Urinary Sugars—A Biomarker of Total Sugars Intake
Abstract
:1. Introduction
2. Development of the 24 h Urinary Sucrose and Fructose Biomarker
2.1. Preliminary Work
2.2. Development of the Urinary Sugars Biomarker under Controlled Conditions
2.3. Investigation of Urinary Fructose as a Biomarker against Self-Report in Children
3. Application of the Urinary Sugars Biomarker in Validation and Calibration Studies with Free-Living Individuals
OPEN | NPAAS | |||||||
---|---|---|---|---|---|---|---|---|
Men | Women | Women | ||||||
FFQ | 24HR † | FFQ | 24HR † | FFQ | 24HR ‡ | 4DFR | ||
Total sugars (g/day) | AF | 0.28 | 0.41 | 0.17 | 0.29 | 0.22 | 0.34 | 0.33 |
Obs RR (true RR = 2) | 1.21 | 1.33 | 1.13 | 1.22 | 1.16 | 1.27 | 1.26 | |
Total sugars density (g/1000 kcal) | AF | 0.39 | 0.41 | 0.33 | 0.35 | 0.48 | 0.57 | 0.32 |
Obs RR (true RR = 2) | 1.31 | 1.33 | 1.26 | 1.27 | 1.39 | 1.48 | 1.25 |
4. Application of the Urinary Sugars Biomarker as a Measure of Dietary Exposure in Diet-Disease Association Studies
5. Summary and Future Research
Acknowledgments
Conflicts of Interest
References
- Moynihan, P.J.; Kelly, S.A. Effect on caries of restricting sugars intake: Systematic review to inform WHO guidelines. J. Dent. Res. 2014, 93, 8–18. [Google Scholar] [CrossRef] [PubMed]
- Te Morenga, L.; Mallard, S.; Mann, J. Dietary sugars and body weight: Systematic review and meta-analyses of randomised controlled trials and cohort studies. BMJ 2013, 346, e7492. [Google Scholar] [CrossRef] [PubMed]
- Malik, V.S.; Pan, A.; Willett, W.C.; Hu, F.B. Sugar-sweetened beverages and weight gain in children and adults: A systematic review and meta-analysis. Am. J. Clin. Nutr. 2013, 98, 1084–1102. [Google Scholar] [CrossRef] [PubMed]
- Hu, F.B. Resolved: There is sufficient scientific evidence that decreasing sugar-sweetened beverage consumption will reduce the prevalence of obesity and obesity-related diseases. Obes. Rev. 2013, 14, 606–619. [Google Scholar] [CrossRef] [PubMed]
- Sonestedt, E.; Overby, N.C.; Laaksonen, D.E.; Birgisdottir, B.E. Does high sugar consumption exacerbate cardiometabolic risk factors and increase the risk of type 2 diabetes and cardiovascular disease? Food Nutr. Res. 2012, 56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tasevska, N.; Park, Y.; Jiao, L.; Hollenbeck, A.; Subar, A.F.; Potischman, N. Sugars and risk of mortality in the NIH-AARP Diet and Health Study. Am. J. Clin. Nutr. 2014, 99, 1077–1088. [Google Scholar] [CrossRef] [PubMed]
- Yang, Q.; Zhang, Z.; Gregg, E.W.; Flanders, W.D.; Merritt, R.; Hu, F.B. Added sugar intake and cardiovascular diseases mortality among US adults. JAMA Intern. Med. 2014, 174, 516–524. [Google Scholar] [CrossRef] [PubMed]
- Te Morenga, L.A.; Howatson, A.J.; Jones, R.M.; Mann, J. Dietary sugars and cardiometabolic risk: Systematic review and meta-analyses of randomized controlled trials of the effects on blood pressure and lipids. Am. J. Clin. Nutr. 2014, 100, 65–79. [Google Scholar] [CrossRef] [PubMed]
- Malik, V.S.; Popkin, B.M.; Bray, G.A.; Despres, J.P.; Hu, F.B. Sugar-sweetened beverages, obesity, type 2 diabetes mellitus, and cardiovascular disease risk. Circulation 2010, 121, 1356–1364. [Google Scholar] [CrossRef] [PubMed]
- Malik, V.S.; Hu, F.B. Sweeteners and Risk of Obesity and Type 2 Diabetes: The Role of Sugar-Sweetened Beverages. Curr. Diabetes Rep. 2012, 12, 195–203. [Google Scholar] [CrossRef] [PubMed]
- World Cancer Research Fund; American Institute for Cancer Research. Food, Nutrition and the Prevention of Cancer: A Global Perspective; American Institute for Cancer Research: Washington, DC, USA, 1997. [Google Scholar]
- Tasevska, N.; Jiao, L.; Cross, A.J.; Kipnis, V.; Subar, A.F.; Hollenbeck, A.; Schatzkin, A.; Potischman, N. Sugars in diet and risk of cancer in the NIH-AARP Diet and Health Study. Int. J. Cancer 2012, 130, 159–169. [Google Scholar] [CrossRef] [PubMed]
- World Cancer Research Fund; American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Colorectal Cancer. Available online: http://www.dietandcancerreport.org/cancer_resource_center/downloads/cu/Colorectal-Cancer-2011-Report.pdf (accessed on 1 April 2015).
- World Cancer Research Fund; American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Endometrial Cancer. Available online: http://www.dietandcancerreport.org/cancer_resource_center/downloads/cu/Endometrial-Cancer-2013-Report.pdf (accessed on 1 April 2015).
- World Cancer Research Fund; American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Pancreatic Cancer. Available online: http://www.dietandcancerreport.org/cancer_resource_center/downloads/cu/Pancreatic-Cancer-2012-Report.pdf (accessed on 1 April 2015).
- Welsh, J.A.; Sharma, A.J.; Grellinger, L.; Vos, M.B. Consumption of added sugars is decreasing in the United States. Am. J. Clin. Nutr. 2011, 94, 726–734. [Google Scholar] [CrossRef] [PubMed]
- McGuire, S.; Ervin, R.B.; Kit, B.K.; Carroll, M.D.; Ogden, C.L. Consumption of Added Sugar among U.S. Children and Adolescents, 2005–2008; NCHS Data Brief No. 87; National Center for Health Statistics: Hyattsville, MD, USA, 2012. [Google Scholar]
- Johnson, R.K.; Appel, L.J.; Brands, M.; Howard, B.V.; Lefevre, M.; Lustig, R.H.; Sacks, F.; Steffen, L.M.; Wylie-Rosett, J. Dietary sugars intake and cardiovascular health: A scientific statement from the American Heart Association. Circulation 2009, 120, 1011–1020. [Google Scholar] [CrossRef] [PubMed]
- Institute of Medicine; Food and Nutrition Board. Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Fatty Acids, Cholsterol, Protein, and Amino Acids; The National Academies Press: Washington, DC, USA, 2005. [Google Scholar]
- U.S. Department of Agriculture; U.S. Department of Health and Human Services. Dietary Guidelines for Americans, 2010, 7th ed.U.S. Government Printing Office: Washington, DC, USA, 2010.
- Popkin, B.M.; Nielsen, S.J. The sweetening of the world’s diet. Obes. Res. 2003, 11, 1325–1332. [Google Scholar] [CrossRef] [PubMed]
- Price, G.M.; Paul, A.A.; Cole, T.J.; Wadsworth, M.E. Characteristics of the low-energy reporters in a longitudinal national dietary survey. Br. J. Nutr. 1997, 77, 833–851. [Google Scholar] [CrossRef] [PubMed]
- Krebs-Smith, S.M.; Graubard, B.I.; Kahle, L.L.; Subar, A.F.; Cleveland, L.E.; Ballard-Barbash, R. Low energy reporters vs others: A comparison of reported food intakes. Eur. J. Clin. Nutr. 2000, 54, 281–287. [Google Scholar] [CrossRef] [PubMed]
- Jenab, M.; Slimani, N.; Bictash, M.; Ferrari, P.; Bingham, S.A. Biomarkers in nutritional epidemiology: Applications, needs and new horizons. Hum. Genet. 2009, 125, 507–525. [Google Scholar] [CrossRef] [PubMed]
- Schatzkin, A.; Kipnis, V.; Carroll, R.J.; Midthune, D.; Subar, A.F.; Bingham, S.; Schoeller, D.A.; Troiano, R.P.; Freedman, L.S. A comparison of a food frequency questionnaire with a 24 hour recall for use in an epidemiological cohort study: Results from the biomarker-based Observing Protein and Energy Nutrition (OPEN) study. Int. J. Epidemiol. 2003, 32, 1054–1062. [Google Scholar] [CrossRef] [PubMed]
- Bingham, S.A.; Gill, C.; Welch, A.; Cassidy, A.; Runswick, S.A.; Oakes, S.; Lubin, R.; Thurnham, D.I.; Key, T.J.; Roe, L.; et al. Validation of dietary assessment methods in the UK arm of EPIC using weighed records, and 24-hour urinary nitrogen and potassium and serum vitamin C and carotenoids as biomarkers. Int. J. Epidemiol. 1997, 26 (Suppl. 1), S137–S151. [Google Scholar] [CrossRef] [PubMed]
- Prentice, R.L.; Mossavar-Rahmani, Y.; Huang, Y.; van Horn, L.; Beresford, S.A.; Caan, B.; Tinker, L.; Schoeller, D.; Bingham, S.; Eaton, C.B.; et al. Evaluation and comparison of food records, recalls, and frequencies for energy and protein assessment by using recovery biomarkers. Am. J. Epidemiol. 2011, 174, 591–603. [Google Scholar] [CrossRef] [PubMed]
- Neuhouser, M.L.; Tinker, L.; Shaw, P.A.; Schoeller, D.; Bingham, S.A.; Horn, L.V.; Beresford, S.A.; Caan, B.; Thomson, C.; Satterfield, S.; et al. Use of recovery biomarkers to calibrate nutrient consumption self-reports in the Women’s Health Initiative. Am. J. Epidemiol. 2008, 167, 1247–1259. [Google Scholar] [CrossRef] [PubMed]
- Huang, Y.; van Horn, L.; Tinker, L.F.; Neuhouser, M.L.; Carbone, L.; Mossavar-Rahmani, Y.; Thomas, F.; Prentice, R.L. Measurement error corrected sodium and potassium intake estimation using 24-hour urinary excretion. Hypertension 2014, 63, 238–244. [Google Scholar] [CrossRef] [PubMed]
- Kyrø, C.; Olsen, A.; Landberg, R.; Skeie, G.; Loft, S.; Åman, P.; Leenders, M.; Dik, V.K.; Siersema, P.D.; Pischon, T.; et al. Plasma alkylresorcinols, biomarkers of whole-grain wheat and rye intake, and incidence of colorectal cancer. J. Natl. Cancer Inst. 2014, 106, djt352. [Google Scholar] [CrossRef] [PubMed]
- Cottet, V.; Collin, M.; Gross, A.S.; Boutron-Ruault, M.C.; Morois, S.; Clavel-Chapelon, F.; Chajès, V. Erythrocyte membrane phospholipid fatty acid concentrations and risk of colorectal adenomas: A case-control nested in the French E3N-EPIC cohort study. Cancer Epidemiol. Biomark. Prev. 2013, 22, 1417–1427. [Google Scholar] [CrossRef] [PubMed]
- Bingham, S.; Luben, R.; Welch, A.; Tasevska, N.; Wareham, N.; Khaw, K.T. Epidemiologic assessment of sugars consumption using biomarkers: Comparisons of obese and nonobese individuals in the European Prospective Investigation of Cancer Norfolk. Cancer Epidemiol. Biomark. Prev. 2007, 16, 1651–1654. [Google Scholar] [CrossRef] [PubMed]
- Kuhnle, G.G.; Tasevska, N.; Lentjes, M.A.; Griffin, J.L.; Sims, M.A.; Richardson, L.; Aspinall, S.M.; Mulligan, A.A.; Luben, R.N.; Khaw, K.T. Association between sucrose intake and risk of overweight and obesity in a prospective sub-cohort of the European Prospective Investigation into Cancer in Norfolk (EPIC-Norfolk). Public Health Nutr. 2015, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Knudsen, M.D.; Kyrø, C.; Olsen, A.; Dragsted, L.O.; Skeie, G.; Lund, E.; Aman, P.; Nilsson, L.M.; Bueno-de-Mesquita, H.B.; Tjønneland, A.; et al. Self-reported whole-grain intake and plasma alkylresorcinol concentrations in combination in relation to the incidence of colorectal cancer. Am. J. Epidemiol. 2014, 179, 1188–1196. [Google Scholar] [CrossRef] [PubMed]
- Freedman, L.S.; Tasevska, N.; Kipnis, V.; Schatzkin, A.; Mares, J.; Tinker, L.; Potischman, N. Gains in statistical power from using a dietary biomarker in combination with self-reported intake to strengthen the analysis of a diet-disease association: An example from CAREDS. Am. J. Epidemiol. 2010, 172, 836–842. [Google Scholar] [CrossRef] [PubMed]
- Marklund, M.; Magnusdottir, O.K.; Rosqvist, F.; Cloetens, L.; Landberg, R.; Kolehmainen, M.; Brader, L.; Hermansen, K.; Poutanen, K.S.; Herzig, K.H.; et al. A dietary biomarker approach captures compliance and cardiometabolic effects of a healthy Nordic diet in individuals with metabolic syndrome. J. Nutr. 2014, 144, 1642–1649. [Google Scholar] [CrossRef] [PubMed]
- Menzies, I.S. Absorption of intact oligosaccharide in health and disease. Biochem. Soc. Trans. 1974, 2, 1042–1047. [Google Scholar]
- Nakamura, H.; Tamura, Z. Gas chromatographic analysis of mono- and disaccharides in human blood and urine after oral administration of disaccharides. Clin. Chim. Acta 1972, 39, 367–381. [Google Scholar] [CrossRef]
- Deane, N.; Smith, H.W. Fate of inulin and sucrose in normal subjects as determined by a urine reinfusion technique. J. Clin. Investig. 1955, 34, 681–684. [Google Scholar] [CrossRef] [PubMed]
- Sun, S.Z.; Empie, M.W. Fructose metabolism in humans—What isotopic tracer studies tell us. Nutr. Metab. Lond. 2012, 9, 89. [Google Scholar] [CrossRef] [PubMed]
- Douard, V.; Ferraris, R.P. Regulation of the fructose transporter GLUT5 in health and disease. Am. J. Physiol. Endocrinol. Metab. 2008, 295, E227–E237. [Google Scholar] [CrossRef] [PubMed]
- Mayes, P.A. Intermediary metabolism of fructose. Am. J. Clin. Nutr. 1993, 58 (Suppl. 5), 754S–765S. [Google Scholar] [PubMed]
- Björkman, O.; Felig, P. Role of the kidney in the metabolism of fructose in 60-hour fasted humans. Diabetes 1982, 31, 516–520. [Google Scholar] [CrossRef] [PubMed]
- Luceri, C.; Caderni, G.; Lodovici, M.; Spagnesi, M.T.; Monserrat, C.; Lancioni, L.; Dolara, P. Urinary excretion of sucrose and fructose as a predictor of sucrose intake in dietary intervention studies. Cancer Epidemiol. Biomark. Prev. 1996, 5, 167–171. [Google Scholar]
- Tasevska, N.; Runswick, S.A.; McTaggart, A.; Bingham, S.A. Urinary sucrose and fructose as biomarkers for sugar consumption. Cancer Epidemiol. Biomark. Prev. 2005, 14, 1287–1294. [Google Scholar] [CrossRef] [PubMed]
- Bingham, S.A.; Cummings, J.H. Creatinine and PABA as markers for completeness of collection of 24-hour urine samples. Hum. Nutr. Clin. Nutr. 1986, 40, 473–476. [Google Scholar] [PubMed]
- Gregory, J.; Foster, K.; Tyler, H.; Wiseman, M. The Dietary and Nutritional Survey of British Adults—A Survey Carried Out by the Social Survey Division of OPCS with Dietary and Nutritional Evaluations by the Ministry of Agriculture, Fisheries and Food and the Department of Health; HMSO: London, UK, 1990; p. 75. [Google Scholar]
- Tasevska, N. Biomarkers for Validation of Dietary Exposure Assessments in Nutritional Epidemiology (Doctoral disseration); University of Cambridge: Cambridge, UK, 2005. [Google Scholar]
- Tasevska, N.; Runswick, S.A.; Welch, A.A.; McTaggart, A.; Bingham, S.A. Urinary sugars biomarker relates better to extrinsic than to intrinsic sugars intake in a metabolic study with volunteers consuming their normal diet. Eur. J. Clin. Nutr. 2008, 63, 653–659. [Google Scholar] [CrossRef] [PubMed]
- Joosen, A.M.; Kuhnle, G.G.; Runswick, S.A.; Bingham, S.A. Urinary sucrose and fructose as biomarkers of sugar consumption: Comparison of normal weight and obese volunteers. Int. J. Obes. Lond. 2008, 32, 1736–1740. [Google Scholar] [CrossRef] [PubMed]
- Kaaks, R.; Riboli, E.; Sinha, R. Biochemical markers of dietary intake. IARC Sci. Publ. 1997, 142, 103–126. [Google Scholar] [PubMed]
- Tasevska, N.; Midthune, D.; Potischman, N.; Subar, A.F.; Cross, A.J.; Bingham, S.A.; Schatzkin, A.; Kipnis, V. Use of the predictive sugars biomarker to evaluate self-reported total sugars intake in the Observing Protein and Energy Nutrition (OPEN) study. Cancer Epidemiol. Biomark. Prev. 2011, 20, 490–500. [Google Scholar] [CrossRef] [PubMed]
- Johner, S.A.; Libuda, L.; Shi, L.; Retzlaff, A.; Joslowski, G.; Remer, T. Urinary fructose: A potential biomarker for dietary fructose intake in children. Eur. J. Clin. Nutr. 2010, 64, 1365–1370. [Google Scholar] [CrossRef] [PubMed]
- Day, N.; McKeown, N.; Wong, M.; Welch, A.; Bingham, S. Epidemiological assessment of diet: A comparison of a 7-day diary with a food frequency questionnaire using urinary markers of nitrogen, potassium and sodium. Int. J. Epidemiol. 2001, 30, 309–317. [Google Scholar] [CrossRef] [PubMed]
- Prentice, R.L.; Tinker, L.F.; Huang, Y.; Neuhouser, M.L. Calibration of self-reported dietary measures using biomarkers: An approach to enhancing nutritional epidemiology reliability. Curr. Atheroscler. Rep. 2013, 15, 353. [Google Scholar] [CrossRef] [PubMed]
- Prentice, R.L.; Shaw, P.A.; Bingham, S.A.; Beresford, S.A.; Caan, B.; Neuhouser, M.L.; Patterson, R.E.; Stefanick, M.L.; Satterfield, S.; Thomson, C.A.; et al. Biomarker-calibrated energy and protein consumption and increased cancer risk among postmenopausal women. Am. J. Epidemiol. 2009, 169, 977–989. [Google Scholar] [CrossRef] [PubMed]
- Prentice, R.L.; Huang, Y.; Kuller, L.H.; Tinker, L.F.; Horn, L.V.; Stefanick, M.L.; Sarto, G.; Ockene, J.; Johnson, K.C. Biomarker-calibrated energy and protein consumption and cardiovascular disease risk among postmenopausal women. Epidemiology 2011, 22, 170–179. [Google Scholar] [CrossRef] [PubMed]
- Prentice, R.L.; Pettinger, M.; Tinker, L.F.; Huang, Y.; Thomson, C.A.; Johnson, K.C.; Beasley, J.; Anderson, G.; Shikany, J.M.; Chlebowski, R.T.; et al. Regression calibration in nutritional epidemiology: Example of fat density and total energy in relationship to postmenopausal breast cancer. Am. J. Epidemiol. 2013, 178, 1663–1672. [Google Scholar] [CrossRef] [PubMed]
- Beasley, J.M.; Lacroix, A.Z.; Larson, J.C.; Huang, Y.; Neuhouser, M.L.; Tinker, L.F.; Jackson, R.; Snetselaar, L.; Johnson, K.C.; Eaton, C.B.; et al. Biomarker-calibrated protein intake and bone health in the Women’s Health Initiative clinical trials and observational study. Am. J. Clin. Nutr. 2014, 99, 934–940. [Google Scholar] [CrossRef] [PubMed]
- Tinker, L.F.; Sarto, G.E.; Howard, B.V.; Huang, Y.; Neuhouser, M.L.; Mossavar-Rahmani, Y.; Beasley, J.M.; Margolis, K.L.; Eaton, C.B.; Phillips, L.S.; et al. Biomarker-calibrated dietary energy and protein intake associations with diabetes risk among postmenopausal women from the Women’s Health Initiative. Am. J. Clin. Nutr. 2011, 94, 1600–1606. [Google Scholar] [CrossRef] [PubMed]
- Tasevska, N.; Midthune, D.; Tinker, L.F.; Potischman, N.; Lampe, J.W.; Neuhouser, M.L.; Beasley, J.M.; van Horn, L.; Prentice, R.; Kipnis, V. 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. 2014, 23, 2874–2883. [Google Scholar] [CrossRef] [PubMed]
- Subar, A.F.; Kipnis, V.; Troiano, R.P.; Midthune, D.; Schoeller, D.A.; Bingham, S.; Sharbaugh, C.O.; Trabulsi, J.; Runswick, S.; Ballard-Barbash, R.; et al. Using intake biomarkers to evaluate the extent of dietary misreporting in a large sample of adults: The OPEN study. Am. J. Epidemiol. 2003, 158, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Kipnis, V.; Subar, A.F.; Midthune, D.; Freedman, L.S.; Ballard-Barbash, R.; Troiano, R.P.; Bingham, S.; Schoeller, D.A.; Schatzkin, A.; Carroll, R.J. Structure of dietary measurement error: Results of the OPEN biomarker study. Am. J. Epidemio. 2003, 158, 14–21. [Google Scholar] [CrossRef]
- Beasley, J.M.; LaCroix, A.Z.; Neuhouser, M.L.; Huang, Y.; Tinker, L.; Woods, N.; Michael, Y.; Curb, J.D.; Prentice, R.L. Protein intake and incident frailty in the Women’s Health Initiative observational study. J. Am. Geriatr. Soc. 2010, 58, 1063–1071. [Google Scholar] [CrossRef] [PubMed]
- Sutherland, L.R.; Verhoef, M.; Wallace, J.L.; van Rosendaal, G.; Crutcher, R.; Meddings, J.B. A simple, non-invasive marker of gastric damage: Sucrose permeability. Lancet 1994, 343, 998–1000. [Google Scholar] [CrossRef]
- Van Wijck, K.; Verlinden, T.J.; van Eijk, H.M.; Dekker, J.; Buurman, W.A.; Dejong, C.H.; Lenaerts, K. Novel multi-sugar assay for site-specific gastrointestinal permeability analysis: A randomized controlled crossover trial. Clin. Nutr. 2013, 32, 245–251. [Google Scholar] [CrossRef] [PubMed]
- Cobden, I.; Rothwell, J.; Axon, A.T. Intestinal permeability and screening tests for coeliac disease. Gut 1980, 21, 512–518. [Google Scholar] [CrossRef] [PubMed]
- Dastych, M.; Novotná, H.; Cíhalová, J. Lactulose/mannitol test and specificity, sensitivity, and area under curve of intestinal permeability parameters in patients with liver cirrhosis and Crohn’s disease. Dig. Dis. Sci. 2008, 53, 2789–2792. [Google Scholar] [CrossRef] [PubMed]
- Sander, P.; Alfalah, M.; Keiser, M.; Korponay-Szabo, I.; Kovács, J.B.; Leeb, T.; Naim, H.Y. Novel mutations in the human sucrase-isomaltase gene (SI) that cause congenital carbohydrate malabsorption. Hum. Mutat. 2006, 27. [Google Scholar] [CrossRef] [PubMed]
- Nichols, B.L.; Adams, B.; Roach, C.M.; Ma, C.X.; Baker, S.S. Frequency of sucrase deficiency in mucosal biopsies. J. Pediatr. Gastroenterol. Nutr. 2012, 55 (Suppl. 2), S28–S30. [Google Scholar] [CrossRef] [PubMed]
- Kerckhoffs, A.P.; Akkermans, L.M.; de Smet, M.B.; Besselink, M.G.; Hietbrink, F.; Bartelink, I.H.; Busschers, W.B.; Samsom, M.; Renooij, W. Intestinal permeability in irritable bowel syndrome patients: Effects of NSAIDs. Dig. Dis. Sci. 2010, 55, 716–723. [Google Scholar] [CrossRef] [PubMed]
- Mullin, J.M.; Valenzano, M.C.; Whitby, M.; Lurie, D.; Schmidt, J.D.; Jain, V.; Tully, O.; Kearney, K.; Lazowick, D.; Mercogliano, G.; et al. Esomeprazole induces upper gastrointestinal tract transmucosal permeability increase. Aliment. Pharmacol. Ther. 2008, 28, 1317–1325. [Google Scholar] [CrossRef] [PubMed]
- Gotteland, M.; Cruchet, S.; Frau, V.; Wegner, M.E.; Lopez, R.; Herrera, T.; Sanchez, A.; Urrutia, C.; Brunser, O. Effect of acute cigarette smoking, alone or with alcohol, on gastric barrier function in healthy volunteers. Dig. Liver Dis. 2002, 34, 702–706. [Google Scholar] [CrossRef]
- Suenaert, P.; Bulteel, V.; den Hond, E.; Hiele, M.; Peeters, M.; Monsuur, F.; Ghoos, Y.; Rutgeerts, P. The effects of smoking and indomethacin on small intestinal permeability. Aliment. Pharmacol. Ther. 2000, 14, 819–822. [Google Scholar] [CrossRef] [PubMed]
- Jones, H.F.; Butler, R.N.; Brooks, D.A. Intestinal fructose transport and malabsorption in humans. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300, G202–G206. [Google Scholar] [CrossRef] [PubMed]
- Haley, S.; Reed, J.; Lin, B.-H.; Cook, A. Sweetener Consumption in the United States: Distribution by Demographic and Product Characteristics; Electronic Outlook Report from the Economic Research Service, SSS-243–01; U.S. Department of Agriculture, Economic Research Service: Washington, DC, USA, 2005.
- Ng, S.W.; Slining, M.M.; Popkin, B.M. Use of caloric and noncaloric sweeteners in US consumer packaged foods, 2005–2009. J. Acad. Nutr. Diet. 2012, 112, 1828–1834. [Google Scholar] [CrossRef] [PubMed]
- Subar, A.F.; Midthune, D.; Tasevska, N.; Kipnis, V.; Freedman, L.S. Checking for completeness of 24-h urine collection using para-amino benzoic acid not necessary in the Observing Protein and Energy Nutrition study. Eur. J. Clin. Nutr. 2013, 67, 863–867. [Google Scholar] [CrossRef] [PubMed]
- Kuhnle, G.G.; Joosen, A.M.; Wood, T.R.; Runswick, S.A.; Griffin, J.L.; Bingham, S.A. Detection and quantification of sucrose as dietary biomarker using gas chromatography and liquid chromatography with mass spectrometry. Rapid Commun. Mass Spectrom. 2008, 22, 279–282. [Google Scholar] [CrossRef] [PubMed]
- Song, X.; Navarro, S.L.; Diep, P.; Thomas, W.K.; Razmpoosh, E.C.; Schwarz, Y.; Wang, C.Y.; Kratz, M.; Neuhouser, M.L.; Lampe, J.W. Comparison and validation of 2 analytical methods for measurement of urinary sucrose and fructose excretion. Nutr. Res. 2013, 33, 696–703. [Google Scholar] [CrossRef] [PubMed]
- Yeung, E.H.; Saudek, C.D.; Jahren, A.H.; Kao, W.H.; Islas, M.; Kraft, R.; Coresh, J.; Anderson, C.A. Evaluation of a novel isotope biomarker for dietary consumption of sweets. Am. J. Epidemiol. 2010, 172, 1045–1052. [Google Scholar] [CrossRef] [PubMed]
- Cook, C.M.; Alvig, A.L.; Liu, Y.Q.; Schoeller, D.A. The natural 13C abundance of plasma glucose is a useful biomarker of recent dietary caloric sweetener intake. J. Nutr. 2010, 140, 333–337. [Google Scholar] [CrossRef] [PubMed]
- Nash, S.H.; Kristal, A.R.; Bersamin, A.; Hopkins, S.E.; Boyer, B.B.; O’Brien, D.M. Carbon and nitrogen stable isotope ratios predict intake of sweeteners in a Yup’ik study population. J. Nutr. 2013, 143, 161–165. [Google Scholar] [CrossRef] [PubMed]
- Choy, K.; Nash, S.H.; Kristal, A.R.; Hopkins, S.; Boyer, B.B.; O’Brien, D.M. The carbon isotope ratio of alanine in red blood cells is a new candidate biomarker of sugar-sweetened beverage intake. J. Nutr. 2013, 143, 878–884. [Google Scholar] [CrossRef] [PubMed]
- Gibbons, H.; McNulty, B.A.; Nugent, A.P.; Walton, J.; Flynn, A.; Gibney, M.J.; Brennan, L. A metabolomics approach to the identification of biomarkers of sugar-sweetened beverage intake. Am. J. Clin. Nutr. 2015, 101, 471–477. [Google Scholar] [CrossRef] [PubMed]
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Tasevska, N. Urinary Sugars—A Biomarker of Total Sugars Intake. Nutrients 2015, 7, 5816-5833. https://doi.org/10.3390/nu7075255
Tasevska N. Urinary Sugars—A Biomarker of Total Sugars Intake. Nutrients. 2015; 7(7):5816-5833. https://doi.org/10.3390/nu7075255
Chicago/Turabian StyleTasevska, Natasha. 2015. "Urinary Sugars—A Biomarker of Total Sugars Intake" Nutrients 7, no. 7: 5816-5833. https://doi.org/10.3390/nu7075255