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Particulate matter and markers of glycemic control and insulin resistance in type 2 diabetic patients: result from Wellcome Trust Genetic study

Journal of Exposure Science & Environmental Epidemiology volume 28, pages 328–336 (2018)Cite this article

Abstract

There is growing evidence that air pollution is associated with increased risk of type 2 diabetes (T2DM). However, information related to whether particulate matter (PM) contributing to worsened metabolic control in T2DM patients is inconsistent. We examined the association of PM10 exposure with glucose-function parameters in young-onset T2DM patients. We investigated the association between a year ambient concentration of PM10 at residential places, using AERMOD dispersion model, with fasting plasma glucose (FPG), hemoglobin A1c (HbA1c), 2 h post meal plasma glucose (2hPG), homeostasis model assessment of insulin resistance (HOMA-IR), β-cell function (HOMA-β) and disposition index (DI) in 1213 diabetic patients from the Wellcome Trust Genetic study at the Diabetes Unit, KEM Hospital Research Center, Pune, India. We used linear regression models and adjusted for a variety of individual and environmental confounding variables. Possible effect modification by age, gender, waist-to-hip ratio (WHR) and smoking status were investigated. Sensitivity analysis assessed the impact of relative humidity (RH) and temperature a day before examination and anti-diabetic and HHR medication (Hydralazine, Hydrochlorothiazide and Reserpine). We found that 1 SD increment in background concentration of PM10 at residential places (43.83 µg/m3) was significantly associated with 2.25 mmol/mol and 0.38 mmol/l increase in arithmetic means of HbA1c and 2hPG, respectively. A similar increase in PM10 was also associated with 4.89% increase in geometric mean of HOMA-IR. The associations remained significant after adjustment to RH and temperature, and WHR and smoking enhanced the size of the effect. Our study suggests that long-term exposure to PM10 is associated with higher glycaemia and insulin resistance. In context of our previous demonstration of association of SO2 and NO x and plasma C-reactive protein, we suggest that air pollution could influence progression of diabetes complications. Prospective studies and interventions are required to define mechanism and confirm causality.

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Fig. 1: Association between exposure to PM10 and biomarkers of glycemic control, HOMA-IR, HOMA-β and DI, adjusted to age, sex, season of enrolment, duration of diabetes, WHR, and smoking
Fig. 2: Association between exposure to PM10 and biomarkers of glycemic control (i.e., 2hPG, HbA1c) adjusted to age, sex, season of enrolment, duration of diabetes, WHR, and smoking
Fig. 3: Effect modification
Fig. 4: Effect modification
Fig. 5: Effect modification

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References

  1. Krämer U, Herder C, Sugiri D, Strassburger K, Schikowski T, Ranft U, et al. Traffic-related air pollution and incident type 2 diabetes: results from the SALIA cohort study. Environ Health Perspect. 2010;118:1273.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Andersen ZJ, Raaschou-Nielsen O, Ketzel M, Jensen SS, Hvidberg M, Loft S, et al. Diabetes incidence and long-term exposure to air pollution: a cohort study. Diabetes Care. 2012;35:92–98.

    Article  PubMed  CAS  Google Scholar 

  3. Pearson JF, Bachireddy C, Shyamprasad S, Goldfine AB, Brownstein JS. Association between fine particulate matter and diabetes prevalence in the US. Diabetes Care. 2010;33:2196–201.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Coogan PF, White LF, Jerrett M, Brook RD, Su JG, Seto E, et al. Air pollution and incidence of hypertension and diabetes mellitus in black women living in Los Angeles clinical perspective. Circulation. 2012;125:767–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Raaschou-Nielsen O, Sorensen M, Ketzel M, Hertel O, Loft S, Tjonneland A, et al. Long-term exposure to traffic-related air pollution and diabetes-associated mortality: a cohort study. Diabetologia. 2013;56:36–46.

  6. Dales RE, Cakmak S, Vidal CB, Rubio MA. Air pollution and hospitalization for acute complications of diabetes in Chile. Environ Int. 2012;46:1–5.

    Article  PubMed  CAS  Google Scholar 

  7. Teichert T, Vossoughi M, Vierkotter A, Sugiri D, Schikowski T, Schulte T, et al. Association between traffic-related air pollution, subclinical inflammation and impaired glucose metabolism: results from the SALIA study. PLoS One. 2013;8:e83042.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Chen Z, Salam MT, Toledo-Corral C, Watanabe RM, Xiang AH, Buchanan TA, et al. Ambient air pollutants have adverse effects on insulin and glucose homeostasis in Mexican Americans. Diabetes Care. 2016;39:547–54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Tamayo T, Rathmann W, Kramer U, Sugiri D, Grabert M, Holl RW. Is particle pollution in outdoor air associated with metabolic control in type 2 diabetes? PLoS One. 2014;9:e91639.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Chuang KJ, Yan YH, Chiu SY, Cheng TJ. Long-term air pollution exposure and risk factors for cardiovascular diseases among the elderly in Taiwan. Occup Environ Med. 2011;68:64–68.

    Article  PubMed  CAS  Google Scholar 

  11. Liu C, Yang C, Zhao Y, Ma Z, Bi J, Liu Y, et al. Associations between long-term exposure to ambient particulate air pollution and type 2 diabetes prevalence, blood glucose and glycosylated hemoglobin levels in China. Environ Int. 2016;92–93:416–21.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Tamayo T, Rathmann W, Stahl-Pehe A, Landwehr S, Sugiri D, Kramer U, et al. No adverse effect of outdoor air pollution on HbA1c in children and young adults with type 1 diabetes. Int J Hyg Environ Health. 2016;219:349–55.

    Article  PubMed  CAS  Google Scholar 

  13. Mousavi F, Jahed SA, Rajab A, Nikousokhan Tayar AK, Tabatabaei R, et al.. Air pollution effect on variation of glycosylated hemoglobin A (HbA1c) level in diabetic patients. Endocr Rev. 2011;32:541

    Google Scholar 

  14. Alderete TL, Habre R, Toledo-Corral CM, Berhane K, Chen Z, Lurmann FW, et al. Longitudinal associations between ambient air pollution with insulin sensitivity, beta-cell function, and adiposity in los angeles latino children. Diabetes. 2017;66:1789–1796.

  15. Donaldson K, Brown DM, Mitchell C, Dineva M, Beswick PH, Gilmour P, et al. Free radical activity of PM10: iron-mediated generation of hydroxyl radicals. Environ Health Perspect. 1997;105:1285. (Suppl 5)

    PubMed  PubMed Central  CAS  Google Scholar 

  16. Lodovici M, Bigagli E. Oxidative stress and air pollution exposure. J Toxicol. 2011;2011:487074.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Khafaie MA, Salvi SS, Ojha A, Khafaie B, Gore SD, Yajnik CS. Systemic inflammation (C-reactive protein) in type 2 diabetic patients is associated with ambient air pollution in Pune City, India. Diabetes Care. 2013;36:625–30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Maddux BA, See W, Lawrence JC Jr., Goldfine AL, Goldfine ID, Evans JL. Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by mircomolar concentrations of alpha-lipoic acid. Diabetes. 2001;50:404–10.

    Article  PubMed  CAS  Google Scholar 

  19. Rudich A, Tirosh A, Potashnik R, Hemi R, Kanety H, Bashan N. Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes. Diabetes. 1998;47:1562–9.

    Article  PubMed  CAS  Google Scholar 

  20. Matsuoka T, Kajimoto Y, Watada H, Kaneto H, Kishimoto M, Umayahara Y, et al. Glycation-dependent, reactive oxygen species-mediated suppression of the insulin gene promoter activity in HIT cells. J Clin Invest. 1997;99:144–50.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Thiering E, Cyrys J, Kratzsch J, Meisinger C, Hoffmann B, Berdel D, et al. Long-term exposure to traffic-related air pollution and insulin resistance in children: results from the GINIplus and LISAplus birth cohorts. Diabetologia. 2013;56:1696–704.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Xu X, Liu C, Xu Z, Tzan K, Zhong M, Wang A, et al. Long-term exposure to ambient fine particulate pollution induces insulin resistance and mitochondrial alteration in adipose tissue. Toxicol Sci: Off J Soc Toxicol. 2011;124:88–98.

    Article  CAS  Google Scholar 

  23. Gaffneya P, M. T., Benjaminc M, Cored J, Ojha A. (2007). India PM10 Emission Inventory Training and Capacity Building Programs: EPA Efforts for Developing a Sustainable Foundation. Paper presented at the 16th Annual International Emission Inventory Conference Emission Inventories: “Integration, Analysis, and Communications”, United States. https://www3.epa.gov/ttn/chief/conference/ei16/session8/gaffney_pres.pdf

    Google Scholar 

  24. Chandak GR, Janipalli CS, Bhaskar S, Kulkarni SR, Mohankrishna P, et al. Common variants in the TCF7L2 gene are strongly associated with type 2 diabetes mellitus in the Indian population. Diabetologia. 2007;50:63–67.

    Article  PubMed  CAS  Google Scholar 

  25. Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care. 1998;21:2191–2.

    Article  PubMed  CAS  Google Scholar 

  26. Matsuda M. Measuring and estimating insulin resistance in clinical and research settings. Nutr Metab Cardiovasc Dis. 2010;20:79–86.

    Article  PubMed  CAS  Google Scholar 

  27. Cimorelli AJ, Perry SG, Venkatram A, Weil JC, Paine RJ, Peters WD. (2004). AERMOD–Description of model formulation (1998) (EPA-454/R-03-004). Retrieved from U.S. Environmental Protection  https://www3.epa.gov/scram001/7thconf/aermod/aermod_mfd.pdf

  28. Ojha A, Kumar R, Boralkar D, Gargava P, Gaffeney P, Benjamin M, Mukkannawar U. (2006). Continual Improvement of Emission Estimates – The Pune Experience (2004 to 2006). Paper presented at the better air quality 2006, Yogyakarta, Indonesia. http://web.archive.org/web/20070205172832/http://www.cleanairnet.org:80/baq2006/1757/propertyvalue-26867.html

  29. Akaike H. (1998). Information Theory and an Extension of the Maximum Likelihood Principle. In: Parzen E., Tanabe K., Kitagawa G. (eds) Selected Papers of Hirotugu Akaike. Springer Series in Statistics (Perspectives in Statistics). Springer, New York, NY. https://link.springer.com/chapter/10.1007/978-1-4612-1694-0_15#citeas

  30. Khafaie MA, Yajnik C, Mojadam M, Khafaie B, Salvi SS, Ojha A, et al. Association between ambient temperature and blood biomarker of systemic inflammation in (C-reactive protien) in diabetes patients. Arch Med. 2016;8:3.

    Google Scholar 

  31. WHO. (2011). Waist circumference and waist-hip ratio: report of a WHO expert consultation, Geneva, 8-11 December 2008 (978 92 4 150149 1). Retrieved from http://www.who.int/iris/handle/10665/44583​

  32. Cersosimo E, Solis-Herrera C, Trautmann ME, Malloy J, Triplitt CL. Assessment of pancreatic beta-cell function: review of methods and clinical applications. Curr Diabetes Rev. 2014;10:2–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. CPCB (Central Pollution Control Board), 2006. Air Quality Trends and Action Plan for Control of Air Pollution from Seventeen Cities, Ministry of Environment and Forest, NAAQMS/29/2006–07, New Delhi, India.

  34. Kesarkar AP, Dalvi M, Kaginalkar A, Ojha A. Coupling of the weather research and forecasting model with AERMOD for pollutant dispersion modeling. A case study for PM10 dispersion over Pune, India. Atmos Environ. 2007;41:1976–88.

    Article  CAS  Google Scholar 

  35. Domingueti CP, LMSA Dusse, MDG Carvalho, de Sousa LP, Gomes KB, Fernandes AP. Diabetes mellitus: The linkage between oxidative stress, inflammation, hypercoagulability and vascular complications. J Diabetes Complicat. 2016;30:738–45.

    Article  PubMed  Google Scholar 

  36. Johnson EL. Glycemic variability in type 2 diabetes mellitus: oxidative stress and macrovascular complications. Adv Exp Med Biol. 2012;771:139–54.

    PubMed  Google Scholar 

  37. Lockwood AH. Diabetes and air pollution. Diabetes Care. 2002;25:1487–8.

    Article  PubMed  Google Scholar 

  38. Brook RD, Jerrett M, Brook JR, Bard RL, Finkelstein MM. The relationship between diabetes mellitus and traffic-related air pollution. J Occup Environ Med. 2008;50:32–38.

    Article  PubMed  CAS  Google Scholar 

  39. Fleisch AF, Gold DR, Rifas-Shiman SL, Koutrakis P, Schwartz JD, Kloog I, et al. Air pollution exposure and abnormal glucose tolerance during pregnancy: the project Viva cohort. Environ Health Perspect. 2014;122:378–83.

    PubMed  PubMed Central  CAS  Google Scholar 

  40. Thiering E, Cyrys J, Kratzsch J, Meisinger C, Hoffmann B, Berdel, D, et al. Long-term exposure to traffic-related air pollution and insulin resistance in children: results from the GINIplus and LISAplus birth cohorts. Diabetologia. 2013;56:1696–1704.

  41. Khafaie MA, Yajnik CS, Salvi S, Ojha A, Critical review of air pollution health effects with specialconcern on respiratory h. J Air Pollut Health (JAPH). 2016;2:73–86.

    Google Scholar 

  42. Li XY, Gilmour PS, Donaldson K, MacNee W. Free radical activity and pro-inflammatory effects of particulate air pollution (PM10) in vivo and in vitro. Thorax. 1996;51:1216–22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Lodovici M, Bigagli E. Oxidative stress and air pollution exposure. J Toxicol. 2011;2011:487074.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Moller P, Loft S. Oxidative damage to DNA and lipids as biomarkers of exposure to air pollution. Environ Health Perspect. 2010;118:1126–36.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Watson JD. Type 2 diabetes as a redox disease. Lancet (Lond, Engl). 2014;383:841–3.

    Article  Google Scholar 

  46. Startev V, Jordanova M, Petev J. (2011). Oxidative stress, obesity and chronic inflammation in smokers according to smoking duration and heaviness. European Respiratory Journal, 38: p1099 (Suppl 55).

  47. Khafaie MA, Salvi SS, Yajnik CS, Ojha A, Khafaie B, Gore SD. Air pollution and respiratory health among diabetic and non-diabetic subjects in Pune, India-results from the Wellcome Trust Genetic Study. Environ Sci Pollut Res Int. 2017;24:15538–46.

    Article  PubMed  CAS  Google Scholar 

  48. Schikowski T, Sugiri D, Reimann V, Pesch B, Ranft U, Krämer U. Contribution of smoking and air pollution exposure in urban areas to social differences in respiratory health. BMC Public Health. 2008;8:179.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Dandona P, Chaudhuri A, Ghanim H, Mohanty P. Insulin as an anti-Inflammatory and antiatherogenic modulator. J Am Coll Cardiol. 2009;53:S14–S20.

    Article  PubMed  CAS  Google Scholar 

  50. Skliros NP, Vlachopoulos C, Tousoulis D. Treatment of diabetes: crossing to the other side. Hell J Cardiol. 2016;57:304–10.

    Article  Google Scholar 

  51. Millstein J, Gilliland F, Berhane K, Gauderman WJ, McConnell R, Avol E, et al. Effects of ambient air pollutants on asthma medication use and wheezing among fourth-grade school children from 12 Southern California communities enrolled in The Children’s Health Study. Arch Environ Health. 2004;59:505–14.

    Article  PubMed  CAS  Google Scholar 

  52. Khafaie MA, Ojha A, Salvi SS, Yajnik CS. Methodological approach in air pollution health effects studies. J Air Pollut Health. 2016;1:219–26.

    Google Scholar 

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Acknowledgements

We acknowledge the contribution made by WellGen study group and Ms. Smita Kulkarni, Diabetes Unit, in data collection and data management, and Mr. Dattatray Bhat, Diabetes Unit, for laboratory measurements. Air pollutants and meteorological data were taken from Maharashtra Pollution Control Board and Meteorological Department, Pune Office, respectively. The WellGen study was supported by the Wellcome Trust (London, UK). None of the authors had any financial or personal conflicts of interest associated with this manuscript.

Author contributions

MAK and CSY researched, wrote, discussed and edited the manuscript. SSS and AO contributed to the discussion and edited the manuscript. BK and SDG contribute to the data analyses and edited the manuscript. CSY is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

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Authors and Affiliations

  1. Social Determinants of Health Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Morteza Abdullatif Khafaie

  2. Department of Public Health, Faculty of Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Morteza Abdullatif Khafaie

  3. Chest Research Foundation (CRF), Pune, Maharashtra, India

    Sundeep Santosh Salvi

  4. Technogreen Environmental Solutions, Pune, Maharashtra, India

    Ajay Ojha

  5. Department of Statistics, Islamic Azad University, Omidiyeh Branch, Omidiyeh, Iran

    Behzad Khafaie

  6. Department of Statistics, University of Pune, Pune, Maharashtra, India

    Sharad Damodar Gore

  7. King Edward Memorial Hospital Research Center, Pune, Maharashtra, India

    Chittaranjan Sakerlal Yajnik

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Khafaie, M.A., Salvi, S.S., Ojha, A. et al. Particulate matter and markers of glycemic control and insulin resistance in type 2 diabetic patients: result from Wellcome Trust Genetic study. J Expo Sci Environ Epidemiol 28, 328–336 (2018). https://doi.org/10.1038/s41370-017-0001-1

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