Skip to main content
Top
Published in: Acta Diabetologica 8/2019

01-08-2019 | Diabetic Retinopathy | Review Article

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

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

Published in: Acta Diabetologica | Issue 8/2019

Login to get access

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.
Literature
1.
go back to reference Stolk RP, Vingerling JR, de Jong PT et al (1995) Retinopathy, glucose, and insulin in an elderly population. The Rotterdam Study Diabetes 44(1):11–15PubMed Stolk RP, Vingerling JR, de Jong PT et al (1995) Retinopathy, glucose, and insulin in an elderly population. The Rotterdam Study Diabetes 44(1):11–15PubMed
2.
4.
go back to reference Beagley J, Guariguata L, Weil C et al (2014) Global estimates of undiagnosed diabetes in adults. Diabetes Res Clin Pract 103(2):150–160PubMedCrossRef Beagley J, Guariguata L, Weil C et al (2014) Global estimates of undiagnosed diabetes in adults. Diabetes Res Clin Pract 103(2):150–160PubMedCrossRef
5.
go back to reference 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):137–149PubMedCrossRef 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):137–149PubMedCrossRef
6.
go back to reference 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):010803PubMedPubMedCentralCrossRef 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):010803PubMedPubMedCentralCrossRef
8.
go back to reference 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):448–457PubMedCrossRef 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):448–457PubMedCrossRef
9.
go back to reference 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):156–163PubMedCrossRef 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):156–163PubMedCrossRef
11.
go back to reference American Diabetes Association (2018) Lifestyle management: standards of medical care in diabetes—2018. Diabetes Care 41:S38–S50CrossRef American Diabetes Association (2018) Lifestyle management: standards of medical care in diabetes—2018. Diabetes Care 41:S38–S50CrossRef
12.
go back to reference 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):2065–2079PubMedPubMedCentralCrossRef 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):2065–2079PubMedPubMedCentralCrossRef
13.
go back to reference 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):267–272PubMedCrossRef 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):267–272PubMedCrossRef
14.
go back to reference Praidou A, Harris M, Niakas D et al (2017) Physical activity and its correlation to diabetic retinopathy. J Diabetes Compl 31(2):456–461CrossRef Praidou A, Harris M, Niakas D et al (2017) Physical activity and its correlation to diabetic retinopathy. J Diabetes Compl 31(2):456–461CrossRef
15.
go back to reference 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):251–257PubMedCrossRef 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):251–257PubMedCrossRef
16.
go back to reference 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):108–114PubMedCrossRef 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):108–114PubMedCrossRef
17.
go back to reference 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):113–119PubMedCrossRef 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):113–119PubMedCrossRef
18.
go back to reference 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):1228–1233CrossRef 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):1228–1233CrossRef
19.
go back to reference Loprinzi PD (2016) Association of accelerometer-assessed sedentary behavior with diabetic retinopathy in the United States. JAMA Ophthalmol 134(10):1197–1198PubMedCrossRef Loprinzi PD (2016) Association of accelerometer-assessed sedentary behavior with diabetic retinopathy in the United States. JAMA Ophthalmol 134(10):1197–1198PubMedCrossRef
20.
go back to reference 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):1177–1182PubMedCrossRef 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):1177–1182PubMedCrossRef
21.
go back to reference 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):1800–1810PubMedCrossRef 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):1800–1810PubMedCrossRef
22.
25.
go back to reference 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):344–349CrossRef 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):344–349CrossRef
26.
go back to reference Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10(1):101–129CrossRef Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10(1):101–129CrossRef
27.
go back to reference Tobias A (1999) Assessing the influence of a single study in the meta-analysis estimate. Stata Tech Bull 47:15–17 Tobias A (1999) Assessing the influence of a single study in the meta-analysis estimate. Stata Tech Bull 47:15–17
29.
go back to reference Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101PubMedCrossRef Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101PubMedCrossRef
30.
go back to reference 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):230–232PubMedCrossRef 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):230–232PubMedCrossRef
31.
32.
go back to reference 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):647–654PubMedCrossRef 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):647–654PubMedCrossRef
33.
go back to reference 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):e0172890PubMedPubMedCentralCrossRef 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):e0172890PubMedPubMedCentralCrossRef
34.
go back to reference 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 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
35.
go back to reference Yan ZP, Ma JX (2016) Risk factors for diabetic retinopathy in northern Chinese patients with type 2 diabetes mellitus. Int J Ophthalmol 9(8):1194–1199PubMedPubMedCentral Yan ZP, Ma JX (2016) Risk factors for diabetic retinopathy in northern Chinese patients with type 2 diabetes mellitus. Int J Ophthalmol 9(8):1194–1199PubMedPubMedCentral
36.
go back to reference 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):1536–1543PubMedCrossRef 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):1536–1543PubMedCrossRef
37.
go back to reference 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):56–66PubMedCrossRef 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):56–66PubMedCrossRef
38.
go back to reference 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):417–423PubMedCrossRef 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):417–423PubMedCrossRef
39.
go back to reference 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):37PubMedPubMedCentralCrossRef 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):37PubMedPubMedCentralCrossRef
40.
go back to reference 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):500–506PubMed 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):500–506PubMed
41.
go back to reference 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):218–224PubMedCrossRef 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):218–224PubMedCrossRef
42.
go back to reference 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):45–49PubMedCrossRef 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):45–49PubMedCrossRef
43.
go back to reference 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):381–393PubMedPubMedCentral 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):381–393PubMedPubMedCentral
44.
go back to reference 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):196–200PubMedCrossRef 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):196–200PubMedCrossRef
45.
go back to reference 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):1027–1033PubMedCrossRef 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):1027–1033PubMedCrossRef
46.
go back to reference 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):1207–1214PubMedCrossRef 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):1207–1214PubMedCrossRef
47.
go back to reference Loprinzi PD, Brodowicz GR, Sengupta S et al (2014) Accelerometer-assessed physical activity and diabetic retinopathy in the United States. JAMA Ophthalmol 132(8):1017–1019PubMedCrossRef Loprinzi PD, Brodowicz GR, Sengupta S et al (2014) Accelerometer-assessed physical activity and diabetic retinopathy in the United States. JAMA Ophthalmol 132(8):1017–1019PubMedCrossRef
48.
go back to reference 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):1267–1272PubMedCrossRef 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):1267–1272PubMedCrossRef
49.
go back to reference 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 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
50.
go back to reference 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):140–149PubMedCrossRef 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):140–149PubMedCrossRef
51.
go back to reference 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 27:205–226CrossRef 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 27:205–226CrossRef
54.
go back to reference 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):1433–1438PubMedCrossRef 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):1433–1438PubMedCrossRef
55.
go back to reference 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):2692–2696PubMedPubMedCentralCrossRef 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):2692–2696PubMedPubMedCentralCrossRef
56.
go back to reference Colberg SR (2013) Exercise and diabetes: a clinician’s guide to prescribing physical activity, 1st edn. American Diabetes Association, Alexandria Colberg SR (2013) Exercise and diabetes: a clinician’s guide to prescribing physical activity, 1st edn. American Diabetes Association, Alexandria
57.
go back to reference Osei K (1987) Ambulatory and exercise-induced blood pressure responses in type I diabetic patients and normal subjects. Diabetes Res Clin Pract 3(3):125–134PubMedCrossRef Osei K (1987) Ambulatory and exercise-induced blood pressure responses in type I diabetic patients and normal subjects. Diabetes Res Clin Pract 3(3):125–134PubMedCrossRef
58.
go back to reference Graham C, Lasko-McCarthey P (1990) Exercise options for persons with diabetic complications. Diabetes Educ 16(3):212–220PubMedCrossRef Graham C, Lasko-McCarthey P (1990) Exercise options for persons with diabetic complications. Diabetes Educ 16(3):212–220PubMedCrossRef
59.
go back to reference Hamdy O, Goodyear LJ, Horton ES (2001) Diet and exercise in type 2 diabetes mellitus. Endocrinol Metab Clin North Am 30(4):883–907PubMedCrossRef Hamdy O, Goodyear LJ, Horton ES (2001) Diet and exercise in type 2 diabetes mellitus. Endocrinol Metab Clin North Am 30(4):883–907PubMedCrossRef
60.
go back to reference American Diabetes Association (2018) Cardiovascular disease and risk management: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1):S86–Ss104CrossRef American Diabetes Association (2018) Cardiovascular disease and risk management: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1):S86–Ss104CrossRef
62.
go back to reference Pemp B, Schmetterer L (2008) Ocular blood flow in diabetes and age-related macular degeneration. Can J Ophthalmol 43(3):295–301PubMedCrossRef Pemp B, Schmetterer L (2008) Ocular blood flow in diabetes and age-related macular degeneration. Can J Ophthalmol 43(3):295–301PubMedCrossRef
63.
go back to reference Kohner EM, Patel V, Rassam SM (1995) Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 44(6):603–607PubMedCrossRef Kohner EM, Patel V, Rassam SM (1995) Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 44(6):603–607PubMedCrossRef
64.
go back to reference 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):1255–1261PubMedCrossRef 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):1255–1261PubMedCrossRef
65.
go back to reference 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):1499–1503PubMedCrossRef 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):1499–1503PubMedCrossRef
66.
go back to reference 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):1622–1627PubMedPubMedCentralCrossRef 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):1622–1627PubMedPubMedCentralCrossRef
67.
68.
go back to reference 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):761–763PubMedCrossRef 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):761–763PubMedCrossRef
69.
go back to reference 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):1561–1567PubMedCrossRef 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):1561–1567PubMedCrossRef
70.
go back to reference 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):6522–6528PubMedCrossRef 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):6522–6528PubMedCrossRef
71.
go back to reference 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):518–525PubMedPubMedCentralCrossRef 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):518–525PubMedPubMedCentralCrossRef
72.
go back to reference 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):301–309PubMedCrossRef 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):301–309PubMedCrossRef
73.
go back to reference 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):2601–2606PubMedCrossRef 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):2601–2606PubMedCrossRef
74.
go back to reference 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):4299–4305PubMedPubMedCentralCrossRef 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):4299–4305PubMedPubMedCentralCrossRef
75.
go back to reference 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):1735–1746PubMedPubMedCentralCrossRef 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):1735–1746PubMedPubMedCentralCrossRef
76.
go back to reference 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 18:42–97PubMed 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 18:42–97PubMed
77.
go back to reference American Diabetes Association (2018) 10. Microvascular complications and foot care: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1):S105–Ss118CrossRef American Diabetes Association (2018) 10. Microvascular complications and foot care: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1):S105–Ss118CrossRef
78.
go back to reference 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)PubMedPubMedCentralCrossRef 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)PubMedPubMedCentralCrossRef
79.
go back to reference 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):631–642PubMedCrossRef 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):631–642PubMedCrossRef
80.
go back to reference 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):1790–1799PubMedCrossRef 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):1790–1799PubMedCrossRef
81.
go back to reference 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):983–991PubMedCrossRef 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):983–991PubMedCrossRef
82.
go back to reference 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 12:92PubMedPubMedCentralCrossRef 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 12:92PubMedPubMedCentralCrossRef
83.
go back to reference 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):581–587CrossRef 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):581–587CrossRef
84.
go back to reference 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):388–392PubMedCrossRef 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):388–392PubMedCrossRef
85.
go back to reference 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):1168–1176PubMedCrossRef 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):1168–1176PubMedCrossRef
86.
go back to reference 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):1154–1162PubMedCrossRef 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):1154–1162PubMedCrossRef
87.
go back to reference 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):3683–3688PubMedPubMedCentralCrossRef 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):3683–3688PubMedPubMedCentralCrossRef
88.
go back to reference 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):521–528PubMedCrossRef 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):521–528PubMedCrossRef
89.
go back to reference 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):1687–1697PubMedCrossRef 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):1687–1697PubMedCrossRef
90.
go back to reference 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):1849–1861PubMedCrossRef 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):1849–1861PubMedCrossRef
91.
go back to reference 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):280–290PubMedCrossRef 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):280–290PubMedCrossRef
92.
go back to reference 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 9:3CrossRef 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 9:3CrossRef
93.
go back to reference 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):451–454PubMedCrossRef 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):451–454PubMedCrossRef
94.
go back to reference Kowluru RA, Kowluru A, Mishra M et al (2015) Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy. Prog Retin Eye Res 48:40–61PubMedPubMedCentralCrossRef Kowluru RA, Kowluru A, Mishra M et al (2015) Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy. Prog Retin Eye Res 48:40–61PubMedPubMedCentralCrossRef
95.
go back to reference Arroba AI, Valverde AM (2017) Modulation of microglia in the retina: new insights into diabetic retinopathy. Acta Diabetol 54(6):527–533PubMedCrossRef Arroba AI, Valverde AM (2017) Modulation of microglia in the retina: new insights into diabetic retinopathy. Acta Diabetol 54(6):527–533PubMedCrossRef
96.
go back to reference Wu Y, Tang L, Chen B (2014) Oxidative stress: implications for the development of diabetic retinopathy and antioxidant therapeutic perspectives. Oxid Med Cell Longev 2014:752387PubMedPubMedCentralCrossRef Wu Y, Tang L, Chen B (2014) Oxidative stress: implications for the development of diabetic retinopathy and antioxidant therapeutic perspectives. Oxid Med Cell Longev 2014:752387PubMedPubMedCentralCrossRef
98.
go back to reference Sallam N, Laher I (2016) Exercise modulates oxidative stress and inflammation in aging and cardiovascular diseases. Oxid Med Cell Longev 2016:7239639PubMedCrossRef Sallam N, Laher I (2016) Exercise modulates oxidative stress and inflammation in aging and cardiovascular diseases. Oxid Med Cell Longev 2016:7239639PubMedCrossRef
99.
go back to reference 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):21008–21020PubMedPubMedCentralCrossRef 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):21008–21020PubMedPubMedCentralCrossRef
100.
go back to reference 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):241–257PubMedCrossRef 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):241–257PubMedCrossRef
101.
go back to reference 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):1254–1265PubMedPubMedCentralCrossRef 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):1254–1265PubMedPubMedCentralCrossRef
102.
go back to reference 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 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
103.
go back to reference 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):1469–1484PubMedPubMedCentralCrossRef 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):1469–1484PubMedPubMedCentralCrossRef
104.
go back to reference 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):363–368PubMedCrossRef 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):363–368PubMedCrossRef
105.
go back to reference 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):1579–1582PubMedPubMedCentralCrossRef 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):1579–1582PubMedPubMedCentralCrossRef
106.
go back to reference 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):194–199PubMed 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):194–199PubMed
Metadata
Title
Physical activity and risk of diabetic retinopathy: a systematic review and meta-analysis
Authors
Chi Ren
Weiming Liu
Jianqing Li
Yihong Cao
Jiayi Xu
Peirong Lu
Publication date
01-08-2019
Publisher
Springer Milan
Published in
Acta Diabetologica / Issue 8/2019
Print ISSN: 0940-5429
Electronic ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-019-01319-4

Other articles of this Issue 8/2019

Acta Diabetologica 8/2019 Go to the issue