Abstract
Purpose
The relationship between obstructive sleep apnea (OSA) and diabetic microvascular complications (DMC) are controversial. Whether low education is associated with increased risk of DMC independently of poor lifestyles are currently unknown. The aim of this study is to explore the independent associations of different PSG index and educational attainment with risks of DR, DKD, and DPN.
Methods
A cross-sectional study of 330 patients with T2DM who underwent overnight polysomnography (PSG) tests. Multivariable logistic regression analysis was performed to determine the associations of PSG index and educational attainments with DR, DKD, and DPN.
Results
The prevalence rates of DMC were 30.6% for DR, 24.9% for DKD, and 64.6% for DPN. All PSG index (AHI, REM-AHI, NREM-AHI, the severity of OSAS, ODI, MAI, and lowest SaO2) were not significantly associated with risks of DR, DKD, or DPN with adjustment for potential confounding factors. Subjects with increasing educational attainments showed significantly decreased prevalence rates of DR (42.6, 27.3, and 21.3%, p = 0.005), DKD (31.7, 25.3, and 14.7%, p = 0.035) and DPN (74.3, 63.6, and 53.3%, p = 0.015), respectively. Logistic regression analyses showed that educational attainment of primary or below showed significantly increased risks of DR (OR (95% CIs): 3.596 (1.453–8.899, p = 0.006)) and DKD (OR (95% CIs): 3.201 (1.244–8.242, p = 0.016)) as compared with that of college or above. There were significant trends of lower educational attainment with increased risks of DR and DKD (p values < 0.05).
Conclusion
PSG index were not significantly associated with DMC. But lower education was significantly associated with increased risks of DR and DKD, and strategies to prevent DMC for those with low education should be strengthened.
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References
Y. Zheng, S.H. Ley, F.B. Hu, Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat. Rev. Endocrinol. 14(2), 88–98 (2018)
A. Menke, S. Casagrande, L. Geiss, C.C. Cowie, Prevalence of and trends in diabetes among adults in the United States, 1988–2012. JAMA 314(10), 1021–1029 (2015)
W.M. Valencia, H. Florez, How to prevent the microvascular complications of type 2 diabetes beyond glucose control. BMJ 356, i6505 (2017)
T. Young, M. Palta, J. Dempsey, J. Skatrud, S. Weber, S. Badr, The occurrence of sleep-disordered breathing among middle-aged adults. N. Engl. J. Med 328(17), 1230–1235 (1993)
T. Young, L. Finn, P.E. Peppard, M. Szklo-Coxe, D. Austin, F.J. Nieto, R. Stubbs, K.M. Hla, Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort. Sleep 31(8), 1071–1078 (2008)
S. Nannapaneni, K. Ramar, S. Surani, Effect of obstructive sleep apnea on type 2 diabetes mellitus: a comprehensive literature review. World J. Diabetes 4(6), 238–244 (2013)
Q.A. Altaf, P. Dodson, A. Ali, N.T. Raymond, H. Wharton, H. Fellows, R. Hampshire-Bancroft, M. Shah, E. Shepherd, J. Miah, A.H. Barnett, A.A. Tahrani, Obstructive sleep apnea and retinopathy in patients with type 2 diabetes. A longitudinal study. Am. J. Respir. Crit. Care Med 196(7), 892–900 (2017)
W.B. Leong, F. Jadhakhan, S. Taheri, G.N. Thomas, P. Adab, The association between obstructive sleep apnea on diabetic kidney disease: a systematic review and meta-analysis. Sleep 39(2), 301–308 (2016)
H. Shen, J. Zhao, Y. Liu, G. Sun, Interactions between and shared molecular mechanisms of diabetic peripheral neuropathy and obstructive sleep apnea in type 2 diabetes patients. J. Diabetes Res 2018, 3458615 (2018)
M.T. Bianchi, B. Goparaju, Potential underestimation of sleep apnea severity by At-home kits: rescoring in-laboratory polysomnography without sleep staging. J. Clin. Sleep. Med 13(4), 551–555 (2017)
G.R. Dagenais, H.C. Gerstein, X. Zhang, M. McQueen, S. Lear, P. Lopez-Jaramillo, V. Mohan, P. Mony, R. Gupta, V.R. Kutty, R. Kumar, O. Rahman, K. Yusoff, K. Zatonska, A. Oguz, A. Rosengren, R. Kelishadi, A. Yusufali, R. Diaz, A. Avezum, F. Lanas, A. Kruger, N. Peer, J. Chifamba, R. Iqbal, N. Ismail, B. **ulin, L. Jiankang, D. Wenqing, Y. Gejie, S. Rangarajan, K. Teo, S. Yusuf, Variations in diabetes prevalence in low-, middle-, andhigh-income countries: results from the prospective urban and rural epidemiological study. Diabetes Care. 39(5), 780–787 (2016)
M.L. Tan, J.A. Manski-Nankervis, S. Thuraisingam, A. Jenkins, D. O’Neal, J. Furler, Socioeconomic status and time in glucose target range in people with type 2 diabetes: a baseline analysis of the GP-OSMOTIC study. BMC Endocr. Disord. 18(1), 47 (2018)
J.I. Blomster, S. Zoungas, M. Woodward, B. Neal, S. Harrap, N. Poulter, M. Marre, B. Williams, J. Chalmers, G.S. Hillis, The impact of level of education on vascular events and mortality in patients with type 2 diabetes mellitus: Results from the ADVANCE study. Diabetes Res Clin. Pr. 127, 212–217 (2017)
H. Vandenheede, P. Deboosere, A. Espelt, M. Bopp, C. Borrell, G. Costa, T.A. Eikemo, R. Gnavi, R. Hoffmann, I. Kulhanova, M. Kulik, M. Leinsalu, P. Martikainen, G. Menvielle, M. Rodriguez-Sanz, J. Rychtarikova, J.P. Mackenbach, Educational inequalities in diabetes mortality across Europe in the 2000s: the interaction with gender. Int J. Public Health 60(4), 401–410 (2015)
T.A. Lakka, J. Kauhanen, J.T. Salonen, Conditioning leisure time physical activity and cardiorespiratory fitness in sociodemographic groups of middle-ages men in eastern Finland. Int J. Epidemiol. 25(1), 86–93 (1996)
American Diabetes Association. Stand. Med. Care Diabetes - 2012 Diabetes Care 35(Suppl 1), S11–S63 (2012)
Y.C. Ma, L. Zuo, J.H. Chen, Q. Luo, X.Q. Yu, Y. Li, J.S. Xu, S.M. Huang, L.N. Wang, W. Huang, M. Wang, G.B. Xu, H.Y. Wang, Modified glomerular filtration rate estimating equation for Chinese patients with chronic kidney disease. J. Am. Soc. Nephrol. 17, 2937–2944 (2006)
R.B. Berry, R. Budhiraja, D.J. Gottlieb, D. Gozal, C. Iber, V.K. Kapur, C.L. Marcus, R. Mehra, S. Parthasarathy, S.F. Quan, S. Redline, K.P. Strohl, S.L. Davidson Ward, M.M. Tangredi; American Academy of Sleep Medicine., Rules for scoring respiratory events in sleep: update of the 2007 AASM manual for the scoring of sleep and associated events. Deliberations of the sleep apnea definitions task force of the American academy of sleep medicine. J. Clin. Sleep. Med 8(5), 597–619 (2012)
Y. Ikeda, T. Kasai, F. Kawana, S. Kasagi, H. Takaya, S. Ishiwata, K. Narui, Comparison between the apnea-hypopnea indices determined by the REMstar Auto M series and those determined by standard in-laboratory polysomnography in patients with obstructive sleep apnea. Intern Med. 51(20), 2877–2885 (2012)
G.D. Foster, M.H. Sanders, R. Millman, G. Zammit, K.E. Borradaile, A.B. Newman, T.A. Wadden, D. Kelley, R.R. Wing, F.X. Sunyer, V. Darcey, S.T. Kuna; Sleep AHEAD Research Group., Obstructive sleep apnea among obese patients with type 2 diabetes. Diabetes Care. 32(6), 1017–1019 (2009)
S. Reutrakul, B. Mokhlesi, Obstructive sleep apnea and diabetes: a state of the art review. Chest 152(5), 1070–1086 (2017)
B. Mokhlesi, D. Grimaldi, G. Beccuti, E. Van Cauter, Effect of one week of CPAP treatment of obstructive sleep apnoea on 24-hour profiles of glucose, insulin and counter-regulatory hormones in type 2 diabetes. Diabetes Obes. Metab. 19(3), 452–456 (2017)
A. Nishimura, T. Kasai, S. Kikuno, K. Nagasawa, M. Okubo, K. Narui, Y. Mori, Apnea hypopnea index during rapid eye movement sleep with diabetic retinopathy in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 104(6), 2075–2082 (2019)
A. Nishimura, T. Kasai, H. Tamura, A. Yamato, D. Yasuda, K. Nagasawa, M. Okubo, K. Narui, Y. Mori, Relationship between sleep disordered breathing and diabetic retinopathy: analysis of 136 patients with diabetes. Diabetes Res Clin. Pr. 109(2), 306–311 (2015)
D. Banerjee, W.B. Leong, T. Arora, M. Nolen, V. Punamiya, R. Grunstein, S. Taheri, The potential association between obstructive sleep apnea and diabetic retinopathy in severe obesity-the role of hypoxemia. PLoS ONE 8(11), e79521 (2013)
R. Zhang, P. Zhang, F. Zhao, X. Han, L. Ji, Association of diabetic microvascular complications and parameters of obstructive sleep apnea in patients with Type 2 diabetes. Diabetes Technol. Ther. 18(7), 415–420 (2016)
B. Buyukaydin, M.E. Akkoyunlu, R. Kazancioglu, F. Karakose, H.K. Ozcelik, R. Erkoc, L. Kart, The effect of sleep apnea syndrome on the development of diabetic nephropathy in patients with type 2 diabetes. Diabetes Res Clin. Pr. 98(1), 140–143 (2012)
A.A. Tahrani, A. Ali, N.T. Raymond, S. Begum, K. Dubb, Q.A. Altaf, M.K. Piya, A.H. Barnett, M.J. Stevens, Obstructive sleep apnea and diabetic nephropathy: a cohort study. Diabetes Care. 36(11), 3718–3725 (2013)
S. Tesfaye, D. Selvarajah, R. Gandhi, M. Greig, P. Shillo, F. Fang, I.D. Wilkinson, Diabetic peripheral neuropathy may not be as its name suggests: evidence from magnetic resonance imaging. Pain 157(Suppl 1), S72–S80 (2016)
V. Rosenfeld, Sleep dysfunction, diabetes, and pain: a troublesome triad. J. Fam. Pr. 63(6 Suppl), S18–S24 (2014)
A.A. Tahrani, A. Ali, N.T. Raymond, S. Begum, K. Dubb, S. Mughal, B. Jose, M.K. Piya, A.H. Barnett, M.J. Stevens, Obstructive sleep apnea and diabetic neuropathy: a novel association in patients with type 2 diabetes. Am. J. Respir. Crit. Care Med 186(5), 434–441 (2012)
Q.A. Altaf, A. Ali, M.K. Piya, N.T. Raymond, A.A. Tahrani, The relationship between obstructive sleep apnea and intra-epidermal nerve fiber density, PARP activation and foot ulceration in patients with type 2 diabetes. J. Diabetes Complicat. 30(7), 1315–1320 (2016)
X. Gu, X. Luo, X. Wang, J. Tang, W. Yang, Z. Cai, The correlation between obstructive sleep apnea and diabetic neuropathy: a meta-analysis. Prim. Care Diabetes 12(5), 460–466 (2018)
K.I. Birkeland, M.E. Jørgensen, B. Carstensen, F. Persson, H.L. Gulseth, M. Thuresson, P. Fenici, D. Nathanson, T. Nyström, J.W. Eriksson, J. Bodegård, A. Norhammar, Cardiovascular mortality and morbidity in patients with type 2 diabetes following initiation of sodium-glucose co-transporter-2 inhibitors versus other glucose-lowering drugs (CVD-REAL Nordic): a multinational observational analysis. Lancet Diabetes Endocrinol. 5(9), 709–717 (2017)
J.I. Blomster, C.K. Chow, S. Zoungas, M. Woodward, A. Patel, N.R. Poulter, M. Marre, S. Harrap, J. Chalmers, G.S. Hillis, The influence of physical activity on vascular complications and mortality in patients with type 2 diabetes mellitus. Diabetes Obes. Metab. 15(11), 1008–1012 (2013)
J.I. Blomster, S. Zoungas, J. Chalmers, Q. Li, C.K. Chow, M. Woodward, G. Mancia, N. Poulter, B. Williams, S. Harrap, B. Neal, A. Patel, G.S. Hillis, The relationship between alcohol consumption and vascular complications and mortality in individuals with type 2 diabetes. Diabetes Care. 37(5), 1353–1359 (2014)
Acknowledgements
We are grateful to all the patients for their participation.
Funding
C.L. was founded by Natural Science Foundation of China grant no: 81870611. Z.L. was founded by the National Key R&D Program of China grant no: 2017YFC0907100.ML was founded by Natural Science Foundation of Fujian Province grant no: 2017J01365.
Author contributions
The study concept and design were framed by C.D., Z.L., and C.L., C.D., C.H., S.Z., L.D., W.W., C.Z., and S.W. collected data. C.D., C.H., Z.L., and C.L. conducted the statistical data analysis and drafted the manuscript. M.L., X.J., and S.Y., contributed to discussion and revision. All authors read and approved the final manuscript.
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These authors contributed equally: Chunmin Du, Chunmei He
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Du, C., He, C., Dong, L. et al. Associations of apnea hypopnea index and educational attainments with microvascular complications in patients with T2DM. Endocrine 67, 363–373 (2020). https://doi.org/10.1007/s12020-020-02192-w
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DOI: https://doi.org/10.1007/s12020-020-02192-w