Influence of smoking and diet on glycated haemoglobin and 'pre-diabetes’ categorisation: a cross-sectional analysis

BMC Public Health

Emilie Combet¹  Michael EJ Lean²  Antonis Vlassopoulos¹ 

[1] Human Nutrition, Yorkhill Hospital, School of Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, England;Human Nutrition, School of Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Walton Building level 4, Glasgow Royal Infirmary, G3 8SJ, Glasgow, UK, England

关键词: Vegetables;    Pre-diabetes;    Oxidative stress;    HbA1c;    Smoking;   

Others  :  1161610
DOI  :  10.1186/1471-2458-13-1013

 received in 2013-04-29, accepted in 2013-10-15,  发布年份 2013

【 摘 要 】

Background

The new HbA1c criteria for diagnosis of pre-diabetes have been criticised for misdiagnosis. It is possible that some elevation of HbA1c is not driven by hyperglycaemia. This study assesses associations of HbA1c, commonly assumed to relate solely to glucose concentration, with (i) smoking, a major source of reactive oxygen species (ROS) and (ii) fruit & vegetables consumption associated with improved redox status.

Methods

One-way ANOVA, Chi-squared and multivariate linear regressions, adjusted for all known confounders were used to explore associations of HbA1c with self-reported smoking status and fruit & vegetables consumptions in the Scottish Health Surveys 2003–2010, among individuals without known diabetes and HbA1c < 6.5%.

Results

Compared to non-smokers (n = 2831), smokers (n = 1457) were younger, consumed less fruit & vegetables, had lower physical activity levels, lower BMI, higher HbA1c and CRP (p < 0.05). HbA1c was higher in smokers by 0.25 SDs (0.08%), and 0.38 SDs higher (0.14%) in heavy smokers (>20 cigarettes/day) than non-smokers (p < 0.001 both). Smokers were twice as likely to have HbA1c in the 'pre-diabetic’ range (5.7-6.4%) (p < 0.001, adj.model). Pre-diabetes and low grade inflammation did not affect the associations. For every extra 80 g vegetable portion consumed, HbA1c was 0.03 SDs (0.01%) lower (p = 0.02), but fruit consumption did not impact on HbA1c, within the low range of consumptions in this population.

Conclusion

This study adds evidence to relate smoking (an oxidative stress proxy) with protein glycation in normoglycaemic subjects, with implications for individuals exposed to ROS and for epidemiological interpretation of HbA1c.

【 授权许可】

   
2013 Vlassopoulos et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Han TS, Sattar N, Lean M: ABC of obesity. Assessment of obesity and its clinical implications. BMJ 2006, 333(7570):695-698.
• [2]Hermsdorff HH, Puchau B, Volp AC, Barbosa KB, Bressan J, Zulet MA, Martinez JA: Dietary total antioxidant capacity is inversely related to central adiposity as well as to metabolic and oxidative stress markers in healthy young adults. Nutr Metab 2011, 8:59. BioMed Central Full Text
• [3]Alberg A: The influence of cigarette smoking on circulating concentrations of antioxidant micronutrients. Toxicology 2002, 180(2):121-137.
• [4]Moriarty SE, Shah JH, Lynn M, Jiang S, Openo K, Jones DP, Sternberg P: Oxidation of glutathione and cysteine in human plasma associated with smoking. Free Radic Biol Med 2003, 35(12):1582-1588.
• [5]Lesgards JF, Durand P, Lassarre M, Stocker P, Lesgards G, Lanteaume A, Prost M, Lehucher-Michel MP: Assessment of lifestyle effects on the overall antioxidant capacity of healthy subjects. Environ Health Perspect 2002, 110(5):479-486.
• [6]Willi C, Bodenmann P, Ghali WA, Faris PD, Cornuz J: Active smoking and the risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 2007, 298(22):2654-2664.
• [7]Fagard RH, Nilsson PM: Smoking and diabetes–the double health hazard! Prim Care Diabetes 2009, 3(4):205-209.
• [8]Naudi A, Jove M, Ayala V, Cassanye A, Serrano J, Gonzalo H, Boada J, Prat J, Portero-Otin M, Pamplona R: Cellular dysfunction in diabetes as maladaptive response to mitochondrial oxidative stress. Exp Diabetes Res 2012, 2012:696215.
• [9]Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, Lee A, AlAbed Y, Vlassara H, Bucala R, et al.: Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci USA 1997, 94(25):13915-13920.
• [10]Esposito K, Di Palo C, Maiorino MI, Petrizzo M, Bellastella G, Siniscalchi I, Giugliano D: Long-term effect of mediterranean-style diet and calorie restriction on biomarkers of longevity and oxidative stress in overweight men. Cardiol Res Pract 2011, 2011:293916.
• [11]Dai J, Jones DP, Goldberg J, Ziegler TR, Bostick RM, Wilson PW, Manatunga AK, Shallenberger L, Jones L, Vaccarino V: Association between adherence to the Mediterranean diet and oxidative stress. Am J Clin Nutr 2008, 88(5):1364-1370.
• [12]Peluso M, Munnia A, Piro S, Jedpiyawongse A, Sangrajrang S, Giese RW, Ceppi M, Boffetta P, Srivatanakul P: Fruit and vegetable and fried food consumption and 3-(2-deoxy-beta-D-erythro-pentafuranosyl)pyrimido[1,2-alpha] purin-10(3H)-one deoxyguanosine adduct formation. Free Radic Res 2012, 46(1):85-92.
• [13]Shaklai N, Garlick RL, Bunn HF: Nonenzymatic glycosylation of human serum albumin alters its conformation and function. J Biol Chem 1984, 259(6):3812-3817.
• [14]Selvin E, Steffes MW, Ballantyne CM, Hoogeveen RC, Coresh J, Brancati FL: Racial differences in glycemic markers: a cross-sectional analysis of community-based data. Ann Intern Med 2011, 154(5):303-309.
• [15]Yan SF, Ramasamy R, Schmidt AM: The RAGE axis: a fundamental mechanism signaling danger to the vulnerable vasculature. Circ Res 2010, 106(5):842-853.
• [16]Goldstein DE, Little RR, Lorenz RA, Malone JI, Nathan D, Peterson CM, Sacks DB: Tests of glycemia in diabetes. Diabetes Care 2004, 27(7):1761-1773.
• [17]Nathan DM, Kuenen J, Borg R, Zheng H, Schoenfeld D, Heine RJ, Grp AS: Translating the A1C assay into estimated average glucose values. Diabetes Care 2008, 31(8):1473-1478.
• [18]Delpierre G, Collard F, Fortpied J, Van Schaftingen E: Fructosamine 3-kinase is involved in an intracellular deglycation pathway in human erythrocytes. Biochem J 2002, 365:801-808.
• [19]Fu MX, Wells-Knecht KJ, Blackledge JA, Lyons TJ, Thorpe SR, Baynes JW: Glycation, glycoxidation, and cross-linking of collagen by glucose. Kinetics, mechanisms, and inhibition of late stages of the Maillard reaction. Diabetes 1994, 43(5):676-683.
• [20]Baynes JW: Role of oxidative stress in development of complications in diabetes. Diabetes 1991, 40(4):405-412.
• [21]Chetyrkin S, Mathis M, Pedchenko V, Sanchez OA, McDonald WH, Hachey DL, Madu H, Stec D, Hudson B, Voziyan P: Glucose Autoxidation Induces Functional Damage to Proteins via Modification of Critical Arginine Residues. Biochemistry-Us 2011, 50(27):6102-6112.
• [22]ADA: Diagnosis and classification of diabetes mellitus. Diabetes Care 2011, 34(1):S62-S69.
• [23]Brewer N, Wright CS, Travier N, Cunningham CW, Hornell J, Pearce N, Jeffreys M: A New Zealand linkage study examining the associations between A1C concentration and mortality. Diabetes Care 2008, 31(6):1144-1149.
• [24]Bates CJ, Lean ME, Mansoor MA, Prentice A: Nutrient intakes; biochemical and risk indices associated with Type 2 diabetes and glycosylated haemoglobin, in the British National Diet and Nutrition Survey of people aged 65 years and over. Diabet Med 2004, 21(7):677-684.
• [25]Vlassopoulos A, Lean ME, Combet E: Role of oxidative stress in physiological albumin glycation: A neglected interaction. Free Radic Biol Med 2013, 60C:318-324.
• [26]Scottish Government: Better Coronary Heart Disease and Stroke Care: A Consultation Document. Edinburgh: The Scottish Executive; 2008.
• [27]Lynch JW, Kaplan GA, Cohen RD, Tuomilehto J, Salonen JT: Do cardiovascular risk factors explain the relation between socioeconomic status, risk of all-cause mortality, cardiovascular mortality, and acute myocardial infarction? Am J Epidemiol 1996, 144(10):934-942.
• [28]Bromley CBP, Given L: The Scottish Health Survey 2008. Edinburgh: The Scottish Government; 2009.
• [29]Bromley CSK, Shelton N: The Scottish Health Survey 2003. Edinburgh: The Scottish Executive; 2005.
• [30]Lean MEJ, Han TS, Morrison CE: Waist Circumference as a Measure for Indicating Need for Weight Management. Brit Med J 1995, 311(6998):158-161.
• [31]Lean ME, Anderson AS, Morrison C, Currall J: Evaluation of a dietary targets monitor. Eur J Clin Nutr 2003, 57(5):667-673.
• [32]Wildman RP, Muntner P, Reynolds K, McGinn AP, Rajpathak S, Wylie-Rosett J, Sowers MR: The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999–2004). Arch Intern Med 2008, 168(15):1617-1624.
• [33]Grundy SM, Cleeman JI, Merz CN, Brewer HB Jr, Clark LT, Hunninghake DB, Pasternak RC, Smith SC Jr, Stone NJ: Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation 2004, 110(2):227-239.
• [34]Lumley T, Diehr P, Emerson S, Chen L: The importance of the normality assumption in large public health data sets. Annu Rev Public Health 2002, 23:151-169.
• [35]Alter DA, Wijeysundera HC, Franklin B, Austin PC, Chong A, Oh PI, Tu JV, Stukel TA: Obesity, lifestyle risk-factors, and health service outcomes among healthy middle-aged adults in Canada. BMC Health Serv Res 2012, 12(1):238. BioMed Central Full Text
• [36]Clair C, Bitton A, Meigs JB, Rigotti NA: Relationships of Cotinine and Self-Reported Cigarette Smoking With Hemoglobin A(1c) in the US. Diabetes Care 2011, 34(10):2250-2255.
• [37]Nilsson PM, Lind L, Pollare T, Berne C, Lithell HO: Increased level of hemoglobin A1c, but not impaired insulin sensitivity, found in hypertensive and normotensive smokers. Metabolism 1995, 44(5):557-561.
• [38]Simon D, Senan C, Garnier P, Saint-Paul M, Papoz L: Epidemiological features of glycated haemoglobin A1c-distribution in a healthy population. The Telecom Study. Diabetologia 1989, 32(12):864-869.
• [39]Boeing H, Weisgerber UM, Jeckel A, Rose HJ, Kroke A: Association between glycated hemoglobin and diet and other lifestyle factors in a nondiabetic population: cross-sectional evaluation of data from the Potsdam cohort of the European Prospective Investigation into Cancer and Nutrition Study. Am J Clin Nutr 2000, 71(5):1115-1122.
• [40]Den Engelsen C, van den Donk M, Gorter KJ, Salome PL, Rutten GE: Advanced glycation end products measured by skin autofluorescence in a population with central obesity. Dermatoendocrinol 2012, 4(1):33-38.
• [41]Monnier L, Lapinski H, Colette C: Contributions of fasting and postprandial plasma glucose increments to the overall diurnal hyperglycemia of type 2 diabetic patients - Variations with increasing levels of HbA(1c). Diabetes Care 2003, 26(3):881-885.
• [42]Bastyr EJ, Stuart CA, Brodows RG, Schwartz S, Graf CJ, Zagar A, Robertson KE, Grp IS: Therapy focused on lowering postprandial glucose, not fasting glucose, may be superior for lowering HbA(1c). Diabetes Care 2000, 23(9):1236-1241.
• [43]Davie SJ, Gould BJ, Yudkin JS: Effect of vitamin C on glycosylation of proteins. Diabetes 1992, 41(2):167-173.
• [44]Krone CA, Ely JT: Ascorbic acid, glycation, glycohemoglobin and aging. Med Hypotheses 2004, 62(2):275-279.
• [45]Selvaraj N, Bobby Z, Koner BC, Das AK: Reassessing the increased glycation of hemoglobin in nondiabetic chronic renal failure patients: A hypothesis on the role of lipid peroxides. Clin Chim Acta 2005, 360(1–2):108-113.
• [46]Nambiar S, Viswanathan S, Zachariah B, Hanumanthappa N, Agrawal A, Nadaradjan RD: Possible modulation of glycated protein levels in prehypertension by lipid peroxides. Clin Exp Hypertens 2012, 34(7):517-522.
• [47]Rondeau P, Bourdon E: The glycation of albumin: structural and functional impacts. Biochimie 2011, 93(4):645-658.
• [48]Sabater J, Quereda C, Herrera I, Pascual J, Villafruela JJ, Ortuno J: Nonenzymatic Glycosylation of Hemoglobin and Total Plasmatic Proteins in End-Stage Renal-Disease. Am J Nephrol 1991, 11(1):37-43.
• [49]Chowdhury TA, Lasker SS: Elevated glycated haemoglobin in non-diabetic patients is associated with an increased mortality in myocardial infarction. Postgrad Med J 1998, 74(874):480-481.