Breath tests and irritable bowel syndrome

World Journal of Gastroenterology

Volumn 20, Issue 24, 2014, Pages 7587-7601

  Rana, Satya Vati ^a   Malik, Aastha ^a  

^a POSTGRADUATE INSTITUTE OF MEDICAL EDUCATION AND RESEARCH   (India)

Author keywords

Bacterial overgrowth; Breath test; Carbohydrate malabsorption; Irritable bowel syndrome; Lactulose breath test; Small intestine; Sorbitol breath test

Indexed keywords

ANTIBIOTIC AGENT; ENEMA; GLUCOSE; LACTULOSE; LAXATIVE; METHANE; RADIOISOTOPE; RIFAXIMIN; SORBITOL; XYLOSE; BIOLOGICAL MARKER; CARBOHYDRATE DIET; GAS;

ARTICLE; BACTERIAL OVERGROWTH; BLOATING; BREATH ANALYSIS; CARBOHYDRATE INTOLERANCE; CONSTIPATION; DIARRHEA; HEREDITARY FRUCTOSE INTOLERANCE; HUMAN; HYDROGEN BREATH TEST; INTESTINE FLORA; IRRITABLE COLON; LACTOSE INTOLERANCE; NONHUMAN; PREDICTIVE VALUE; QUALITY OF LIFE; SENSITIVITY AND SPECIFICITY; SYMPTOM; BACTERIA; CARBOHYDRATE DIET; COMPLICATION; DIAGNOSTIC USE; DIET THERAPY; FERMENTATION; GAS; INTESTINE; IRRITABLE BOWEL SYNDROME; METABOLISM; MICROBIOLOGY; PROGNOSIS;

BACTERIA; BIOLOGICAL MARKERS; BREATH TESTS; DIETARY CARBOHYDRATES; FERMENTATION; GASES; HUMANS; INTESTINES; IRRITABLE BOWEL SYNDROME; LACTOSE INTOLERANCE; PREDICTIVE VALUE OF TESTS; PROGNOSIS;

EID: 84903120216     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i24.7587     Document Type: Article

References (124)

1. Newcomer AD, McGill DB, Thomas PJ, Hofmann AF. Prospective comparison of indirect methods for detecting lactase deficiency. N Engl J Med 1975; 293: 1232-1236 [PMID: 1186802 DOI: 10.1056/NEJM197512112932405]
2. Bond JH, Levitt MD. Effect of dietary fiber on intestinal gas production and small bowel transit time in man. Am J Clin Nutr 1978; 31: S169-S174 [PMID: 707369]
3. Urita Y, Ishihara S, Akimoto T, Kato H, Hara N, Honda Y, Nagai Y, Nakanishi K, Shimada N, Sugimoto M, Miki K. Seventy-five gram glucose tolerance test to assess carbohydrate malabsorption and small bowel bacterial overgrowth. World J Gastroenterol 2006; 12: 3092-3095 [PMID: 16718794]
4. Hamilton L. Breath tests and gastroenterology. 2nd ed. Milwaukee: QuinTron Instrument Company, 1998
5. Bond JH, Levitt MD. Use of breath hydrogen (H2) to quantitate small bowel transit time following partial gastrectomy. J Lab Clin Med 1977; 90: 30-36 [PMID: 874370]
6. Drossman DA, Corazziari E, Delvaux M, Spiller RC, Talley NJ, Thompson WG, Whitehead WE, editors. Rome III. The Functional Gastrointestinal Disorders. 3rd ed. McLean, VA: Degnon Associates, Inc., 2006
7. Ringel Y, Williams RE, Kalilani L, Cook SF. Prevalence, characteristics, and impact of bloating symptoms in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 2009; 7: 68-72; quiz 3[PMID: 19124113 DOI: 10.1016/j.cgh.2008.07.008]
8. King TS, Elia M, Hunter JO. Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998; 352: 1187-1189 [PMID: 9777836 DOI: 10.1016/S0140-6736(98)02146-1]
9. Cuoco L, Salvagnini M. Small intestine bacterial overgrowth in irritable bowel syndrome: a retrospective study with rifaximin. Minerva Gastroenterol Dietol 2006; 52: 89-95 [PMID: 16554709]
10. Majewski M, Reddymasu SC, Sostarich S, Foran P, McCallum RW. Efficacy of rifaximin, a nonabsorbed oral antibiotic, in the treatment of small intestinal bacterial overgrowth. Am J Med Sci 2007; 333: 266-270 [PMID: 17505166 DOI: 10.1097/MAJ.0b013e3180536784]
11. King CE, Toskes PP. Breath tests in the diagnosis of small intestine bacterial overgrowth. Crit Rev Clin Lab Sci 1984; 21: 269-281 [PMID: 6439469 DOI: 10.3109/10408368409165785]
12. Ford AC, Spiegel BM, Talley NJ, Moayyedi P. Small intestinal bacterial overgrowth in irritable bowel syndrome: systematic review and meta-analysis. Clin Gastroenterol Hepatol 2009; 7: 1279-1286 [PMID: 19602448 DOI: 10.1016/ j.cgh.2009.06.031]
13. Ghoshal UC, Kumar S, Mehrotra M, Lakshmi C, Misra A. Frequency of small intestinal bacterial overgrowth in patients with irritable bowel syndrome and chronic nonspecific diarrhea. J Neurogastroenterol Motil 2010; 16: 40-46 [PMID: 20535325 DOI: 10.5056/jnm.2010.16.1.40]
14. Bond JH, Levitt MD. Use of pulmonary hydrogen (H 2) measurements to quantitate carbohydrate absorption. Study of partially gastrectomized patients. J Clin Invest 1972; 51: 1219-1225 [PMID: 5020434 DOI: 10.1172/JCI106916]
15. Reddymasu SC, Sostarich S, McCallum RW. Small intestinal bacterial overgrowth in irritable bowel syndrome: are there any predictors? BMC Gastroenterol 2010; 10: 23 [PMID: 20175924 DOI: 10.1186/1471-230X-10-23]
16. Kerlin P, Wong L. Breath hydrogen testing in bacterial overgrowth of the small intestine. Gastroenterology 1988; 95: 982-988 [PMID: 3410238]
17. Lee KJ, Tack J. Altered intestinal microbiota in irritable bowel syndrome. Neurogastroenterol Motil 2010; 22: 493-498 [PMID: 20414959]
18. Gasbarrini A, Lauritano EC, Gabrielli M, Scarpellini E, Lupascu A, Ojetti V, Gasbarrini G. Small intestinal bacterial overgrowth: diagnosis and treatment. Dig Dis 2007; 25: 237-240 [PMID: 17827947 DOI: 10.1159/000103892]
19. Ghoshal UC. How to interpret hydrogen breath tests. J Neurogastroenterol Motil 2011; 17: 312-317 [PMID: 21860825 DOI: 10.5056/jnm.2011.17.3.312]
20. Posserud I, Stotzer PO, Björnsson ES, Abrahamsson H, Simrén M. Small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Gut 2007; 56: 802-808 [PMID: 17148502 DOI: 10.1136/gut.2006.108712]
21. Lupascu A, Gabrielli M, Lauritano EC, Scarpellini E, Santoliquido A, Cammarota G, Flore R, Tondi P, Pola P, Gasbarrini G, Gasbarrini A. Hydrogen glucose breath test to detect small intestinal bacterial overgrowth: a prevalence case-control study in irritable bowel syndrome. Aliment Pharmacol Ther 2005; 22: 1157-1160 [PMID: 16305730 DOI: 10.1111/j.1365-2036.2005.02690.x]
22. 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: 412-419 [PMID: 12591062]
23. Bures J, Cyrany J, Kohoutova D, Förstl M, Rejchrt S, Kvetina J, Vorisek V, Kopacova M. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol 2010; 16: 2978-2990 [PMID: 20572300]
24. Madrid AM, Defilippi C C, Defilippi G C, Slimming A J, Quera P R. [Small intestinal bacterial overgrowth in patients with functional gastrointestinal diseases]. Rev Med Chil 2007; 135: 1245-1252 [PMID: 18180830]
25. Swart GR, van den Berg JW. 13C breath test in gastroenterological practice. Scand J Gastroenterol Suppl 1998; 225: 13-18 [PMID: 9515746]
26. King CE, Toskes PP. Comparison of the 1-gram [14C]xylose, 10-gram lactulose-H2, and 80-gram glucose-H2 breath tests in patients with small intestine bacterial overgrowth. Gastroenterology 1986; 91: 1447-1451 [PMID: 3770368]
27. Fromm H, Hofmann AF. Breath test for altered bile-acid metabolism. Lancet 1971; 2: 621-625 [PMID: 4105944 DOI: 10.1016/S0140-6736(71)80068-5]
28. Lin HC. Small intestinal bacterial overgrowth: a framework for understanding irritable bowel syndrome. JAMA 2004; 292: 852-858 [PMID: 15316000]
29. Pimentel M, Wallace D, Hallegua D, Chow E, Kong Y, Park S, Lin HC. A link between irritable bowel syndrome and fibromyalgia may be related to findings on lactulose breath testing. Ann Rheum Dis 2004; 63: 450-452 [PMID: 15020342 DOI: 10.1136/ard.2003.011502]
30. Van Citters GW, Lin HC. Management of small intestinal bacterial overgrowth. Curr Gastroenterol Rep 2005; 7: 317-320 [PMID: 16042917 DOI: 10.1007/s11894-005-0025-x]
31. Park JS, Yu JH, Lim HC, Kim JH, Yoon YH, Park HJ, Lee SI. [Usefulness of lactulose breath test for the prediction of small intestinal bacterial overgrowth in irritable bowel syndrome]. Korean J Gastroenterol 2010; 56: 242-248 [PMID: 20962560 DOI: 10.4166/kjg.2010.56.4.242]
32. 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: 1084-1093 [PMID: 23066911 DOI: 10.1111/apt.12087]
33. Peralta S, Cottone C, Doveri T, Almasio PL, Craxi A. Small intestine bacterial overgrowth and irritable bowel syndrome-related symptoms: experience with Rifaximin. World J Gastroenterol 2009; 15: 2628-2631 [PMID: 19496193 DOI: 10.3748/wjg.15.2628]
34. Menees SB, Maneerattannaporn M, Kim HM, Chey WD. The efficacy and safety of rifaximin for the irritable bowel syndrome: a systematic review and meta-analysis. Am J Gastroenterol 2012; 107: 28-35; quiz 36 [PMID: 22045120 DOI: 10.1038/ajg.2011.355]
35. 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: 139-142 [PMID: 18217406]
36. Scarpellini E, Giorgio V, Gabrielli M, Filoni S, Vitale G, Tortora A, Ojetti V, Gigante G, Fundarò C, Gasbarrini A. Rifaximin treatment for small intestinal bacterial overgrowth in children with irritable bowel syndrome. Eur Rev Med Pharmacol Sci 2013; 17: 1314-1320 [PMID: 23740443]
37. Pimentel M, Lembo A, Chey WD, Zakko S, Ringel Y, Yu J, Mareya SM, Shaw AL, Bortey E, Forbes WP. Rifaximin therapy for patients with irritable bowel syndrome without constipation. N Engl J Med 2011; 364: 22-32 [PMID: 21208106 DOI: 10.1056/NEJMoa1004409]
38. 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: 2302-2308 [PMID: 19834807 DOI: 10.1007/s10620-009-1010-2]
39. Parodi A, Dulbecco P, Savarino E, Giannini EG, Bodini G, Corbo M, Isola L, De Conca S, Marabotto E, Savarino V. 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: 962-966 [PMID: 19525858 DOI: 10.1097/MCG.0b013e3181a099a5]
40. Yakoob J, Abbas Z, Khan R, Hamid S, Awan S, Jafri W. Small intestinal bacterial overgrowth and lactose intolerance contribute to irritable bowel syndrome symptomatology in Pakistan. Saudi J Gastroenterol 2011; 17: 371-375 [PMID: 22064333 DOI: 10.4103/1319-3767.87176]
41. Grover M, Kanazawa M, Palsson OS, Chitkara DK, Gangarosa LM, Drossman DA, Whitehead WE. Small intestinal bacterial overgrowth in irritable bowel syndrome: association with colon motility, bowel symptoms, and psychological distress. Neurogastroenterol Motil 2008; 20: 998-1008 [PMID: 18482250 DOI: 10.1111/j.1365-2982.2008.01142.x]
42. Sachdeva S, Rawat AK, Reddy RS, Puri AS. Small intestinal bacterial overgrowth (SIBO) in irritable bowel syndrome: frequency and predictors. J Gastroenterol Hepatol 2011; 26 Suppl 3: 135-138 [PMID: 21443727 DOI: 10.1111/j.1440-1746.2011.06654. x]
43. Scarpellini E, Giorgio V, Gabrielli M, Lauritano EC, Pantanella A, Fundarò C, Gasbarrini A. Prevalence of small intestinal bacterial overgrowth in children with irritable bowel syndrome: a case-control study. J Pediatr 2009; 155: 416-420 [PMID: 19535093 DOI: 10.1016/j.jpeds.2009.03.033]
44. Rana SV, Sinha SK, Sikander A, Bhasin DK, Singh K. Study of small intestinal bacterial overgrowth in North Indian patients with irritable bowel syndrome: a case control study. Trop Gastroenterol 2008; 29: 23-25 [PMID: 18564663]
45. Rana SV, Sharma S, Kaur J, Sinha SK, Singh K. Comparison of lactulose and glucose breath test for diagnosis of small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Digestion 2012; 85: 243-247 [PMID: 22472730 DOI: 10.1159/000336174]
46. Yu D, Cheeseman F, Vanner S. Combined oro-caecal scintigraphy and lactulose hydrogen breath testing demonstrate that breath testing detects oro-caecal transit, not small intestinal bacterial overgrowth in patients with IBS. Gut 2011; 60: 334-340 [PMID: 21112950 DOI: 10.1136/gut.2009.205476]
47. 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: 958-963 [PMID: 18371134 DOI: 10.1111/j.1572-0241.2008.01785.x]
48. 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: 1566-1570 [PMID: 15984983 DOI: 10.1111/j.1572-0241.2005.40795.x]
49. Eisenmann A, Amann A, Said M, Datta B, Ledochowski M. Implementation and interpretation of hydrogen breath tests. J Breath Res 2008; 2: 046002 [PMID: 21386189 DOI: 10.1088/1 752-7155/2/4/046002]
50. Corazza GR, Benati G, Strocchi A, Malservisi S, Gasbarrini G. The possible role of breath methane measurement in detecting carbohydrate malabsorption. J Lab Clin Med 1994; 124: 695-700 [PMID: 7964127]
51. Matthews SB, Waud JP, Roberts AG, Campbell AK. Systemic lactose intolerance: a new perspective on an old problem. Postgrad Med J 2005; 81: 167-173 [PMID: 15749792 DOI: 10.1136/pgmj.2004.025551]
52. Romagnuolo J, Schiller D, Bailey RJ. Using breath tests wisely in a gastroenterology practice: an evidence-based review of indications and pitfalls in interpretation. Am J Gastroenterol 2002; 97: 1113-1126 [PMID: 12014715 DOI: 10.1111/ j.1572-0241.2002.05664.x]
53. Farup PG, Monsbakken KW, Vandvik PO. Lactose malabsorption in a population with irritable bowel syndrome: prevalence and symptoms. A case-control study. Scand J Gastroenterol 2004; 39: 645-649 [PMID: 15370685 DOI: 10.1080/00 365520410005405]
54. Rana SV, Mandal AK, Kochhar R, Katyal R, Singh K. Lactose intolerance in different types of irritable bowel syndrome in north Indians. Trop Gastroenterol 2001; 22: 202-204 [PMID: 11963325]
55. Vernia P, Marinaro V, Argnani F, Di Camillo M, Caprilli R. Self-reported milk intolerance in irritable bowel syndrome: what should we believe? Clin Nutr 2004; 23: 996-1000 [PMID: 15380888 DOI: 10.1016/j.clnu.2003.12.005]
56. Böhmer CJ, Tuynman HA. The effect of a lactose-restricted diet in patients with a positive lactose tolerance test, earlier diagnosed as irritable bowel syndrome: a 5-year follow-up study. Eur J Gastroenterol Hepatol 2001; 13: 941-944 [PMID: 11507359 DOI: 10.1097/00042737-200108000-00011]
57. Burden S. Dietary treatment of irritable bowel syndrome: current evidence and guidelines for future practice. J Hum Nutr Diet 2001; 14: 231-241 [PMID: 11424515 DOI: 10.1046/ j.1365-277X.2001.00284.x]
58. Sciarretta G, Giacobazzi G, Verri A, Zanirato P, Garuti G, Malaguti P. Hydrogen breath test quantification and clinical correlation of lactose malabsorption in adult irritable bowel syndrome and ulcerative colitis. Dig Dis Sci 1984; 29: 1098-1104 [PMID: 6548690 DOI: 10.1007/BF01317083]
59. Böhmer CJ, Tuynman HA. The clinical relevance of lactose malabsorption in irritable bowel syndrome. Eur J Gastroenterol Hepatol 1996; 8: 1013-1016 [PMID: 8930569 DOI: 10.1097 /00042737-199610000-00015]
60. Parker TJ, Woolner JT, Prevost AT, Tuffnell Q, Shorthouse M, Hunter JO. Irritable bowel syndrome: is the search for lactose intolerance justified? Eur J Gastroenterol Hepatol 2001; 13: 219-225 [PMID: 11293439 DOI: 10.1097/00042737-200103 000-00001]
61. Alpers DH. Diet and irritable bowel syndrome. Curr Opin Gastroenterol 2006; 22: 136-139 [PMID: 16462169 DOI: 10.1097/01. mog.0000208462.92136.02]
62. Hamm LR, Sorrells SC, Harding JP, Northcutt AR, Heath AT, Kapke GF, Hunt CM, Mangel AW. Additional investigations fail to alter the diagnosis of irritable bowel syndrome in subjects fulfilling the Rome criteria. Am J Gastroenterol 1999; 94: 1279-1282 [PMID: 10235207 DOI: 10.1111/ j.1572-0241.1999.01077.x]
63. Vesa TH, Seppo LM, Marteau PR, Sahi T, Korpela R. Role of irritable bowel syndrome in subjective lactose intolerance. Am J Clin Nutr 1998; 67: 710-715 [PMID: 9537618]
64. Tolliver BA, Herrera JL, DiPalma JA. Evaluation of patients who meet clinical criteria for irritable bowel syndrome. Am J Gastroenterol 1994; 89: 176-178 [PMID: 8304298]
65. Tolliver BA, Jackson MS, Jackson KL, Barnett ED, Chastang JF, DiPalma JA. Does lactose maldigestion really play a role in the irritable bowel? J Clin Gastroenterol 1996; 23: 15-17 [PMID: 8835892 DOI: 10.1097/00004836-199607000-00005]
66. Gupta D, Ghoshal UC, Misra A, Misra A, Choudhuri G, Singh K. Lactose intolerance in patients with irritable bowel syndrome from northern India: a case-control study. J Gastroenterol Hepatol 2007; 22: 2261-2265 [PMID: 17559357 DOI: 10.1111/j.1440-1746.2007.04986.x]
67. Knudsen CD, Di Palma JA. Carbohydrate challenge tests: do you need to measure methane? South Med J 2012; 105: 251-253 [PMID: 22561536 DOI: 10.1097/SMJ.0b013e318252d428]
68. Zhu Y, Zheng X, Cong Y, Chu H, Fried M, Dai N, Fox M. Bloating and distention in irritable bowel syndrome: the role of gas production and visceral sensation after lactose ingestion in a population with lactase deficiency. Am J Gastroenterol 2013; 108: 1516-1525 [PMID: 23917444 DOI: 10.1038/ ajg.2013.198]
69. Yang J, Deng Y, Chu H, Cong Y, Zhao J, Pohl D, Misselwitz B, Fried M, Dai N, Fox M. Prevalence and presentation of lactose intolerance and effects on dairy product intake in healthy subjects and patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 2013; 11: 262-268.e1 [PMID: 23246646 DOI: 10.1016/j.cgh.2012.11.034]
70. Gremse DA, Nguyenduc GH, Sacks AI, DiPalma JA. Irritable bowel syndrome and lactose maldigestion in recurrent abdominal pain in childhood. South Med J 1999; 92: 778-781 [PMID: 10456715 DOI: 10.1097/00007611-199908000-00006]
71. Vernia P, Camillo MD, Marinaro V, Caprilli R. Effect of predominant methanogenic flora on the outcome of lactose breath test in irritable bowel syndrome patients. Eur J Clin Nutr 2003; 57: 1116-1119 [PMID: 12947430 DOI: 10.1038/ sj.ejcn.1601651]
72. Rana SV, Sinha SK, Sharma S, Kaur H, Bhasin DK, Singh K. Effect of predominant methanogenic flora on outcome of lactose hydrogen breath test in controls and irritable bowel syndrome patients of north India. Dig Dis Sci 2009; 54: 1550-1554 [PMID: 19003533 DOI: 10.1007/s10620-008-0532-3]
73. Lee KN, Lee OY, Koh DH, Sohn W, Lee SP, Jun DW, Lee HL, Yoon BC, Choi HS, Hahm JS. Association between symptoms of irritable bowel syndrome and methane and hydrogen on lactulose breath test. J Korean Med Sci 2013; 28: 901-907 [PMID: 23772156 DOI: 10.3346/jkms.2013.28.6.901]
74. Corlew-Roath M, Di Palma JA. Clinical impact of identifying lactose maldigestion or fructose malabsorption in irritable bowel syndrome or other conditions. South Med J 2009; 102: 1010-1012 [PMID: 19738525 DOI: 10.1097/SMJ.0b013e3181b64c7f]
75. Vernia P, Di Camillo M, Marinaro V. Lactose malabsorption, irritable bowel syndrome and self-reported milk intolerance. Dig Liver Dis 2001; 33: 234-239 [PMID: 11407668 DOI: 10.1016/S1590-8658(01)80713-1]
76. Litschauer-Poursadrollah M, El-Sayad S, Wantke F, Fellinger C, Jarisch R. [Abdominal spasms, meteorism, diarrhea: fructose intolerance, lactose intolerance or IBS?]. Wien Med Wochenschr 2012; 162: 506-512 [PMID: 23224632 DOI: 10.1007/s10354-012-0158-0]
77. Ledochowski M, Widner B, Bair H, Probst T, Fuchs D. Fructoseand sorbitol-reduced diet improves mood and gastrointestinal disturbances in fructose malabsorbers. Scand J Gastroenterol 2000; 35: 1048-1052 [PMID: 11099057 DOI: 10.1080/003655200451162]
78. Goldstein R, Braverman D, Stankiewicz H. Carbohydrate malabsorption and the effect of dietary restriction on symptoms of irritable bowel syndrome and functional bowel complaints. Isr Med Assoc J 2000; 2: 583-587 [PMID: 10979349]
79. Nucera G, Gabrielli M, Lupascu A, Lauritano EC, Santoliquido A, Cremonini F, Cammarota G, Tondi P, Pola P, Gasbarrini G, Gasbarrini A. 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: 1391-1395 [PMID: 15932370 DOI: 10.1111/j.1365-2036.2005.02493.x]
80. Swagerty DL, Walling AD, Klein RM. Lactose intolerance. Am Fam Physician 2002; 65: 1845-1850 [PMID: 12018807]
81. Moukarzel AA, Lesicka H, Ament ME. Irritable bowel syndrome and nonspecific diarrhea in infancy and childhood--relationship with juice carbohydrate malabsorption. Clin Pediatr (Phila) 2002; 41: 145-150 [PMID: 11999677 DOI: 10.1177/000992280204100303]
82. Wilder-Smith CH, Materna A, Wermelinger C, Schuler J. Fructose and lactose intolerance and malabsorption testing: the relationship with symptoms in functional gastrointestinal disorders. Aliment Pharmacol Ther 2013; 37: 1074-1083 [PMID: 23574302 DOI: 10.1111/apt.12306]
83. Born P, Zech J, Stark M, Classen M, Lorenz R. [Carbohydrate substitutes: comparative study of intestinal absorption of fructose, sorbitol and xylitol]. Med Klin (Munich) 1994; 89: 575-578 [PMID: 7815983]
84. Skoog SM, Bharucha AE. Dietary fructose and gastrointestinal symptoms: a review. Am J Gastroenterol 2004; 99: 2046-2050 [PMID: 15447771 DOI: 10.1111/j.1572-0241.2004.40266.x]
85. Choi YK, Johlin FC, Summers RW, Jackson M, Rao SS. Fructose intolerance: an under-recognized problem. Am J Gastroenterol 2003; 98: 1348-1353 [PMID: 12818280 DOI: 10.1111/j.1572-0241.2003.07476.x]
86. Rumessen JJ, Gudmand-Høyer E. Functional bowel disease: malabsorption and abdominal distress after ingestion of fructose, sorbitol, and fructose-sorbitol mixtures. Gastroenterology 1988; 95: 694-700 [PMID: 3396816]
87. Rumessen JJ, Gudmand-Høyer E. Absorption capacity of fructose in healthy adults. Comparison with sucrose and its constituent monosaccharides. Gut 1986; 27: 1161-1168 [PMID: 3781328 DOI: 10.1136/gut.27.10.1161]
88. Truswell AS, Seach JM, Thorburn AW. Incomplete absorption of pure fructose in healthy subjects and the facilitating effect of glucose. Am J Clin Nutr 1988; 48: 1424-1430 [PMID: 3202090]
89. Fernández-Bañares F, Esteve-Pardo M, de Leon R, Humbert P, Cabré E, Llovet JM, Gassull MA. Sugar malabsorption in functional bowel disease: clinical implications. Am J Gastroenterol 1993; 88: 2044-2050 [PMID: 8249972]
90. Johlin FC, Panther M, Kraft N. Dietary fructose intolerance: diet modification can impact self-rated health and symptom control. Nutr Clin Care 2004; 7: 92-97 [PMID: 15624540]
91. Choi YK, Kraft N, Zimmerman B, Jackson M, Rao SS. Fructose intolerance in IBS and utility of fructose-restricted diet. J Clin Gastroenterol 2008; 42: 233-238 [PMID: 18223504]
92. Reyes-Huerta JU, dela Cruz-Patiño E, Ramírez-Gutiérrezde Velasco A, Zamudio C, Remes-Troche JM. [Fructose intolerance in patients with irritable bowel syndrome: a casecontrol study]. Rev Gastroenterol Mex 2010; 75: 405-411 [PMID: 21169107]
93. Skoog SM, Bharucha AE, Zinsmeister AR. Comparison of breath testing with fructose and high fructose corn syrups in health and IBS. Neurogastroenterol Motil 2008; 20: 505-511 [PMID: 18221251 DOI: 10.1111/j.1365-2982.2007.01074.x]
94. Fernández-Bañares F, Rosinach M, Esteve M, Forné M, Espinós JC, Maria Viver J. Sugar malabsorption in functional abdominal bloating: a pilot study on the long-term effect of dietary treatment. Clin Nutr 2006; 25: 824-831 [PMID: 16410032 DOI: 10.1016/j.clnu.2005.11.010]
95. Shepherd SJ, Gibson PR. Fructose malabsorption and symptoms of irritable bowel syndrome: guidelines for effective dietary management. J Am Diet Assoc 2006; 106: 1631-1639 [PMID: 17000196 DOI: 10.1016/j.jada.2006.07.010]
96. Berg LK, Fagerli E, Martinussen M, Myhre AO, Florholmen J, Goll R. Effect of fructose-reduced diet in patients with irritable bowel syndrome, and its correlation to a standard fructose breath test. Scand J Gastroenterol 2013; 48: 936-943 [PMID: 23834159 DOI: 10.3109/00365521.2013.812139]
97. Hyams JS. Sorbitol intolerance: an unappreciated cause of functional gastrointestinal complaints. Gastroenterology 1983; 84: 30-33 [PMID: 6847853]
98. Madsen JL, Linnet J, Rumessen JJ. Effect of nonabsorbed amounts of a fructose-sorbitol mixture on small intestinal transit in healthy volunteers. Dig Dis Sci 2006; 51: 147-153 [PMID: 16416228 DOI: 10.1007/s10620-006-3100-8]
99. Cherbut C, Aubé AC, Blottière HM, Galmiche JP. Effects of short-chain fatty acids on gastrointestinal motility. Scand J Gastroenterol Suppl 1997; 222: 58-61 [PMID: 9145449]
100. Pimentel M, Constantino T, Kong Y, Bajwa M, Rezaei A, Park S. A 14-day elemental diet is highly effective in normalizing the lactulose breath test. Dig Dis Sci 2004; 49: 73-77 [PMID: 14992438 DOI: 10.1023/B:DDAS.0000011605.43979.e1]
101. Yao CK, Tan HL, van Langenberg DR, Barrett JS, Rose R, Liels K, Gibson PR, Muir JG. Dietary sorbitol and mannitol: food content and distinct absorption patterns between healthy individuals and patients with irritable bowel syndrome. J Hum Nutr Diet 2014; 27 Suppl 2: 263-275 [PMID: 23909813 DOI: 10.1111/jhn.12144]
102. Bond JH, Levitt MD, Prentiss R. Investigation of small bowel transit time in man utilizing pulmonary hydrogen (H2) measurements. J Lab Clin Med 1975; 85: 546-555 [PMID: 1120927]
103. Lembcke B, Bornholdt C, Kirchhoff S, Lankisch PG. Clinical evaluation of a 25 g D-xylose hydrogen (H2) breath test. Z Gastroenterol 1990; 28: 555-560 [PMID: 2275252]
104. Ong DK, Mitchell SB, Barrett JS, Shepherd SJ, Irving PM, Biesiekierski JR, Smith S, Gibson PR, Muir JG. Manipulation of dietary short chain carbohydrates alters the pattern of gas production and genesis of symptoms in irritable bowel syndrome. J Gastroenterol Hepatol 2010; 25: 1366-1373 [PMID: 20659225 DOI: 10.1111/j.1440-1746.2010.06370.x]
105. de Roest RH, Dobbs BR, Chapman BA, Batman B, O'Brien LA, Leeper JA, Hebblethwaite CR, Gearry RB. The low FODMAP diet improves gastrointestinal symptoms in patients with irritable bowel syndrome: a prospective study. Int J Clin Pract 2013; 67: 895-903 [PMID: 23701141 DOI: 10.1111/ ijcp.12128]
106. Christl SU, Murgatroyd PR, Gibson GR, Cummings JH. Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology 1992; 102: 1269-1277 [PMID: 1551534]
107. Macfarlane GT, Gibson GR, Cummings JH. Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 1992; 72: 57-64 [PMID: 1541601]
108. Lin HC, Pimentel M, Chen JH. Intestinal transit is slowed by luminal CH4. NeurogastroenterolMotil 2002; 14: 437
109. Ghoshal UC, Srivastava D, Verma A, Misra A. Slow transit constipation associated with excess methane production and its improvement following rifaximin therapy: a case report. J Neurogastroenterol Motil 2011; 17: 185-188 [PMID: 21602997]
110. Le Nevé B, Posserud I, Böhn L, Guyonnet D, Rondeau P, Tillisch K, Naliboff B, Mayer EA, Simrén M. A combined nutrient and lactulose challenge test allows symptom-based clustering of patients with irritable bowel syndrome. Am J Gastroenterol 2013; 108: 786-795 [PMID: 23588235 DOI: 10.1038/ajg.2013.75]
111. Pimentel M, Mayer AG, Park S, Chow EJ, Hasan A, Kong Y. Methane production during lactulose breath test is associated with gastrointestinal disease presentation. Dig Dis Sci 2003; 48: 86-92 [PMID: 12645795 DOI: 10.1023/A:1021738515885]
112. Furnari M, Savarino E, Bruzzone L, Moscatelli A, Gemignani L, Giannini EG, Zentilin P, Dulbecco P, Savarino V. Reassessment of the role of methane production between irritable bowel syndrome and functional constipation. J Gastrointestin Liver Dis 2012; 21: 157-163 [PMID: 22720304]
113. Kajs TM, Fitzgerald JA, Buckner RY, Coyle GA, Stinson BS, Morel JG, Levitt MD. Influence of a methanogenic flora on the breath H2 and symptom response to ingestion of sorbitol or oat fiber. Am J Gastroenterol 1997; 92: 89-94 [PMID: 8995944]
114. Pimentel M, Lin HC, Enayati P, van den Burg B, Lee HR, Chen JH, Park S, Kong Y, Conklin J. Methane, a gas produced by enteric bacteria, slows intestinal transit and augments small intestinal contractile activity. Am J Physiol Gastrointest Liver Physiol 2006; 290: G1089-G1095 [PMID: 16293652 DOI: 0.1152/ajpgi.00574.2004]
115. Fiedorek SC, Pumphrey CL, Casteel HB. Breath methane production in children with constipation and encopresis. J Pediatr Gastroenterol Nutr 1990; 10: 473-477 [PMID: 2162940 DOI: 10.1097/00005176-199005000-00010]
116. Peled Y, Weinberg D, Hallak A, Gilat T. Factors affecting methane production in humans. Gastrointestinal diseases and alterations of colonic flora. Dig Dis Sci 1987; 32: 267-271 [PMID: 3816480 DOI: 10.1007/BF01297052]
117. Pitcher MC, Cummings JH. Hydrogen sulphide: a bacterial toxin in ulcerative colitis? Gut 1996; 39: 1-4 [PMID: 8881797 DOI: 10.1136/gut.39.1.1]
118. Gibson GR, Macfarlane GT, Cummings JH. Occurrence of sulphate-reducing bacteria in human faeces and the relationship of dissimilatory sulphate reduction to methanogenesis in the large gut. J Appl Bacteriol 1988; 65: 103-111 [PMID: 3204069 DOI: 10.1111/j.1365-2672.1988.tb01498.x]
119. Gibson GR, Cummings JH, Macfarlane GT. Competition for hydrogen between sulphate-reducing bacteria and methanogenic bacteria from the human large intestine. J Appl Bacteriol 1988; 65: 241-247 [PMID: 2852666 DOI: 10.1111/ j.1365-2672.1988.tb01891.x]
120. Kunkel D, Basseri RJ, Makhani MD, Chong K, Chang C, Pimentel M. Methane on breath testing is associated with constipation: a systematic review and meta-analysis. Dig Dis Sci 2011; 56: 1612-1618 [PMID: 21286935 DOI: 10.1007/ s10620-011-1590-5]
121. Dima G, Peralta D, Novillo A, Lasa J, Besasso H, Soifer L. [Predominance of constipation in subjects with hydrogenconsuming intestinal flora]. Acta Gastroenterol Latinoam 2012; 42: 182-185 [PMID: 23214347]
122. Cloarec D, Bornet F, Gouilloud S, Barry JL, Salim B, Galmiche JP. Breath hydrogen response to lactulose in healthy subjects: relationship to methane producing status. Gut 1990; 31: 300-304 [PMID: 2323593 DOI: 10.1136/gut.31.3.300]
123. Lasa J, Peralta D, Dima G, Novillo A, Besasso H, Soifer L. Comparison of abdominal bloating severity between Irritable Bowel Syndrome patients with high and low levels of breath hydrogen excretion in a lactulose breath test. Rev Gastroenterol Mex 2012; 77: 53-57 [PMID: 22658548 DOI: 10.1016/j.rgmx.2012.02.002]
124. Kim G, Deepinder F, Morales W, Hwang L, Weitsman S, Chang C, Gunsalus R, Pimentel M. Methanobrevibacter smithii is the predominant methanogen in patients with constipation-predominant IBS and methane on breath. Dig Dis Sci 2012; 57: 3213-3218 [PMID: 22573345 DOI: 10.1007/ s10620-012-2197-1]