, Volume 66, Issue 2, pp 201–209 | Cite as

Risk factors for prevalent diabetic retinopathy and proliferative diabetic retinopathy in type 1 diabetes

  • Rita Laiginhas
  • Carolina Madeira
  • Miguel Lopes
  • João Sérgio Neves
  • Margarida Barbosa
  • Vitor Rosas
  • Davide Carvalho
  • Fernando Falcão-Reis
  • Manuel FalcãoEmail author
Original Article



Age at diagnosis of type 1 diabetes (DM1) has been implied as an important factor associated with the development of the microvascular complications. Our aim was to identify factors associated with prevalent diabetic retinopathy (DR) and proliferative diabetic retinopathy (PDR) in DM1 people with early and late-onset.


We reviewed medical records from all DM1 people from the reference area of a tertiary center (about 340,000 persons). Univariate and multivariate logistic regression were used to assess the relationship between potential risk factors (sociodemographic, diabetes-related, co-morbidities, and laboratory parameters) and prevalent DR/PDR. We performed an analysis comparing patients diagnosed before (early-onset) and after (late-onset) 18 years of age.


We included 140 patients in early-onset DM1 group and 169 in late-onset DM1 group. Longer duration of diabetes and HbA1c remained associated with prevalent DR in both groups after adjusting for potential risk factors. Nephropathy was associated with prevalent DR in the late-onset group but not in the early-onset group. Peripheral neuropathy remained associated with prevalent PDR when modeled together in the multivariate model. High BMI demonstrated a significative association with PDR in early but not in the late-onset DM1 group.


Although previous reports suggest that age at DM1 diagnosis may have a role in DR prevalence, the risk factors for DR in early and late-onset DM1 were similar for both groups. Duration of disease and lifelong metabolic control were the major predictors for DR in both groups. Nephropathy was associated with DR in patients with late-onset disease. Neuropathy was associated with PDR occurrence in both groups. BMI was associated with PDR early-onset DM1 group.


diabetic retinopathy type 1 diabetes late-onset risk factors microvascular disease 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    W.-P. You, M. Henneberg, Type 1 diabetes prevalence increasing globally and regionally: the role of natural selection and life expectancy at birth. BMJ Open Diabetes Res. Care. 4(1), e000161 (2016). CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    International Diabetes Federation. Diabetes Atlas, 8th edn. 2018. Accessed 8 Aug 2018.
  3. 3.
    D.M. Maahs, N.A. West, J.M. Lawrence, E.J. Mayer-Davis, Chapter 1: epidemiology of type 1 diabetes. Endocrinol. Metab. Clin. North Am. 39(3), 481–497 (2010). CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    P.A. Diaz-Valencia, P. Bougnères, A.-J. Valleron, Global epidemiology of type 1 diabetes in young adults and adults: a systematic review. BMC Public Health 15(1), 255 (2015). CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    N.J. Thomas, S.E. Jones, M.N. Weedon, B.M. Shields, R.A. Oram, A.T. Hattersley, Frequency and phenotype of type 1 diabetes in the first six decades of life: a cross-sectional, genetically stratified survival analysis from UK Biobank. Lancet Diabetes Endocrinol. 6(2), 122–129 (2018). CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    T. Bulum, M. Tomic, L. Duvnjak, Total serum cholesterol increases risk for development and progression of nonproliferative retinopathy in patients with type 1 diabetes without therapeutic intervention: Prospective, Observational Study. Arch. Med Res. 48(5), 467–471 (2017). CrossRefPubMedGoogle Scholar
  7. 7.
    J.E. Grunwald, J. Alexander, G.-S. Ying, et al., Retinopathy and chronic kidney disease in the Chronic Renal Insufficiency Cohort (CRIC) study. Arch. Ophthalmol. (Chic., Ill. 1960). 130(9), 1136–1144 (2012). CrossRefGoogle Scholar
  8. 8.
    J. Mehlsen, M. Erlandsen, P.L. Poulsen, T. Bek, Identification of independent risk factors for the development of diabetic retinopathy requiring treatment. Acta Ophthalmol. 89(6), 515–521 (2011). CrossRefPubMedGoogle Scholar
  9. 9.
    D.A. Stram, X. Jiang, R. Varma, et al., Factors associated with prevalent diabetic retinopathy in Chinese Americans: The Chinese American Eye Study. Ophthalmol Retin. 1–10. (2017) CrossRefGoogle Scholar
  10. 10.
    R.W. Jansson, K.O. Hufthammer, J. Krohn, Diabetic retinopathy in type 1 diabetes patients in Western Norway. Acta Ophthalmol. 1–10 (2018) CrossRefGoogle Scholar
  11. 11.
    E.Y.-C. Kang, F.-S. Lo, J.-P. Wang, et al., Nomogram for prediction of non-proliferative diabetic retinopathy in juvenile-onset type 1 diabetes: a cohort study in an Asian population. Sci. Rep. 8(1), 12164 (2018). CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    A.M. Diallo, J.L. Novella, C. Lukas, et al., Early predictors of diabetic retinopathy in type 1 diabetes: The Retinopathy Champagne Ardenne Diabète (ReCAD) study. J. Diabetes Complicat. 32(8), 753–758 (2018). CrossRefPubMedGoogle Scholar
  13. 13.
    S.Y. Wang, C.A. Andrews, W.H. Herman, T.W. Gardner, J.D. Stein, Incidence and risk factors for developing diabetic retinopathy among youths with type 1 or type 2 diabetes throughout the United States. Ophthalmology 124(4), 424–430 (2017). CrossRefPubMedGoogle Scholar
  14. 14.
    A. Penman, H. Hancock, E. Papavasileiou, et al., Risk factors for proliferative diabetic retinopathy in african americans with type 2 diabetes risk factors for proliferative diabetic retinopathy in African Americans with. 6586 (2016). CrossRefGoogle Scholar
  15. 15.
    R.V. Rivera-Virtudazo, A.K.G. Tapia, J.F.B. Valenzuela, L.D. Cruz, H.D. Mendoza, E.V. Castriciones, Lacunarity Analysis of TEM Images of Heat-Treated Hybrid Organosilica Materials. In: Innovations in Chemical Biology. Dordrecht: Springer Netherlands, Dordrechtp. 397–403.
  16. 16.
    M. Nordwall, M. Fredriksson, J. Ludvigsson, H.J. Arnqvist, Impact of age of onset, puberty, and glycemic control followed from diagnosis on incidence of retinopathy in type 1 diabetes: The VISS study. Diabetes Care. 42(4), 609–616 (2019). CrossRefPubMedGoogle Scholar
  17. 17.
    J.N. Kostraba, J.S. Dorman, T.J. Orchard, et al., Contribution of diabetes duration before puberty to development of microvascular complications in IDDM subjects. Diabetes Care. 12(10), 686–693 (1989). CrossRefPubMedGoogle Scholar
  18. 18.
    C.E. Kullberg, M. Abrahamsson, H.J. Arnqvist, K. Finnström, J. Ludvigsson, VISS Study Group. Prevalence of retinopathy differs with age at onset of diabetes in a population of patients with Type 1 diabetes. Diabet Med. 19(11):924–931. (2002). Accessed 29 Aug 2018CrossRefGoogle Scholar
  19. 19.
    Census 2011. INE, Instituto Nacional de Estatística (Statistics Portugal). (2011) Accessed 20 Aug 2008.
  20. 20.
    Z. Jorge, E. Lacerda Nobre, A. Macedo, J. Jácomede Castro, Prevalěncia da diabetes mellitus tipo 1 em Portugal, 1995-1999: Coorte de jovens do sexo masculino. Acta Med Port. 16(4), 251–253 (2003)PubMedGoogle Scholar
  21. 21.
    N.D.D. Group, Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. National Diabetes Data Group. Diabetes 28(12), 1039–1057 (1979). CrossRefGoogle Scholar
  22. 22.
    Diabetes Control and Complications Trial Research Group, D.M. Nathan, S. Genuth, et al., 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. 329(14), 977–986 (1993). CrossRefGoogle Scholar
  23. 23.
    UKPDS., Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet (Lond., Engl.). 352(9131), 837–853 (1998). Accessed 7 Oct 2018.
  24. 24.
    H.P. Hammes, W. Kerner, S. Hofer, et al., Diabetic retinopathy in type 1 diabetes—a contemporary analysis of 8,784 patients. Diabetologia 54(8), 1977–1984 (2011). CrossRefPubMedGoogle Scholar
  25. 25.
    K. Hietala, V. Harjutsalo, C. Forsblom, P. Summanen, P.-H. Groop, FinnDiane Study Group on behalf of the FS. Age at onset and the risk of proliferative retinopathy in type 1 diabetes. Diabetes Care. 33(6), 1315–1319 (2010). CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    L. Forga, M.J. Goñi, B. Ibáñez, K. Cambra, M. García-Mouriz, A. Iriarte, Influence of age at diagnosis and time-dependent risk factors on the development of diabetic retinopathy in patients with type 1 diabetes. J. Diabetes Res. 2016, 9898309 (2016). CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    N. Patel, L. Verchinina, M. Wichorek, et al., Identification of population characteristics through implementation of the Comprehensive Diabetic Retinopathy Program. Clin. Diabetes Endocrinol. 5(1), 1–8 (2019). CrossRefGoogle Scholar
  28. 28.
    A.R. Shah, A.N. Van Horn, L. Verchinina, et al., Blood Pressure Is Associated with Receiving Intravitreal Anti–Vascular Endothelial Growth Factor Treatment in Patients with Diabetes. Ophthalmol. Retin. 3(5), 410–416 (2019). CrossRefGoogle Scholar
  29. 29.
    M.B. Larsen, J.E. Henriksen, J. Grauslund, T. Peto, Prevalence and risk factors for diabetic retinopathy in 17 152 patients from the island of Funen, Denmark. Acta Ophthalmol. 95(8), 778–786 (2017). CrossRefPubMedGoogle Scholar
  30. 30.
    B.E.K. Klein, K.L. Horak, K.E. Lee, et al., Neural dysfunction and retinopathy in persons with type 1 diabetes. Ophthalmic Epidemiol. 25(5–6), 373–378 (2018). CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    B. Pemp, S. Palkovits, K. Howorka, et al., Correlation of retinal neurodegeneration with measures of peripheral autonomic neuropathy in type 1 diabetes. Acta Ophthalmol. 96(7), e804–810. (2018). CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Rita Laiginhas
    • 1
    • 2
  • Carolina Madeira
    • 3
  • Miguel Lopes
    • 1
  • João Sérgio Neves
    • 4
    • 5
  • Margarida Barbosa
    • 1
    • 6
    • 7
  • Vitor Rosas
    • 3
  • Davide Carvalho
    • 4
    • 8
  • Fernando Falcão-Reis
    • 3
    • 5
  • Manuel Falcão
    • 3
    • 5
    Email author
  1. 1.Faculty of MedicinePorto UniversityPortoPortugal
  2. 2.Department of OphthalmologyCentro Hospitalar de Entre o Douro e VougaSanta Maria da FeiraPortugal
  3. 3.Department of OphthalmologyCentro Hospitalar de São JoãoPortoPortugal
  4. 4.Department of Endocrinology, Diabetes and MetabolismCentro Hospitalar de São JoãoPortoPortugal
  5. 5.Department of Surgery and PhysiologyFaculty of Medicine of Porto UniversityPortoPortugal
  6. 6.Department of AnesthesiologyCentro Hospitalar de São JoãoPortoPortugal
  7. 7.I3S Instituto de Investigação e Inovação em SaúdeUniversity of PortoPortoPortugal
  8. 8.Department of Endocrinology, Diabetes and MetabolismFaculty of Medicine of Porto UniversityPortoPortugal

Personalised recommendations