1932

Abstract

High sugar intake may increase cancer risk by promoting insulin–glucose dysregulation, oxidative stress, inflammation, and body adiposity, but epidemiologic evidence is unclear. Associations between dietary sugars and lifestyle-related cancer risk from longitudinal studies were evaluated. We systematically searched PubMed, Embase, and CINAHL and identified 37 prospective cohort studies (1990–2017) reporting multivariable adjusted risk estimates for dietary sugars in relation to cancer. Of 15 and 14 studies on total sugar and sucrose respectively, 11 reported a null association in relation to cancer. Of 14 studies on fructose, 8 reported null associations, and 2 reported protective and 4 reported detrimental associations. In two of five studies on added sugars, a 60–95% increased cancer risk was observed with higher intakes. In 8 of 15 studies on sugary foods and beverages, a 23–200% higher cancer risk was observed with higher sugary beverage consumption. In conclusion, most studies were indicative of a null association, but suggestive detrimental associations were reported for added sugars and sugary beverages.

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2018-08-21
2024-10-12
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Literature Cited

  1. 1.  Aune D, Chan D, Vieira A, Rosenblatt DN, Vieira R et al. 2012. Dietary fructose, carbohydrates, glycemic indices and pancreatic cancer risk: a systematic review and meta-analysis of cohort studies. Ann. Oncol. 23:2536–46
    [Google Scholar]
  2. 2.  Austin GL, Ogden LG, Hill JO 2011. Trends in carbohydrate, fat, and protein intakes and association with energy intake in normal-weight, overweight, and obese individuals: 1971–2006. Am. J. Clin. Nutr. 93:836–43
    [Google Scholar]
  3. 3.  Bao Y, Stolzenberg-Solomon R, Jiao L, Silverman DT, Subar AF et al. 2008. Added sugar and sugar-sweetened foods and beverages and the risk of pancreatic cancer in the National Institutes of Health–AARP diet and health study. Am. J. Clin. Nutr. 88:431–40
    [Google Scholar]
  4. 4.  Bostick RM, Potter JD, Kushi LH, Sellers TA, Steinmetz KA et al. 1994. Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 5:38–52
    [Google Scholar]
  5. 5.  Buyken AE, Goletzke J, Joslowski G, Felbick A, Cheng G et al. 2014. Association between carbohydrate quality and inflammatory markers: systematic review of observational and interventional studies. Am. J. Clin. Nutr. 99:813–33
    [Google Scholar]
  6. 6.  Calle EE, Kaaks R 2004. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4:579–91
    [Google Scholar]
  7. 7.  Coleman HG, Kitahara CM, Murray LJ, Dodd KW, Black A et al. 2014. Dietary carbohydrate intake, glycemic index, and glycemic load and endometrial cancer risk: a prospective cohort study. Am. J. Epidemiol. 179:75–84
    [Google Scholar]
  8. 8.  Cust AE, Slimani N, Kaaks R, Van Bakel M, Biessy C et al. 2007. Dietary carbohydrates, glycemic index, glycemic load, and endometrial cancer risk within the European Prospective Investigation into Cancer and Nutrition Cohort. Am. J. Epidemiol. 166:912–23
    [Google Scholar]
  9. 9.  Drake I, Sonestedt E, Gullberg B, Ahlgren G, Bjartell A et al. 2012. Dietary intakes of carbohydrates in relation to prostate cancer risk: a prospective study in the Malmö Diet and Cancer cohort. Am. J. Clin. Nutr. 96:1409–18
    [Google Scholar]
  10. 10.  El Mjiyad N, Caro-Maldonado A, Ramírez-Peinado S, Munoz-Pinedo C 2010. Sugar-free approaches to cancer cell killing. Oncogene 30:253–64
    [Google Scholar]
  11. 11.  Elliott SS, Keim NL, Stern JS, Teff K, Havel PJ 2002. Fructose, weight gain, and the insulin resistance syndrome. Am. J. Clin. Nutr. 76:911–22
    [Google Scholar]
  12. 12.  Fedirko V, Lukanova A, Bamia C, Trichopolou A, Trepo E et al. 2013. Glycemic index, glycemic load, dietary carbohydrate, and dietary fiber intake and risk of liver and biliary tract cancers in Western Europeans. Ann. Oncol. 24:543–53
    [Google Scholar]
  13. 13.  Ford ES, Dietz WH 2013. Trends in energy intake among adults in the United States: findings from NHANES. Am. J. Clin. Nutr. 97:848–53
    [Google Scholar]
  14. 14.  Freeman HP 2004. Poverty, culture, and social injustice: determinants of cancer disparities. CA Cancer J. Clin. 54:72–77
    [Google Scholar]
  15. 15.  Friberg E, Wallin A, Wolk A 2011. Sucrose, high-sugar foods, and risk of endometrial cancer—a population-based cohort study. Cancer Epidemiol. Biomark. Prev. 20:1831–37
    [Google Scholar]
  16. 16.  Giovannucci E 2001. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J. Nutr. 131:3109S–20S
    [Google Scholar]
  17. 17.  Giovannucci E, Harlan DM, Archer MC, Bergenstal RM, Gapstur SM et al. 2010. Diabetes and cancer: a consensus report. CA Cancer J. Clin. 60:207–21
    [Google Scholar]
  18. 18.  Giovannucci E, Rimm EB, Wolk A, Ascherio A, Stampfer MJ et al. 1998. Calcium and fructose intake in relation to risk of prostate cancer. Cancer Res 58:442–47
    [Google Scholar]
  19. 19.  Heinen MM, Verhage BA, Lumey L, Brants HA, Goldbohm RA, van den Brandt PA 2008. Glycemic load, glycemic index, and pancreatic cancer risk in the Netherlands Cohort Study. Am. J. Clin. Nutr. 87:970–77
    [Google Scholar]
  20. 20.  Hess J, Latulippe ME, Ayoob K, Slavin J 2012. The confusing world of dietary sugars: definitions, intakes, food sources and international dietary recommendations. Food Funct 3:477–86
    [Google Scholar]
  21. 21.  Higginbotham S, Zhang Z, Lee I, Cook NR, Giovannucci E et al. 2004. Dietary glycemic load and risk of colorectal cancer in the Women's Health Study. J. Natl. Cancer Inst. 96:229–33
    [Google Scholar]
  22. 22.  Howarth NC, Murphy SP, Wilkens LR, Henderson BE, Kolonel LN 2008. The association of glycemic load and carbohydrate intake with colorectal cancer risk in the Multiethnic Cohort Study. Am. J. Clin. Nutr. 88:1074–82
    [Google Scholar]
  23. 23.  Hu FB, Rimm E, Smith-Warner SA, Feskanich D, Stampfer MJ et al. 1999. Reproducibility and validity of dietary patterns assessed with a food-frequency questionnaire. Am. J. Clin. Nutr. 69:243–49
    [Google Scholar]
  24. 24.  Inoue-Choi M, Robien K, Mariani A, Cerhan JR, Anderson KE 2013. Sugar-sweetened beverage intake and the risk of type I and type II endometrial cancer among postmenopausal women. Cancer Epidemiol. Biomark. Prev. 22:2384–94
    [Google Scholar]
  25. 25.  Jiao L, Flood A, Subar AF, Hollenbeck AR, Schatzkin A, Stolzenberg-Solomon R 2009. Glycemic index, carbohydrates, glycemic load, and the risk of pancreatic cancer in a prospective cohort study. Cancer Epidemiol. Biomark. Prev. 18:1144–51
    [Google Scholar]
  26. 26.  Johnson RJ, Segal MS, Sautin Y, Nakagawa T, Feig DI et al. 2007. Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am. J. Clin. Nutr. 86:899–906
    [Google Scholar]
  27. 27.  Johnson RK, Appel LJ, Brands M, Howard BV, Lefevre M et al. 2009. Dietary sugars intake and cardiovascular health: a scientific statement from the American Heart Association. Circulation 120:1011–20
    [Google Scholar]
  28. 28.  Kabat GC, Shikany JM, Beresford SA, Caan B, Neuhouser ML et al. 2008. Dietary carbohydrate, glycemic index, and glycemic load in relation to colorectal cancer risk in the Women's Health Initiative. Cancer Causes Control 19:1291–98
    [Google Scholar]
  29. 29.  Klement RJ, Kämmerer U 2011. Is there a role for carbohydrate restriction in the treatment and prevention of cancer?. Nutr. Metab. 8:75
    [Google Scholar]
  30. 30.  Larson NI, Story MT, Nelson MC 2009. Neighborhood environments: disparities in access to healthy foods in the U.S. Am. J. Prev. Med. 36:74–81
    [Google Scholar]
  31. 31.  Larsson SC, Bergkvist L, Wolk A 2006. Consumption of sugar and sugar-sweetened foods and the risk of pancreatic cancer in a prospective study. Am. J. Clin. Nutr. 84:1171–76
    [Google Scholar]
  32. 32.  Larsson SC, Giovannucci EL, Wolk A 2016. Sweetened beverage consumption and risk of biliary tract and gallbladder cancer in a prospective study. J. Natl. Cancer Inst. 108:djw125
    [Google Scholar]
  33. 33.  Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC et al. 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLOS Med 6:e1000100
    [Google Scholar]
  34. 34.  Liu H, Heaney AP 2011. Refined fructose and cancer. Expert Opin. Ther. Targets 15:1049–59
    [Google Scholar]
  35. 35.  Malik VS, Popkin BM, Bray GA, Després J, Hu FB 2010. Sugar-sweetened beverages, obesity, type 2 diabetes mellitus, and cardiovascular disease risk. Circulation 121:1356–64
    [Google Scholar]
  36. 36.  Malik VS, Popkin BM, Bray GA, Després JP, Willett WC, Hu FB 2010. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care 33:2477–83
    [Google Scholar]
  37. 37.  McCullough ML, Teras LR, Shah R, Diver WR, Gaudet MM, Gapstur SM 2014. Artificially and sugar-sweetened carbonated beverage consumption is not associated with risk of lymphoid neoplasms in older men and women. J. Nutr. 144:2041–49
    [Google Scholar]
  38. 38.  Meinhold CL, Dodd KW, Jiao L, Flood A, Shikany JM et al. 2010. Available carbohydrates, glycemic load, and pancreatic cancer: Is there a link?. Am. J. Epidemiol. 171:1174–82
    [Google Scholar]
  39. 39.  Michaud DS, Fuchs CS, Liu S, Willett WC, Colditz GA, Giovannucci E 2005. Dietary glycemic load, carbohydrate, sugar, and colorectal cancer risk in men and women. Cancer Epidemiol. Biomark. Prev. 14:138–47
    [Google Scholar]
  40. 40.  Michaud DS, Liu S, Giovannucci E, Willett WC, Colditz GA, Fuchs CS 2002. Dietary sugar, glycemic load, and pancreatic cancer risk in a prospective study. J. Natl. Cancer Inst. 94:1293–300
    [Google Scholar]
  41. 41.  Mueller NT, Odegaard A, Anderson K, Yuan JM, Gross M et al. 2010. Soft drink and juice consumption and risk of pancreatic cancer: the Singapore Chinese Health Study. Cancer Epidemiol. Biomark. Prev. 19:447–55
    [Google Scholar]
  42. 42.  Navarrete-Muñoz EM, Wark PA, Romaguera D, Bhoo-Pathy N, Michaud D et al. 2016. Sweet-beverage consumption and risk of pancreatic cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). Am. J. Clin. Nutr. 104:760–68
    [Google Scholar]
  43. 43.  Nielsen TG, Olsen A, Christensen J, Overvad K, Tjonneland A 2005. Dietary carbohydrate intake is not associated with the breast cancer incidence rate ratio in postmenopausal Danish women. J. Nutr. 135:124–28
    [Google Scholar]
  44. 44.  Nomura SJ, Dash C, Rosenberg L, Yu J, Palmer JR, Adams-Campbell LL 2016. Adherence to diet, physical activity and body weight recommendations and breast cancer incidence in the Black Women's Health Study. Int. J. Cancer 139:2738–52
    [Google Scholar]
  45. 45.  Nothlings U, Murphy SP, Wilkens LR, Henderson BE, Kolonel LN 2007. Dietary glycemic load, added sugars, and carbohydrates as risk factors for pancreatic cancer: the Multiethnic Cohort Study. Am. J. Clin. Nutr. 86:1495–501
    [Google Scholar]
  46. 46. Off. Dis. Prev. Health Promot. 2015. Dietary Guidelines for Americans 2015–2020 Rockville, MD: Off. Dis. Prev. Health Promot. , 8th ed.. https://Health.gov/dietaryguidelines/2015/guidelines/
    [Google Scholar]
  47. 47.  Pittas AG, Joseph NA, Greenberg AS 2004. Adipocytokines and insulin resistance. J. Clin. Endocrinol. Metab. 89:447–52
    [Google Scholar]
  48. 48.  Pollak M 2008. Insulin and insulin-like growth factor signalling in neoplasia. Nat. Rev. Cancer 8:915–28
    [Google Scholar]
  49. 49.  Popkin BM, Hawkes C 2015. Sweetening of the global diet, particularly beverages: patterns, trends, and policy responses. Lancet Diabetes Endocrinol 4:174–86
    [Google Scholar]
  50. 50.  Popkin BM, Nielsen SJ 2012. The sweetening of the world's diet. Obes. Res. 11:1325–32
    [Google Scholar]
  51. 51.  Poppitt S, Swann D, Black A, Prentice A 1998. Assessment of selective under-reporting of food intake by both obese and non-obese women in a metabolic facility. Int. J. Obes. Rel. Metab. Disord. 22:303–11
    [Google Scholar]
  52. 52.  Roberts DL, Dive C, Renehan AG 2010. Biological mechanisms linking obesity and cancer risk: new perspectives. Annu. Rev. Med. 61:301–16
    [Google Scholar]
  53. 53.  Schernhammer ES, Bertrand KA, Birmann BM, Sampson L, Willett WC, Feskanich D 2012. Consumption of artificial sweetener- and sugar-containing soda and risk of lymphoma and leukemia in men and women. Am. J. Clin. Nutr. 96:1419–28
    [Google Scholar]
  54. 54.  Schernhammer ES, Hu FB, Giovannucci E, Michaud DS, Colditz GA et al. 2005. Sugar-sweetened soft drink consumption and risk of pancreatic cancer in two prospective cohorts. Cancer Epidemiol. Biomark. Prev. 14:2098–105
    [Google Scholar]
  55. 55.  Seyfried TN, Kiebish MA, Marsh J, Shelton LM, Huysentruyt LC, Mukherjee P 2011. Metabolic management of brain cancer. Biochim. Biophys. Acta 1807:577–94
    [Google Scholar]
  56. 56.  Seyfried TN, Shelton LM 2010. Cancer as a metabolic disease. Nutr. Metab. 7:7
    [Google Scholar]
  57. 57.  Shikany JM, Redden DT, Neuhouser ML, Chlebowski RT, Rohan TE et al. 2011. Dietary glycemic load, glycemic index, and carbohydrate and risk of breast cancer in the Women's Health Initiative. Nutr. Cancer 63:899–907
    [Google Scholar]
  58. 58.  Siegel RL, Miller KD, Jemal A 2015. Cancer statistics, 2016. CA Cancer J. Clin. 66:7–30
    [Google Scholar]
  59. 59.  Sigman-Grant M, Morita J 2003. Defining and interpreting intakes of sugars. Am. J. Clin. Nutr. 78:815S–26S
    [Google Scholar]
  60. 60.  Silvera SAN, Jain M, Howe GR, Miller AB, Rohan TE 2005. Dietary carbohydrates and breast cancer risk: a prospective study of the roles of overall glycemic index and glycemic load. Int. J. Cancer 114:653–58
    [Google Scholar]
  61. 61.  Silvera SAN, Jain M, Howe GR, Miller AB, Rohan TE 2007. Glycaemic index, glycaemic load and ovarian cancer risk: a prospective cohort study. Public Health Nutr 10:1076–81
    [Google Scholar]
  62. 62.  Silvera SAN, Rohan TE, Jain M, Terry PD, Howe GR, Miller AB 2005. Glycaemic index, glycaemic load and risk of endometrial cancer: a prospective cohort study. Public Health Nutr 8:912–19
    [Google Scholar]
  63. 63.  Silvera SAN, Rohan TE, Jain M, Terry PD, Howe GR, Miller AB 2005. Glycemic index, glycemic load, and pancreatic cancer risk (Canada). Cancer Causes Control 16:431–36
    [Google Scholar]
  64. 64.  Simon M, Shikany J, Neuhouser M, Rohan T, Nirmal K et al. 2010. Glycemic index, glycemic load, and the risk of pancreatic cancer among postmenopausal women in the Women's Health Initiative observational study and clinical trial. Cancer Causes Control 21:2129–36
    [Google Scholar]
  65. 65.  Stanhope KL 2012. Role of fructose-containing sugars in the epidemics of obesity and metabolic syndrome. Annu. Rev. Med. 63:329–43
    [Google Scholar]
  66. 66.  Stepien M, Duarte-Salles T, Fedirko V, Trichopoulou A, Lagiou P et al. 2016. Consumption of soft drinks and juices and risk of liver and biliary tract cancers in a European cohort. Eur. J. Nutr. 55:7–20
    [Google Scholar]
  67. 67.  Tasevska N 2015. Urinary sugars—a biomarker of total sugars intake. Nutrients 7:5816–33
    [Google Scholar]
  68. 68.  Tasevska N, Jiao L, Cross AJ, Kipnis V, Subar AF et al. 2012. Sugars in diet and risk of cancer in the NIH–AARP Diet and Health Study. Int. J. Cancer 130:159–69
    [Google Scholar]
  69. 69.  Tasevska N, Midthune D, Tinker LF, Potischman N, Lampe JW et al. 2014. Use of a urinary sugars biomarker to assess measurement error in self-reported sugars intake in the Nutrition and Physical Activity Assessment Study (NPAAS). Cancer Epidemiol. Biomark. Prev. 23:2874–83
    [Google Scholar]
  70. 70.  Terry PD, Jain M, Miller AB, Howe GR, Rohan TE 2003. Glycemic load, carbohydrate intake, and risk of colorectal cancer in women: a prospective cohort study. J. Natl. Cancer Inst. 95:914–16
    [Google Scholar]
  71. 71.  Thompson FE, McNeel TS, Dowling EC, Midthune D, Morrissette M, Zeruto CA 2009. Interrelationships of added sugars intake, socioeconomic status, and race/ethnicity in adults in the United States: National Health Interview Survey, 2005. J. Am. Diet. Assoc. 109:1376–83
    [Google Scholar]
  72. 72.  Turner DP 2015. Advanced glycation end-products: a biological consequence of lifestyle contributing to cancer disparity. Cancer Res 75:1925–29
    [Google Scholar]
  73. 73.  Warburg O 1956. On respiratory impairment in cancer cells. Science 124:269–70
    [Google Scholar]
  74. 74. WHO (World Health Organ.). 2015. Guideline: Sugars Intake for Adults and Children Geneva: World Health Organ.
    [Google Scholar]
  75. 75. World Cancer Res. Fund Int., Am. Inst. Cancer Res. 2007. Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective Washington, DC: Am. Inst. Cancer Res.
    [Google Scholar]
  76. 76.  Zamora-Ros R, Béraud V, Franceschi S, Cayssials V, Tsilidis KK et al. 2018. Consumption of fruits, vegetables, and fruit juices and differentiated thyroid carcinoma risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Int. J. Cancer 142:449–59
    [Google Scholar]
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