Effects of the non-nutritive sweeteners on glucose metabolism and appetite regulating hormones: Systematic review of observational prospective studies and clinical Trials

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Romo Romo, Alonso ^a   Aguilar Salinas, Carlos A ^a   Brito Cordova, Griselda X ^a   Diaz, Rita A Gomez ^b   Valentin, David Vilchis ^a   Almeda Valdes, Paloma ^a  

^a INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^b HOSPITAL DE ESPECIALIDADES   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ACESULFAME; ASPARTAME; CHOLECYSTOKININ; GASTRIC INHIBITORY POLYPEPTIDE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HEMOGLOBIN A1C; INSULIN; NONNUTRITIVE SWEETENER; PEPTIDE YY; SACCHARIN; SUCRALOSE; SUCROSE; TRIACYLGLYCEROL;

ARTICLE; BEVERAGE; BODY MASS; CALORIC INTAKE; DISEASE ASSOCIATION; FOOD INTAKE; GLUCOSE METABOLISM; HUMAN; INSULIN CLEARANCE; INSULIN SENSITIVITY; INTESTINE FLORA; META ANALYSIS; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OBSERVATIONAL STUDY; PANCREAS ISLET BETA CELL; PROSPECTIVE STUDY; STOMACH EMPTYING; SYSTEMATIC REVIEW; VISUAL ANALOG SCALE; ADVERSE EFFECTS; CARBONATED BEVERAGE; CLINICAL TRIAL (TOPIC); DIABETES MELLITUS, TYPE 2; METABOLISM; PHYSIOLOGY;

CARBONATED BEVERAGES; CHOLECYSTOKININ; CLINICAL TRIALS AS TOPIC; DIABETES MELLITUS, TYPE 2; GHRELIN; GLUCOSE; HUMANS; NON-NUTRITIVE SWEETENERS; OBSERVATIONAL STUDIES AS TOPIC; PEPTIDE YY; PROSPECTIVE STUDIES;

EID: 84984972714     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0161264     Document Type: Article

References (49)

1. Barquera S, Hernandez-Barrera L, Tolentino ML, Espinosa J, Ng SW, Rivera JA, et al. Energy intake from beverages is increasing among Mexican adolescents and adults. The Journal of nutrition. 2008; 138(12):2454-61. doi: 10.3945/jn.108.092163 PMID: 19022972.
2. Shankar P, Ahuja S, Sriram K. Non-nutritive sweeteners: review and update. Nutrition. 2013; 29(11-12):1293-9. doi: 10.1016/j.nut.2013.03.024 PMID: 23845273.
3. Food U.S. and Drug Administration. Additional Information about High-Intensity Sweeteners Permitted for use in Food in the United States 2015 [updated 05/25/2015; cited 2016 02/01/2016]. Available: http://www.fda.gov/food/ingredientspackaginglabeling/foodadditivesingredients/ucm397725.htm.
4. European Food Safety Authority [Internet]. Sweetners [cited 2016 Feb 01]. Available: http://www.efsa. europa.eu/en/topics/topic/sweeteners.
5. Pepino MY. Metabolic effects of non-nutritive sweeteners. Physiology & behavior. 2015; 152(Pt B):450-5. doi: 10.1016/j.physbeh.2015.06.024 PMID: 26095119; PubMed Central PMCID: PMC4661066.
6. Qurrat ul A, Khan SA. Artificial sweeteners: safe or unsafe? JPMAThe Journal of the Pakistan Medical Association. 2015; 65(2):225-7. PMID: 25842566.
7. Bhupathiraju SN, Pan A, Malik VS, Manson JE, Willett WC, van Dam RM, et al. Caffeinated and caffeine-free beverages and risk of type 2 diabetes. The American journal of clinical nutrition. 2013; 97 (1):155-66. doi: 10.3945/ajcn.112.048603 PMID: 23151535; PubMed Central PMCID: PMC3522135.
8. Schulze MB, Manson JE, Ludwig DS, Colditz GA, Stampfer MJ, Willett WC, et al. Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. Jama. 2004; 292(8):927-34. doi: 10.1001/jama.292.8.927 PMID: 15328324.
9. de Koning L, Malik VS, Rimm EB, Willett WC, Hu FB. Sugar-sweetened and artificially sweetened beverage consumption and risk of type 2 diabetes in men. The American journal of clinical nutrition. 2011; 93(6):1321-7. doi: 10.3945/ajcn.110.007922 PMID: 21430119; PubMed Central PMCID: PMC3095502.
10. InterActC, Romaguera D, Norat T, Wark PA, Vergnaud AC, Schulze MB, et al. Consumption of sweet beverages and type 2 diabetes incidence in European adults: results from EPIC-InterAct. Diabetologia. 2013; 56(7):1520-30. doi: 10.1007/s00125-013-2899-8 PMID: 23620057.
11. Dhingra R, Sullivan L, Jacques PF, Wang TJ, Fox CS, Meigs JB, et al. Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community. Circulation. 2007; 116(5):480-8. doi: 10.1161/CIRCULATIONAHA.107.689935 PMID: 17646581.
12. Lutsey PL, Steffen LM, Stevens J. Dietary intake and the development of the metabolic syndrome: the Atherosclerosis Risk in Communities study. Circulation. 2008; 117(6):754-61. doi: 10.1161/CIRCULATIONAHA.107.716159 PMID: 18212291.
13. Fowler SP, Williams K, Resendez RG, Hunt KJ, Hazuda HP, Stern MP. Fueling the obesity epidemic? Artificially sweetened beverage use and long-term weight gain. Obesity. 2008; 16(8):1894-900. doi: 10.1038/oby.2008.284 PMID: 18535548.
14. Palmer JR, Boggs DA, Krishnan S, Hu FB, Singer M, Rosenberg L. Sugar-sweetened beverages and incidence of type 2 diabetes mellitus in African American women. Archives of internal medicine. 2008; 168(14):1487-92. doi: 10.1001/archinte.168.14.1487 PMID: 18663160; PubMed Central PMCID: PMC2708080.
15. Nettleton JA, Lutsey PL, Wang Y, Lima JA, Michos ED, Jacobs DR Jr. Diet soda intake and risk of incident metabolic syndrome and type 2 diabetes in the Multi-Ethnic Study of Atherosclerosis (MESA). Diabetes care. 2009; 32(4):688-94. doi: 10.2337/dc08-1799 PMID: 19151203; PubMed Central PMCID: PMC2660468.
16. Duffey KJ, Steffen LM, Van Horn L, Jacobs DR Jr., Popkin BM. Dietary patterns matter: diet beverages and cardiometabolic risks in the longitudinal Coronary Artery Risk Development in Young Adults (CAR-DIA) Study. The American journal of clinical nutrition. 2012; 95(4):909-15. doi: 10.3945/ajcn.111. 026682 PMID: 22378729; PubMed Central PMCID: PMC3302365.
17. Fagherazzi G, Vilier A, Saes Sartorelli D, Lajous M, Balkau B, Clavel-Chapelon F. Consumption of artificially and sugar-sweetened beverages and incident type 2 diabetes in the Etude Epidemiologique aupres desfemmes de la Mutuelle Generale de l'Education Nationale-European Prospective Investigation into Cancer and Nutrition cohort. The American journal of clinical nutrition. 2013; 97(3):517-23. doi: 10.3945/ajcn.112.050997 PMID: 23364017.
18. Sakurai M, Nakamura K, Miura K, Takamura T, Yoshita K, Nagasawa SY, et al. Sugar-sweetened beverage and diet soda consumption and the 7-year risk for type 2 diabetes mellitus in middle-aged Japanese men. European journal of nutrition. 2014; 53(4):1137-8. doi: 10.1007/s00394-014-0681-4 PMID: 24633756.
19. O'Connor L, Imamura F, Lentjes MA, Khaw KT, Wareham NJ, Forouhi NG. Prospective associations and population impact of sweet beverage intake and type 2 diabetes, and effects of substitutions with alternative beverages. Diabetologia. 2015; 58(7):1474-83. doi: 10.1007/s00125-015-3572-1 PMID: 25944371; PubMed Central PMCID: PMC4473082.
20. Pepino MY, Tiemann CD, Patterson BW, Wice BM, Klein S. Sucralose affects glycemic and hormonal responses to an oral glucose load. Diabetes care. 2013; 36(9):2530-5. doi: 10.2337/dc12-2221 PMID: 23633524; PubMed Central PMCID: PMC3747933.
21. Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014; 514(7521):181-6. doi: 10. 1038/nature13793 PMID: 25231862.
22. Hall WL, Millward DJ, Rogers PJ, Morgan LM. Physiological mechanisms mediating aspartame-induced satiety. Physiology & behavior. 2003; 78(4-5):557-62. PMID: 12782208.
23. Brown AW, Bohan Brown MM, Onken KL, Beitz DC. Short-term consumption of sucralose, anonnutri-tive sweetener, is similar to water with regard to select markers of hunger signaling and short-term glucose homeostasis in women. Nutrition research. 2011; 31(12):882-8. doi: 10.1016/j.nutres.2011.10. 004 PMID: 22153513.
24. Temizkan S, Deyneli O, Yasar M, Arpa M, Gunes M, Yazici D, et al. Sucralose enhances GLP-1 release and lowers blood glucose in the presence of carbohydrate in healthy subjects but not in patients with type 2 diabetes. European journal of clinical nutrition. 2015; 69(2):162-6. doi: 10.1038/ejcn.2014.208 PMID: 25271009.
25. Nehrling JK, Kobe P, McLane MP, Olson RE, Kamath S, Horwitz DL. Aspartame use by persons with diabetes. Diabetes care. 1985; 8(5):415-7. PMID: 3902420.
26. Okuno G, Kawakami F, Tako H, Kashihara T, Shibamoto S, Yamazaki T, et al. Glucose tolerance, blood lipid, insulin and glucagon concentration after single or continuous administration of aspartame in diabetics. Diabetes research and clinical practice. 1986; 2(1):23-7. PMID: 3522147.
27. Horwitz DL, McLane M, Kobe P. Response to single dose of aspartame or saccharin by NIDDM patients. Diabetes care. 1988; 11(3):230-4. PMID: 3046854.
28. Cooper PL, Wahlqvist ML, Simpson RW. Sucrose versus saccharin as an added sweetener in non-insulin-dependent diabetes: short-and medium-term metabolic effects. Diabetic medicine: a journal of the British Diabetic Association. 1988; 5(7):676-80. PMID: 2975554.
29. Colagiuri S, Miller JJ, Edwards RA. Metabolic effects of adding sucrose and aspartame to the diet of subjects with noninsulin-dependent diabetes mellitus. The American journal of clinical nutrition. 1989; 50(3):474-8. PMID: 2672774.
30. Rodin J. Comparative effects of fructose, aspartame, glucose, and water preloads on calorie and mac-ronutrient intake. The American journal of clinical nutrition. 1990; 51(3):428-35. PMID: 2178391.
31. Härtel BG H. Schneider B. Bier A. The influence of sweetener solutions on the secretion of insulin and blood glucose level. Ernährungsunschau. 1993; 40(4):152-5.
32. Mezitis NH, Maggio CA, Koch P, Quddoos A, Allison DB, Pi-Sunyer FX. Glycemic effect of a single high oral dose of the novel sweetener sucralose in patients with diabetes. Diabetes care. 1996; 19(9):1004-5. PMID: 8875098.
33. Melanson KJ, Westerterp-Plantenga MS, Campfield LA, Saris WH. Blood glucose and meal patterns in time-blinded males, after aspartame, carbohydrate, and fat consumption, in relation to sweetness perception. The British journal of nutrition. 1999; 82(6):437-46. PMID: 10690159.
34. Grotz VL, Henry RR, McGill JB, Prince MJ, Shamoon H, Trout JR, et al. Lack of effect of sucralose on glucose homeostasis in subjects with type 2 diabetes. Journal of the American Dietetic Association. 2003; 103(12):1607-12. doi: 10.1016/j.jada.2003.09.021 PMID: 14647086.
35. Gregersen S, Jeppesen PB, Holst JJ, Hermansen K. Antihyperglycemic effects of stevioside in type 2 diabetic subjects. Metabolism: clinical and experimental. 2004; 53(1):73-6. PMID: 14681845.
36. Barriocanal LA, Palacios M, Benitez G, Benitez S, Jimenez JT, Jimenez N, et al. Apparent lack of pharmacological effect of steviol glycosides used as sweeteners in humans. A pilot study of repeated exposures in some normotensive and hypotensive individuals and in Type 1 and Type 2 diabetics. Regulatory toxicology and pharmacology: RTP. 2008; 51(1):37-41. doi: 10.1016/j.yrtph.2008.02.006 PMID: 18397817.
37. Maki KC, Curry LL, Reeves MS, Toth PD, McKenney JM, Farmer MV, et al. Chronic consumption of rebaudioside A, a steviol glycoside, in men and women with type 2 diabetes mellitus. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association. 2008; 46 Suppl 7:S47-53. doi: 10.1016/j.fct.2008.05.007 PMID: 18555575.
38. Ma J, Bellon M, Wishart JM, Young R, Blackshaw LA, Jones KL, et al. Effect of the artificial sweetener, sucralose, on gastric emptying and incretin hormone release in healthy subjects. American journal of physiology Gastrointestinal and liver physiology. 2009; 296(4):G735-9. doi: 10.1152/ajpgi.90708.2008 PMID: 19221011; PubMed Central PMCID: PMC2670679.
39. Anton SD, Martin CK, Han H, Coulon S, Cefalu WT, Geiselman P, et al. Effects of stevia, aspartame, and sucrose on food intake, satiety, and postprandial glucose and insulin levels. Appetite. 2010; 55 (1):37-43. doi: 10.1016/j.appet.2010.03.009 PMID: 20303371; PubMed Central PMCID: PMC2900484.
40. Ma J, Chang J, Checklin HL, Young RL, Jones KL, Horowitz M, et al. Effect of the artificial sweetener, sucralose, on small intestinal glucose absorption in healthy human subjects. The British journal of nutrition. 2010; 104(6):803-6. doi: 10.1017/S0007114510001327 PMID: 20420761.
41. Ford HE, Peters V, Martin NM, Sleeth ML, Ghatei MA, Frost GS, et al. Effects of oral ingestion of sucralose on gut hormone response and appetite in healthy normal-weight subjects. European journal of clinical nutrition. 2011; 65(4):508-13. doi: 10.1038/ejcn.2010.291 PMID: 21245879.
42. Steinert RE, Frey F, Topfer A, Drewe J, Beglinger C. Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. The British journal of nutrition. 2011; 105(9):1320-8. doi: 10.1017/S000711451000512X PMID: 21255472.
43. Maersk M, Belza A, Holst JJ, Fenger-Gron M, Pedersen SB, Astrup A, et al. Satiety scores and satiety hormone response after sucrose-sweetened soft drink compared with isocaloric semi-skimmed milk and with non-caloric soft drink: a controlled trial. European journal of clinical nutrition. 2012; 66(4):523-9. doi: 10.1038/ejcn.2011.223 PMID: 22252107.
44. Wu T, Zhao BR, Bound MJ, Checklin HL, Bellon M, Little TJ, et al. Effects of different sweet preloads on incretin hormone secretion, gastric emptying, and postprandial glycemia in healthy humans. The American journal of clinical nutrition. 2012; 95(1):78-83. doi: 10.3945/ajcn.111.021543 PMID: 22158727.
45. Brown RJ, Walter M, Rother KI. Effects of diet soda on gut hormones in youths with diabetes. Diabetes care. 2012; 35(5):959-64. doi: 10.2337/dc11-2424 PMID: 22410815; PubMed Central PMCID: PMC3329835.
46. Olalde-Mendoza L, Moreno-Gonzalez YE. [Modification of fasting blood glucose in adults with diabetes mellitus type 2 after regular soda and diet soda intake in the State of Queretaro, Mexico]. Archivos lati-noamericanos de nutricion. 2013; 63(2):142-7. PMID: 24934070.
47. Bryant CE, Wasse LK, Astbury N, Nandra G, McLaughlin JT. Non-nutritive sweeteners: no class effect on the glycaemic or appetite responses to ingested glucose. European journal of clinical nutrition. 2014; 68(5):629-31. doi: 10.1038/ejcn.2014.19 PMID: 24595225; PubMed Central PMCID: PMC4012981.
48. Greenwood DC, Threapleton DE, Evans CE, Cleghorn CL, Nykjaer C, Woodhead C, et al. Association between sugar-sweetened and artificially sweetened soft drinks and type 2 diabetes: systematic review and dose-response meta-analysis of prospective studies. The British journal of nutrition. 2014; 112 (5):725-34. doi: 10.1017/S0007114514001329 PMID: 24932880.
49. Imamura F, O'Connor L, Ye Z, Mursu J, Hayashino Y, Bhupathiraju SN, et al. Consumption of sugar sweetened beverages, artificially sweetened beverages, and fruit juice and incidence of type 2 diabetes: systematic review, meta-analysis, and estimation of population attributable fraction. Bmj. 2015; 351:h3576. doi: 10.1136/bmj.h3576 PMID: 26199070; PubMed Central PMCID: PMC4510779.