough H2BT with lactulose had a lower mean BMI of 28.69 kg/m2, in comparison with the positive group, which presented a mean BMI of 33.04 kg/m2 (p value = 0.041).


Our data point to a high prevalence of SIBO (38.8%) in patients undergoing BGYR with a value in accordance with the literature. Moreover, the differences in BMI between negative and positive groups by H2BT with lactulose evidenced a weight gain relapse in participants with SIBO.


Bacterial overgrowth Bariatric surgery Breath test Lactulose Obesity Small intestine 


Author Contribution

All authors have approved the manuscript and agreed with its submission. Moreover, LKC, NSC, TNR, and PJCC idealized the project; collected patients’ data; worked on supervision, realization, and validation based on repeatability of the exams; contribute with the safety analysis; conducted the writing and critical review of the study; FALM conducted the writing and critical review of the study, also, performed the statistical analysis of the data. All authors have contributed to manuscript writing.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Statement

The project was approved by the research ethics committee from the institution.

Consent Statement

Informed consent was obtained from each participant.


  1. 1.
    Kopelman PG. Obesity as a medical problem. Nature. 2000;404:635–43.Google Scholar
  2. 2.
    Fried M, Yumuk V, Oppert JM, et al. International Federation for Surgery of Obesity and Metabolic Disorders-European Chapter (IFSO-EC); European Association for the Study of Obesity (EASO); European Association for the Study of Obesity Management Task Force (EASO OMTF). Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Surg. 2014;24:42–55.PubMedGoogle Scholar
  3. 3.
    Aron-Wisnewsky J, Dore J, Clement K. The importance of the gut microbiota after bariatric surgery. Nat Rev Gastroenterol Hepatol. 2012;9:590–8.Google Scholar
  4. 4.
    Ierardi E, Losurdo G, Sorrentino C, et al. Macronutrient intakes in obese subjects with or without small intestinal bacterial overgrowth: an alimentary survey. Scand J Gastroenterol. 2016;51:277–80.Google Scholar
  5. 5.
    Ishida RK, Faintuch J, Ribeiro AS, et al. Asymptomatic gastric bacterial overgrowth after bariatric surgery: are long-term metabolic consequence possible? Obes Surg. 2014;24:1856–61.Google Scholar
  6. 6.
    Kobyliak N, Virchenko O, Falalyeyeva T. Pathophysiological role of host microbiota in the development of obesity. Nutr J. 2016;15:43.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Liou AP, Paziuk M, Luevano Jr JM, et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5:178ra41.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Paik CN, Choi MG, Lim CH, et al. The role of small intestinal bacterial overgrowth in postgastrectomy patients. Neurogastroenterol Motil. 2011;23:e191–6.Google Scholar
  9. 9.
    Schwiertz A, Taras D, Schafer K, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010;18:190–5.Google Scholar
  10. 10.
    Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.PubMedGoogle Scholar
  11. 11.
    Woodard GA, Encarnacion B, Downey JR, et al. Probiotics improve outcomes after Roux-en-Y gastric bypass surgery: a prospective randomized trial. J Gastrointest Surg. 2009;13:1198–204.Google Scholar
  12. 12.
    Roland BC, Lee D, Miller LS, et al. Obesity increases the risk of small intestinal bacterial overgrowth (SIBO). Neurogastroenterol Motil. 2018;7:303–9.Google Scholar
  13. 13.
    Sabaté JM, Jouët P, Harnois F, et al. High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis. Obes Surg. 2008;18:371–7.Google Scholar
  14. 14.
    Bulanda M, Gosiewski T, Brzychczy-Włoch M. Small intestinal bacterial overgrowth in adult patients with type 1 diabetes. Pol Arch Med Wewn. 2016;126:623–4.Google Scholar
  15. 15.
    Chang CS, Chen GH, Lien HC, et al. Small intestine dysmotility and bacterial overgrowth in cirrhotic patients with spontaneous bacterial peritonitis. Hepatology. 1998;28:1187–90.Google Scholar
  16. 16.
    Bures J, Cyrany J, Kohoutova D, et al. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol. 2010;16:2978–90.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Lindberg DA. Hydrogen breath testing in adults: what is it and why is it performed? Gastroenterol Nurs. 2009;32:19–24.Google Scholar
  18. 18.
    Dukowicz AC, Lacy BE, Levine GM. Small intestinal bacterial overgrowth: a comprehensive review. Gastroenterol Hepatol (NY). 2007;3:112–22.Google Scholar
  19. 19.
    Erdogan A, Rao SSC, Gulley D, et al. Small intestinal bacterial overgrowth: duodenal aspiration vs glucose breath test. Neurogastroenterol Motil. 2015;27:481–9.Google Scholar
  20. 20.
    Gasbarrini A, Corazza GR, Gasbarrini G, et al. 1st Rome H2-breath testing consensus conference working group. Methodology and indications of H2-breath testing in gastrointestinal diseases: the Rome consensus conference. Aliment Pharmacol Ther. 2009;29:1–49.Google Scholar
  21. 21.
    Khoshini R, Dai SC, Lezcano S, et al. A systematic review of diagnostic tests for small intestinal bacterial overgrowth. Dig Dis Sci. 2008;53:1443–54.Google Scholar
  22. 22.
    Newberry C, Tierney A, Pickett-Blakely O. Lactulose hydrogen breath test result is associated with age and gender. Bio Med Res Int. 2016;2016:10640291–5.Google Scholar
  23. 23.
    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;85:243–7.Google Scholar
  24. 24.
    Rezaie A, Buresi M, Lembo A, et al. Hydrogen and methane-based breath testing in gastrointestinal disorders. The North American consensus. Am J Gastroenterol. 2017;112:775–84.PubMedPubMedCentralGoogle Scholar
  25. 25.
    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;56:242–8.Google Scholar
  26. 26.
    Pimentel M, Chow EJ, Lin HC. Normalization of lactulose breath testing correlates with symptom improvement in irritable bowel syndrome: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol. 2003;98:412–9.Google Scholar
  27. 27.
    Stotzer PO, Hilander KF. Comparison of the 1-gram 14 C D-xylose breath test and comparison of the 50-gram hydrogen glucose breath test for diagnosis of the small intestinal bacterial overgrowth. Digestion. 2000;61:165–71.Google Scholar
  28. 28.
    Rezaie A, Pimentel M, Rao SS. How to test and treat small intestinal bacterial overgrowth: an evidence-based approach. Curr Gastroenterol Rep. 2016;18:8.Google Scholar
  29. 29.
    Sachdev AH, Pimentel M. Gastrointestinal bacterial overgrowth: pathogenesis and clinical significance. Ther Adv Chronic Dis. 2013;4:223–31.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Sekirov I, Russell SL, Antunes LC, et al. Gut microbiota in health and disease. Physiol Rev. 2010;90:859–904.Google Scholar
  31. 31.
    Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–6.Google Scholar
  32. 32.
    Gabbard SL, Lacy BE, Levine GM, et al. The impact of alcohol consumption and cholecystectomy on small intestinal bacterial overgrowth. Dig Dis Sci. 2014;59:638–44.Google Scholar
  33. 33.
    George NS, Sankineni A, Parkman HP. Small intestinal bacterial overgrowth in gastroparesis. Dig Dis Sci. 2014;59:645–52.Google Scholar
  34. 34.
    Kumar K, Ghoshal UC, Srivastava D, et al. Small intestinal bacterial overgrowth is common both among patients with alcoholic and idiopathic chronic pancreatitis. Pancreatology. 2014;14:280–3.Google Scholar
  35. 35.
    Lauritano EC, Bilotta AL, Gabrielli M, et al. Association between hypothyroidism and small intestinal bacterial overgrowth. J Clin Endocrinol Metab. 2007;92:4180–4.Google Scholar
  36. 36.
    Lauritano EC, Gabrielli M, Scarpellini E, et al. Small intestinal bacterial overgrowth recurrence after antibiotic therapy. Am J Gastroenterol. 2008;103:2031–5.Google Scholar
  37. 37.
    Pande C, Kumar A, Sarin SK. Small-intestinal bacterial overgrowth in cirrhosis is related to the severity of liver disease. Aliment Pharmacol Ther. 2009;29:1273–81.Google Scholar
  38. 38.
    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;63:450–2.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Reddymasu SC, McCallum RW. Small intestinal bacterial overgrowth in gastroparesis: are there any predictors? J Clin Gastroenterol. 2010;44:e8–13.Google Scholar
  40. 40.
    Shanab AA, Scully P, Crosbie O, et al. Small intestinal bacterial overgrowth in nonalcoholic steatohepatitis: association with toll like receptor 4 expression and plasma levels of interleukin-8. Dig Dis Sci. 2011;56:1524–34.Google Scholar
  41. 41.
    Shimura S, Ishimura N, Mikami H, et al. Small intestinal bacterial overgrowth in patients with refractory functional gastrointestinal disorders. J Neurogastroenterol Motil. 2016;22:60–8.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Wigg AJ, Roberts-Thomson IC, Dymock RB, et al. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis. Gut. 2001;48:206–11.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Vanner S. The small intestinal bacterial overgrowth. Irritable bowel syndrome hypothesis: implications for treatment. Gut. 2008;57:1315–21.Google Scholar
  44. 44.
    Flourie B, Turk J, Lemann M, et al. Breath hydrogen in bacterial overgrowth. Gastroenterology. 1989;96:1225–6.Google Scholar
  45. 45.
    Simrén M, Stotzer PO. Use and abuse of hydrogen breath tests. Gut. 2006;55:297–303.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Uday C, Ghoshal RS, Ghoshal U. Small intestinal bacterial overgrowth and irritable bowel syndrome: a bridge between functional organic dichotomy. Gut Liver. 2017;11:196–208.Google Scholar
  47. 47.
    Walters B, Vanner SJ. Detection of bacterial overgrowth in IBS using the lactulose H2 breath test: comparison with 14C-D-xylose and healthy controls. Am J Gastroenterol. 2005;100:1566–70.Google Scholar
  48. 48.
    Posserud I, Stotzer PO, Björnsson ES, et al. Small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Gut. 2007;56:802–8.Google Scholar
  49. 49.
    Bratten JR, Spanier J, Jones MP. Lactulose breath testing does not discriminate patients with irritable bowel syndrome from healthy controls. Am J Gastroenterol. 2008;103:958–63.Google Scholar
  50. 50.
    Scarpelini E, Giorgio V, Gabrielli M. Prevalence of small intestinal bacterial overgrowth in children with irritable bowel syndrome: a case control study. J Pediatr. 2009;46:4574–82.Google Scholar
  51. 51.
    Zhao J, Zheng X, Chu H, et al. A study of the methodological and clinical validity of the combined lactulose hydrogen with scintigraphy oro-cecal transit test for diagnosing small intestinal bacterial overgrowth in IBS patients. Eurogastroenterol Motil. 2014;26:794–802.Google Scholar
  52. 52.
    Madrid AM, Poniachik J, Quera R, et al. Small intestinal clustered contractions and bacterial overgrowth: a frequent finding in obese patients. Dig Dis Sci. 2011;56:155–60.Google Scholar
  53. 53.
    Sabaté JM, Coupaye M, Ledoux S, et al. Consequences of small intestinal bacterial overgrowth in obese patients before and after bariatric surgery. Obes Surg. 2016;16:2343–5.Google Scholar
  54. 54.
    Fialho A, Thota P, McCullough AJ, et al. Small intestinal bacterial overgrowth is associated with non-alcoholic fatty liver disease. J Gastrointestin Liver Dis. 2016;25:159–65.Google Scholar
  55. 55.
    Jung SE, Joo NS, Han KS. Obesity is inversely related to hydrogen producing small intestinal bacterail overgrowth in non-constipation irritable bowel sydrome. J Korean Med Sci. 2017;32:948–53.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Ishida RK, Faintuch J, Paula AM, et al. Microbial flora of the stomach after gastric bypass for morbid obesity. Obes Surg. 2007;17:752–8.Google Scholar
  57. 57.
    Lakhani SV, Shah HN, Alexander K, et al. Small intestinal bacterial overgrowth and thiamine deficiency after Roux-en-Y gastric bypass surgery in obese patients. Nutr Res. 2008;28:293–8.Google Scholar
  58. 58.
    Andalib I, Shah H, Bal BS, et al. Breath hydrogen as a biomarker for glucose malabsorption after Roux-en-Y gastric bypass surgery. Dis Markers. 2015;2015:102760.PubMedPubMedCentralGoogle Scholar
  59. 59.
    Brechmann T, Sperlbaum A, Schmiegel W. Levothyroxine therapy and impaired clearance are the strongest contributors to small intestinal bacterial overgrowth: results of a retrospective cohort study. World J Gastroenterol. 2017;23:842–52.PubMedPubMedCentralGoogle Scholar
  60. 60.
    Quigley EM. Small intestinal bacterial overgrowth: what it is and what it is not. Curr Opin Gastroenterol. 2014;30:141–6.Google Scholar
  61. 61.
    Saad RJ, Chey WD. Breath testing for small intestinal bacterial overgrowth: maximizing test accuracy. Clin Gastroenterol Hepatol. 2014;12:1964–72.Google Scholar
  62. 62.
    Siddiqui I, Ahmed S, Abid S. Update on diagnostic value of breath test in gastrointestinal and liver diseases. World J Gastrointest Pathophysiol. 2016;7:256–65.PubMedPubMedCentralGoogle Scholar
  63. 63.
    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;21:1391–195.Google Scholar
  64. 64.
    Furet JP, Kong LC, Tap J, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59:3049–57.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Petrof EO, Claud EC, Gloor GB, et al. Microbial ecosystems therapeutics: a new paradigm in medicine? Benefic Microbes. 2013;4:53–65.Google Scholar
  66. 66.
    Basilisco G, Camboni G, Bozzani A, et al. Orocecal transit delay in obese patients. Dig Dis Sci. 1989;34:509–12.Google Scholar
  67. 67.
    Miedema B, Kelly K, Camilleri M, et al. Human gastric and jejunal transit and motility after roux gastrojejunostomy. Gastroenterology. 1992;103:1133–43.Google Scholar
  68. 68.
    Nguyen NQ, Debreceni TL, Bambrick JE, et al. Rapid gastric and intestinal transit is a major determinant of changes in blood glucose, intestinal hormones, glucose absorption and postprandial symptoms after gastric by-pass. Obesity. 2014;22:2003–9.Google Scholar
  69. 69.
    Machado JD, Campos CS, Lopes Dah Silva C, et al. Intestinal bacterial overgrowth after Roux-em-Y gastric bypass. Obes Surg. 2007;17:1529–33.Google Scholar
  70. 70.
    Dirksen C, Damgaard M, Bojsen-Moller KN, et al. Fast pouch emptying, delayed small intestinal transit, and exaggerated gut hormone responses after Y-en-Roux gastric by-pass. Neurogastroenterol Motil. 2013;25:346–e255.Google Scholar
  71. 71.
    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;53:27–36.Google Scholar
  72. 72.
    Graessler J, Qin Y, Zhong H, et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J. 2012;13:514–22.Google Scholar
  73. 73.
    Palleja A, Kashani A, Allin KH, et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med. 2016;8:67.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Nucleus of Physiolgy GastrointestinalInstituto Israelita de Ensino e Pesquisa e Hospital Israelita Albert EinsteinSão PauloBrazil
  2. 2.Department of Gastroenterology, Faculdade de MedicinaUniversidade de São PauloSão PauloBrazil
  3. 3.Hospital de ClínicasSão PauloBrazil
  4. 4.Department of Pediatrics, Department of Medical Genetics and Genomic Medicine and Center of Investigation in Pediatrics, Faculty of Medical SciencesState University of CampinasCampinasBrazil

Personalised recommendations