Skip to main content

Advertisement

SpringerLink
Log in

Physical activity and risk of diabetic retinopathy: a systematic review and meta-analysis

  • Review Article
  • Published:
Acta Diabetologica Aims and scope Submit manuscript

A Letter to the Editor to this article was published on 06 February 2020

Abstract

Aims

Diabetic retinopathy (DR) is an important microvascular complication of diabetes mellitus (DM) and a leading cause of visual impairment and blindness among people of working age. Physical activity (PA) or exercise is critical and beneficial for DM patients, whereas studies evaluating the relationship between PA and DR have yielded inconsistent and inconclusive results. The American Diabetes Association’s “Standards of Medical Care in Diabetes” has also pointed out the indeterminate roles of PA in DR prevention. The purpose of this systematic review and meta-analysis was to explore the association between PA and DR risk.

Methods

Medline (accessed by PubMed), EmBase, and Cochrane Library were systematically searched for studies up to June 2018, and the reference lists of the published articles were searched manually. The association between PA and DR risk was assessed using random-effect meta-analysis.

Results

Twenty-two studies were included in this meta-analysis. PA was found to have a protective association with DR [risk ratio (RR) = 0.94, 95% confidence interval (95% CI) 0.90–0.98, p = 0.005] in diabetic patients, and the impact was more pronounced on vision-threatening DR (RR = 0.89, 95% CI 0.80–0.98, p = 0.02). Sedentary behavior could increase the risk of DR (RR = 1.18, 95% CI 1.01–1.37, p = 0.04). Moderate-intensity PA was likely to have a slight protective effect (RR = 0.76, 95% CI 0.58–1.00, p = 0.05).

Conclusion

PA is associated with lower DR risk, and more studies should focus on the causality between them.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Stolk RP, Vingerling JR, de Jong PT et al (1995) Retinopathy, glucose, and insulin in an elderly population. The Rotterdam Study Diabetes 44(1):11–15

    CAS  PubMed  Google Scholar 

  2. Aiello LP, Gardner TW, King GL et al (1998) Diabetic retinopathy. Diabetes Care 21(1):143–156

    Article  CAS  PubMed  Google Scholar 

  3. Cho NH, Kirigia J, Mbanya JC et al (2017) IDF Diabetes Atlas. 8th edn. International Diabetes Federation (IDF). http://www.diabetesatlas.org. Accessed 12 Oct 2018

  4. Beagley J, Guariguata L, Weil C et al (2014) Global estimates of undiagnosed diabetes in adults. Diabetes Res Clin Pract 103(2):150–160

    Article  PubMed  Google Scholar 

  5. Guariguata L, Whiting DR, Hambleton I et al (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103(2):137–149

    Article  CAS  PubMed  Google Scholar 

  6. Song P, Yu J, Chan KY et al (2018) Prevalence, risk factors and burden of diabetic retinopathy in China: a systematic review and meta-analysis. J Glob Health 8(1):010803

    Article  PubMed  PubMed Central  Google Scholar 

  7. National Eye Institute (2010) Diabetic retinopathy. National eye institute (NEI). https://nei.nih.gov/eyedata/diabetic. Accessed 12 Oct 2018

  8. Dowse GK, Humphrey AR, Collins VR et al (1998) Prevalence and risk factors for diabetic retinopathy in the multiethnic population of Mauritius. Am J Epidemiol 147(5):448–457

    Article  CAS  PubMed  Google Scholar 

  9. Stratton IM, Kohner EM, Aldington SJ et al (2001) UKPDS 50: risk factors for incidence and progression of retinopathy in Type II diabetes over 6 years from diagnosis. Diabetologia 44(2):156–163

    Article  CAS  PubMed  Google Scholar 

  10. Atchison E, Barkmeier A (2016) The role of systemic risk factors in diabetic retinopathy. Curr Ophthalmol Rep 4(2):84–89

    Article  PubMed  PubMed Central  Google Scholar 

  11. American Diabetes Association (2018) Lifestyle management: standards of medical care in diabetes—2018. Diabetes Care 41:S38–S50

    Article  Google Scholar 

  12. Colberg SR, Sigal RJ, Yardley JE et al (2016) Physical activity/exercise and diabetes: a position statement of the American diabetes association. Diabetes Care 39(11):2065–2079

    Article  PubMed  PubMed Central  Google Scholar 

  13. Magliano DJ, Barr EL, Zimmet PZ et al (2008) Glucose indices, health behaviors, and incidence of diabetes in Australia: the Australian Diabetes, Obesity and Lifestyle Study. Diabetes Care 31(2):267–272

    Article  PubMed  Google Scholar 

  14. Praidou A, Harris M, Niakas D et al (2017) Physical activity and its correlation to diabetic retinopathy. J Diabetes Compl 31(2):456–461

    Article  Google Scholar 

  15. Janevic MR, McLaughlin SJ, Connell CM (2013) The association of diabetes complications with physical activity in a representative sample of older adults in the United States. Chronic Illn 9(4):251–257

    Article  PubMed  Google Scholar 

  16. Bener A, Al-Laftah F, Al-Hamaq AO et al (2014) A study of diabetes complications in an endogamous population: an emerging public health burden. Diabetes Metab Syndr 8(2):108–114

    Article  PubMed  Google Scholar 

  17. Dharmastuti DP, Agni AN, Widyaputri F et al (2018) Associations of physical activity and sedentary behaviour with vision-threatening diabetic retinopathy in indonesian population with type 2 diabetes mellitus: Jogjakarta Eye Diabetic Study in the Community (JOGED.COM). Ophthalmic Epidemiol 25(2):113–119

    Article  CAS  PubMed  Google Scholar 

  18. Chen Y, Sloan FA, Yashkin AP (2015) Adherence to diabetes guidelines for screening, physical activity and medication and onset of complications and death. J Diabetes Compl 29(8):1228–1233

    Article  Google Scholar 

  19. Loprinzi PD (2016) Association of accelerometer-assessed sedentary behavior with diabetic retinopathy in the United States. JAMA Ophthalmol 134(10):1197–1198

    Article  PubMed  Google Scholar 

  20. Cruickshanks KJ, Moss SE, Klein R et al (1995) Physical activity and the risk of progression of retinopathy or the development of proliferative retinopathy. Ophthalmology 102(8):1177–1182

    Article  CAS  PubMed  Google Scholar 

  21. Schneider SH, Khachadurian AK, Amorosa LF et al (1992) Ten-year experience with an exercise-based outpatient life-style modification program in the treatment of diabetes mellitus. Diabetes Care 15(11):1800–1810

    Article  CAS  PubMed  Google Scholar 

  22. Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535

    Article  PubMed  PubMed Central  Google Scholar 

  23. Wells G, Shea B, O’connell D et al (2014) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 12 Oct 2018

  24. Rostom A, Dube C, Cranney A et al (2004) Celiac disease. (Evidence Reports/Technology Assessments, No. 104). Agency for Healthcare Research and Quality (AHRQ), Rockville, US. https://www.ncbi.nlm.nih.gov/books/NBK35156/. Accessed 12 Oct 2018

  25. von Elm E, Altman DG, Egger M et al (2008) The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 61(4):344–349

    Article  Google Scholar 

  26. Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10(1):101–129

    Article  Google Scholar 

  27. Tobias A (1999) Assessing the influence of a single study in the meta-analysis estimate. Stata Tech Bull 47:15–17

    Google Scholar 

  28. Egger M, Davey Smith G, Schneider M et al (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101

    Article  CAS  PubMed  Google Scholar 

  30. Waden J, Forsblom C, Thorn LM et al (2008) Physical activity and diabetes complications in patients with type 1 diabetes: the Finnish Diabetic Nephropathy (FinnDiane) Study. Diabetes Care 31(2):230–232

    Article  PubMed  Google Scholar 

  31. Slotte JP (2013) Biological functions of sphingomyelins. Prog Lipid Res 52(4):424–437

    Article  CAS  PubMed  Google Scholar 

  32. Balducci S, Vulpiani MC, Pugliese L et al (2014) Effect of supervised exercise training on musculoskeletal symptoms and function in patients with type 2 diabetes: The Italian Diabetes Exercise Study (IDES). Acta Diabetol 51(4):647–654

    Article  PubMed  Google Scholar 

  33. Kuwata H, Okamura S, Hayashino Y et al (2017) Higher levels of physical activity are independently associated with a lower incidence of diabetic retinopathy in Japanese patients with type 2 diabetes: a prospective cohort study, Diabetes Distress and Care Registry at Tenri (DDCRT15). PLoS One 12(3):e0172890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. She C, Shang F, Zhou K et al (2017) Serum carotenoids and risks of diabetes and diabetic retinopathy in a Chinese Population Sample. Metallomics 17(4):287–297

    CAS  Google Scholar 

  35. Yan ZP, Ma JX (2016) Risk factors for diabetic retinopathy in northern Chinese patients with type 2 diabetes mellitus. Int J Ophthalmol 9(8):1194–1199

    PubMed  PubMed Central  Google Scholar 

  36. Bohn B, Herbst A, Pfeifer M et al (2015) Impact of physical activity on glycemic control and prevalence of cardiovascular risk factors in adults with type 1 diabetes: a cross-sectional multicenter study of 18,028 patients. Diabetes Care 38(8):1536–1543

    Article  PubMed  Google Scholar 

  37. Li Y, Wu QH, Jiao ML et al (2015) Gene-environment interaction between adiponectin gene polymorphisms and environmental factors on the risk of diabetic retinopathy. J Diabetes Investig 6(1):56–66

    Article  CAS  PubMed  Google Scholar 

  38. Wang J, Chen H, Zhang H et al (2014) The performance of a diabetic retinopathy risk score for screening for diabetic retinopathy in Chinese overweight/obese patients with type 2 diabetes mellitus. Ann Med 46(6):417–423

    Article  PubMed  Google Scholar 

  39. Makura CB, Nirantharakumar K, Girling AJ et al (2013) Effects of physical activity on the development and progression of microvascular complications in type 1 diabetes: retrospective analysis of the DCCT study. BMC Endocr Disord 13(1):37

    Article  PubMed  PubMed Central  Google Scholar 

  40. Li N, Yang XF, Deng Y et al (2013) Diabetes self-management and its association with diabetic retinopathy in patients with type 2 diabetes. Zhonghua Yan Ke Za Zhi 49(6):500–506

    CAS  PubMed  Google Scholar 

  41. Yang JY, Kim NK, Lee YJ et al (2013) Prevalence and factors associated with diabetic retinopathy in a Korean adult population: the 2008–2009 Korea National Health and Nutrition Examination Survey. Diabetes Res Clin Pract 102(3):218–224

    Article  PubMed  Google Scholar 

  42. Carral F, Gutiérrez JV, Ayala MDC et al (2013) Intense physical activity is associated with better metabolic control in patients with type 1 diabetes. Diabetes Res Clin Pract 101(1):45–49

    Article  CAS  PubMed  Google Scholar 

  43. Tikellis G, Anuradha S, Klein R et al (2010) Association between physical activity and retinal microvascular signs: the Atherosclerosis Risk in Communities (ARIC) Study. Microcirculation 17(5):381–393

    PubMed  PubMed Central  Google Scholar 

  44. Ahmed KR, Karim MN, Bukht MS et al (2011) Risk factors of diabetic retinopathy in Bangladeshi type 2 diabetic patients. Diabetes Metab Syndr 5(4):196–200

    Article  PubMed  Google Scholar 

  45. LaPorte RE, Dorman JS, Tajima N et al (1986) Pittsburgh insulin-dependent diabetes mellitus morbidity and mortality study: physical activity and diabetic complications. Pediatrics 78(6):1027–1033

    Article  CAS  PubMed  Google Scholar 

  46. Kriska AM, LaPorte RE, Patrick SL et al (1991) The association of physical activity and diabetic complications in individuals with insulin-dependent diabetes mellitus: the Epidemiology of Diabetes Complications Study—VII. J Clin Epidemiol 44(11):1207–1214

    Article  CAS  PubMed  Google Scholar 

  47. Loprinzi PD, Brodowicz GR, Sengupta S et al (2014) Accelerometer-assessed physical activity and diabetic retinopathy in the United States. JAMA Ophthalmol 132(8):1017–1019

    Article  PubMed  Google Scholar 

  48. Cruickshanks KJ, Moss SE, Klein R et al (1992) Physical activity and proliferative retinopathy in people diagnosed with diabetes before age 30 year. Diabetes Care 15(10):1267–1272

    Article  CAS  PubMed  Google Scholar 

  49. Diabetes Canada Clinical Practice Guidelines Expert Committe (2018) Diabetes Canada 2018 clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes 42(Suppl1):S1–S325

    Google Scholar 

  50. Inzucchi SE, Bergenstal RM, Buse JB et al (2015) Management of hyperglycemia in type 2 diabetes, 2015: a patient-centered approach: update to a position statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care 38(1):140–149

    Article  PubMed  Google Scholar 

  51. Adolfsson P, Riddell MC, Taplin CE et al (2018) ISPAD clinical practice consensus guidelines 2018: exercise in children and adolescents with diabetes. Pediatr Diabetes 19 Suppl 27:205–226

    Article  Google Scholar 

  52. World Health Organization (2010) WHO guidelines approved by the guidelines review committee. Global recommendations on physical activity for health. World Health Organization (WHO), Switzerland. http://www.who.int/dietphysicalactivity/factsheet_recommendations/en/. Accessed 12 Oct 2018

  53. World Health Organization (2009) Global health risks: mortality and burden of disease attributable to selected major risks. World Health Organization (WHO), Switzerland. http://www.who.int/healthinfo/global_burden_disease/

  54. Sigal RJ, Kenny GP, Wasserman DH et al (2006) Physical activity/exercise and type 2 diabetes: a consensus statement from the American Diabetes Association. Diabetes Care 29(6):1433–1438

    Article  PubMed  Google Scholar 

  55. Colberg SR, Sigal RJ, Fernhall B et al (2010) Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement executive summary. Diabetes Care 33(12):2692–2696

    Article  PubMed  PubMed Central  Google Scholar 

  56. Colberg SR (2013) Exercise and diabetes: a clinician’s guide to prescribing physical activity, 1st edn. American Diabetes Association, Alexandria

    Google Scholar 

  57. Osei K (1987) Ambulatory and exercise-induced blood pressure responses in type I diabetic patients and normal subjects. Diabetes Res Clin Pract 3(3):125–134

    Article  CAS  PubMed  Google Scholar 

  58. Graham C, Lasko-McCarthey P (1990) Exercise options for persons with diabetic complications. Diabetes Educ 16(3):212–220

    Article  CAS  PubMed  Google Scholar 

  59. Hamdy O, Goodyear LJ, Horton ES (2001) Diet and exercise in type 2 diabetes mellitus. Endocrinol Metab Clin North Am 30(4):883–907

    Article  CAS  PubMed  Google Scholar 

  60. American Diabetes Association (2018) Cardiovascular disease and risk management: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1):S86–Ss104

    Article  Google Scholar 

  61. Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376(9735):124–136

    Article  PubMed  Google Scholar 

  62. Pemp B, Schmetterer L (2008) Ocular blood flow in diabetes and age-related macular degeneration. Can J Ophthalmol 43(3):295–301

    Article  PubMed  Google Scholar 

  63. Kohner EM, Patel V, Rassam SM (1995) Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 44(6):603–607

    Article  CAS  PubMed  Google Scholar 

  64. Frederiksen CA, Jeppesen P, Knudsen ST et al (2006) The blood pressure-induced diameter response of retinal arterioles decreases with increasing diabetic maculopathy. Graefes Arch Clin Exp Ophthalmol 244(10):1255–1261

    Article  PubMed  Google Scholar 

  65. Alibrahim E, Donaghue KC, Rogers S et al (2006) Retinal vascular caliber and risk of retinopathy in young patients with type 1 diabetes. Ophthalmology 113(9):1499–1503

    Article  PubMed  Google Scholar 

  66. Benitez-Aguirre P, Craig ME, Sasongko MB et al (2011) Retinal vascular geometry predicts incident retinopathy in young people with type 1 diabetes: a prospective cohort study from adolescence. Diabetes Care 34(7):1622–1627

    Article  PubMed  PubMed Central  Google Scholar 

  67. Sasongko MB, Wang JJ, Donaghue KC et al (2010) Alterations in retinal microvascular geometry in young type 1 diabetes. Diabetes Care 33(6):1331–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Rogers SL, Tikellis G, Cheung N et al (2008) Retinal arteriolar caliber predicts incident retinopathy: the Australian diabetes, obesity and lifestyle (AusDiab) study. Diabetes Care 31(4):761–763

    Article  PubMed  Google Scholar 

  69. Pedersen L, Jeppesen P, Knudsen ST et al (2014) Improvement of mild retinopathy in type 2 diabetic patients correlates with narrowing of retinal arterioles. A prospective observational study. Graefes Arch Clin Exp Ophthalmol 252(10):1561–1567

    Article  PubMed  Google Scholar 

  70. Anuradha S, Healy GN, Dunstan DW et al (2011) Associations of physical activity and television viewing time with retinal vascular caliber in a multiethnic Asian population. Invest Ophthalmol Vis Sci 52(9):6522–6528

    Article  PubMed  Google Scholar 

  71. Anuradha S, Healy GN, Dunstan DW et al (2011) Physical activity, television viewing time, and retinal microvascular caliber: the multi-ethnic study of atherosclerosis. Am J Epidemiol 173(5):518–525

    Article  PubMed  PubMed Central  Google Scholar 

  72. Keel S, Itsiopoulos C, Koklanis K et al (2017) Vascular risk factors are associated with retinal arteriolar narrowing and venular widening in children and adolescents with type 1 diabetes. J Pediatr Endocrinol Metab 30(3):301–309

    Article  CAS  PubMed  Google Scholar 

  73. Hayashi N, Ikemura T, Someya N (2011) Effects of dynamic exercise and its intensity on ocular blood flow in humans. Eur J Appl Physiol 111(10):2601–2606

    Article  PubMed  Google Scholar 

  74. Zhang Y, San Emeterio Nateras O, Peng Q et al (2012) Blood flow MRI of the human retina/choroid during rest and isometric exercise. Invest Ophthalmol Vis Sci 53(7):4299–4305

    Article  PubMed  PubMed Central  Google Scholar 

  75. Kellawan JM, Johansson RE, Harrell JW et al (2015) Exercise vasodilation is greater in women: contributions of nitric oxide synthase and cyclooxygenase. Eur J Appl Physiol 115(8):1735–1746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Paulsen G, Mikkelsen UR, Raastad T et al (2012) Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exerc Immunol Rev 18:42–97

    PubMed  Google Scholar 

  77. American Diabetes Association (2018) 10. Microvascular complications and foot care: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1):S105–Ss118

    Article  Google Scholar 

  78. Solomon SD, Chew E, Duh EJ et al (2017) Erratum. Diabetic retinopathy: a position statement by the american diabetes association. Diabetes Care 40(9):412–418 (Diabetes Care 40:1285)

    Article  PubMed  PubMed Central  Google Scholar 

  79. Lachin JM, White NH, Hainsworth DP et al (2015) Effect of intensive diabetes therapy on the progression of diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the DCCT/EDIC. Diabetes 64(2):631–642

    Article  CAS  PubMed  Google Scholar 

  80. Umpierre D, Ribeiro PA, Kramer CK et al (2011) Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: a systematic review and meta-analysis. JAMA 305(17):1790–1799

    Article  CAS  PubMed  Google Scholar 

  81. Boniol M, Dragomir M (2017) Physical activity and change in fasting glucose and HbA1c: a quantitative meta-analysis of randomized trials. Acta Diabetol 54(11):983–991

    Article  CAS  PubMed  Google Scholar 

  82. Al-Othman A, Al-Musharaf S, Al-Daghri NM et al (2012) Effect of physical activity and sun exposure on vitamin D status of Saudi children and adolescents. BMC Pediatr 12:92

    Article  PubMed  PubMed Central  Google Scholar 

  83. Scott D, Blizzard L, Fell J et al (2010) A prospective study of the associations between 25-hydroxy-vitamin D, sarcopenia progression and physical activity in older adults. Clin Endocrinol (Oxf) 73(5):581–587

    Article  CAS  Google Scholar 

  84. Klenk J, Rapp K, Denkinger M et al (2015) Objectively measured physical activity and vitamin D status in older people from Germany. J Epidemiol Community Health 69(4):388–392

    Article  PubMed  Google Scholar 

  85. Makanae Y, Ogasawara R, Sato K et al (2015) Acute bout of resistance exercise increases vitamin D receptor protein expression in rat skeletal muscle. Exp Physiol 100(10):1168–1176

    Article  CAS  PubMed  Google Scholar 

  86. Black LJ, Burrows SA, Jacoby P et al (2014) Vitamin D status and predictors of serum 25-hydroxyvitamin D concentrations in Western Australian adolescents. Br J Nutr 112(7):1154–1162

    Article  CAS  PubMed  Google Scholar 

  87. Anand S, Kaysen GA, Chertow GM et al (2011) Vitamin D deficiency, self-reported physical activity and health-related quality of life: the Comprehensive Dialysis Study. Nephrol Dial Transplant 26(11):3683–3688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Herrmann M, Sullivan DR, Veillard AS et al (2015) Serum 25-hydroxyvitamin D: a predictor of macrovascular and microvascular complications in patients with type 2 diabetes. Diabetes Care 38(3):521–528

    Article  CAS  PubMed  Google Scholar 

  89. Keech AC, Mitchell P, Summanen PA et al (2007) Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): a randomised controlled trial. Lancet 370(9600):1687–1697

    Article  CAS  PubMed  Google Scholar 

  90. Keech A, Simes RJ, Barter P et al (2005) Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet 366(9500):1849–1861

    Article  CAS  PubMed  Google Scholar 

  91. Davis TM, Ting R, Best JD et al (2011) Effects of fenofibrate on renal function in patients with type 2 diabetes mellitus: the Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) Study. Diabetologia 54(2):280–290

    Article  CAS  PubMed  Google Scholar 

  92. Luo BA, Gao F, Qin LL (2017) The association between vitamin D deficiency and diabetic retinopathy in type 2 diabetes: a meta-analysis of observational studies. Nutrients 9:3

    Article  CAS  Google Scholar 

  93. Ortlepp JR, Metrikat J, Albrecht M et al (2003) The vitamin D receptor gene variant and physical activity predicts fasting glucose levels in healthy young men. Diabet Med 20(6):451–454

    Article  CAS  PubMed  Google Scholar 

  94. Kowluru RA, Kowluru A, Mishra M et al (2015) Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy. Prog Retin Eye Res 48:40–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Arroba AI, Valverde AM (2017) Modulation of microglia in the retina: new insights into diabetic retinopathy. Acta Diabetol 54(6):527–533

    Article  PubMed  Google Scholar 

  96. Wu Y, Tang L, Chen B (2014) Oxidative stress: implications for the development of diabetic retinopathy and antioxidant therapeutic perspectives. Oxid Med Cell Longev 2014:752387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Zorena K (2014) Anti-inflammatory therapy in diabetic retinopathy. Mediators Inflamm 2014:947896

    Article  PubMed  PubMed Central  Google Scholar 

  98. Sallam N, Laher I (2016) Exercise modulates oxidative stress and inflammation in aging and cardiovascular diseases. Oxid Med Cell Longev 2016:7239639

    Article  PubMed  CAS  Google Scholar 

  99. Kim CS, Park S, Chun Y et al (2015) Treadmill exercise attenuates retinal oxidative stress in naturally-aged mice: an immunohistochemical study. Int J Mol Sci 16(9):21008–21020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Kruk J, Kubasik-Kladna K, Aboul-Enein HY (2015) The role oxidative stress in the pathogenesis of eye diseases: current status and a dual role of physical activity. Mini Rev Med Chem 16(3):241–257

    Article  PubMed  CAS  Google Scholar 

  101. Allen RS, Hanif AM, Gogniat MA et al (2018) TrkB signalling pathway mediates the protective effects of exercise in the diabetic rat retina. Eur J Neurosci 47(10):1254–1265

    Article  PubMed  PubMed Central  Google Scholar 

  102. Cui JZ, Wong M, Wang A et al (2016) Exercise inhibits progression of diabetic retinopathy by reducing inflammatory, oxidative stress, and ER stress gene expression in the retina of db/db mice. Invest Ophthalmol Vis Sci 57(12):5434

    Google Scholar 

  103. Lu Y, Dong Y, Tucker D et al (2017) Treadmill exercise exerts neuroprotection and regulates microglial polarization and oxidative stress in a streptozotocin-induced rat model of sporadic alzheimer’s disease. J Alzheimers Dis 56(4):1469–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Sprouse C, Gordish-Dressman H, Orkunoglu-Suer EF et al (2014) SLC30A8 nonsynonymous variant is associated with recovery following exercise and skeletal muscle size and strength. Diabetes 63(1):363–368

    Article  CAS  PubMed  Google Scholar 

  105. He MA, Workalemahu T, Cornelis MC et al (2011) Genetic variants near the IRS1 gene, physical activity and type 2 diabetes in US men and women. Diabetologia 54(6):1579–1582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Fu LL, Lin Y, Yang ZL et al (2012) Association analysis of genetic polymorphisms of TCF7L2, CDKAL1, SLC30A8, HHEX genes and microvascular complications of type 2 diabetes mellitus. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 29(2):194–199

    CAS  PubMed  Google Scholar 

  107. Lavin DP, White MF, Brazil DP (2016) IRS proteins and diabetic complications. Diabetologia 59(11):2280–2291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was partly supported by the National Natural Science Foundation of China (NSFC No. 81671641), Natural Science Foundation of Jiangsu Province (No. BK20151208), Jiangsu Provincial Medical Innovation Team (No. CXTDA2017039), and the Soochow Scholar Project of Soochow University (No. R5122001).

Author information

Authors and Affiliations

  1. Department of Ophthalmology, The First Affiliated Hospital of Soochow University, 188 Shizi Street, Suzhou, 215006, People’s Republic of China

    Chi Ren, Weiming Liu, Jianqing Li, Yihong Cao, Jiayi Xu & Peirong Lu

Authors
  1. Chi Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weiming Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianqing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yihong Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiayi Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peirong Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CR and PL conceived of the idea and designed the study. CR, WL, and JL collected the data. CR, JX, and YC performed the data analysis. CR, WL, and PL participated in the critical revision of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Peirong Lu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Ethical approval

As this was a review study, no ethics approval was required.

Informed consent

For this type of study, informed consent was not required.

Additional information

Managed By Antonio Secchi.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, C., Liu, W., Li, J. et al. Physical activity and risk of diabetic retinopathy: a systematic review and meta-analysis. Acta Diabetol 56, 823–837 (2019). https://doi.org/10.1007/s00592-019-01319-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00592-019-01319-4

Keywords

Search

Navigation