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BioMed Research International
Volume 2016 (2016), Article ID 7952891, 12 pages
http://dx.doi.org/10.1155/2016/7952891
Research Article

Use of the Biphasic 13C-Sucrose/Glucose Breath Test to Assess Sucrose Maldigestion in Adults with Functional Bowel Disorders

1Division of Gastroenterology and Hepatology, Department of Internal Medicine, Baylor College of Medicine, Houston, TX 77030, USA
2Division of Gastroenterology, Nutrition and Hepatology, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, USA

Received 19 March 2016; Accepted 10 July 2016

Academic Editor: Louise E. Glover

Copyright © 2016 Antone R. Opekun et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. D. Chey, J. Kurlander, and S. Eswaran, “Irritable bowel syndrome: a clinical review,” The Journal of the American Medical Association, vol. 313, no. 9, pp. 949–958, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. Rome III diagnostic criteria for functional gastrointestinal disorders, May 2016, http://www.romecriteria.org/assets/pdf/19_RomeIII_apA_885-898.pdf.
  3. A. L. Engsbro, L. M. Begtrup, J. Kjeldsen et al., “Patients suspected of irritable bowel syndrome—cross-sectional study exploring the sensitivity of rome III criteria in primary care,” The American Journal of Gastroenterology, vol. 108, no. 6, pp. 972–980, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. N. J. Talley, G. Holtmann, and M. M. Walker, “Therapeutic strategies for functional dyspepsia and irritable bowel syndrome based on pathophysiology,” Journal of Gastroenterology, vol. 50, no. 6, pp. 601–613, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. G. F. Longstreth, W. G. Thompson, W. D. Chey, L. A. Houghton, F. Mearin, and R. C. Spiller, “Functional bowel disorders,” Gastroenterology, vol. 130, no. 5, pp. 1480–1491, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Rey and N. J. Talley, “Irritable bowel syndrome: novel views on the epidemiology and potential risk factors,” Digestive and Liver Disease, vol. 41, no. 11, pp. 772–780, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. E. A. Mayer, T. Savidge, and R. J. Shulman, “Brain-gut microbiome interactions and functional bowel disorders,” Gastroenterology, vol. 146, no. 6, pp. 1500–1512, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Sood, G. R. Law, and A. C. Ford, “Diagnosis of IBS: Symptoms, symptom-based criteria, biomarkers or ‘psychomarkers’?” Nature Reviews Gastroenterology and Hepatology, vol. 11, no. 11, pp. 683–691, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. J. A. Tibble, G. Sigthorsson, R. Foster, I. Forgacs, and I. Bjarnason, “Use of surrogate markers of inflammation and Rome criteria to distinguish organic from nonorganic intestinal disease,” Gastroenterology, vol. 123, no. 2, pp. 450–460, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. B. M. R. Spiegel, M. Farid, E. Esrailian, J. Talley, and L. Chang, “Is irritable bowel syndrome a diagnosis of exclusion?: a survey of primary care providers, gastroenterologists, and IBS experts,” American Journal of Gastroenterology, vol. 105, no. 4, pp. 848–858, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. R. L. Levy, K. R. Jones, W. E. Whitehead, S. I. Feld, N. J. Talley, and L. A. Corey, “Irritable bowel syndrome in twins: heredity and social learning both contribute to etiology,” Gastroenterology, vol. 121, no. 4, pp. 799–804, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. M. El-Salhy, “Recent advances in the diagnosis of irritable bowel syndrome,” Expert Review of Gastroenterology and Hepatology, vol. 9, no. 9, pp. 1161–1174, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Camilleri, “Peripheral mechanisms in irritable bowel syndrome,” The New England Journal of Medicine, vol. 367, no. 17, pp. 1626–1635, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. D. A. Drossman, L. Chang, N. Bellamy et al., “Severity in irritable bowel syndrome: a rome foundation working team report,” American Journal of Gastroenterology, vol. 106, no. 10, pp. 1749–1759, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. E. P. Halmos, V. A. Power, S. J. Shepherd, P. R. Gibson, and J. G. Muir, “A diet low in FODMAPs reduces symptoms of irritable bowel syndrome,” Gastroenterology, vol. 146, no. 1, pp. 67–75.e5, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Böhn, S. Störsrud, T. Liljebo, P. Lindfors, H. Törnblom, and M. Simrén, “A randomized, controlled trial comparing a diet low in FODMAPs with traditional dietary advice in patients with IBS,” Gastroenterology, vol. 148, no. 4, p. S-654, 2015. View at Google Scholar
  17. M.-I. Park and M. Camilleri, “Is there a role of food allergy in irritable bowel syndrome and functional dyspepsia? A systematic review,” Neurogastroenterology and Motility, vol. 18, no. 8, pp. 595–607, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. K. El-Chammas, S. E. Williams, and A. Miranda, “Disaccharidase deficiencies in children with chronic abdominal pain,” Journal of Parenteral and Enteral Nutrition, 2015. View at Publisher · View at Google Scholar
  19. M. Corlew-Roath and J. A. Di Palma, “Clinical impact of identifying lactose maldigestion or fructose malabsorption in irritable bowel syndrome or other conditions,” Southern Medical Journal, vol. 102, no. 10, pp. 1010–1012, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. S. J. Shepherd and P. R. Gibson, “Fructose malabsorption and symptoms of irritable bowel syndrome: guidelines for effective dietary management,” Journal of the American Dietetic Association, vol. 106, no. 10, pp. 1631–1639, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Gudmand-Høøyer and H. Skovbjerg, “Disaccharide digestion and maldigestion,” Scandinavian Journal of Gastroenterology. Supplement, vol. 216, pp. 111–121, 1996. View at Google Scholar · View at Scopus
  22. G. Neale, M. Clark, and B. Levin, “Intestinal sucrase deficiency presenting as sucrose intolerance in adult life,” The British Medical Journal, vol. 2, pp. 1223–1225, 1965. View at Publisher · View at Google Scholar · View at Scopus
  23. J. J. Rumessen and E. Gudmand-Hoyer, “Absorption capacity of fructose in healthy adults: comparison with sucrose and its constituent monosaccharides,” Gut, vol. 27, no. 10, pp. 1161–1168, 1986. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Auricchio, F. Ciccimarra, L. Moauro, F. Rey, J. Jos, and J. Rey, “Intraluminal and mucosal starch digestion in congenital deficiency of intestinal sucrase and isomaltase activities,” Pediatric Research, vol. 6, no. 11, pp. 832–839, 1972. View at Publisher · View at Google Scholar · View at Scopus
  25. T. S. King, M. Elia, and J. O. Hunter, “Abnormal colonic fermentation in irritable bowel syndrome,” The Lancet, vol. 352, no. 9135, pp. 1187–1189, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. E. E. Sterchi, M. J. Lentze, and H. Y. Naim, “Molecular aspects of disaccharidase deficiencies,” Bailliere's Clinical Gastroenterology, vol. 4, no. 1, pp. 79–96, 1990. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Ohman and M. Simrén, “Intestinal microbiota and its role in irritable bowel syndrome (IBS),” Current Gastroenterology Reports, vol. 15, article 323, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. T. M. Bayless, B. Rothfeld, C. Massa, L. Wise, D. Paige, and M. S. Bedine, “Lactose and milk intolerance: clinical implications,” The New England Journal of Medicine, vol. 292, no. 22, pp. 1156–1159, 1975. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Born, M. Sekatcheva, T. Rösch, and M. Classen, “Carbohydrate malabsorption in clinical routine: a prospective observational study,” Hepato-Gastroenterology, vol. 53, no. 71, pp. 673–677, 2006. View at Google Scholar · View at Scopus
  30. D. Rating and C. D. Langhans, “Breath tests: concepts, applications and limitations,” European Journal of Pediatrics, vol. 156, supplement 1, pp. S18–S23, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Nucera, M. Gabrielli, A. Lupascu et al., “Abnormal breath tests to lactose, fructose and sorbitol in irritable bowel syndrome may be explained by small intestinal bacterial overgrowth,” Alimentary Pharmacology and Therapeutics, vol. 21, no. 11, pp. 1391–1395, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Simrén and P.-O. Stotzer, “Use and abuse of hydrogen breath tests,” Gut, vol. 55, no. 3, pp. 297–303, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. C. S. Irving, W. W. Wong, R. J. Shulman, E. O. Smith, and P. D. Klein, “[13C]bicarbonate kinetics in humans: intra—vs. interindividual variations,” The American Journal of Physiology, vol. 245, no. 2, pp. R190–R202, 1983. View at Google Scholar · View at Scopus
  34. R. Steele, C. Bjerknes, I. Rathgeb, and N. Altszuler, “Glucose uptake and production during the oral glucose tolerance test,” Diabetes, vol. 17, no. 7, pp. 415–421, 1968. View at Publisher · View at Google Scholar · View at Scopus
  35. R. C. A. Schellekens, G. G. Olsder, S. M. C. H. Langenberg et al., “Proof-of-concept study on the suitability of 13C-urea as a marker substance for assessment of in vivo behaviour of oral colon-targeted dosage forms,” British Journal of Pharmacology, vol. 158, no. 2, pp. 532–540, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. C. W. Swart, K. Dithebe, C. H. Pohl et al., “Gas bubble formation in the cytoplasm of a fermenting yeast,” FEMS Yeast Research, vol. 12, no. 7, pp. 867–869, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Fernandez-Banares, M. Esteve-Pardo, R. de Leon et al., “Sugar malabsorption in functional bowel disease: clinical implications,” American Journal of Gastroenterology, vol. 88, no. 12, pp. 2044–2050, 1993. View at Google Scholar · View at Scopus
  38. B. L. Nichols Jr., B. Adams, C. M. Roach, C.-X. Ma, and S. S. Baker, “Frequency of sucrase deficiency in mucosal biopsies,” Journal of Pediatric Gastroenterology and Nutrition, vol. 55, supplement 2, pp. S28–S30, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Metz, D. J. Jenkins, A. Newman, and L. M. Blendis, “Breath hydrogen in hyposucrasia,” The Lancet, vol. 307, no. 7951, pp. 119–120, 1976. View at Publisher · View at Google Scholar
  40. S. V. Rana and A. Malik, “Breath tests and irritable bowel syndrome,” World Journal of Gastroenterology, vol. 28, pp. 7587–7601, 2014. View at Google Scholar
  41. R. Goldstein, D. Braverman, and H. Stankiewicz, “Carbohydrate malabsorption and the effect of dietary restriction on symptoms of irritable bowel syndrome and functional bowel complaints,” Israel Medical Association Journal, vol. 2, no. 8, pp. 583–587, 2000. View at Google Scholar · View at Scopus
  42. K. L. Tooley, G. S. Howarth, K. A. Lymn, and R. N. Butler, “Optimization of the non-invasive 13C-sucrose breath test in a rat model of methotrexate-induced mucositis,” Cancer Chemotherapy and Pharmacology, vol. 65, no. 5, pp. 913–921, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. C. C. Robayo-Torres, A. R. Opekun, R. Quezada-Calvillo et al., “13C-breath tests for sucrose digestion in congenital sucrase isomaltase-deficient and sacrosidase-supplemented patients,” Journal of Pediatric Gastroenterology and Nutrition, vol. 48, no. 4, pp. 412–418, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Zhu, M. Bosch, I. Woo et al., “The use of mobile devices in aiding dietary assessment and evaluation,” IEEE Journal on Selected Topics in Signal Processing, vol. 4, no. 4, pp. 756–766, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. Metabolic Solutions, “Sucrose Breath Test,” http://www.metsol.com/assets/sites/3/Sucrose-Breath-Test.pdf.
  46. S. S. C. Rao, A. Attaluri, L. Anderson, and P. Stumbo, “Ability of the normal human small intestine to absorb fructose: evaluation by breath testing,” Clinical Gastroenterology and Hepatology, vol. 5, no. 8, pp. 959–963, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. M. E. Latulippe and S. M. Skoog, “Fructose malabsorption and intolerance: effects of fructose with and without simultaneous glucose ingestion,” Critical Reviews in Food Science and Nutrition, vol. 51, no. 7, pp. 583–592, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. C. H. Wilder-Smith, A. Materna, C. Wermelinger, and J. Schuler, “Fructose and lactose intolerance and malabsorption testing: the relationship with symptoms in functional gastrointestinal disorders,” Alimentary Pharmacology and Therapeutics, vol. 37, no. 11, pp. 1074–1083, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Fernández-Bañares, M. Rosinach, M. Esteve, M. Forné, J. C. Espinós, and J. Maria Viver, “Sugar malabsorption in functional abdominal bloating: a pilot study on the long-term effect of dietary treatment,” Clinical Nutrition, vol. 25, no. 5, pp. 824–831, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. W. Karnsakul, U. Luginbuehl, D. Hahn et al., “Disaccharidase activities in dyspeptic children: biochemical and molecular investigations of maltase-glucoamylase activity,” Journal of Pediatric Gastroenterology and Nutrition, vol. 35, no. 4, pp. 551–556, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Uhrich, Z. Wu, J.-Y. Huang, and C. R. Scott, “Four mutations in the SI gene are responsible for the majority of clinical symptoms of CSID,” Journal of Pediatric Gastroenterology and Nutrition, vol. 55, supplement 2, pp. S34–S35, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Y. Naim, M. Heine, and K.-P. Zimmer, “Congenital sucrase-isomaltase deficiency: heterogeneity of inheritance, trafficking, and function of an intestinal enzyme complex,” Journal of Pediatric Gastroenterology and Nutrition, vol. 55, supplement 2, pp. S13–S20, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Richardson and R. Dobish, “Chemotherapy induced diarrhea,” Journal of Oncology Pharmacy Practice, vol. 13, no. 4, pp. 181–198, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. C. H. Wilder-Smith, X. Li, S. S. Ho et al., “Fructose transporters GLUT5 and GLUT2 expression in adult patients with fructose intolerance,” United European Gastroenterology Journal, vol. 2, no. 1, pp. 14–21, 2014. View at Publisher · View at Google Scholar
  55. R. Terry, W. H. van Wettere, A. L. Whittaker, P. J. Herde, and G. S. Howarth, “Using the noninvasive 13C-sucrose breath test to measure intestinal sucrase activity in swine,” Comparative Medicine, vol. 62, no. 6, pp. 504–507, 2012. View at Google Scholar
  56. M. Hiele, Y. Ghoos, P. Rutgeerts, G. Vantrappen, and K. De Buyser, “13CO2 breath test to measure the hydrolysis of various starch formulations in healthy subjects,” Gut, vol. 31, no. 2, pp. 175–178, 1990. View at Publisher · View at Google Scholar · View at Scopus
  57. B. K. Ritchie, D. R. Brewster, G. P. Davidson et al., “13C-sucrose breath test: novel use of a noninvasive biomarker of environmental gut health,” Pediatrics, vol. 124, no. 2, pp. 620–626, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. P. D. Klein and E. R. Klein, “Stable isotopes: origins and safety,” Journal of Clinical Pharmacology, vol. 26, no. 6, pp. 378–382, 1986. View at Publisher · View at Google Scholar · View at Scopus
  59. B. Braden, B. Lembcke, W. Kuker, and W. F. Caspary, “13C-breath tests: current state of the art and future directions,” Digestive and Liver Disease, vol. 39, no. 9, pp. 795–805, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Graham, D. Evans Jr., L. Alpert et al., “Campylobacter pylori detected noninvasively by the 13C-urea breath test,” The Lancet, vol. 329, no. 8543, pp. 1174–1177, 1987. View at Publisher · View at Google Scholar · View at Scopus
  61. A. R. Opekun, A. B. Gotschall, N. Abdalla et al., “Improved infrared spectrophotometer for point-of-care patient 13C-urea breath testing in the primary care setting,” Clinical Biochemistry, vol. 38, no. 8, pp. 731–734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. Deng, “Fuzzy analytical hierarchy process based on canonical representation on fuzzy numbers,” Journal of Computational Analysis and Applications, vol. 22, no. 2, pp. 201–228, 2017. View at Google Scholar
  63. W. N. Schofield, “Predicting basal metabolic rate, new standards and review of previous work,” Human Nutrition. Clinical Nutrition, vol. 39, supplement 1, pp. 5–41, 1985. View at Google Scholar · View at Scopus
  64. P. D. Klein, H. M. Malaty, S. J. Czinn, S. C. Emmons, R. F. Martin, and D. Y. Graham, “Normalizing results of 13C-urea breath testing for CO2 production rates in children,” Journal of Pediatric Gastroenterology and Nutrition, vol. 29, no. 3, pp. 297–301, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. C. S. Irving, W. W. Wong, R. J. Shulman, E. O. Smith, and P. D. Klein, “[13C]bicarbonate kinetics in humans: intra- vs. interindividual variations,” The American Journal of Physiology, vol. 245, no. 2, pp. R190–R202, 1983. View at Google Scholar · View at Scopus
  66. J. J. Robert, J. Koziet, D. Chauvet, D. Darmaun, J. F. Desjeux, and V. R. Young, “Use of 13C-labeled glucose for estimating glucose oxidation: some design considerations,” Journal of Applied Physiology, vol. 63, no. 5, pp. 1725–1732, 1987. View at Google Scholar · View at Scopus
  67. B. Koletzko, H. Demmelmair, W. Hartl et al., “The use of stable isotope techniques for nutritional and metabolic research in paediatrics,” Early Human Development, vol. 53, supplement, pp. S77–S97, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. L. J. Cohen, H.-S. Kang, J. Chu et al., “Functional metagenomic discovery of bacterial effectors in the human microbiome and isolation of commendamide, a GPCR G2A/132 agonist,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 35, pp. E4825–E4834, 2015. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Spencer, W. D. Chey, and S. Eswaran, “Dietary renaissance in IBS: has food replaced medications as a primary treatment strategy?” Current Treatment Options in Gastroenterology, vol. 12, no. 4, pp. 424–440, 2014. View at Publisher · View at Google Scholar
  70. B. P. Chumpitazi, J. L. Cope, E. B. Hollister et al., “Randomized clinical trial: gut microbiome biomarkers are associated with clinical response to a low FODMAP diet in children with the irritable bowel syndrome,” Alimentary Pharmacology and Therapeutics, vol. 42, no. 4, pp. 418–427, 2015. View at Publisher · View at Google Scholar · View at Scopus
  71. US Patent & Trademark Web site: United States Patent Application Notice: Enzyme formulation for use as food supplement, 2016, http://appft.uspto.gov/netacgi/nph-Parser?Sect1=PTO1&Sect2=HITOFF&d=PG01&p=1&u=%2Fnetahtml%2FPTO%2Fsrchnum.html&r=1&f=G&l=50&s1=%2220160114012%22.PGNR.&OS=DN/20160114012&RS=DN/2016011401.
  72. S. Karani, M. S. Kataria, and A. E. Barber, “A double-blind clinical trial with a digestive enzyme product,” British Journal of Clinical Practice, vol. 25, no. 8, pp. 375–377, 1971. View at Google Scholar · View at Scopus
  73. M. Di Stefano, E. Miceli, S. Gotti, A. Missanelli, S. Mazzocchi, and G. R. Corazza, “The effect of oral α-galactosidase on intestinal gas production and gas-related symptoms,” Digestive Diseases and Sciences, vol. 52, no. 1, pp. 78–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Simadibrata, R. J. A. Wanders, G. Jan et al., “Examination of small bowel enzymes in chronic diarrhea,” Journal of Gastroenterology and Hepatology, vol. 18, no. 1, pp. 53–56, 2003. View at Publisher · View at Google Scholar · View at Scopus