Reshaping the gut microbiota: Impact of low calorie sweeteners and the link to insulin resistance?

Physiology and Behavior

Volumn 164, Issue , 2016, Pages 488-493

  Nettleton, Jodi E ^a   Reimer, Raylene A ^a,b   Shearer, Jane ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Glucoregulation; Insulin resistance; Low calorie sweetener; Microbiota; Non nutritive sweeteners

Indexed keywords

ASPARTAME; SACCHARIN; SUCRALOSE; NONNUTRITIVE SWEETENER;

CALORIE; CHRONIC INFLAMMATION; EPIDEMIOLOGICAL DATA; HUMAN; IMPAIRED GLUCOSE TOLERANCE; INNATE IMMUNITY; INSULIN RESISTANCE; INTESTINE FLORA; KNOWLEDGE; METABOLITE; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; SATIETY; WEIGHT REDUCTION; ANIMAL; CHEMISTRY; DRUG EFFECTS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; GASTROINTESTINAL MICROBIOME; HUMANS; INSULIN RESISTANCE; NON-NUTRITIVE SWEETENERS; OBESITY;

EID: 84975129722     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2016.04.029     Document Type: Review

References (82)

1. [1] Abou-Donia, M.B., El-Masry, E.M., Abdel-Rahman, A.A., McLendon, R.E., Schiffman, S.S., Splenda alters gut microflora and increases intestinal p-glycoprotein and cytochrome P-450 in male rats. J. Toxic. Environ. Health A 71 (2008), 1415–1429.
2. [2] Anderson, R.L., Effect of saccharin ingestion on stool composition in relation to caecal enlargement and increased stool hydration. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 21 (1983), 255–257.
3. [3] Anderson, R. L. & Kirkland, J. J. The effect of sodium saccharin in the diet on caecal microflora. Food Cosmet. Toxicol. 18, 353–355 (1980).
4. [4] Bäckhed, F., et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 15718–15723.
5. [5] Bleich, S.N., Wolfson, J.A., Vine, S., Wang, Y.C., Diet-beverage consumption and caloric intake among US adults, overall and by body weight. Am. J. Public Health 104 (2014), e72–e78.
6. [6] Caesar, R., Tremaroli, V., Kovatcheva-Datchary, P., Cani, P.D., Bäckhed, F., Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab. 22 (2015), 658–668.
7. [7] Caldwell, D.R., Effects of methanol on the growth of gastrointestinal anaerobes. Can. J. Microbiol. 35 (1989), 313–317.
8. [8] Cani, P. D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761 + (2007).
9. [9] Cho, I., et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488 (2012), 621–626.
10. [10] Ciappuccini, R., Ansemant, T., Maillefert, J.-F., Tavernier, C., Ornetti, P., Aspartame-induced fibromyalgia, an unusual but curable cause of chronic pain. Clin. Exp. Rheumatol. 28 (2010), S131–S133.
11. [11] Clarke, S.F., et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63 (2014), 1913–1920.
12. [12] Collison, K.S., et al. Interactive effects of neonatal exposure to monosodium glutamate and aspartame on glucose homeostasis. Nutr. Metab. (Lond.), 9, 2012, 58.
13. [13] Cordain, L., et al. Origins and evolution of the Western diet: health implications for the 21st century. Am. J. Clin. Nutr. 81 (2005), 341–354.
14. [14] Cotillard, A., et al. Dietary intervention impact on gut microbial gene richness. Nature 500 (2013), 585–588.
15. [15] De Filippis, F., et al. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut, 2015, 10.1136/gutjnl-2015-309957.
16. [16] De Vadder, F., et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156 (2014), 84–96.
17. [17] Dhingra, R., et al. Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community. Circulation 116 (2007), 480–488.
18. [18] Dicksved, J., Ellström, P., Engstrand, L., Rautelin, H., Susceptibility to Campylobacter infection is associated with the species composition of the human fecal microbiota. mBio 5 (2014), e01212–e01214.
19. [19] Everard, A., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 9066–9071.
20. [20] Fagherazzi, G., et al. Consumption of artificially and sugar-sweetened beverages and incident type 2 diabetes in the Etude Epidemiologique aupres des femmes de la Mutuelle Generale de l'Education Nationale-European prospective investigation into cancer and nutrition cohort. Am. J. Clin. Nutr. 97 (2013), 517–523.
21. [21] Frankenfeld, C.L., Sikaroodi, M., Lamb, E., Shoemaker, S., Gillevet, P.M., High-intensity sweetener consumption and gut microbiome content and predicted gene function in a cross-sectional study of adults in the United States. Ann. Epidemiol., 2015, 10.1016/j.annepidem.2015.06.083.
22. [22] Fugmann, M., et al. The stool microbiota of insulin resistant women with recent gestational diabetes, a high risk group for type 2 diabetes. Sci. Rep., 5, 2015, 13212.
23. [23] Gómez-Hurtado, I., et al. Gut microbiota dysbiosis is associated with inflammation and bacterial translocation in mice with CCl4-induced fibrosis. PLoS ONE, 6, 2011, e23037.
24. [24] Government of Canada, H. C. 9. List of Permitted Sweeteners (Lists of Permitted Food Additives)- Health Canada, 2016 Available at http://www.hc-sc.gc.ca/fn-an/securit/addit/list/9-sweetener-edulcorant-eng.php (Accessed: 13th March 2016).
25. [25] Graf, D., et al. Contribution of diet to the composition of the human gut microbiota. Microb. Ecol. Health Dis., 26, 2015, 26164.
26. [26] Gravitz, L., Microbiome: the critters within. Nature 485 (2012), S12–S13.
27. [27] Nutrition, C. for F. S. and A. food additives & ingredients - additional information about high-intensity sweeteners permitted for use in food in the United States. Available at: http://www.fda.gov/Food/IngredientsPackagingLabeling/FoodAdditivesIngredients/ucm397725.htm. (Accessed: 11th March 2016).
28. [28] Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
29. [29] Hur, K.Y., Lee, M.-S., New mechanisms of metformin action: focusing on mitochondria and the gut. J. Diabetes Investig. 6 (2015), 600–609.
30. [30] Insulin resistance and prediabetes. (2014).
31. [31] Johnston, C.A., Foreyt, J.P., Robust scientific evidence demonstrates benefits of artificial sweeteners. Trends Endocrinol. Metab. TEM, 25, 2014, 1.
32. [32] Kaakoush, N.O., et al. Alternating or continuous exposure to cafeteria diet leads to similar shifts in gut microbiota compared to chow diet. Mol. Nutr. Food Res., 2016, 10.1002/mnfr.201500815.
33. [33] Kaoutari, A. El, Armougom, F., Gordon, J.I., Raoult, D., Henrissat, B., The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11 (2013), 497–504.
34. [34] Karlsson, F.H., et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun., 3, 2012, 1245.
35. [35] Kuk, J. L. & Brown, R. E. Aspartame intake is associated with greater glucose intolerance in individuals with obesity. Appl. Physiol. Nutr. Metab. In Press, (2016).
36. [36] Kuwahara, A., Contributions of colonic short-chain fatty acid receptors in energy homeostasis. Front. Endocrinol., 5, 2014, 144.
37. [37] Lambert, J.E., et al. Exercise training modifies gut microbiota in normal and diabetic mice. Appl. Physiol. Nutr. Metab. Physiol. Appliquée Nutr. Métabolisme 40 (2015), 749–752.
38. [38] Le Chatelier, E., et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
39. [39] Ley, R.E., et al. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 11070–11075.
40. [40] Lozupone, C.A., Stombaugh, J.I., Gordon, J.I., Jansson, J.K., Knight, R., Diversity, stability and resilience of the human gut microbiota. Nature 489 (2012), 220–230.
41. [41] Lutsey, P.L., Steffen, L.M., Stevens, J., Dietary intake and the development of the metabolic syndrome: the atherosclerosis risk in communities study. Circulation 117 (2008), 754–761.
42. [42] Martins, M.B., Carvalho, I., Diketopiperazines: biological activity and synthesis. Tetrahedron 63 (2007), 9923–9932.
43. [43] Mennella, J.A., Ontogeny of taste preferences: basic biology and implications for health12345. Am. J. Clin. Nutr. 99 (2014), 704S–711S.
44. [44] Mithieux, G., Nutrient control of energy homeostasis via gut-brain neural circuits. Neuroendocrinology 100 (2014), 89–94.
45. [45] Neish, A.S., Microbes in gastrointestinal health and disease. Gastroenterology 136 (2009), 65–80.
46. [46] Nettleton, J.A., et al. Diet soda intake and risk of incident metabolic syndrome and type 2 diabetes in the Multi-Ethnic Study of Atherosclerosis (MESA). Diabetes Care 32 (2009), 688–694.
47. [47] Palmnäs, M.S.A., et al. Low-dose aspartame consumption differentially affects gut microbiota-host metabolic interactions in the diet-induced obese rat. PLoS ONE, 9, 2014, e109841.
48. [48] Parnell, J.A., Reimer, R.A., Prebiotic fiber modulation of the gut microbiota improves risk factors for obesity and the metabolic syndrome. Gut Microbes 3 (2012), 29–34.
49. [49] Pope, E., Koren, G., Bozzo, P., Sugar substitutes during pregnancy. Can. Fam. Physician 60 (2014), 1003–1005.
50. [50] Ranney, R.E., Oppermann, J.A., Muldoon, E., McMahon, F.G., Comparative metabolism of aspartame in experimental animals and humans. J. Toxicol. Environ. Health 2 (1976), 441–451.
51. [51] Rastall, R.A., Bacteria in the gut: friends and foes and how to alter the balance. J. Nutr. 134 (2004), 2022S–2026S.
52. [52] Renwick, A.G., The metabolism of intense sweeteners. Xenobiotica Fate Foreign Compd. Biol. Syst. 16 (1986), 1057–1071.
53. [53] Roberts, A., Renwick, A.G., Sims, J., Snodin, D.J., Sucralose metabolism and pharmacokinetics in man. Food Chem. Toxicol. 38:Supplement 2 (2000), 31–41.
54. [54] Round, J.L., Mazmanian, S.K., The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9 (2009), 313–323.
55. [55] Savage, D.C., Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31 (1977), 107–133.
56. [56] Scher, J.U., et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. Hoboken NJ 67 (2015), 128–139.
57. [57] Schwiertz, A., et al. Microbiota and SCFA in lean and overweight healthy subjects. Obes. Silver Spring Md 18 (2010), 190–195.
58. [58] Scientific Report of the 2015 Dietary Guidelines Advisory Committee. (2015).
59. [59] Seto, C.T., Jeraldo, P., Orenstein, R., Chia, N., DiBaise, J.K., Prolonged use of a proton pump inhibitor reduces microbial diversity: implications for Clostridium difficile susceptibility. Microbiome, 2, 2014, 42.
60. [60] Sharon, G., et al. Specialized metabolites from the microbiome in health and disease. Cell Metab. 20 (2014), 719–730.
61. [61] Siurana, A. The effect of dietary supplementation of artificial sweetener on performance of milk-fed calves. in (Asas, 2014).
62. [62] Sjöström, L., et al. Bariatric surgery and long-term cardiovascular events. JAMA 307 (2012), 56–65.
63. [63] Sterk, A., Schlegel, P., Mul, A.J., Ubbink-Blanksma, M., Bruininx, E., M. a., M., Effects of sweeteners on individual feed intake characteristics and performance in group-housed weanling pigs. J. Anim. Sci. 86 (2008), 2990–2997.
64. [64] Suez, J., et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature, 2014, 10.1038/nature13793.
65. [65] Swartz, T.D., Duca, F.A., de Wouters, T., Sakar, Y., Covasa, M., Up-regulation of intestinal type 1 taste receptor 3 and sodium glucose luminal transporter-1 expression and increased sucrose intake in mice lacking gut microbiota. Br. J. Nutr. 107 (2012), 621–630.
66. [66] Swidsinski, A., et al. Mucosal flora in inflammatory bowel disease. Gastroenterology 122 (2002), 44–54.
67. [67] Swithers, S.E., Artificial sweeteners produce the counterintuitive effect of inducing metabolic derangements. Trends Endocrinol. Metab. 24 (2013), 431–441.
68. [68] Sylvetsky, A.C., Welsh, J.A., Brown, R.J., Vos, M.B., Low-calorie sweetener consumption is increasing in the United States. Am. J. Clin. Nutr. 96 (2012), 640–646.
69. [69] Sylvetsky, A.C., et al. Nonnutritive sweeteners in breast milk. J. Toxic. Environ. Health A 78 (2015), 1029–1032.
70. [70] Tremaroli, V., et al. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab. 22 (2015), 228–238.
71. [71] Turnbaugh, P.J., et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1131.
72. [72] Turnbaugh, P.J., Bäckhed, F., Fulton, L., Gordon, J.I., Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3 (2008), 213–223.
73. [73] Turnbaugh, P.J., et al. A core gut microbiome in obese and lean twins. Nature 457 (2009), 480–484.
74. [74] van Munster, I.P., Tangerman, A., Nagengast, F.M., Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig. Dis. Sci. 39 (1994), 834–842.
75. [75] Veien, N.K., Lomholt, H.B., Systemic allergic dermatitis presumably caused by formaldehyde derived from aspartame. Contact Dermatitis 67 (2012), 315–316.
76. [76] Vrieze, A. et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913–916.e7 (2012).
77. [77] WHO | Controlling the global obesity epidemic. WHO Available at: http://www.who.int/nutrition/topics/obesity/en/. (Accessed: 24th August 2015).
78. [78] WHO | Obesity and overweight. WHO Available at: http://www.who.int/mediacentre/factsheets/fs311/en/. (Accessed: 13th March 2016).
79. [79] WHO | Diabetes. WHO Available at: http://www.who.int/mediacentre/factsheets/fs312/en/. (Accessed: 13th March 2016).
80. [80] Wu, G.D., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334 (2011), 105–108.
81. [81] Yadav, H., Lee, J.-H., Lloyd, J., Walter, P., Rane, S.G., Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J. Biol. Chem. 288 (2013), 25088–25097.
82. [82] Yang, Q., Gain weight by ‘going diet?’ Artificial sweeteners and the neurobiology of sugar cravings: neuroscience 2010. Yale J. Biol. Med. 83 (2010), 101–108.