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ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

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Review Article

Obesity, Metabolic Syndrome and the Risk of Microvascular Complications in Patients with Diabetes mellitus

Author(s): Niki Katsiki*, Panagiotis Anagnostis, Kalliopi Kotsa, Dimitrios G. Goulis and Dimitri P. Mikhailidis

Volume 25, Issue 18, 2019

Page: [2051 - 2059] Pages: 9

DOI: 10.2174/1381612825666190708192134

Price: $65

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Abstract

Background: Obesity frequently co-exists with type 2 diabetes mellitus (T2DM), leading to the socalled “diabesity epidemic”. The metabolic syndrome (MetS), a cluster of central obesity, hypertension, dysglycemia, insulin resistance and/or atherogenic dyslipidemia, as well as non-alcoholic fatty liver disease (NAFLD), a hepatic manifestation of MetS, has been associated with increased cardiovascular disease (CVD), T2DM and chronic kidney disease (CKD) incidence. However, the association between obesity, MetS (including NAFLD) and diabetic microvascular complications is less evident.

Methods: The present narrative review discusses the associations of obesity, MetS and NAFLD with diabetic kidney disease (DKD), diabetic retinopathy (DR) and diabetic peripheral neuropathy (DPN) as well as cardiac autonomic neuropathy (CAN). The available data on the effects of lifestyle measures and bariatric surgery on these diabetic complications are also briefly discussed.

Results: Overall, both obesity and MetS have been related to DKD, DR and DPN, although conflicting results exist. Links between NAFLD and diabetic microvascular complications have also been reported but data are still limited. Lifestyle intervention and bariatric surgery may prevent the development and/or progression of these microvascular complications but more evidence is needed.

Conclusion: Clinicians should be aware of the frequent co-existence of MetS and/or NAFLD in T2DM patients to prevent or treat these metabolic disorders, thus potentially minimizing the risk for both CVD and diabetic microvascular complications.

Keywords: Obesity, metabolic syndrome, non-alcoholic fatty liver disease, diabetic retinopathy, diabetic peripheral neuropathy, diabetic kidney disease.

« Previous Next »
[1]
Meldrum DR, Morris MA, Gambone JC. Obesity pandemic: causes, consequences, and solutions-but do we have the will? Fertil Steril 2017; 107(4): 833-9.
[http://dx.doi.org/10.1016/j.fertnstert.2017.02.104] [PMID: 28292617]
[2]
Bhupathiraju SN, Hu FB. Epidemiology of obesity and diabetes and their cardiovascular complications. Circ Res 2016; 118(11): 1723-35.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306825] [PMID: 27230638]
[3]
Ndumele CE, Matsushita K, Lazo M, et al. Obesity and subtypes of incident cardiovascular disease. J Am Heart Assoc 2016; 5(8): e003921.
[http://dx.doi.org/10.1161/JAHA.116.003921] [PMID: 27468925]
[4]
Katsiki N, Athyros VG, Mikhailidis DP. Does metabolic syndrome influence outcome following percutaneous coronary intervention? Angiology 2011; 62(6): 437-9.
[http://dx.doi.org/10.1177/0003319710394166] [PMID: 21421618]
[5]
Gluba A, Mikhailidis DP, Lip GY, Hannam S, Rysz J, Banach M. Metabolic syndrome and renal disease. Int J Cardiol 2013; 164(2): 141-50.
[http://dx.doi.org/10.1016/j.ijcard.2012.01.013] [PMID: 22305775]
[6]
Katsiki N, Athyros VG, Karagiannis A, Mikhailidis DP. Metabolic syndrome and non-cardiac vascular diseases: An update from human studies. Curr Pharm Des 2014; 20(31): 4944-52.
[http://dx.doi.org/10.2174/1381612819666131206100750] [PMID: 24320038]
[7]
Katsiki N, Athyros VG, Karagiannis A, Mikhailidis DP. Characteristics other than the diagnostic criteria associated with metabolic syndrome: An overview. Curr Vasc Pharmacol 2014; 12(4): 627-41.
[http://dx.doi.org/10.2174/15701611113119990131] [PMID: 23627982]
[8]
Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: Diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 1998; 15(7): 539-53.
[http://dx.doi.org/10.1002/(SICI)1096-9136(199807)15:7<539:AID-DIA668>3.0.CO;2-S] [PMID: 9686693]
[9]
Third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high bloodcholesterol in adults (adult treatment panel III) final report. Circulation 2002; 106(25): 3143-421.
[http://dx.doi.org/10.1161/circ.106.25.3143] [PMID: 12485966]
[10]
Alberti KG, Zimmet P, Shaw J. The metabolic syndrome--a new worldwide definition. Lancet 2005; 366(9491): 1059-62.
[http://dx.doi.org/10.1016/S0140-6736(05)67402-8] [PMID: 16182882]
[11]
Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome: An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005; 112(17): 2735-52.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.105.169404] [PMID: 16157765]
[12]
Katsiki N, Athyros VG, Mikhailidis DP. Metabolic syndrome: Different definitions and gender-specific associations with cardiovascular risk factors. Diab Vasc Dis Res 2015; 12(6): 471-2.
[http://dx.doi.org/10.1177/1479164115598913] [PMID: 26316574]
[13]
Lioudaki E, Vrentzos GE, Mavrogeni H, et al. Prevalence of metabolic syndrome according to different definitions in a hypertensive population. Angiology 2012; 63(1): 39-47.
[http://dx.doi.org/10.1177/0003319711407303] [PMID: 21555311]
[14]
Athyros VG, Ganotakis ES, Tziomalos K, et al. Comparison of four definitions of the metabolic syndrome in a Greek (Mediterranean) population. Curr Med Res Opin 2010; 26(3): 713-9.
[http://dx.doi.org/10.1185/03007991003590597] [PMID: 20078335]
[15]
Kolovou GD, Anagnostopoulou KK, Salpea KD, Mikhailidis DP. The prevalence of metabolic syndrome in various populations. Am J Med Sci 2007; 333(6): 362-71.
[http://dx.doi.org/10.1097/MAJ.0b013e318065c3a1] [PMID: 17570989]
[16]
Milionis HJ, Kostapanos MS, Liberopoulos EN, et al. Different definitions of the metabolic syndrome and risk of first-ever acute ischaemic non-embolic stroke in elderly subjects. Int J Clin Pract 2007; 61(4): 545-51.
[http://dx.doi.org/10.1111/j.1742-1241.2006.01269.x] [PMID: 17394429]
[17]
Anagnostis P. Metabolic syndrome in the Mediterranean region: Current status. Indian J Endocrinol Metab 2012; 16(1): 72-80.
[http://dx.doi.org/10.4103/2230-8210.91195] [PMID: 22276255]
[18]
Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009; 120(16): 1640-5.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.192644] [PMID: 19805654]
[19]
Katsiki N, Perez-Martinez P, Anagnostis P, Mikhailidis DP, Karagiannis A. Is nonalcoholic fatty liver disease indeed the hepatic manifestation of metabolic syndrome? Curr Vasc Pharmacol 2018; 16(3): 219-27.
[http://dx.doi.org/10.2174/1570161115666170621075619] [PMID: 28669328]
[20]
Mullish BH, Forlano R, Manousou P, Mikhailidis DP. Non-alcoholic fatty liver disease and cardiovascular risk: An update. Expert Rev Gastroenterol Hepatol 2018; 12(12): 1175-7.
[http://dx.doi.org/10.1080/17474124.2018.1533117] [PMID: 30791787]
[21]
Katsiki N, Athyros VG, Karagiannis A, Wierzbicki AS, Mikhailidis DP. Should we expand the concept of coronary heart disease equivalents? Curr Opin Cardiol 2014; 29(4): 389-95.
[http://dx.doi.org/10.1097/HCO.0000000000000068] [PMID: 25029454]
[22]
Katsiki N, Athyros VG, Mikhailidis DP. Non-alcoholic fatty liver disease in patients with type 2 diabetes mellitus: Effects of statins and antidiabetic drugs. J Diabetes Complications 2017; 31(3): 521-2.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.12.006] [PMID: 28089090]
[23]
Katsiki N, Mikhailidis DP, Mantzoros CS. Non-alcoholic fatty liver disease and dyslipidemia: An update. Metabolism 2016; 65(8): 1109-23.
[http://dx.doi.org/10.1016/j.metabol.2016.05.003] [PMID: 27237577]
[24]
Athyros VG, Tziomalos K, Katsiki N, Doumas M, Karagiannis A, Mikhailidis DP. Cardiovascular risk across the histological spectrum and the clinical manifestations of non-alcoholic fatty liver disease: An update. World J Gastroenterol 2015; 21(22): 6820-34.
[http://dx.doi.org/10.3748/wjg.v21.i22.6820] [PMID: 26078558]
[25]
Athyros VG, Mikhailidis DP. High incidence of metabolic syndrome further increases cardiovascular risk in patients with type 2 diabetes. Implications for everyday practice. J Diabetes Complications 2016; 30(1): 9-11.
[http://dx.doi.org/10.1016/j.jdiacomp.2015.07.012] [PMID: 26275865]
[26]
Sharma K. Obesity and Diabetic Kidney Disease: Role of Oxidant Stress and Redox Balance. Antioxid Redox Signal 2016; 25(4): 208-16.
[http://dx.doi.org/10.1089/ars.2016.6696] [PMID: 26983586]
[27]
Maric C, Hall JE. Obesity, metabolic syndrome and diabetic nephropathy. Contrib Nephrol 2011; 170: 28-35.
[http://dx.doi.org/10.1159/000324941] [PMID: 21659755]
[28]
Ruan X, Guan Y. Metabolic syndrome and chronic kidney disease. J Diabetes 2009; 1(4): 236-45.
[http://dx.doi.org/10.1111/j.1753-0407.2009.00042.x] [PMID: 20923524]
[29]
Hill CJ, Cardwell CR, Maxwell AP, et al. Obesity and kidney disease in type 1 and 2 diabetes: An analysis of the National Diabetes Audit. QJM 2013; 106(10): 933-42.
[http://dx.doi.org/10.1093/qjmed/hct123] [PMID: 23696677]
[30]
Man REK, Gan ATL, Fenwick EK, et al. The relationship between generalized and abdominal obesity with diabetic kidney disease in type 2 diabetes: A multiethnic asian study and meta-analysis. Nutrients 2018; 10(11): 10.
[http://dx.doi.org/10.3390/nu10111685] [PMID: 30400648]
[31]
Mohammedi K, Chalmers J, Herrington W, et al. Associations between body mass index and the risk of renal events in patients with type 2 diabetes. Nutr Diabetes 2018; 8(1): 7.
[http://dx.doi.org/10.1038/s41387-017-0012-y] [PMID: 29343817]
[32]
Chung HF, Al Mamun A, Huang MC, et al. Obesity, weight change, and chronic kidney disease in patients with type 2 diabetes mellitus: A longitudinal study in Taiwan. J Diabetes 2017; 9(11): 983-93.
[http://dx.doi.org/10.1111/1753-0407.12514] [PMID: 27976508]
[33]
Ma CM, Wang R, Liu XL, Lu N, Lu Q, Yin FZ. The relationship between hypertriglyceridemic waist phenotype and early diabetic nephropathy in type 2 diabetes. Cardiorenal Med 2017; 7(4): 295-300.
[http://dx.doi.org/10.1159/000477828] [PMID: 29118768]
[34]
Todd JN, Dahlström EH, Salem RM, et al. Genetic evidence for a causal role of obesity in diabetic kidney disease. Diabetes 2015; 64(12): 4238-46.
[http://dx.doi.org/10.2337/db15-0254] [PMID: 26307587]
[35]
de Boer IH, Sibley SD, Kestenbaum B, et al. Central obesity, incident microalbuminuria, and change in creatinine clearance in the epidemiology of diabetes interventions and complications study. J Am Soc Nephrol 2007; 18(1): 235-43.
[http://dx.doi.org/10.1681/ASN.2006040394] [PMID: 17151331]
[36]
Kittiskulnam P, Thokanit NS, Katavetin P, et al. The magnitude of obesity and metabolic syndrome among diabetic chronic kidney disease population: A nationwide study. PLoS One 2018; 13(5): e0196332.
[http://dx.doi.org/10.1371/journal.pone.0196332] [PMID: 29742114]
[37]
Huang WH, Chen CY, Lin JL, Lin-Tan DT, Hsu CW, Yen TH. High body mass index reduces glomerular filtration rate decline in type II diabetes mellitus patients with stage 3 or 4 chronic kidney disease. Medicine (Baltimore) 2014; 93(7): e41.
[http://dx.doi.org/10.1097/MD.0000000000000041] [PMID: 25101985]
[38]
Bentata Y, Latrech H, Abouqal R. Does body mass index influence the decline of glomerular filtration rate in diabetic type 2 patients with diabetic nephropathy in a developing country? Ren Fail 2014; 36(6): 838-46.
[http://dx.doi.org/10.3109/0886022X.2014.899472] [PMID: 24673339]
[39]
Mohsen A, Brown R, Hoefield R, et al. Body mass index has no effect on rate of progression of chronic kidney disease in subjects with type 2 diabetes mellitus. J Nephrol 2012; 25(3): 384-93.
[http://dx.doi.org/10.5301/jn.5000062] [PMID: 22241634]
[40]
Chen HM, Shen WW, Ge YC, Zhang YD, Xie HL, Liu ZH. The relationship between obesity and diabetic nephropathy in China. BMC Nephrol 2013; 14: 69.
[http://dx.doi.org/10.1186/1471-2369-14-69] [PMID: 23521842]
[41]
Ruggenenti P, Abbate M, Ruggiero B, et al. Renal and Systemic Effects of Calorie Restriction in Patients With Type 2 Diabetes With Abdominal Obesity: A Randomized Controlled Trial. Diabetes 2017; 66(1): 75-86.
[http://dx.doi.org/10.2337/db16-0607] [PMID: 27634224]
[42]
Onyenwenyi C, Ricardo AC. Impact of Lifestyle Modification on Diabetic Kidney Disease. Curr Diab Rep 2015; 15(9): 60.
[http://dx.doi.org/10.1007/s11892-015-0632-3] [PMID: 26194155]
[43]
Docherty NG, Canney AL, le Roux CW. Weight loss interventions and progression of diabetic kidney disease. Curr Diab Rep 2015; 15(8): 55.
[http://dx.doi.org/10.1007/s11892-015-0625-2] [PMID: 26122095]
[44]
Effect of a long-term behavioural weight loss intervention on nephropathy in overweight or obese adults with type 2 diabetes: A secondary analysis of the Look AHEAD randomised clinical trial. Lancet Diabetes Endocrinol 2014; 2(10): 801-9.
[http://dx.doi.org/10.1016/S2213-8587(14)70156-1] [PMID: 25127483]
[45]
Larina II, Severina AS, Shamkhalova MS, Shestakova MV. Renal experiences of bariatric surgery in patients with type 2 diabetes mellitus. Ter Arkh 2018; 90(10): 99-108.
[PMID: 30701804]
[46]
Nair M, le Roux CW, Docherty NG. Mechanisms underpinning remission of albuminuria following bariatric surgery. Curr Opin Endocrinol Diabetes Obes 2016; 23(5): 366-72.
[http://dx.doi.org/10.1097/MED.0000000000000279] [PMID: 27584009]
[47]
Young L, Nor Hanipah Z, Brethauer SA, Schauer PR, Aminian A. Long-term impact of bariatric surgery in diabetic nephropathy. Surg Endosc 2019; 33(5): 1654-60.
[PMID: 30251143]
[48]
Heneghan HM, Cetin D, Navaneethan SD, Orzech N, Brethauer SA, Schauer PR. Effects of bariatric surgery on diabetic nephropathy after 5 years of follow-up. Surg Obes Relat Dis 2013; 9(1): 7-14.
[http://dx.doi.org/10.1016/j.soard.2012.08.016] [PMID: 23211651]
[49]
O’Brien R, Johnson E, Haneuse S, et al. Microvascular Outcomes in Patients With Diabetes After Bariatric Surgery Versus Usual Care: A Matched Cohort Study. Ann Intern Med 2018; 169(5): 300-10.
[http://dx.doi.org/10.7326/M17-2383] [PMID: 30083761]
[50]
Billeter AT, Scheurlen KM, Probst P, et al. Meta-analysis of metabolic surgery versus medical treatment for microvascular complications in patients with type 2 diabetes mellitus. Br J Surg 2018; 105(3): 168-81.
[http://dx.doi.org/10.1002/bjs.10724] [PMID: 29405276]
[51]
Zhou X, Li L, Kwong JS, Yu J, Li Y, Sun X. Impact of bariatric surgery on renal functions in patients with type 2 diabetes: Systematic review of randomized trials and observational studies. Surg Obes Relat Dis 2016; 12(10): 1873-82.
[http://dx.doi.org/10.1016/j.soard.2016.05.003] [PMID: 27421689]
[52]
Upala S, Wijarnpreecha K, Congrete S, Rattanawong P, Sanguankeo A. Bariatric surgery reduces urinary albumin excretion in diabetic nephropathy: A systematic review and meta-analysis. Surg Obes Relat Dis 2016; 12(5): 1037-44.
[http://dx.doi.org/10.1016/j.soard.2015.11.019] [PMID: 26948447]
[53]
Friedman AN, Wolfe B. Is Bariatric Surgery an Effective Treatment for Type II Diabetic Kidney Disease? Clin J Am Soc Nephrol 2016; 11(3): 528-35.
[http://dx.doi.org/10.2215/CJN.07670715] [PMID: 26450931]
[54]
Moehlecke M, Leitão CB, Kramer CK, et al. Effect of metabolic syndrome and of its individual components on renal function of patients with type 2 diabetes mellitus. Braz J Med Biol Res 2010; 43(7): 687-93.
[http://dx.doi.org/10.1590/S0100-879X2010007500054] [PMID: 20549138]
[55]
Sheikhbahaei S, Fotouhi A, Hafezi-Nejad N, Nakhjavani M, Esteghamati A. Serum uric acid, the metabolic syndrome, and the risk of chronic kidney disease in patients with type 2 diabetes. Metab Syndr Relat Disord 2014; 12(2): 102-9.
[http://dx.doi.org/10.1089/met.2013.0119] [PMID: 24447037]
[56]
Raman R, Gupta A, Pal SS, et al. Prevalence of Metabolic Syndrome and its influence on microvascular complications in the Indian population with Type 2 Diabetes Mellitus. Sankara Nethralaya Diabetic Retinopathy Epidemiology And Molecular Genetic Study (SN-DREAMS, report 14). Diabetol Metab Syndr 2010; 2: 67.
[http://dx.doi.org/10.1186/1758-5996-2-67] [PMID: 21067623]
[57]
Bianchi C, Penno G, Daniele G, et al. The metabolic syndrome is related to albuminuria in Type 2 diabetes. Diabet Med 2008; 25(12): 1412-8.
[http://dx.doi.org/10.1111/j.1464-5491.2008.02603.x] [PMID: 19046239]
[58]
Billow A, Anjana RM, Ngai M, et al. Prevalence and clinical profile of metabolic syndrome among type 1 diabetes mellitus patients in southern India. J Diabetes Complications 2015; 29(5): 659-64.
[http://dx.doi.org/10.1016/j.jdiacomp.2015.03.014] [PMID: 25899474]
[59]
Thorn LM, Forsblom C, Fagerudd J, et al. Metabolic syndrome in type 1 diabetes: Association with diabetic nephropathy and glycemic control (the FinnDiane study). Diabetes Care 2005; 28(8): 2019-24.
[http://dx.doi.org/10.2337/diacare.28.8.2019] [PMID: 16043748]
[60]
Thorn LM, Forsblom C, Wadén J, et al. Metabolic syndrome as a risk factor for cardiovascular disease, mortality, and progression of diabetic nephropathy in type 1 diabetes. Diabetes Care 2009; 32(5): 950-2.
[http://dx.doi.org/10.2337/dc08-2022] [PMID: 19196885]
[61]
Thomas B. The Global Burden of Diabetic Kidney Disease: Time Trends and Gender Gaps. Curr Diab Rep 2019; 19(4): 18.
[http://dx.doi.org/10.1007/s11892-019-1133-6] [PMID: 30826889]
[62]
Duran-Perez EG, Almeda-Valdes P, Cuevas-Ramos D, Campos-Barrera E, Muñoz-Hernandez L, Gomez-Perez FJ. Treatment of metabolic syndrome slows progression of diabetic nephropathy. Metab Syndr Relat Disord 2011; 9(6): 483-9.
[http://dx.doi.org/10.1089/met.2011.0056] [PMID: 21875335]
[63]
Laranjinha I, Matias P, Mateus S, et al. Diabetic kidney disease: Is there a non-albuminuric phenotype in type 2 diabetic patients? Nefrologia 2016; 36(5): 503-9.
[http://dx.doi.org/10.1016/j.nefro.2016.03.025] [PMID: 27445098]
[64]
Targher G, Lonardo A, Byrne CD. Nonalcoholic fatty liver disease and chronic vascular complications of diabetes mellitus. Nat Rev Endocrinol 2018; 14(2): 99-114.
[http://dx.doi.org/10.1038/nrendo.2017.173] [PMID: 29286050]
[65]
Orlić L, Mikolasevic I, Bagic Z, Racki S, Stimac D, Milic S. Chronic kidney disease and nonalcoholic Fatty liver disease-is there a link? Gastroenterol Res Pract 2014; 2014: 847539.
[http://dx.doi.org/10.1155/2014/847539] [PMID: 24729784]
[66]
Jia G, Di F, Wang Q, et al. Non-Alcoholic Fatty Liver Disease Is a Risk Factor for the Development of Diabetic Nephropathy in Patients with Type 2 Diabetes Mellitus. PLoS One 2015; 10(11): e0142808.
[http://dx.doi.org/10.1371/journal.pone.0142808] [PMID: 26566287]
[67]
Targher G, Bertolini L, Rodella S, et al. Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia 2008; 51(3): 444-50.
[http://dx.doi.org/10.1007/s00125-007-0897-4] [PMID: 18058083]
[68]
Targher G, Mantovani A, Pichiri I, et al. Nonalcoholic fatty liver disease is independently associated with an increased incidence of chronic kidney disease in patients with type 1 diabetes. Diabetes Care 2014; 37(6): 1729-36.
[http://dx.doi.org/10.2337/dc13-2704] [PMID: 24696459]
[69]
Yeung MW, Wong GL, Choi KC, et al. Advanced liver fibrosis but not steatosis is independently associated with albuminuria in Chinese patients with type 2 diabetes. J Hepatol 2017.S0168- 8278(17)32334-6.
[PMID: 28989092]
[70]
Chinnadurai R, Chrysochou C, Kalra PA. Increased Risk for Cardiovascular Events in Patients with Diabetic Kidney Disease and Non-Alcoholic Fatty Liver Disease. Nephron 2019; 141(1): 24-30.
[http://dx.doi.org/10.1159/000493472] [PMID: 30384370]
[71]
Wijarnpreecha K, Thongprayoon C, Boonpheng B, et al. Nonalcoholic fatty liver disease and albuminuria: A systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2018; 30(9): 986-94.
[http://dx.doi.org/10.1097/MEG.0000000000001169] [PMID: 29787418]
[72]
Jenks SJ, Conway BR, Hor TJ, et al. Hepatic steatosis and non-alcoholic fatty liver disease are not associated with decline in renal function in people with Type 2 diabetes. Diabet Med 2014; 31(9): 1039-46.
[http://dx.doi.org/10.1111/dme.12456] [PMID: 24684407]
[73]
Zhan YT, Zhang C, Li L, Bi CS, Song X, Zhang ST. Non-alcoholic fatty liver disease is not related to the incidence of diabetic nephropathy in Type 2 Diabetes. Int J Mol Sci 2012; 13(11): 14698-706.
[http://dx.doi.org/10.3390/ijms131114698] [PMID: 23203089]
[74]
Zhu W, Wu Y, Meng YF, Xing Q, Tao JJ, Lu J. Association of obesity and risk of diabetic retinopathy in diabetes patients: A meta-analysis of prospective cohort studies. Medicine (Baltimore) 2018; 97(32): e11807.
[http://dx.doi.org/10.1097/MD.0000000000011807] [PMID: 30095648]
[75]
Zhou Y, Zhang Y, Shi K, Wang C. Body mass index and risk of diabetic retinopathy: A meta-analysis and systematic review. Medicine (Baltimore) 2017; 96(22): e6754.
[http://dx.doi.org/10.1097/MD.0000000000006754] [PMID: 28562529]
[76]
Man RE, Sabanayagam C, Chiang PP, et al. Differential Association of Generalized and Abdominal Obesity With Diabetic Retinopathy in Asian Patients With Type 2 Diabetes. JAMA Ophthalmol 2016; 134(3): 251-7.
[http://dx.doi.org/10.1001/jamaophthalmol.2015.5103] [PMID: 26720805]
[77]
Raman R, Rani PK, Gnanamoorthy P, Sudhir RR, Kumaramanikavel G, Sharma T. Association of obesity with diabetic retinopathy: Sankara Nethralaya Diabetic Retinopathy Epidemiology and Molecular Genetics Study (SN-DREAMS Report no. 8). Acta Diabetol 2010; 47(3): 209-15.
[http://dx.doi.org/10.1007/s00592-009-0113-8] [PMID: 19326040]
[78]
van Leiden HA, Dekker JM, Moll AC, et al. Risk factors for incident retinopathy in a diabetic and nondiabetic population: The Hoorn study. Arch Ophthalmol 2003; 121(2): 245-51.
[http://dx.doi.org/10.1001/archopht.121.2.245] [PMID: 12583792]
[79]
Moh A, Neelam K, Zhang X, et al. Excess visceral adiposity is associated with diabetic retinopathy in a multiethnic Asian cohort with longstanding type 2 diabetes. Endocr Res 2018; 43(3): 186-94.
[http://dx.doi.org/10.1080/07435800.2018.1451541] [PMID: 29624091]
[80]
Merlotti C, Ceriani V, Morabito A, Pontiroli AE. Bariatric surgery and diabetic retinopathy: A systematic review and meta-analysis of controlled clinical studies. Obes Rev 2017; 18(3): 309-16.
[http://dx.doi.org/10.1111/obr.12490] [PMID: 28085992]
[81]
Cheung D, Switzer NJ, Ehmann D, Rudnisky C, Shi X, Karmali S. The Impact of Bariatric Surgery on Diabetic Retinopathy: A Systematic Review and Meta-Analysis. Obes Surg 2015; 25(9): 1604-9.
[http://dx.doi.org/10.1007/s11695-014-1539-9] [PMID: 25515499]
[82]
Kim YJ, Kim BH, Choi BM, Sun HJ, Lee SJ, Choi KS. Bariatric surgery is associated with less progression of diabetic retinopathy: A systematic review and meta-analysis. Surg Obes Relat Dis 2017; 13(2): 352-60.
[http://dx.doi.org/10.1016/j.soard.2016.10.002] [PMID: 27919835]
[83]
Murphy R, Jiang Y, Booth M, et al. Progression of diabetic retinopathy after bariatric surgery. Diabet Med 2015; 32(9): 1212-20.
[http://dx.doi.org/10.1111/dme.12727] [PMID: 25689226]
[84]
Zhou Y, Wang C, Shi K, Yin X. Relation of metabolic syndrome and its components with risk of diabetic retinopathy: A meta-analysis of observational studies. Medicine (Baltimore) 2018; 97(38): e12433.
[http://dx.doi.org/10.1097/MD.0000000000012433] [PMID: 30235724]
[85]
Mbata O, Abo El-Magd NF, El-Remessy AB. Obesity, metabolic syndrome and diabetic retinopathy: Beyond hyperglycemia. World J Diabetes 2017; 8: 317-29.
[86]
Zhang X, Cui X, Li F, et al. Association between diabetes mellitus with metabolic syndrome and diabetic microangiopathy. Exp Ther Med 2014; 8(6): 1867-73.
[http://dx.doi.org/10.3892/etm.2014.1992] [PMID: 25371746]
[87]
Lee MY, Hsiao PJ, Huang JC, Hsu WH, Chen SC, Shin SJ. Association Between Metabolic Syndrome and Microvascular and Macrovascular Disease in Type 2 Diabetic Mellitus. Am J Med Sci 2018; 355(4): 342-9.
[http://dx.doi.org/10.1016/j.amjms.2017.12.004] [PMID: 29661347]
[88]
Gao L, Xin Z, Yuan MX, et al. High Prevalence of Diabetic Retinopathy in Diabetic Patients Concomitant with Metabolic Syndrome. PLoS One 2016; 11(1): e0145293.
[http://dx.doi.org/10.1371/journal.pone.0145293] [PMID: 26745177]
[89]
Karaca C, Karaca Z. Beyond Hyperglycemia, Evidence for Retinal Neurodegeneration in Metabolic Syndrome. Invest Ophthalmol Vis Sci 2018; 59(3): 1360-7.
[http://dx.doi.org/10.1167/iovs.17-23376] [PMID: 29625459]
[90]
Kawasaki R, Tielsch JM, Wang JJ, et al. The metabolic syndrome and retinal microvascular signs in a Japanese population: The Funagata study. Br J Ophthalmol 2008; 92(2): 161-6.
[http://dx.doi.org/10.1136/bjo.2007.127449] [PMID: 17965107]
[91]
Liu L, Yue S, Wu J, et al. Prevalence and risk factors of retinopathy in patients with or without metabolic syndrome: A population-based study in Shenyang. BMJ Open 2015; 5(12): e008855.
[http://dx.doi.org/10.1136/bmjopen-2015-008855] [PMID: 26667013]
[92]
Kim TK, Won JY, Shin JA, Park YM, Yim HW, Park YH. The association of metabolic syndrome with diabetic retinopathy: The korean national health and nutrition examination survey 2008-2012. PLoS One 2016; 11(6): e0157006.
[http://dx.doi.org/10.1371/journal.pone.0157006] [PMID: 27275953]
[93]
Chen JJ, Wendel LJ, Birkholz ES, et al. The metabolic syndrome and severity of diabetic retinopathy. Clin Ophthalmol 2015; 9: 757-64.
[http://dx.doi.org/10.2147/OPTH.S80355] [PMID: 25995613]
[94]
Lin TY, Chen YJ, Chen WL, Peng TC. The Relationship between Nonalcoholic Fatty Liver Disease and Retinopathy in NHANES III. PLoS One 2016; 11(11): e0165970.
[http://dx.doi.org/10.1371/journal.pone.0165970] [PMID: 27802330]
[95]
Kim BY, Jung CH, Mok JO, Kang SK, Kim CH. Prevalences of diabetic retinopathy and nephropathy are lower in Korean type 2 diabetic patients with non-alcoholic fatty liver disease. J Diabetes Investig 2014; 5(2): 170-5.
[http://dx.doi.org/10.1111/jdi.12139] [PMID: 24843757]
[96]
Lv WS, Sun RX, Gao YY, et al. Nonalcoholic fatty liver disease and microvascular complications in type 2 diabetes. World J Gastroenterol 2013; 19(20): 3134-42.
[http://dx.doi.org/10.3748/wjg.v19.i20.3134] [PMID: 23716995]
[97]
Targher G, Bertolini L, Chonchol M, et al. Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and retinopathy in type 1 diabetic patients. Diabetologia 2010; 53(7): 1341-8.
[http://dx.doi.org/10.1007/s00125-010-1720-1] [PMID: 20369224]
[98]
Andersen ST, Witte DR, Dalsgaard EM, et al. Risk Factors for Incident Diabetic Polyneuropathy in a Cohort With Screen-Detected Type 2 Diabetes Followed for 13 Years: Addition-Denmark. Diabetes Care 2018; 41(5): 1068-75.
[http://dx.doi.org/10.2337/dc17-2062] [PMID: 29487078]
[99]
Salvotelli L, Stoico V, Perrone F, et al. Prevalence of neuropathy in type 2 diabetic patients and its association with other diabetes complications: The verona diabetic foot screening program. J Diabetes Complications 2015; 29(8): 1066-70.
[http://dx.doi.org/10.1016/j.jdiacomp.2015.06.014] [PMID: 26227575]
[100]
Bulum T, Blaslov K, Duvnjak L. The use of anthropometric measurements of obesity in prediction of microvascular complications in obese type 2 diabetic patients. Acta Clin Croat 2016; 55(2): 217-23.
[http://dx.doi.org/10.20471/acc.2016.55.02.06] [PMID: 28394108]
[101]
Wang DD, Bakhotmah BA, Hu FB, Alzahrani HA. Prevalence and correlates of diabetic peripheral neuropathy in a Saudi Arabic population: A cross-sectional study. PLoS One 2014; 9(9): e106935.
[http://dx.doi.org/10.1371/journal.pone.0106935] [PMID: 25184511]
[102]
Jaiswal M, Divers J, Dabelea D, et al. Prevalence of and risk factors for diabetic peripheral neuropathy in youth with type 1 and type 2 diabetes: SEARCH for diabetes in youth study. Diabetes Care 2017; 40(9): 1226-32.
[http://dx.doi.org/10.2337/dc17-0179] [PMID: 28674076]
[103]
Ylitalo KR, Sowers M, Heeringa S. Peripheral vascular disease and peripheral neuropathy in individuals with cardiometabolic clustering and obesity: National Health and Nutrition Examination Survey 2001-2004. Diabetes Care 2011; 34(7): 1642-7.
[http://dx.doi.org/10.2337/dc10-2150] [PMID: 21593304]
[104]
Papanas N, Ziegler D. Risk factors and comorbidities in diabetic neuropathy: An update 2015. Rev Diabet Stud 2015; 12(1-2): 48-62.
[http://dx.doi.org/10.1900/RDS.2015.12.48] [PMID: 26676661]
[105]
Smith AG, Singleton JR. Obesity and hyperlipidemia are risk factors for early diabetic neuropathy. J Diabetes Complications 2013; 27(5): 436-42.
[http://dx.doi.org/10.1016/j.jdiacomp.2013.04.003] [PMID: 23731827]
[106]
Sujanitha V, Sivansuthan S, Selvakaran P, Parameswaran P. Overweight, obesity and chronic complications of diabetes mellitus in patients attending Diabetic Centre, Teaching Hospital, Jaffna, Sri Lanka. Ceylon Med J 2015; 60(3): 94-6.
[http://dx.doi.org/10.4038/cmj.v60i3.8065] [PMID: 26520862]
[107]
Zeve JL, Tomaz CA, Nassif PA, Lima JH, Sansana LR, Zeve CH. Obese patients with diabetes mellitus type 2 undergoing gastric bypass in Roux-en-Y: Analysis of results and its influence in complications. Arq Bras Cir Dig 2013; 26(Suppl. 1): 47-52.
[http://dx.doi.org/10.1590/S0102-67202013000600011] [PMID: 24463899]
[108]
Müller-Stich BP, Fischer L, Kenngott HG, et al. Gastric bypass leads to improvement of diabetic neuropathy independent of glucose normalization--results of a prospective cohort study (DiaSurg 1 study). Ann Surg 2013; 258(5): 760-5.
[http://dx.doi.org/10.1097/SLA.0b013e3182a618b2] [PMID: 23979278]
[109]
Jackson S, le Roux CW, Docherty NG. Bariatric surgery and microvascular complications of type 2 diabetes mellitus. Curr Atheroscler Rep 2014; 16(11): 453.
[http://dx.doi.org/10.1007/s11883-014-0453-x] [PMID: 25239035]
[110]
Cohen R, Pechy F, Petry T, Correa JL, Caravatto PP, Tzanno-Martins C. Bariatric and metabolic surgery and microvascular complications of type 2 diabetes mellitus. J Bras Nefrol 2015; 37(3): 399-409.
[http://dx.doi.org/10.5935/0101-2800.20150061] [PMID: 26398651]
[111]
Stino AM, Smith AG. Peripheral neuropathy in prediabetes and the metabolic syndrome. J Diabetes Investig 2017; 8(5): 646-55.
[http://dx.doi.org/10.1111/jdi.12650] [PMID: 28267267]
[112]
Grisold A, Callaghan BC, Feldman EL. Mediators of diabetic neuropathy: Is hyperglycemia the only culprit? Curr Opin Endocrinol Diabetes Obes 2017; 24(2): 103-11.
[http://dx.doi.org/10.1097/MED.0000000000000320] [PMID: 28098594]
[113]
Bonadonna R, Cucinotta D, Fedele D, Riccardi G, Tiengo A. The metabolic syndrome is a risk indicator of microvascular and macrovascular complications in diabetes: Results from Metascreen, a multicenter diabetes clinic-based survey. Diabetes Care 2006; 29(12): 2701-7.
[http://dx.doi.org/10.2337/dc06-0942] [PMID: 17130208]
[114]
Cortez M, Singleton JR, Smith AG. Glucose intolerance, metabolic syndrome, and neuropathy. Handb Clin Neurol 2014; 126: 109-22.
[http://dx.doi.org/10.1016/B978-0-444-53480-4.00009-6] [PMID: 25410218]
[115]
Hanewinckel R, Drenthen J, Ligthart S, et al. Metabolic syndrome is related to polyneuropathy and impaired peripheral nerve function: A prospective population-based cohort study. J Neurol Neurosurg Psychiatry 2016; 87(12): 1336-42.
[http://dx.doi.org/10.1136/jnnp-2016-314171] [PMID: 27656045]
[116]
Zhou L, Li J, Ontaneda D, Sperling J. Metabolic syndrome in small fiber sensory neuropathy. J Clin Neuromuscul Dis 2011; 12(4): 235-43.
[http://dx.doi.org/10.1097/CND.0b013e3182196e3c] [PMID: 22361523]
[117]
Casellini CM, Vinik AI. Clinical manifestations and current treatment options for diabetic neuropathies. Endocr Pract 2007; 13(5): 550-66.
[http://dx.doi.org/10.4158/EP.13.5.550] [PMID: 17872358]
[118]
Iwasaki T, Togashi Y, Ohshige K, et al. Neither the presence of metabolic syndrome as defined by the IDF guideline nor an increased waist circumference increased the risk of microvascular or macrovascular complications in Japanese patients with type 2 diabetes. Diabetes Res Clin Pract 2008; 79(3): 427-32.
[http://dx.doi.org/10.1016/j.diabres.2007.10.035] [PMID: 18207278]
[119]
Yan LH, Mu B, Guan Y, et al. Assessment of the relationship between non-alcoholic fatty liver disease and diabetic complications. J Diabetes Investig 2016; 7(6): 889-94.
[http://dx.doi.org/10.1111/jdi.12518] [PMID: 27181828]
[120]
Mantovani A, Rigolon R, Mingolla L, et al. Nonalcoholic fatty liver disease is associated with an increased prevalence of distal symmetric polyneuropathy in adult patients with type 1 diabetes. J Diabetes Complications 2017; 31(6): 1021-6.
[http://dx.doi.org/10.1016/j.jdiacomp.2017.01.024] [PMID: 28254449]
[121]
Spallone V. Update on the Impact, Diagnosis and Management of Cardiovascular Autonomic Neuropathy in Diabetes: What Is Defined, What Is New, and What Is Unmet. Diabetes Metab J 2019; 43(1): 3-30.
[http://dx.doi.org/10.4093/dmj.2018.0259] [PMID: 30793549]
[122]
Katsilambros NL, Boulton AJ, Tentolouris N, Kokkinos A, Liatis S. Autonomic neuropathy in diabetes mellitus and obesity: An update. Exp Diabetes Res 2011; 2011: 607309.
[http://dx.doi.org/10.1155/2011/607309] [PMID: 22203830]
[123]
Vinik AI, Erbas T. Diabetic autonomic neuropathy. Handb Clin Neurol 2013; 117: 279-94.
[http://dx.doi.org/10.1016/B978-0-444-53491-0.00022-5] [PMID: 24095132]
[124]
Laitinen T, Lindström J, Eriksson J, et al. Cardiovascular autonomic dysfunction is associated with central obesity in persons with impaired glucose tolerance. Diabet Med 2011; 28(6): 699-704.
[http://dx.doi.org/10.1111/j.1464-5491.2011.03278.x] [PMID: 21388444]
[125]
Andersen ST, Witte DR, Fleischer J, et al. Risk Factors for the Presence and Progression of Cardiovascular Autonomic Neuropathy in Type 2 Diabetes: Addition-Denmark. Diabetes Care 2018; 41(12): 2586-94.
[http://dx.doi.org/10.2337/dc18-1411] [PMID: 30305347]
[126]
Jang EH, Kim NY, Park YM, et al. Influence of visceral adiposity on cardiovascular autonomic neuropathy in patients with type 2 diabetes mellitus. Diabetes Metab J 2012; 36(4): 285-92.
[http://dx.doi.org/10.4093/dmj.2012.36.4.285] [PMID: 22950060]
[127]
Cho YH, Craig ME, Jopling T, Chan A, Donaghue KC. Higher body mass index predicts cardiac autonomic dysfunction: A longitudinal study in adolescent type 1 diabetes. Pediatr Diabetes 2018; 19(4): 794-800.
[http://dx.doi.org/10.1111/pedi.12642] [PMID: 29383813]
[128]
Kseneva SI, Borodulina EV, Trifonova OY, Timofeev MS, Udut VV. Pathogenetic Mechanisms of Outbreak and Development of Cardiac Autonomic Neuropathy in Patients with Metabolic Syndrome. Bull Exp Biol Med 2017; 164(1): 10-4.
[http://dx.doi.org/10.1007/s10517-017-3914-8] [PMID: 29124537]
[129]
Stein PK, Barzilay JI, Domitrovich PP, et al. The relationship of heart rate and heart rate variability to non-diabetic fasting glucose levels and the metabolic syndrome: The Cardiovascular Health Study. Diabet Med 2007; 24(8): 855-63.
[http://dx.doi.org/10.1111/j.1464-5491.2007.02163.x] [PMID: 17403115]
[130]
Ziegler D, Strom A, Kupriyanova Y, et al. Association of Lower Cardiovagal Tone and Baroreflex Sensitivity With Higher Liver Fat Content Early in Type 2 Diabetes. J Clin Endocrinol Metab 2018; 103(3): 1130-8.
[http://dx.doi.org/10.1210/jc.2017-02294] [PMID: 29267946]
[131]
Virdis A, Masi S, Colucci R, et al. Microvascular Endothelial Dysfunction in Patients with Obesity. Curr Hypertens Rep 2019; 21(4): 32.
[http://dx.doi.org/10.1007/s11906-019-0930-2] [PMID: 30949772]
[132]
Foroughi M, Maghsoudi Z, Khayyatzadeh S, Ghiasvand R, Askari G, Iraj B. Relationship between non-alcoholic fatty liver disease and inflammation in patients with non-alcoholic fatty liver. Adv Biomed Res 2016; 5: 28.
[http://dx.doi.org/10.4103/2277-9175.176368] [PMID: 27014655]
[133]
Roebuck KA. Oxidant stress regulation of IL-8 and ICAM-1 gene expression: Differential activation and binding of the transcription factors AP-1 and NF-kappaB (Review). Int J Mol Med 1999; 4(3): 223-30.
[http://dx.doi.org/10.3892/ijmm.4.3.223] [PMID: 10425270]
[134]
Mima A. Inflammation and oxidative stress in diabetic nephropathy: New insights on its inhibition as new therapeutic targets. J Diabetes Res 2013; 2013: 248563.
[http://dx.doi.org/10.1155/2013/248563] [PMID: 23862164]
[135]
Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010; 107(9): 1058-70.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.223545] [PMID: 21030723]
[136]
Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes 2015; 6(3): 456-80.
[http://dx.doi.org/10.4239/wjd.v6.i3.456] [PMID: 25897356]
[137]
Bhatta A, Yao L, Xu Z, et al. Obesity-induced vascular dysfunction and arterial stiffening requires endothelial cell arginase 1. Cardiovasc Res 2017; 113(13): 1664-76.
[http://dx.doi.org/10.1093/cvr/cvx164] [PMID: 29048462]
[138]
Giugliano D, Ceriello A, Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care 1996; 19(3): 257-67.
[http://dx.doi.org/10.2337/diacare.19.3.257] [PMID: 8742574]
[139]
Barradas MA, Mikhailidis DP, Dandona P. The effect of non-esterified fatty acids on vascular ADP-degrading enzyme activity. Diabetes Res Clin Pract 1987; 3(1): 9-19.
[http://dx.doi.org/10.1016/S0168-8227(87)80003-7] [PMID: 3028742]
[140]
Lima Júnior JC, Moura-Assis A, Cintra RM, Quinaglia T, Velloso LA, Sposito AC. Central role of obesity in endothelial cell dysfunction and cardiovascular risk Rev Assoc Med Bras (1992) 2019; 65(1): 87-97.
[http://dx.doi.org/10.1590/1806-9282.65.1.87] [PMID: 30758424]
[141]
Steinberg HO, Baron AD. Vascular function, insulin resistance and fatty acids. Diabetologia 2002; 45(5): 623-34.
[http://dx.doi.org/10.1007/s00125-002-0800-2] [PMID: 12107742]
[142]
Virdis A, Santini F, Colucci R, et al. Vascular generation of tumor necrosis factor-α reduces nitric oxide availability in small arteries from visceral fat of obese patients. J Am Coll Cardiol 2011; 58(3): 238-47.
[http://dx.doi.org/10.1016/j.jacc.2011.01.050] [PMID: 21737013]
[143]
Bulló M, García-Lorda P, Megias I, Salas-Salvadó J. Systemic inflammation, adipose tissue tumor necrosis factor, and leptin expression. Obes Res 2003; 11(4): 525-31.
[http://dx.doi.org/10.1038/oby.2003.74] [PMID: 12690081]
[144]
Athyros VG, Tziomalos K, Karagiannis A, Anagnostis P, Mikhailidis DP. Should adipokines be considered in the choice of the treatment of obesity-related health problems? Curr Drug Targets 2010; 11(1): 122-35.
[http://dx.doi.org/10.2174/138945010790030992] [PMID: 20017725]
[145]
Li J, Shen X. Oxidative stress and adipokine levels were significantly correlated in diabetic patients with hyperglycemic crises. Diabetol Metab Syndr 2019; 11: 13.
[http://dx.doi.org/10.1186/s13098-019-0410-5] [PMID: 30774721]
[146]
Yuan HP, Sun L, Li XH, et al. Association of Adiponectin Polymorphism with Metabolic Syndrome Risk and Adiponectin Level with Stroke Risk: A Meta-Analysis. Sci Rep 2016; 6: 31945.
[http://dx.doi.org/10.1038/srep31945] [PMID: 27578536]
[147]
Anagnostis P, Athyros VG, Kita M, Karagiannis A. Is there any association between adiponectin gene polymorphisms and cardiovascular disease? Angiology 2013; 64(4): 253-6.
[http://dx.doi.org/10.1177/0003319712455686] [PMID: 23277634]
[148]
Wei L, Xiao Y, Li L, et al. The Susceptibility Genes in Diabetic Nephropathy. Kidney Dis (Basel) 2018; 4(4): 226-37.
[http://dx.doi.org/10.1159/000492633] [PMID: 30574499]

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