Skip to main content

Higher oxidative balance score is associated with better glycemic control among Iranian adults with type-2 diabetes

Published Online: Doi: https://doi.org/10.1024/0300-9831/a000596

Abstract. The oxidative balance score (OBS) is a measure of combined pro- and anti-oxidant exposure status, with a higher OBS representing a predominance of anti- over pro-oxidant exposures. We aimed to examine the association of OBS and glycemic control among Iranian adults with type-2 diabetes. This cross-sectional study was conducted among 476 adults with type-2 diabetes (mean age 56.2 y; 66.6% female). Fasting glycosylated hemoglobin (HbA1c) and serum glucose (FSG) levels were measured as markers of glycemic control. The OBS was calculated by combining information from a total of 18 a priori selected pro- and anti-oxidant components. These components were comprised of the following four categories: dietary anti-oxidants (i.e., dietary intakes of selenium, fiber, retinol, α-carotene, β-carotene, β-cryptoxanthin, lutein, lycopene, vitamin D, vitamin E, folate, and vitamin C); dietary pro-oxidants (i.e., dietary intakes of iron, saturated fatty acid, and poly-unsaturated fatty acid); non-dietary anti-oxidants (i.e., physical activity); and non-dietary pro-oxidants (i.e., smoking and obesity). After adjusting for several potential confounders in the analysis of covariance models, multivariable adjusted means of HbA1c and FSG of subjects in the highest tertile of OBS were significantly lower than those in the lowest tertile (for HbA1c: mean difference –0.73%; and for FSG: mean difference –10.2 mg/dL; both P < 0.050). The findings suggest that a higher OBS, indicating a predominance of anti- over pro-oxidant exposures, is associated with a better glycemic control among Iranian adults with type-2 diabetes. However, future prospective studies of adequate methodological quality are warranted to confirm these findings.

References

  • 1 Guariguata L., Whiting D.R., Hambleton I., Beagley J., Linnenkamp U., Shaw J.E. (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 103, 137–149. First citation in articleCrossref MedlineGoogle Scholar

  • 2 Esteghamati A., Etemad K., Koohpayehzadeh J., Abbasi M., Meysamie A., Noshad S., Asgari F., Mousavizadeh M., Rafei A., Khajeh E., Neishaboury M., Sheikhbahaei S., Nakhjavani M. (2014) Trends in the prevalence of diabetes and impaired fasting glucose in association with obesity in Iran: 2005–2011. Diabetes Res Clin Pract. 103, 319–327. First citation in articleCrossref MedlineGoogle Scholar

  • 3 Homayouni-Rad A., Soroush A.R., Khalili L., Norouzi-Panahi L., Kasaie Z., Ejtahed H.S. (2016) Diabetes Management by Probiotics: Current Knowledge and Future Pespective. Int J Vitam Nutr Res. 86, 215–227. First citation in articleLinkGoogle Scholar

  • 4 Murea M., Ma L., Freedman B.I. (2012) Genetic and environmental factors associated with type 2 diabetes and diabetic vascular complications. Rev Diabet Stud. 9, 6–22. First citation in articleCrossref MedlineGoogle Scholar

  • 5 Rehman K., Akash M.S.H. (2017) Mechanism of Generation of Oxidative Stress and Pathophysiology of Type 2 Diabetes Mellitus: How Are They Interlinked? J Cell Biochem. 118, 3577–3585. First citation in articleCrossref MedlineGoogle Scholar

  • 6 Rehman K., Akash M.S.H. (2016) Nutrition and diabetes mellitus: how are they interlinked? Crit Rev Eukaryot Gene Expr. 26, 317–332. First citation in articleCrossref MedlineGoogle Scholar

  • 7 Liu S., Ajani U., Chae C., Hennekens C., Buring J.E., Manson J.E. (1999) Long-term beta-carotene supplementation and risk of type 2 diabetes mellitus: a randomized controlled trial. JAMA. 282, 1073–1075. First citation in articleCrossref MedlineGoogle Scholar

  • 8 Rytter E., Vessby B., Asgard R., Ersson C., Moussavian S., Sjodin A., Abramsson-Zetterberg L., Moller L., Basu S. (2010) Supplementation with a combination of antioxidants does not affect glycaemic control, oxidative stress or inflammation in type 2 diabetes subjects. Free Radic Res. 44, 1445–1453. First citation in articleCrossref MedlineGoogle Scholar

  • 9 Suksomboon N., Poolsup N., Sinprasert S. (2011) Effects of vitamin E supplementation on glycaemic control in type 2 diabetes: systematic review of randomized controlled trials. J Clin Pharm Ther. 36, 53–63. First citation in articleCrossref MedlineGoogle Scholar

  • 10 Valero M.A., Vidal A., Burgos R., Calvo F.L., Martinez C., Luengo L.M., Cuerda C. (2011) Meta-analysis on the role of lycopene in type 2 diabetes mellitus. Nutr Hosp. 26, 1236–1241. First citation in articleMedlineGoogle Scholar

  • 11 Bao W., Rong Y., Rong S., Liu L. (2012) Dietary iron intake, body iron stores, and the risk of type 2 diabetes: a systematic review and meta-analysis. BMC Med. 10, 119. First citation in articleCrossref MedlineGoogle Scholar

  • 12 Sudchada P., Saokaew S., Sridetch S., Incampa S., Jaiyen S., Khaithong W. (2012) Effect of folic acid supplementation on plasma total homocysteine levels and glycemic control in patients with type 2 diabetes: a systematic review and meta-analysis. Diabetes Res Clin Pract. 98, 151–158. First citation in articleCrossref MedlineGoogle Scholar

  • 13 Silva F.M., Kramer C.K., de Almeida J.C., Steemburgo T., Gross J.L., Azevedo M.J. (2013) Fiber intake and glycemic control in patients with type 2 diabetes mellitus: a systematic review with meta-analysis of randomized controlled trials. Nutr Rev. 71, 790–801. First citation in articleCrossref MedlineGoogle Scholar

  • 14 Tabatabaei-Malazy O., Nikfar S., Larijani B., Abdollahi M. (2014) Influence of ascorbic acid supplementation on type 2 diabetes mellitus in observational and randomized controlled trials; a systematic review with meta-analysis. J Pharm Pharm Sci. 17, 554–582. First citation in articleCrossref MedlineGoogle Scholar

  • 15 de Souza R.J., Mente A., Maroleanu A., Cozma A.I., Ha V., Kishibe T., Uleryk E., Budylowski P., Schunemann H., Beyene J., Anand S.S. (2015) Intake of saturated and trans unsaturated fatty acids and risk of all cause mortality, cardiovascular disease, and type 2 diabetes: systematic review and meta-analysis of observational studies. BMJ. 351, h3978. First citation in articleCrossref MedlineGoogle Scholar

  • 16 Franz M.J., Boucher J.L., Rutten-Ramos S., VanWormer J.J. (2015) Lifestyle weight-loss intervention outcomes in overweight and obese adults with type 2 diabetes: a systematic review and meta-analysis of randomized clinical trials. J Acad Nutr Diet. 115, 1447–1463. First citation in articleCrossref MedlineGoogle Scholar

  • 17 Pan A., Wang Y., Talaei M., Hu F.B., Wu T. (2015) Relation of active, passive, and quitting smoking with incident type 2 diabetes: a systematic review and meta-analysis. Lancet Diabetes Endocrinol. 3, 958–967. First citation in articleCrossref MedlineGoogle Scholar

  • 18 Sluijs I., Cadier E., Beulens J.W., van der A.D., Spijkerman A.M., van der Schouw Y.T. (2015) Dietary intake of carotenoids and risk of type 2 diabetes. Nutr Metab Cardiovasc Dis. 25, 376–381. First citation in articleCrossref MedlineGoogle Scholar

  • 19 Vitale M., Masulli M., Rivellese A.A., Babini A.C., Boemi M., Bonora E., Buzzetti R., Ciano O., Cignarelli M., Cigolini M., Clemente G., Citro G., Corsi L., Dall’Aglio E., Del Prato S., Di Cianni G., Dolci M.A., Giordano C., Iannarelli R., Iovine C., Lapolla A., Lauro D., Leotta S., Mazzucchelli C., Montani V., Perriello G., Romano G., Romeo F., Santarelli L., di Cola R.S., Squatrito S., Tonutti L., Trevisan R., Turco A.A., Zamboni C., Riccardi G., Vaccaro O. (2016) Influence of dietary fat and carbohydrates proportions on plasma lipids, glucose control and low-grade inflammation in patients with type 2 diabetes-The TOSCA.IT Study. Eur J Nutr. 55, 1645–1651. First citation in articleCrossref MedlineGoogle Scholar

  • 20 Boniol M., Dragomir M., Autier P., Boyle P. (2017) Physical activity and change in fasting glucose and HbA1c: a quantitative meta-analysis of randomized trials. Acta Diabetol. 54, 983–991. First citation in articleCrossref MedlineGoogle Scholar

  • 21 Wang F., Wang Y., Zhu Y., Liu X., Xia H., Yang X., Sun G. (2017) Treatment for 6 months with fish oil-derived n-3 polyunsaturated fatty acids has neutral effects on glycemic control but improves dyslipidemia in type 2 diabetic patients with abdominal obesity: a randomized, double-blind, placebo-controlled trial. Eur J Nutr. 56, 2415–2422. First citation in articleCrossref MedlineGoogle Scholar

  • 22 Li X., Liu Y., Zheng Y., Wang P., Zhang Y. (2018) The Effect of Vitamin D Supplementation on Glycemic Control in Type 2 Diabetes Patients: A Systematic Review and Meta-Analysis. Nutrients. 10, 375. First citation in articleCrossrefGoogle Scholar

  • 23 Liu S., van der Schouw Y.T., Soedamah-Muthu S.S., Spijkerman A.M.W., Sluijs I. (2018) Intake of dietary saturated fatty acids and risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition-Netherlands cohort: associations by types, sources of fatty acids and substitution by macronutrients. Eur J Nutr. doi: 10.1007/s00394-018-1630-4. First citation in articleCrossrefGoogle Scholar

  • 24 O’Mahoney L.L., Matu J., Price O.J., Birch K.M., Ajjan R.A., Farrar D., Tapp R., West D.J., Deighton K., Campbell M.D. (2018) Omega-3 polyunsaturated fatty acids favourably modulate cardiometabolic biomarkers in type 2 diabetes: a meta-analysis and meta-regression of randomized controlled trials. Cardiovasc Diabetol. 17, 98. First citation in articleCrossref MedlineGoogle Scholar

  • 25 Vinceti M., Filippini T., Rothman K.J. (2018) Selenium exposure and the risk of type 2 diabetes: a systematic review and meta-analysis. Eur J Epidemiol. 33, 789–810. First citation in articleCrossref MedlineGoogle Scholar

  • 26 Ilori T.O., Wang X., Huang M., Gutierrez O.M., Narayan K.M., Goodman M., McClellan W., Plantinga L., Ojo A.O. (2017) Oxidative Balance Score and the Risk of End-Stage Renal Disease and Cardiovascular Disease. Am J Nephrol. 45, 338–345. First citation in articleCrossref MedlineGoogle Scholar

  • 27 Lee H.S., Park T. (2017) Pathway-driven approaches of interaction between oxidative balance and genetic polymorphism on metabolic syndrome. Oxid Med Cell Longev. 2017, 6873197. First citation in articleCrossref MedlineGoogle Scholar

  • 28 Goodman M., Bostick R.M., Gross M., Thyagarajan B., Dash C., Flanders W.D. (2010) Combined measure of pro- and anti-oxidant exposures in relation to prostate cancer and colorectal adenoma risk: an update. Ann Epidemiol. 20, 955–957. First citation in articleCrossref MedlineGoogle Scholar

  • 29 Lakkur S., Judd S., Bostick R.M., McClellan W., Flanders W.D., Stevens V.L., Goodman M. (2015) Oxidative stress, inflammation, and markers of cardiovascular health. Atherosclerosis. 243, 38–43. First citation in articleCrossref MedlineGoogle Scholar

  • 30 Dash C., Bostick R.M., Goodman M., Flanders W.D., Patel R., Shah R., Campbell P.T., McCullough M.L. (2015) Oxidative balance scores and risk of incident colorectal cancer in a US prospective cohort study. Am J Epidemiol. 181, 584–594. First citation in articleCrossref MedlineGoogle Scholar

  • 31 Slattery M.L., John E.M., Torres-Mejia G., Lundgreen A., Lewinger J.P., Stern M.C., Hines L., Baumgartner K.B., Giuliano A.R., Wolff R.K. (2014) Angiogenesis genes, dietary oxidative balance and breast cancer risk and progression: the Breast Cancer Health Disparities Study. Int J Cancer. 134, 629–644. First citation in articleCrossref MedlineGoogle Scholar

  • 32 Slattery M.L., Herrick J.S., Mullany L.E., Stevens J.R., Wolff R.K. (2017) Diet and lifestyle factors associated with miRNA expression in colorectal tissue. Pharmgenomics Pers Med. 10, 1–16. First citation in articleMedlineGoogle Scholar

  • 33 Kong S.Y., Goodman M., Judd S., Bostick R.M., Flanders W.D., McClellan W. (2015) Oxidative balance score as predictor of all-cause, cancer, and noncancer mortality in a biracial US cohort. Ann Epidemiol. 25, 256–262. First citation in articleCrossref MedlineGoogle Scholar

  • 34 Saif M. (2000) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 284, 3043–3045. First citation in articleCrossref MedlineGoogle Scholar

  • 35 American Diabetes Association. (2018) 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes—2018. Diabetes Care. 41, S13–S27. First citation in articleCrossref MedlineGoogle Scholar

  • 36 Mirmiran P., Esfahani F.H., Mehrabi Y., Hedayati M., Azizi F. (2010) Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public Health Nutr. 13, 654–662. First citation in articleCrossref MedlineGoogle Scholar

  • 37 Esfahani F.H., Asghari G., Mirmiran P., Azizi F. (2010) Reproducibility and relative validity of food group intake in a food frequency questionnaire developed for the Tehran Lipid and Glucose Study. J Epidemiol. 20, 150–158. First citation in articleCrossref MedlineGoogle Scholar

  • 38 Hosseini-Esfahani F., Moslehi N., Asghari G., Hosseinpour-Niazi S., Bahadoran Z., Yuzbashian E., Mirmiran P., Azizi F. (2018) Nutrition and Diabetes, Cardiovascular and Chronic Kidney Diseases: Findings from 20 Years of the Tehran Lipid and Glucose Study. Int J Endocrinol Metab. 16, e84791. First citation in articleCrossref MedlineGoogle Scholar

  • 39 Ghane Basiri M., Sotoudeh G., Djalali M., Eshraghian M.R., Noorshahi N., Rafiee M., Nikbazm R., Karimi Z., Koohdani F. (2015) Association of Major Dietary Patterns with General and Abdominal Obesity in Iranian Patients with Type 2 Diabetes Mellitus. Int J Vitam Nutr Res. 85, 145–155. First citation in articleLinkGoogle Scholar

  • 40 Ghaffarpour M., Houshiar-Rad A., Kianfar H. (1999) The manual for household measures, cooking yields factors, and edible portion of foods. Agriculture Sciences Press, Tehran. First citation in articleGoogle Scholar

  • 41 Willett W., Stampfer M.J. (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol. 124, 17–27. First citation in articleCrossref MedlineGoogle Scholar

  • 42 The IPAQ group. Guidelines for the Data Processing and Analysis of the International Physical Activity Questionnaire. Available from: http://www.ipaq.ki.se. First citation in articleGoogle Scholar

  • 43 Craig C.L., Marshall A.L., Sjostrom M., Bauman A.E., Booth M.L., Ainsworth B.E., Pratt M., Ekelund U., Yngve A., Sallis J.F., Oja P. (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 35, 1381–1395. First citation in articleCrossref MedlineGoogle Scholar

  • 44 Moghaddam M.H.B., Aghdam F.B., Jafarabadi M.A., Allahverdipour H., Nikookheslat S.D., Safarpour S. (2012) The Iranian Version of International Physical Activity Questionnaire (IPAQ) in Iran: content and construct validity, factor structure, internal consistency and stability. World Appl Sci. 18, 1073–1080. First citation in articleGoogle Scholar

  • 45 Cho A.R., Kwon Y.J., Lim H.J., Lee H.S., Kim S., Shim J.Y., Lee H.R., Lee Y.J. (2018) Oxidative balance score and serum gamma-glutamyltransferase level among Korean adults: a nationwide population-based study. Eur J Nutr. 57, 1237–1244. First citation in articleCrossref MedlineGoogle Scholar

  • 46 Zal F., Mahdian Z., Zare R., Soghra B., Mostafavi-Pour Z. (2014) Combination of vitamin E and folic acid ameliorate oxidative stress and apoptosis in diabetic rat uterus. Int J Vitam Nutr Res. 84, 55–64. First citation in articleLinkGoogle Scholar

  • 47 Koul A., Angmo S., Bharati S. (2016) Preventive Role of Vitamin D in Silica-Induced Skin Fibrosis: A Study in Relation to Oxidative Stress and Pro-Inflammatory Cytokines. Int J Vitam Nutr Res. 86, 88–96. First citation in articleLinkGoogle Scholar

  • 48 Gul Baykalir B., Aksit D., Dogru M.S., Hanim Yay A., Aksit H., Seyrek K., Attesahin A. (2016) Lycopene Ameliorates Experimental Colitis in Rats via Reducing Apoptosis and Oxidative Stress. Int J Vitam Nutr Res. 86, 27–35. First citation in articleLinkGoogle Scholar

  • 49 Lakkur S., Bostick R.M., Roblin D., Ndirangu M., Okosun I., Annor F., Judd S., Dana Flanders W., Stevens V.L., Goodman M. (2014) Oxidative balance score and oxidative stress biomarkers in a study of Whites, African Americans, and African immigrants. Biomarkers. 19, 471–480. First citation in articleCrossref MedlineGoogle Scholar

  • 50 Kong S.Y., Bostick R.M., Flanders W.D., McClellan W.M., Thyagarajan B., Gross M.D., Judd S., Goodman M. (2014) Oxidative balance score, colorectal adenoma, and markers of oxidative stress and inflammation. Cancer Epidemiol Biomarkers Prev. 23, 545–554. First citation in articleCrossref MedlineGoogle Scholar

  • 51 Gohel M.G., Chacko A.N. (2013) Serum GGT activity and hsCRP level in patients with type 2 diabetes mellitus with good and poor glycemic control: An evidence linking oxidative stress, inflammation and glycemic control. J Diabetes Metab Disord. 12, 56. First citation in articleCrossref MedlineGoogle Scholar

  • 52 Annadurai T., Vasanthakumar A., Geraldine P., Thomas P.A. (2014) Variations in erythrocyte antioxidant levels and lipid peroxidation status and in serum lipid profile parameters in relation to blood haemoglobin A1c values in individuals with type 2 diabetes mellitus. Diabetes Res Clin Pract. 105, 58–69. First citation in articleCrossref MedlineGoogle Scholar

  • 53 Gawlik K., Naskalski J.W., Fedak D., Pawlica-Gosiewska D., Grudzien U., Dumnicka P., Malecki M.T., Solnica B. (2016) Markers of Antioxidant Defense in Patients with Type 2 Diabetes. Oxid Med Cell Longev. 2016, 2352361. First citation in articleCrossref MedlineGoogle Scholar

  • 54 Pieme C.A., Tatangmo J.A., Simo G., Nya P.C.B., Moor V.J.A., Moukette B.M., Nzufo F.T., Nono B.L.N., Sobngwi E. (2017) Relationship between hyperglycemia, antioxidant capacity and some enzymatic and non-enzymatic antioxidants in African patients with type 2 diabetes. BMC Res Notes. 10, 141. First citation in articleCrossref MedlineGoogle Scholar

  • 55 Chrysostomou S. (2016) Vitamin D Daily short-term Supplementation does not Affect Glycemic Outcomes of Patients with Type 2 Diabetes. Int J Vitam Nutr Res. 86, 169–183. First citation in articleLinkGoogle Scholar

  • 56 Mahmood S.F., Idiculla J., Joshi R., Joshi S., Kulkarni S. (2016) Vitamin D Supplementation in Adults with Vitamin D Deficiency and Its Effect on Metabolic Syndrome – A Randomized Controlled Study. Int J Vitam Nutr Res. 86, 121–126. First citation in articleLinkGoogle Scholar

  • 57 Bohn T. (2017) Bioactivity of Carotenoids – Chasms of Knowledge. Int J Vitam Nutr Res. doi: 10.1024/0300-9831/a000400. First citation in articleLinkGoogle Scholar

  • 58 Opara E.C. (2004) Role of oxidative stress in the etiology of type 2 diabetes and the effect of antioxidant supplementation on glycemic control. J Investig Med. 52, 19–23. First citation in articleCrossref MedlineGoogle Scholar

  • 59 Tangvarasittichai S. (2015) Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes. 6, 456–480. First citation in articleCrossref MedlineGoogle Scholar

  • 60 Livingstone M. (1995) Assessment of food intakes: are we measuring what people eat? Br J Biomed Sci. 52, 58–67. First citation in articleMedlineGoogle Scholar

  • 61 Sarnowski C., Hivert M.F. (2018) Impact of Genetic Determinants of HbA1c on Type 2 Diabetes Risk and Diagnosis. Curr Diab Rep. 18, 52. First citation in articleCrossref MedlineGoogle Scholar

Access content

To read the fulltext, please use one of the options below to sign in or purchase access.