Gastrointestinal Disturbances Associated with the Consumption of Sugar Alcohols with Special Consideration of Xylitol: Scientific Review and Instructions for Dentists and Other Health-Care Professionals

International Journal of Dentistry

Volumn 2016, Issue , 2016, Pages

  Mäkinen, Kauko K ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

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EID: 84995394480     PISSN: 16878728     EISSN: 16878736     Source Type: Journal    
DOI: 10.1155/2016/5967907     Document Type: Review

References (99)

1. K. K. Mäkinen, "Sugar alcohol sweeteners as alternatives to sugar with special consideration of xylitol, " Medical Principles and Practice, vol. 20, no. 4, pp. 303-320, 2011.
2. K. K. Mäkinen, "Oral care gum products, " in Food Constituents and Oral Health, M. Wilson, Ed., pp. 435-454, Woodhead, Oxford, UK, 2009.
3. U. C. Dubach, E. Feiner, and I. Forgó, "Oral tolerance of Xylit in subjects with normal metabolism, " Schweizerische medizinische Wochenschrift, vol. 99, no. 6, pp. 190-194, 1969.
4. K. K. Mäkinen and A. Scheinin, "Turku sugar studies VI. The administration of the trial and the control of the dietary regimen, " Acta Odontologica Scandinavica, vol. 33, supplement 70, pp. 105-127, 1975.
5. S. Salminen, E. Salminen, and V. Marks, "The effects of xylitol on the secretion of insulin and gastric inhibitory polypeptide in man and rats, " Diabetologia, vol. 22, no. 6, pp. 480-482, 1982.
6. S. Salminen, E. Salminen, P. Koivistoinen, J. Bridges, and V. Marks, "Gut microflora interactions with xylitol in the mouse, rat and man, " Food and Chemical Toxicology, vol. 23, no. 11, pp. 985-990, 1985.
7. H. K. Akerblom, T. Koivukangas, R. Puukka, and M. Mononen, "The tolerance of increasing amounts of dietary xylitol in children, " International Journal for Vitamin and Nutrition Research, vol. 22, pp. 53-66, 1982.
8. D. Storey, A. Lee, F. Bornet, and F. Brouns, "Gastrointestinal tolerance of erythritol and xylitol ingested in a liquid, " European Journal of Clinical Nutrition, vol. 61, no. 3, pp. 349-354, 2007.
9. C. K. Yao, H.-L. Tan, D. R. van Langenberg et al., "Dietary sorbitol and mannitol: food content and distinct absorption patterns between healthy individuals and patients with irritable bowel syndrome, " Journal ofHumanNutrition andDietetics, vol. 27, no. 2, pp. 263-275, 2014.
10. L. Beaugerie, B. Flouríe, P. Marteau, P. Pellier, C. Franchisseur, and J.-C. Rambaud, "Digestion and absorption in the human intestine of three sugar alcohols, " Gastroenterology, vol. 99, no. 3, pp. 717-723, 1990.
11. S. Nakamura, R. Hongo, K. Moji, and T. Oku, "Suppressive effect of partially hydrolyzed guar gum on transitory diarrhea induced by ingestion ofmaltitol and lactitol in healthy humans, " European Journal of Clinical Nutrition, vol. 61, no. 9, pp. 1086-1093, 2007.
12. C. J. Tuck, J. G. Muir, J. S. Barrett, andP. R. Gibson, "Fermentable oligosaccharides, disaccharides, monosaccharides and polyols: role in irritable bowel syndrome, " Expert Review of Gastroenterology and Hepatology, vol. 8, no. 7, pp. 819-834, 2014.
13. M. F. Nesterin, "Xylitol. Experimental and clinical investigations conducted in the USSR, " Zeitschrift für Ernährungswissenschaft, vol. 19, no. 2, pp. 88-94, 1980.
14. J. Xiao, B. U. Metzler-Zebeli, and Q. Zebeli, "Gut functionenhancing properties and metabolic effects of dietary indigestible sugars in rodents and rabbits, " Nutrients, vol. 7, no. 10, pp. 8348-8365, 2015.
15. P. de Cock, "Erythritol, " in Sweeteners and Sugar Alternatives in Food Technology, A. O'Donnell and W. Kearsley, Eds., pp. 215-241, Wiley-Blackwell, Oxford, UK, 2012.
16. J. R. Biesiekierski, O. Rosella, R. Rose et al., "Quantification of fructans, galacto-oligosacharides and other short-chain carbohydrates in processed grains and cereals, " Journal of Human Nutrition and Dietetics, vol. 24, no. 2, pp. 154-176, 2011.
17. J. G. Muir, R. Rose, O. Rosella et al., "Measurement of shortchain carbohydrates in common Australian vegetables and fruits by high-performance liquid chromatography (HPLC), " Journal of Agricultural and Food Chemistry, vol. 57, no. 2, pp. 554-565, 2009.
18. P. Symons, M. P. Jones, and J. E. Kellow, "Symptom provocation in irritable bowel syndrome effects of differing doses of fructose-sorbitol, " Scandinavian Journal of Gastroenterology, vol. 27, no. 11, pp. 940-944, 1992.
19. M. Georgieff, L. L. Moldawer, B. R. Bistrian, and G. L. Blackburn, "Xylitol, an energy source for intravenous nutrition after trauma, " Journal of Parenteral and Enteral Nutrition, vol. 9, no. 2, pp. 199-209, 1985.
20. A. Scheinin and K. K. Mäkinen, "Turku sugar studies. An overview, " Acta Odontologica Scandinavica, vol. 33, supplement 70, pp. 345-348, 1975.
21. P. R. Gibson and S. J. Shepherd, "Evidence-based dietary management of functional gastrointestinal symptoms: the FODMAP approach, " Journal of Gastroenterology and Hepatology, vol. 25, no. 2, pp. 252-258, 2010.
22. S. Shepherd, Low FODMAP Recipes, Penguin, Melbourne, Australia, 2013.
23. Low FODMAP Diet Application, [Mobile app] Monash University, Android version, http://www. med. monash. edu/cecs/gastro/fodmap/.
24. S. Magge and A. Lembo, "Low-FODMAP diet for treatment of irritable bowel syndrome, " Gastroenterology and Hepatology, vol. 8, no. 11, pp. 739-745, 2012.
25. W. S. Nanayakkara, P. M. L. Skidmore, L. O'Brien, T. J. Wilkinson, and R. B. Gearry, "Efficacy of the low FODMAP diet for treating irritable bowel syndrome: the evidence to date, " Clinical and Experimental Gastroenterology, vol. 9, pp. 131-142, 2016.
26. A. Dahlqvist and U. Telenius, "The utilization of a presumably low-cariogenic carbohydrate derivative, " Acta Physiologica Scandinavica, vol. 63, pp. 156-163, 1965.
27. E. B. Charney and J. N. Bodurtha, "Intractable diarrhea associated with the use of sorbitol, " The Journal of Pediatrics, vol. 98, no. 1, pp. 157-161, 1981.
28. M. J. R. Ravry, "Dietetic food diarrhea, " Journal of the American Medical Association, vol. 244, no. 3, p. 270, 1980.
29. C. J. McClain, J. P. Kromhout, L. Zieve, and W. C. Duane, "Effect of sorbitol on psychomotor function. Its use in alcoholic cirrhosis, " Archives of Internal Medicine, vol. 141, no. 7, pp. 901-903, 1981.
30. H. Mehnert, K. Stuhlfauth, B. Mehnert, R. Lausch, and W. Seitz, "Vergleichende untersuchungen zur resorption von glucose, fructose und sorbit beim menschen, " Klinische Wochenschrift, vol. 37, no. 21, pp. 1138-1142, 1959.
31. J. D. Gryboski, "Diarrhea from dietetic candies, " The New England Journal of Medicine, vol. 275, no. 13, p. 718, 1966.
32. L. D. Goldberg and N. T. Ditchek, "Chewing gum diarrhea, " The American Journal of Digestive Diseases, vol. 23, no. 6, p. 568, 1978.
33. R. E. Hill and K. R. Kamath, "Pink' diarrhoea from a sorbitolcontaining vitamin C supplement, " Medical Journal of Australia, vol. 1, no. 9, pp. 387-389, 1982.
34. S. L. Taylor and B. Byron, "Probable case of sorbitol-induced diarrhea, " Journal of Food Protection, vol. 47, article 249, 1984.
35. A. N. Payne, C. Chassard, and C. Lacroix, "Gut microbial adaptation to dietary consumption of fructose, artificial sweeteners and sugar alcohols: implications for host-microbe interactions contributing to obesity, " Obesity Reviews, vol. 13, no. 9, pp. 799-809, 2012.
36. P. Mansueto, A. Seidita, A. D'Alcamo, and A. Carroccio, "Role of FODMAPs in patients with irritable bowel syndrome, " Nutrition in Clinical Practice, vol. 30, no. 5, pp. 665-682, 2015.
37. F. W. Ellis and J. C. Krantz, "Sugar alcohols. XXII. Metabolism and toxicity studies with mannitol and sorbitol in man and animals, " Journal of Biological Chemistry, vol. 141, pp. 147-154, 1941.
38. S. J. Shepherd, M. C. E. Lomer, and P. R. Gibson, "Short-chain carbohydrates and functional gastrointestinal disorders, " The American Journal of Gastroenterology, vol. 108, no. 5, pp. 707-717, 2013.
39. F. Respondek, C. Hilpipre, P. Chauveau et al., "Digestive tolerance and postprandial glycaemic and insulinaemic responses after consumption of dairy desserts containing maltitol and fructo-oligosaccharides in adults, " European Journal of Clinical Nutrition, vol. 68, no. 5, pp. 575-580, 2014.
40. M. Goebel-Stengel and H. Mönnikes, "Malabsorption of fermentable oligo-, di-, or monosaccharides and polyols (FODMAP) as a common cause of unclear abdominal discomfort, " Deutsche Medizinische Wochenschrift, vol. 139, no. 24, pp. 1310-1314, 2014 (German).
41. M. El-Salhy, "Recent developments in the pathophysiology of irritable bowel syndrome, " World Journal of Gastroenterology, vol. 21, no. 25, pp. 7621-7636, 2015.
42. J. Beaven, A. Bjørneklett, E. Jenssen, J. P. Blomhoff, and S. Skrede, "Pulmonary hydrogen and methane and plasma ammonia after the administration of lactulose or sorbitol, " Scandinavian Journal of Gastroenterology, vol. 18, no. 3, pp. 343-347, 1983.
43. L. Beaugerie, B. Flouríe, P. Pernet, L. Achour, C. Franchisseur, and J. C. Rambaud, "Glucose does not facilitate the absorption of sorbitol perfused in situ in the human small intestine, " Journal of Nutrition, vol. 127, no. 2, pp. 341-344, 1997.
44. H.-J. Zunft, J. Schulze, H. Gärtner, and F.-K. Grütte, "Digestion of maltitol in man, rat, and rabbit, " Annals of Nutrition and Metabolism, vol. 27, no. 6, pp. 470-476, 1983.
45. D. M. Storey, G. A. Koutsou, A. Lee et al., "Tolerance and breath hydrogen excretion following ingestion ofmaltitol incorporated at two levels into milk chocolate consumed by healthy young adults with and without fasting, " Journal of Nutrition, vol. 128, no. 3, pp. 587-592, 1998.
46. A. Ruskoné-Fourmestraux, A. Attar, D. Chassard, B. Coffin, F. Bornet, and Y. Bouhnik, "A digestive tolerance study of maltitol after occasional and regular consumption in healthy humans, " European Journal of Clinical Nutrition, vol. 57, no. 1, pp. 26-30, 2003.
47. M. Tsukamura, H. Goto, T. Arisawa et al., "Dietary maltitol decreases the incidence of 1, 2-dimethylhydrazine-induced cecum and proximal colon tumors in rats, " Journal of Nutrition, vol. 128, no. 3, pp. 536-540, 1998.
48. H. Mineo, H. Hara, H. Kikuchi, H. Sakurai, andF. Tomita, "Various indigestible saccharides enhance net calcium transport from the epithelium of the small and large intestine of rats in vitro, " Journal of Nutrition, vol. 131, no. 12, pp. 3243-3246, 2001.
49. T. Goda, K. Kishi, I. Ezawa, and S. Takase, "The maltitolinduced increase in intestinal calcium transport increases the calciumcontent and breaking force of femoral bone in weanling rats, " Journal of Nutrition, vol. 128, no. 11, pp. 2028-2031, 1998.
50. M. Svanberg and M. Knuuttila, "Dietary xylitol retards bone resorption in rats, " Mineral and Electrolyte Metabolism, vol. 20, no. 3, pp. 153-157, 1994.
51. M. H. G. Dehghan, V. R. M. Gupta, S. M. Asif, Y. Darwis, M. Rizwan, and V. P. Mundada, "Assessment of isomalt for colonspecific delivery and its comparison with lactulose, " AAPS PharmSciTech, vol. 14, no. 1, pp. 53-59, 2013.
52. A. Lee, A. Zumbe, and D. Storey, "Breath hydrogen after ingestion of the bulk sweeteners sorbitol, isomalt and sucrose in chocolate, " British Journal of Nutrition, vol. 71, no. 5, pp. 731-737, 1994.
53. M. Finney, J. Smullen, H. A. Foster, S. Brokx, and D. M. Storey, "Effects of low doses of lactitol on faecal microflora, pH, short chain fatty acids and gastrointestinal symptomology, " European Journal of Nutrition, vol. 46, no. 6, pp. 307-314, 2007.
54. S. S. Natah, K. R. Hussien, J. A. Tuominen, and V. A. Koivisto, "Metabolic response to lactitol and xylitol in healthy men, " American Journal of Clinical Nutrition, vol. 65, no. 4, pp. 947-950, 1997.
55. E. Cristofaro, F. Mottu, and J. J. Wuhrmann, "Involvement of the raffinose family of oligosaccharides in flatulence, " in Sugars in Nutrition, H. L. Sipple and K. W. McNutt, Eds., pp. 313-336, Academic Press, New York, NY, USA, 1974.
56. Y. Hata, M. Yamamoto, and K. Nakajima, "Effects of soybean oligosaccharides on human digestive organs-estimation of fifty percent effective dose and maximum non-effective dose based on diarrhea, " Journal of Clinical Biochemistry and Nutrition, vol. 10, no. 2, pp. 135-144, 1991.
57. F. Askevold, "Investigations on the influence of diet on the quantity and composition of intestinal gas in humans, " Scandinavian Journal of Clinical and Laboratory Investigation, vol. 8, no. 2, pp. 87-94, 1956.
58. S. E. Fleming, "A study of relationships between flatus potential and carbohydrate distribution in legume seeds, " Journal of Food Science, vol. 46, no. 3, pp. 794-798, 1981.
59. D. R. Saunders and H. S. Wiggins, "Conservation of mannitol, lactulose, and raffinose by the human colon, " The American Journal of Physiology, vol. 241, no. 5, pp. G397-G402, 1981.
60. A. N. Galiullin, "Evaluation of the caries-preventive action of xylitol, " KazanMedical Journal, vol. 67, pp. 16-18, 1981 (Russian).
61. T. Asano, M. D. Levitt, and F. C. Goetz, "Xylitol absorption in healthy men, " Diabetes, vol. 22, no. 4, pp. 279-281, 1973.
62. J. J. Burns and J. Kanfer, "Formation of l-xylulose froml-gulonolactone in rat kidney, " Journal of the American Chemical Society, vol. 79, no. 13, pp. 3604-3605, 1957.
63. O. Touster, "Metabolismand physiological effects of the polyols (alditols), " in Physiological Effects of Food Carbohydrates, A. Jeanes and and J. Hodge, Eds., pp. 123-124, American Chemical Society, Washington, DC, USA, 1975.
64. O. Touster and D. R. D. Shaw, "Biochemistry of the acyclic polyols, " Physiological Reviews, vol. 42, pp. 181-225, 1962.
65. D. B. McCormick and O. Touster, "The conversion in vivo of xylitol to glycogen via the pentose phosphate pathway, " The Journal of Biological Chemistry, vol. 229, no. 1, pp. 451-461, 1957.
66. R. Ylikahri, "Metabolic and nutritional effects of xylitol, " Advances in Food Research, vol. 15, pp. 159-180, 1979.
67. K. H. Bässler, "Biochemistry of xylitol, " in Xylitol, J. N. Counsell, Ed., pp. 35-41, Applied Science, Essex, UK, 1978.
68. H. Förster, "Tolerance in the human, adults and children, " in Xylitol, J. N. Counsell, Ed., pp. 43-66, Applied Science Publishers, Barking, UK, 1978.
69. M. Brin and O. N. Miller, "The safety of oral xylitol, " in Sugars in Nutrition, H. L. Sipple and K. W. McNutt, Eds., pp. 591-612, Academic Press, New York, NY, USA, 1974.
70. Y.-M. Wang, S. J. Culbert, H. A. Fritsche Jr., and D. B. Carr, "Oral xylitol in humans, " Federations Proceedings, vol. 40, pp. 878-885, 1981.
71. K. K. Mäkinen, R. Ylikahri, L. Mäkinen, E. Söderling, and M. Hämäläinen, "Turku sugar studies XXIII. Comparison of metabolic tolerance in human volunteers to high oral doses of xylitol and sucrose after long-term regular consumption of xylitol, " International Journal of Vitamin and Nutrition Research. Supplement, vol. 22, pp. 29-51, 1982.
72. K. K. Mäkinen, "Effect of long-term, peroral administration of sugar alcohols onman, " SwedishDental Journal, vol. 8, no. 3, pp. 113-124, 1984.
73. H. Förster, R. Quadbeck, andU. Gottstein, "Metabolic tolerance to high doses of oral xylitol in human volunteers not previously adapted to xylitol, " International Journal for Vitamin and Nutrition Research, vol. 22, pp. 67-88, 1982.
74. K. K. Mäkinen and K. K. Virtanen, "Effect of 4. 5-year use of xylitol and sorbitol on plaque, " Journal of Dental Research, vol. 57, no. 3, pp. 441-446, 1978.
75. R. B. Shafer, A. S. Levine, J. M. Marlette, andJ. E. Morley, "Effects of xylitol on gastric emptying and food intake, " The American Journal of Clinical Nutrition, vol. 45, no. 4, pp. 744-747, 1987.
76. J. Bánóczy, A. Scheinin, R. Pados, G. Ember, P. Kertész, and K. Pienihäkkinen, "Collaborative WHO xylitol Field studies in Hungary II. General background and control of the dietary regimen, " Acta Odontologica Scandinavica, vol. 43, no. 6, pp. 349-357, 1985.
77. S. J. Culbert, Y.-M. Wang, H. A. Fritsche, D. Carr Jr., E. Lantin, and J. V. Eys, "Oral xylitol in American adults, " Nutrition Research, vol. 6, no. 8, pp. 913-922, 1986.
78. M. Lam, C. A. Riedy, S. E. Coldwell, P. Milgrom, and R. Craig, "Children's acceptance of xylitol-based foods, " CommunityDentistry and Oral Epidemiology, vol. 28, no. 2, pp. 97-101, 2000.
79. J. L. Castillo, P. Milgrom, S. E. Coldwell, R. Castillo, and R. Lazo, "Children's acceptance ofmilk with xylitol or sorbitol for dental caries prevention, " BMC Oral Health, vol. 5, article 6, 2005.
80. K. K. Mäkinen, K. P. Isotupa, P.-L. Mäkinen et al., "Six-month polyol chewing-gum programme in kindergarten-age children: a feasibility study focusing on mutans streptococci and dental plaque, " International Dental Journal, vol. 55, no. 2, pp. 81-88, 2005.
81. L. Vernacchio, R. M. Vezina, and A. A. Mitchell, "Tolerability of oral xylitol solution in young children: implications for otitis media prophylaxis, " International Journal of Pediatric Otorhinolaryngology, vol. 71, no. 1, pp. 89-94, 2007.
82. T. Oku and S. Nakamura, "Threshold for transitory diarrhea induced by ingestion of xylitol and lactitol in young male and female adults, " Journal of Nutritional Science and Vitaminology, vol. 53, no. 1, pp. 13-20, 2007.
83. M. Seki, F. Karakama, T. Kawato, H. Tanaka, Y. Saeki, and Y. Yamashita, "Effect of xylitol gum on the level of oral mutans streptococci of preschoolers: block-randomised trial, " International Dental Journal, vol. 61, no. 5, pp. 274-280, 2011.
84. US Department of Health and Human Services, Health Aspects of Sugar Alcohols and Lactose (Report Prepared for Center for Food Safety and Applied Nutrition, Food and Drug Administration, Contract No. FDA 223-83-2020), Life Sciences Research Office, Federation of American Societies for Experimental Biology, Bethesda, Md, USA, 1986.
85. US Department ofHealth andHuman Services, "Food Labeling: Health Claims; Sugar Alcohols and Dental Caries, " Food and Drug Administration, Federal Register 1996, August 23, vol. 61, no. 165, Rules andRegulations, pp. 43433-43447, Bethesda, Md, USA, 1996.
86. A. Bär, "Sugar alcohols in the diabetic diet, " in Sugars and Sweeteners, N. Kretchmer and C. B. Hollenbeck, Eds., pp. 131-150, CRC Press, Boca Raton, Fla, USA, 1991.
87. K. K. Mäkinen, "Authorized EU health claims for xylitol and sugar-free chewing gum (SGFCG), " in Foods, Nutrients and Food Ingredients with Authorised EUHealth Claims, M. J. Sadler, Ed., vol. 1, pp. 46-72, Woodhead Publishing, Cambridge, UK, 2014.
88. M. T. Flood, M. H. Auerbach, and S. A. S. Craig, "A review of the clinical toleration studies of polydextrose in food, " Food and Chemical Toxicology, vol. 42, no. 9, pp. 1531-1542, 2004.
89. P. de Cock and C.-L. Bechert, "Erythritol: functionality in noncaloric functional beverages, " Pure and Applied Chemistry, vol. 74, no. 7, pp. 1281-1289, 2002.
90. G. J. M. den Hartog, A. W. Boots, A. Adam-Perrot et al., "Erythritol is a sweet antioxidant, " Nutrition, vol. 26, no. 4, pp. 449-458, 2010.
91. F. R. J. Bornet, A. Blayo, F. Dauchy, and G. Slama, "Gastrointestinal response and plasma and urine determinations in human subjects given erythritol, " Regulatory Toxicology and Pharmacology, vol. 24, no. 2, part 2, pp. S296-S302, 1996.
92. W. Tetzloff, F. Dauchy, S. Medimagh, D. Carr, and A. Bär, "Tolerance to subchronic, high-dose ingestion of erythritol in human volunteers, " Regulatory Toxicology and Pharmacology, vol. 24, no. 2, pp. S286-S295, 1996.
93. E. Jacqz-Aigrain, B. Kassai, C. Cornu et al., "Gastrointestinal tolerance of erythritol-containing beverage in young children: a double-blind, randomised controlled trial, " European Journal of Clinical Nutrition, vol. 69, no. 6, pp. 746-751, 2015.
94. E. Arrigoni, F. Brouns, and R. Amadò, "Human gut microbiota does not ferment erythritol, " British Journal of Nutrition, vol. 94, no. 5, pp. 643-646, 2005.
95. Y. Kim, S. C. Park, B. W. Wolf, and S. R. Hertzler, "Combination of erythritol and fructose increases gastrointestinal symptoms in healthy adults, " Nutrition Research, vol. 31, no. 11, pp. 836-841, 2011.
96. L. Putkonen, C. K. Yao, and P. R. Gibson, "Fructosemalabsorption syndrome, " CurrentOpinion inClinicalNutrition andMetabolic Care, vol. 16, no. 4, pp. 473-477, 2013.
97. S. Honkala, R. Runnel, M. Saag et al., "Effect of erythritol and xylitol on dental caries prevention in children, " Caries Research, vol. 48, no. 5, pp. 482-490, 2014.
98. P. deCock, K. Mäkinen, E. Honkala, M. Saag, E. Kennepohl, and A. Eapen, "Erythritol is more effective than xylitol and sorbitol in managing oral health endpoints, " International Journal of Dentistry, vol. 2016, Article ID 9868421, 15 pages, 2016.
99. T. Takeda, S. Takeda, A. Kakigi, R. Nishioka, and M. Nishimura, "Decompression effects of erythritol on endolymphatic hydrops, " Auris, Nasus, Larynx, vol. 36, pp. 146-151, 2009.