Skip to main content
Top
Published in: BMC Public Health 1/2018

Open Access 01-12-2018 | Research article

Current epidemiology of diabetic retinopathy in patients with type 1 diabetes: a national multicenter study in Brazil

Authors: Laura Gomes Nunes Melo, Paulo Henrique Morales, Karla Rezende Guerra Drummond, Deborah Conte Santos, Marcela Haas Pizarro, Bianca Senger Vasconcelos Barros, Tessa Cerqueria Lemos Mattos, André Araújo Pinheiro, Felipe Mallmann, Franz Schubert Lopes Leal, Fernando Korn Malerbi, Marilia Brito Gomes

Published in: BMC Public Health | Issue 1/2018

Login to get access

Abstract

Background

Diabetic retinopathy is the leading cause of blindness in economically active populations. The aims of this study were to estimate the prevalence and to identify risk factors for diabetic retinopathy in patients with type 1 diabetes in Brazil.

Methods

This was a nationwide, cross-sectional study conducted between August 2010 and August 2014. The study included 1760 patients with type 1 diabetes. Patients underwent a standard questionnaire, clinical and laboratory analyses and were screened for diabetic retinopathy. To analyze the risk factors related to diabetic retinopathy, two models of logistic regression models were performed, one considering vision-threatening cases and the other with any diabetic retinopathy cases as dependent variables. The group with vision-threatening included patients with severe non-proliferative diabetic retinopathy, proliferative diabetic retinopathy and macular edema.

Results

In total, 1644 patients (mean age, 30.1± 12.0 years; duration of diabetes, 15.3 ± 9.3 years; female, 55.8%) were studied. 35.7% presented diabetic retinopathy and 12% presented vision-threatening diabetic retinopathy. Three risk factors associated with diabetic retinopathy were in common to both groups: longer diabetes duration (OR 1.07; 95% CI, 1.05–1.09), higher levels of HbA1c (OR 1.24; CI, 1.17–1.32) and higher levels of serum uric acid (OR 1.22; CI, 1.13–1.31) (p < 0.001 for all comparisons).

Conclusion

The higher rate of vision-threatening retinopathy found in our study highlights the need to improve access to eye care and screening programs for diabetic retinopathy in Brazil. In addition to traditional risk factors, we found an association between serum uric acid levels and diabetic retinopathy. Further studies are needed to address this association.
Appendix
Available only for authorised users
Literature
3.
go back to reference Patterson C, Guariguata L, Dahlquist G, Soltész G, Ogle G, Silink M. Diabetes in the young–a global view and worldwide estimates of numbers of children with type 1 diabetes. Diabetes Res Clin Pract. 2014;103(2):161–75.CrossRefPubMed Patterson C, Guariguata L, Dahlquist G, Soltész G, Ogle G, Silink M. Diabetes in the young–a global view and worldwide estimates of numbers of children with type 1 diabetes. Diabetes Res Clin Pract. 2014;103(2):161–75.CrossRefPubMed
4.
go back to reference Leasher JL, Bourne RRA, Flaxman SR, et al. Global estimates on the number of people blind or visually impaired by diabetic retinopathy: a meta-analysis from 1990 to 2010. Diabetes Care. 2016;39(9):1643–9.CrossRefPubMed Leasher JL, Bourne RRA, Flaxman SR, et al. Global estimates on the number of people blind or visually impaired by diabetic retinopathy: a meta-analysis from 1990 to 2010. Diabetes Care. 2016;39(9):1643–9.CrossRefPubMed
6.
go back to reference Grunwald JE, Alexander J, Ying G-S, et al. Retinopathy and chronic kidney disease in the chronic renal insufficiency cohort (CRIC) study. Arch Ophthalmol. 2012;130(9):1136–44.CrossRefPubMedPubMedCentral Grunwald JE, Alexander J, Ying G-S, et al. Retinopathy and chronic kidney disease in the chronic renal insufficiency cohort (CRIC) study. Arch Ophthalmol. 2012;130(9):1136–44.CrossRefPubMedPubMedCentral
7.
go back to reference The Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group. 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. 2015;64(2):631-642i. https://doi.org/10.2337/db14-0930. The Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group. 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. 2015;64(2):631-642i. https://​doi.​org/​10.​2337/​db14-0930.
8.
go back to reference Group DER. Frequency of evidence-based screening for retinopathy in type 1 diabetes. N Engl J Med. 2017;376(16):1507–16.CrossRef Group DER. Frequency of evidence-based screening for retinopathy in type 1 diabetes. N Engl J Med. 2017;376(16):1507–16.CrossRef
9.
go back to reference Malerbi FK, Morales PH, Farah ME, et al. Comparison between binocular indirect ophthalmoscopy and digital retinography for diabetic retinopathy screening: the multicenter Brazilian type 1 diabetes study. Diabetol Metab Syndr. 2015;7(1):116.CrossRefPubMedPubMedCentral Malerbi FK, Morales PH, Farah ME, et al. Comparison between binocular indirect ophthalmoscopy and digital retinography for diabetic retinopathy screening: the multicenter Brazilian type 1 diabetes study. Diabetol Metab Syndr. 2015;7(1):116.CrossRefPubMedPubMedCentral
11.
go back to reference Raum P, Lamparter J, Ponto KA, et al. Prevalence and cardiovascular associations of diabetic retinopathy and maculopathy: results from the Gutenberg health study. PLoS One. 2015;10(6):e0127188.CrossRefPubMedPubMedCentral Raum P, Lamparter J, Ponto KA, et al. Prevalence and cardiovascular associations of diabetic retinopathy and maculopathy: results from the Gutenberg health study. PLoS One. 2015;10(6):e0127188.CrossRefPubMedPubMedCentral
12.
go back to reference Gomes MB, Negrato CA. Adherence to insulin therapeutic regimens in patients with type 1 diabetes. A nationwide survey in Brazil. Diabetes Res Clin Pract. 2016;120:47–55.CrossRefPubMed Gomes MB, Negrato CA. Adherence to insulin therapeutic regimens in patients with type 1 diabetes. A nationwide survey in Brazil. Diabetes Res Clin Pract. 2016;120:47–55.CrossRefPubMed
13.
go back to reference Von Elm E, Altman DG, Egger M, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4(10):e296.CrossRefPubMedPubMedCentral Von Elm E, Altman DG, Egger M, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4(10):e296.CrossRefPubMedPubMedCentral
14.
go back to reference Silverstein J, Klingensmith G, Copeland K, et al. Care of children and adolescents with type 1 diabetes: a statement of the American Diabetes Association. Diabetes Care. 2005;28(1):186–212.CrossRefPubMed Silverstein J, Klingensmith G, Copeland K, et al. Care of children and adolescents with type 1 diabetes: a statement of the American Diabetes Association. Diabetes Care. 2005;28(1):186–212.CrossRefPubMed
15.
go back to reference Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, Feldman HI. CKD-EPI (chronic kidney disease epidemiology collaboration). CKD-EPI (chronic kidney disease epidemiology collaboration). A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150:604–12.CrossRefPubMedPubMedCentral Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, Feldman HI. CKD-EPI (chronic kidney disease epidemiology collaboration). CKD-EPI (chronic kidney disease epidemiology collaboration). A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150:604–12.CrossRefPubMedPubMedCentral
16.
go back to reference Wilkinson CP, Ferris FL, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110(9):1677–82.CrossRefPubMed Wilkinson CP, Ferris FL, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110(9):1677–82.CrossRefPubMed
20.
go back to reference Esteves JF, Kramer CK, Azevedo MJ, et al. Prevalence of diabetic retinopathy in patients with type 1 diabetes mellitus. Rev Assoc Med Bras. 2009;55(3):268–73.CrossRefPubMed Esteves JF, Kramer CK, Azevedo MJ, et al. Prevalence of diabetic retinopathy in patients with type 1 diabetes mellitus. Rev Assoc Med Bras. 2009;55(3):268–73.CrossRefPubMed
21.
go back to reference Davison KAK, Negrato CA, Cobas R, et al. Relationship between adherence to diet, glycemic control and cardiovascular risk factors in patients with type 1 diabetes: a nationwide survey in Brazil. Nutr J. 2014;13(1):19.CrossRefPubMedPubMedCentral Davison KAK, Negrato CA, Cobas R, et al. Relationship between adherence to diet, glycemic control and cardiovascular risk factors in patients with type 1 diabetes: a nationwide survey in Brazil. Nutr J. 2014;13(1):19.CrossRefPubMedPubMedCentral
22.
go back to reference Kim H, Elmi A, Henderson CL, Cogen FR, Kaplowitz PB. Characteristics of children with type 1 diabetes and persistent suboptimal glycemic control. J Clin Res Pediatr Endocrinol. 2012;4(2):82.CrossRefPubMedPubMedCentral Kim H, Elmi A, Henderson CL, Cogen FR, Kaplowitz PB. Characteristics of children with type 1 diabetes and persistent suboptimal glycemic control. J Clin Res Pediatr Endocrinol. 2012;4(2):82.CrossRefPubMedPubMedCentral
23.
go back to reference Gomes MB, Rodacki M, Pavin EJ, et al. The impact of ethnicity, educational and economic status on the prescription of insulin therapeutic regimens and on glycemic control in patients with type 1 diabetes. A nationwide study in Brazil. Diabetes Res Clin Pract. 2017;134:44–52.CrossRefPubMed Gomes MB, Rodacki M, Pavin EJ, et al. The impact of ethnicity, educational and economic status on the prescription of insulin therapeutic regimens and on glycemic control in patients with type 1 diabetes. A nationwide study in Brazil. Diabetes Res Clin Pract. 2017;134:44–52.CrossRefPubMed
24.
go back to reference Gerstein HC, Ambrosius WT, Danis R, et al. Diabetic retinopathy, its progression, and incident cardiovascular events in the ACCORD trial. Diabetes Care. 2013;36(5):1266–71.CrossRefPubMedPubMedCentral Gerstein HC, Ambrosius WT, Danis R, et al. Diabetic retinopathy, its progression, and incident cardiovascular events in the ACCORD trial. Diabetes Care. 2013;36(5):1266–71.CrossRefPubMedPubMedCentral
25.
go back to reference Klein R, Klein BEK, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy: II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol. 1984;102(4):520–6.CrossRefPubMed Klein R, Klein BEK, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy: II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol. 1984;102(4):520–6.CrossRefPubMed
26.
go back to reference Bjornstad P, Maahs DM, Rivard CJ, et al. Serum uric acid predicts vascular complications in adults with type 1 diabetes: the coronary artery calcification in type 1 diabetes study. Acta Diabetol. 2014;51(5):783–91.CrossRefPubMedPubMedCentral Bjornstad P, Maahs DM, Rivard CJ, et al. Serum uric acid predicts vascular complications in adults with type 1 diabetes: the coronary artery calcification in type 1 diabetes study. Acta Diabetol. 2014;51(5):783–91.CrossRefPubMedPubMedCentral
27.
go back to reference Krizova L, Kalousova M, Kubena AA, et al. Correlation of Vitreous Vascular Endothelial Growth Factor and Uric Acid Concentration Using Optical Coherence Tomography in Diabetic Macular Edema. Journal of Ophthalmology. 2015;2015:478509. https://doi.org/10.1155/2015/478509. Krizova L, Kalousova M, Kubena AA, et al. Correlation of Vitreous Vascular Endothelial Growth Factor and Uric Acid Concentration Using Optical Coherence Tomography in Diabetic Macular Edema. Journal of Ophthalmology. 2015;2015:478509. https://​doi.​org/​10.​1155/​2015/​478509.
28.
go back to reference Liang C-C, Lin P-C, Lee M-Y, et al. Association of serum uric acid concentration with diabetic retinopathy and albuminuria in Taiwanese patients with type 2 diabetes mellitus. Int J Mol Sci. 2016;17(8):1248.CrossRefPubMedCentral Liang C-C, Lin P-C, Lee M-Y, et al. Association of serum uric acid concentration with diabetic retinopathy and albuminuria in Taiwanese patients with type 2 diabetes mellitus. Int J Mol Sci. 2016;17(8):1248.CrossRefPubMedCentral
29.
go back to reference Kuwata H, Okamura S, Hayashino Y, Tsujii S, Ishii H. erum uric acid levels are associated with increased risk of newly developed diabetic retinopathy among Japanese male patients with type 2 diabetes: A prospective cohort study (diabetes distress and care registry at Tenri [ddcrt 13]). Diabetes Metab Res Rev. 2017;33(7):e2905.CrossRef Kuwata H, Okamura S, Hayashino Y, Tsujii S, Ishii H. erum uric acid levels are associated with increased risk of newly developed diabetic retinopathy among Japanese male patients with type 2 diabetes: A prospective cohort study (diabetes distress and care registry at Tenri [ddcrt 13]). Diabetes Metab Res Rev. 2017;33(7):e2905.CrossRef
30.
go back to reference Johnson RJ, Kang D-H, Feig D, et al. Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease? Hypertension. 2003;41(6):1183–90.CrossRefPubMed Johnson RJ, Kang D-H, Feig D, et al. Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease? Hypertension. 2003;41(6):1183–90.CrossRefPubMed
31.
go back to reference Pasalic D, Marinkovic N, Feher-Turkovic L. Uric acid as one of the important factors in multifactorial disorders–facts and controversies. Bio Med. 2012;22(1):63–75.CrossRef Pasalic D, Marinkovic N, Feher-Turkovic L. Uric acid as one of the important factors in multifactorial disorders–facts and controversies. Bio Med. 2012;22(1):63–75.CrossRef
32.
go back to reference Netea MG, Kullberg BJ, Blok WL, Netea RT, Van der Meer JWM. The role of hyperuricemia in the increased cytokine production after lipopolysaccharide challenge in neutropenic mice. Blood. 1997;89(2):577–82.PubMed Netea MG, Kullberg BJ, Blok WL, Netea RT, Van der Meer JWM. The role of hyperuricemia in the increased cytokine production after lipopolysaccharide challenge in neutropenic mice. Blood. 1997;89(2):577–82.PubMed
33.
go back to reference Control D, Complications Trial Research G. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993;329(14):977–86.CrossRef Control D, Complications Trial Research G. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993;329(14):977–86.CrossRef
34.
go back to reference Stephenson JM, Fuller JH, Viberti GC, Sjolie AK, Navalesi R, Group EICS. Blood pressure, retinopathy and urinary albumin excretion in IDDM: the EURODIAB IDDM complications study. Diabetologia. 1995;38(5):599–603.CrossRefPubMed Stephenson JM, Fuller JH, Viberti GC, Sjolie AK, Navalesi R, Group EICS. Blood pressure, retinopathy and urinary albumin excretion in IDDM: the EURODIAB IDDM complications study. Diabetologia. 1995;38(5):599–603.CrossRefPubMed
35.
go back to reference Joussen AM, Gardner TW, Kirchhof B, Ryan SJ. Retinal vascular disease: Springer; 2007. p. 97–104. Joussen AM, Gardner TW, Kirchhof B, Ryan SJ. Retinal vascular disease: Springer; 2007. p. 97–104.
36.
go back to reference Van Hecke MV, Dekker JM, Stehouwer CDA, et al. Diabetic retinopathy is associated with mortality and cardiovascular disease incidence: the EURODIAB prospective complications study. Diabetes Care. 2005;28(6):1383–9.CrossRefPubMed Van Hecke MV, Dekker JM, Stehouwer CDA, et al. Diabetic retinopathy is associated with mortality and cardiovascular disease incidence: the EURODIAB prospective complications study. Diabetes Care. 2005;28(6):1383–9.CrossRefPubMed
37.
go back to reference Nathan DM. The diabetes control and complications trial/epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care. 2014;37(1):9–16.CrossRefPubMed Nathan DM. The diabetes control and complications trial/epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care. 2014;37(1):9–16.CrossRefPubMed
39.
go back to reference Chew EY, Davis MD, Danis RP, Lovato JF, Perdue LH, Greven C, et al. The effects of medical management on the progression of diabetic retinopathy in persons with type 2 diabetes: The action to control cardiovascular risk in diabetes (ACCORD) eye study. Ophthalmology. 2014;121(12):2443–51. Available from: http://dx.doi.org/10.1016/j.ophtha.2014.07.019. Chew EY, Davis MD, Danis RP, Lovato JF, Perdue LH, Greven C, et al. The effects of medical management on the progression of diabetic retinopathy in persons with type 2 diabetes: The action to control cardiovascular risk in diabetes (ACCORD) eye study. Ophthalmology. 2014;121(12):2443–51. Available from: http://​dx.​doi.​org/​10.​1016/​j.​ophtha.​2014.​07.​019.
40.
go back to reference Okura Y, Urban LH, Mahoney DW, Jacobsen SJ, Rodeheffer RJ. Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure. J Clin Epidemiol. 2004;57(10):1096–103.CrossRefPubMed Okura Y, Urban LH, Mahoney DW, Jacobsen SJ, Rodeheffer RJ. Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure. J Clin Epidemiol. 2004;57(10):1096–103.CrossRefPubMed
41.
go back to reference Early Treatment Diabetic Retinopathy Study Research G. Photocoagulation for diabetic macular edema: early treatment diabetic retinopathy study report number 1. Arch Ophthalmol. 1985;103:1796–806.CrossRef Early Treatment Diabetic Retinopathy Study Research G. Photocoagulation for diabetic macular edema: early treatment diabetic retinopathy study report number 1. Arch Ophthalmol. 1985;103:1796–806.CrossRef
42.
go back to reference Malone JI, Morrison AD, Pavan PR, Cuthbertson DD. Prevalence and Significance of Retinopathy in Subjects With Type 1 Diabetes of Less Than 5 Years ’ Duration. Diabetes Care. 2001;24(3):522–6.CrossRefPubMed Malone JI, Morrison AD, Pavan PR, Cuthbertson DD. Prevalence and Significance of Retinopathy in Subjects With Type 1 Diabetes of Less Than 5 Years ’ Duration. Diabetes Care. 2001;24(3):522–6.CrossRefPubMed
Metadata
Title
Current epidemiology of diabetic retinopathy in patients with type 1 diabetes: a national multicenter study in Brazil
Authors
Laura Gomes Nunes Melo
Paulo Henrique Morales
Karla Rezende Guerra Drummond
Deborah Conte Santos
Marcela Haas Pizarro
Bianca Senger Vasconcelos Barros
Tessa Cerqueria Lemos Mattos
André Araújo Pinheiro
Felipe Mallmann
Franz Schubert Lopes Leal
Fernando Korn Malerbi
Marilia Brito Gomes
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2018
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-018-5859-x

Other articles of this Issue 1/2018

BMC Public Health 1/2018 Go to the issue