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Review
. 2023 Feb 22;2(2):CD013775.
doi: 10.1002/14651858.CD013775.pub2.

Prognostic factors for the development and progression of proliferative diabetic retinopathy in people with diabetic retinopathy

Jennifer Perais  1 , Ridhi Agarwal  2 , Jennifer R Evans  3 , Emma Loveman  4 , Jill L Colquitt  4 , David Owens  5 , Ruth E Hogg  6 , John G Lawrenson  7 , Yemisi Takwoingi  2 , Noemi Lois  8
Affiliations
Review

Prognostic factors for the development and progression of proliferative diabetic retinopathy in people with diabetic retinopathy

Jennifer Perais et al. Cochrane Database Syst Rev. .

Abstract
in English, Spanish

Background: Diabetic retinopathy (DR) is characterised by neurovascular degeneration as a result of chronic hyperglycaemia. Proliferative diabetic retinopathy (PDR) is the most serious complication of DR and can lead to total (central and peripheral) visual loss. PDR is characterised by the presence of abnormal new blood vessels, so-called "new vessels," at the optic disc (NVD) or elsewhere in the retina (NVE). PDR can progress to high-risk characteristics (HRC) PDR (HRC-PDR), which is defined by the presence of NVD more than one-fourth to one-third disc area in size plus vitreous haemorrhage or pre-retinal haemorrhage, or vitreous haemorrhage or pre-retinal haemorrhage obscuring more than one disc area. In severe cases, fibrovascular membranes grow over the retinal surface and tractional retinal detachment with sight loss can occur, despite treatment. Although most, if not all, individuals with diabetes will develop DR if they live long enough, only some progress to the sight-threatening PDR stage. OBJECTIVES: To determine risk factors for the development of PDR and HRC-PDR in people with diabetes and DR.

Search methods: We searched the Cochrane Central Register of Controlled Trials (CENTRAL; which contains the Cochrane Eyes and Vision Trials Register; 2022, Issue 5), Ovid MEDLINE, and Ovid Embase. The date of the search was 27 May 2022. Additionally, the search was supplemented by screening reference lists of eligible articles. There were no restrictions to language or year of publication. SELECTION CRITERIA: We included prospective or retrospective cohort studies and case-control longitudinal studies evaluating prognostic factors for the development and progression of PDR, in people who have not had previous treatment for DR. The target population consisted of adults (≥18 years of age) of any gender, sexual orientation, ethnicity, socioeconomic status, and geographical location, with non-proliferative diabetic retinopathy (NPDR) or PDR with less than HRC-PDR, diagnosed as per standard clinical practice. Two review authors independently screened titles and abstracts, and full-text articles, to determine eligibility; discrepancies were resolved through discussion. We considered prognostic factors measured at baseline and any other time points during the study and in any clinical setting. Outcomes were evaluated at three and eight years (± two years) or lifelong. DATA COLLECTION AND ANALYSIS: Two review authors independently extracted data from included studies using a data extraction form that we developed and piloted prior to the data collection stage. We resolved any discrepancies through discussion. We used the Quality in Prognosis Studies (QUIPS) tool to assess risk of bias. We conducted meta-analyses in clinically relevant groups using a random-effects approach. We reported hazard ratios (HR), odds ratios (OR), and risk ratios (RR) separately for each available prognostic factor and outcome, stratified by different time points. Where possible, we meta-analysed adjusted prognostic factors. We evaluated the certainty of the evidence with an adapted version of the GRADE framework. MAIN RESULTS: We screened 6391 records. From these, we identified 59 studies (87 articles) as eligible for inclusion. Thirty-five were prospective cohort studies, 22 were retrospective studies, 18 of which were cohort and six were based on data from electronic registers, and two were retrospective case-control studies. Twenty-three studies evaluated participants with type 1 diabetes (T1D), 19 with type 2 diabetes (T2D), and 17 included mixed populations (T1D and T2D). Studies on T1D included between 39 and 3250 participants at baseline, followed up for one to 45 years. Studies on T2D included between 100 and 71,817 participants at baseline, followed up for one to 20 years. The studies on mixed populations of T1D and T2D ranged from 76 to 32,553 participants at baseline, followed up for four to 25 years. We found evidence indicating that higher glycated haemoglobin (haemoglobin A1c (HbA1c)) levels (adjusted OR ranged from 1.11 (95% confidence interval (CI) 0.93 to 1.32) to 2.10 (95% CI 1.64 to 2.69) and more advanced stages of retinopathy (adjusted OR ranged from 1.38 (95% CI 1.29 to 1.48) to 12.40 (95% CI 5.31 to 28.98) are independent risk factors for the development of PDR in people with T1D and T2D. We rated the evidence for these factors as of moderate certainty because of moderate to high risk of bias in the studies. There was also some evidence suggesting several markers for renal disease (for example, nephropathy (adjusted OR ranged from 1.58 (95% CI not reported) to 2.68 (2.09 to 3.42), and creatinine (adjusted meta-analysis HR 1.61 (95% CI 0.77 to 3.36)), and, in people with T1D, age at diagnosis of diabetes (< 12 years of age) (standardised regression estimate 1.62, 95% CI 1.06 to 2.48), increased triglyceride levels (adjusted RR 1.55, 95% CI 1.06 to 1.95), and larger retinal venular diameters (RR 4.28, 95% CI 1.50 to 12.19) may increase the risk of progression to PDR. The certainty of evidence for these factors, however, was low to very low, due to risk of bias in the included studies, inconsistency (lack of studies preventing the grading of consistency or variable outcomes), and imprecision (wide CIs). There was no substantial and consistent evidence to support duration of diabetes, systolic or diastolic blood pressure, total cholesterol, low- (LDL) and high- (HDL) density lipoproteins, gender, ethnicity, body mass index (BMI), socioeconomic status, or tobacco and alcohol consumption as being associated with incidence of PDR. There was insufficient evidence to evaluate prognostic factors associated with progression of PDR to HRC-PDR. AUTHORS' CONCLUSIONS: Increased HbA1c is likely to be associated with progression to PDR; therefore, maintaining adequate glucose control throughout life, irrespective of stage of DR severity, may help to prevent progression to PDR and risk of its sight-threatening complications. Renal impairment in people with T1D or T2D, as well as younger age at diagnosis of diabetes mellitus (DM), increased triglyceride levels, and increased retinal venular diameters in people with T1D may also be associated with increased risk of progression to PDR. Given that more advanced DR severity is associated with higher risk of progression to PDR, the earlier the disease is identified, and the above systemic risk factors are controlled, the greater the chance of reducing the risk of PDR and saving sight.

Antecedentes: La retinopatía diabética (RD) se caracteriza por la degeneración neurovascular como consecuencia de la hiperglucemia crónica. La retinopatía diabética proliferativa (RDP) es la complicación más grave de la RD y puede provocar una pérdida total (central y periférica) de la visión. La RDP se caracteriza por la presencia de vasos sanguíneos de neoformación anormales, neovascularización, en la papila óptica (NVP) o en cualquier otra parte de la retina (NVE). La RDP puede evolucionar a una RDP con características de alto riesgo (RDP‐CAR), que se define por la presencia de NVP de más de un cuarto a un tercio del área discal más hemorragia vítrea o prerretiniana, o hemorragia vítrea o prerretiniana que oscurece más de un área papilar. En los casos graves, crecen membranas fibrovasculares sobre la superficie retiniana y se puede producir un desprendimiento de retina por tracción con pérdida de la visión, a pesar del tratamiento. Aunque la mayoría de las personas con diabetes, si no todas, desarrollarán RD si viven lo suficiente, solo algunas llegan a la fase de RDP, que pone en peligro la vista.

Objetivos: Determinar los factores de riesgo de aparición de la RDP y RDP‐CAR en personas con diabetes y RD. MÉTODOS DE BÚSQUEDA: Se hicieron búsquedas en el Registro Cochrane central de ensayos controlados (Cochrane Central Register of Controlled Trials, CENTRAL; que contiene el Registro de ensayos del Grupo Cochrane de Salud ocular y de la visión [Cochrane Eyes and Vision]; 2022, número 5), Ovid MEDLINE y Ovid Embase. La fecha de búsqueda fue el 27 de mayo de 2022. Además, la búsqueda se complementó con el cribado de las listas de referencias de los artículos elegibles. No hubo restricciones en cuanto al idioma ni al año de publicación. CRITERIOS DE SELECCIÓN: Se incluyeron estudios de cohortes prospectivos o retrospectivos y estudios longitudinales de casos y controles que evaluaran los factores pronósticos para la aparición y la progresión de la RDP, en personas que no habían recibido tratamiento previo para la RD. La población de interés estaba formada por adultos (≥18 años de edad) de cualquier sexo, orientación sexual, etnia, nivel socioeconómico y ubicación geográfica, con retinopatía diabética no proliferativa (RDNP) o RDP sin llegar a RDP‐CAR, diagnosticada según la práctica clínica habitual. Dos autores de la revisión examinaron de forma independiente los títulos y resúmenes, así como los artículos completos, para determinar la elegibilidad; las discrepancias se resolvieron mediante debate. Se tuvieron en cuenta los factores pronósticos medidos al inicio del estudio y en cualquier otro punto temporal durante el estudio y en cualquier contexto clínico. Los desenlaces se evaluaron a los tres y ocho años (± dos años) o de por vida. OBTENCIÓN Y ANÁLISIS DE LOS DATOS: Dos autores de la revisión extrajeron de forma independiente los datos de los estudios incluidos mediante un formulario de extracción de datos que se desarrolló y evaluó antes de la etapa de obtención de datos. Las discrepancias se resolvieron mediante debate. Para evaluar el riesgo de sesgo se utilizó la herramienta Quality in Prognosis Studies (QUIPS). Se realizaron metanálisis en grupos clínicamente relevantes utilizando un enfoque de efectos aleatorios. Se proporcionaron los cociente de riesgos instantáneos (CRI), los odds ratios (OR) y las razones de riesgos (RR) por separado para cada factor pronóstico y desenlace disponibles, estratificados por diferentes puntos temporales. Cuando fue posible, se realizó un metanálisis de los factores pronósticos ajustados. La certeza de la evidencia se evaluó con una versión adaptada del método GRADE.

Resultados principales: Se han examinado 6391 registros. A partir de estos se identificaron 59 estudios (87 artículos) elegibles para inclusión. Treinta y cinco fueron estudios de cohortes prospectivos, 22 fueron estudios retrospectivos, 18 de los cuales fueron de cohortes y 6 se basaron en datos de registros electrónicos, y 2 fueron estudios retrospectivos de casos y controles. Veintitrés estudios evaluaron a participantes con diabetes tipo 1 (DT1), 19 con diabetes tipo 2 (DT2) y 17 incluyeron poblaciones mixtas (DT1 y DT2). Los estudios sobre la DT1 incluyeron entre 39 y 3250 participantes al inicio del estudio, con un seguimiento de 1 a 45 años. Los estudios sobre la DT2 incluyeron entre 100 y 71 817 participantes al inicio del estudio, con un seguimiento de 1 a 20 años. Los estudios sobre poblaciones mixtas de DT1 y DT2 variaron entre 76 y 32 553 participantes al inicio del estudio, con un seguimiento de 4 a 25 años. Se encontró evidencia que indicó que los niveles más altos de hemoglobina glucosilada (hemoglobina A1c [HbA1c]) (OR ajustado que varió de 1,11 [intervalo de confianza (IC) del 95%: 0,93 a 1,32] a 2,10 [IC del 95%: 1,64 a 2,69]) y los estadios más avanzados de retinopatía (OR ajustado que varió entre 1,38 [IC del 95%: 1,29 a 1,48] y 12,40 [IC del 95%: 5,31 a 28,98]) son factores de riesgo independientes para el desarrollo de RDP en personas con DT1 y DT2. La evidencia para estos factores se consideró de certeza moderada debido al riesgo moderado a alto de sesgo en los estudios. También hubo alguna evidencia que indicó varios marcadores de enfermedad renal (por ejemplo, nefropatía [OR ajustado que varió entre 1,58 (IC del 95% no proporcionado) y 2,68 (2,09 a 3,42)] y creatinina [metanálisis ajustado CRI 1,61 (IC del 95%: 0,77 a 3.36)]), y, en las personas con DT1, la edad en el momento del diagnóstico de la diabetes (< 12 años) (estimación de la regresión estandarizada 1,62; IC del 95%: 1,06 a 2,48), el aumento de los niveles de triglicéridos (RR ajustado 1,55; IC del 95%: 1,06 a 1,95) y los diámetros venulares retinianos mayores (RR 4,28; IC del 95%: 1,50 a 12,19) podrían aumentar el riesgo de progresión a RDP. Sin embargo, la certeza de la evidencia para estos factores fue de baja a muy baja, debido al riesgo de sesgo en los estudios incluidos, la inconsistencia (falta de estudios que impide la calificación de consistencia o desenlaces variables) y la imprecisión (IC amplios). No hubo evidencia importante ni consistente que apoyara que la duración de la diabetes, la presión arterial sistólica o diastólica, el colesterol total, las lipoproteínas de baja (LDL) y alta (HDL) densidad, el sexo, el origen étnico, el índice de masa corporal (IMC), el nivel socioeconómico o el consumo de tabaco y alcohol estuvieran asociados con la incidencia de RDP. No hubo evidencia suficiente para evaluar los factores pronósticos asociados con la progresión de la RDP a RDP‐CAR.

Conclusiones de los autores: Es probable que el aumento de la HbA1c se asocie con la progresión a la RDP; por lo tanto, mantener un control adecuado de la glucosa durante toda la vida, independientemente del estadio de gravedad de la RD, podría ayudar a prevenir la progresión a la RDP y el riesgo de sus complicaciones que ponen en peligro la vista. La insuficiencia renal en personas con DT1 o DT2, así como una menor edad en el momento del diagnóstico de la diabetes mellitus (DM), el aumento de los niveles de triglicéridos y el aumento de los diámetros venulares retinianos en personas con DT1 también se podrían asociar con un mayor riesgo de progresión a RDP. Dado que la gravedad más avanzada de la RD se asocia con un mayor riesgo de progresión a RDP, cuanto antes se identifique la enfermedad y se controlen los factores de riesgo sistémicos mencionados, mayores serán las posibilidades de reducir el riesgo de RDP y conservar la vista.

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Conflict of interest statement

JP: none known. RA: none known. RF: none known. RH has participated in Novartis Advisory boards relating to biomarkers and clinical trial outcomes for age‐related macular degeneration. JL: none known. JE: none known. YT: none known. NL: none known.

Figures

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PRISMA study flow diagram
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Risk of bias summary: review authors' judgements about each methodological quality item for each included study
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Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies
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Forest plot of unadjusted hazard ratio estimates
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5
Forest plot of adjusted hazard ratio estimates for diastolic blood pressure and creatinine
See this image and copyright information in PMC

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References

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Rodriguez‐Villalobos 2005 {published data only}
    1. Rodriguez-Villalobos E, Cervantes-Aguayo F, Vargas-Salado E, Avalos-Munoz ME, Juarez-Becerril DM, Ramirez-Barba EJ. Diabetic retinopathy: twelve-year incidence and progression. Cirugia y Cirujanos 2005;73(2):79-84. - PubMed
Roy 2006 {published data only}
    1. Roy MS, Affouf M. Six-year progression of retinopathy and associated risk factors in African American patients with type 1 diabetes mellitus: the New Jersey 725. Archives of Ophthalmology 2006;124(9):1297-306. - PubMed
    1. Roy MS, Klein R, Janal MN. Retinal venular diameter as an early indicator of progression to proliferative diabetic retinopathy with and without high-risk characteristics in African Americans with type 1 diabetes mellitus. Archives of Ophthalmology 2011;129(1):8-15. - PubMed
Rudnisky 2017 {published data only}
    1. Rudnisky CJ, Wong BK, Virani H, Tennant MT. Risk factors for progression of diabetic retinopathy in Alberta First Nations communities. Canadian Journal of Ophthalmology 2017;52(Suppl 1):S19-29. - PubMed
Silva 2015 {published data only}
    1. Silva PS, Cavallerano JD, Haddad NM, Kwak H, Dyer KH, Omar AF, et al. Peripheral lesions identified on ultrawide field imaging predict increased risk of diabetic retinopathy progression over 4 years. Ophthalmology 2015;122(5):949-56. - PubMed
Simonsen 1980 {published data only}
    1. Simonsen SE. The value of the oscillatory potential in selecting juvenile diabetics at risk of developing proliferative retinopathy. Acta Ophthalmologica 1980;58(6):865-78. - PubMed
Skrivarhaug 2006 {published data only}
    1. Skrivarhaug T, Fosmark DS, Stene LC, Bangstad HJ, Sandvik L, Hanssen KF, et al. Low cumulative incidence of proliferative retinopathy in childhood-onset type 1 diabetes: a 24-year follow-up study. Diabetologia 2006;49(10):2281-90. - PubMed
Styles 2000 {published data only}
    1. Styles CJ, Dodds W, Watkins P, McHugh D, Blach R. Development of proliferative retinopathy in patients with long-standing insulin-dependent diabetes mellitus. Eye 2000;14(Pt 6):851-4. - PubMed
Teuscher 1988 {published data only}
    1. Diabetes Drafting Group. Prevalence of small vessel and large vessel disease in diabetic patients from 14 centres. The World Health Organization Multinational Study of Vascular Disease in Diabetics. Diabetologia 1985;28(Suppl):615-40. - PubMed
    1. Teuscher A, Schnell H, Wilson PW. Incidence of diabetic retinopathy and relationship to baseline plasma glucose and blood pressure. Diabetes Care 1988;11(3):246-51. - PubMed
Valone 1981 {published data only}
    1. Valone JA Jr, McMeel JW, Franks EP. Unilateral proliferative diabetic retinopathy. II. Clinical course. Archives of Ophthalmology 1981;99(8):1362-6. - PubMed
Varma 2010 {published data only}
    1. Varma R, Choudhury F, Klein R, Chung J, Torres M, Azen SP, et al. Four-year incidence and progression of diabetic retinopathy and macular edema: the Los Angeles Latino Eye Study. American Journal of Ophthalmology 2010;149(5):752-3. - PMC - PubMed
Verdaguer 2009 {published data only}
    1. Verdaguer J, Zanolli M, Sepulveda G, Garcia de Los Rios M, Dominguez A. Natural history of diabetic retinopathy in a retrospective cohort of type 1 diabetics. Revista Medica de Chile 2009;137(9):1145-52. - PubMed
Vesteinsdottir 2010 {published data only}
    1. Vesteinsdottir E, Bjornsdottir S, Hreidarsson AB, Stefansson E. Risk of retinal neovascularization in the second eye in patients with proliferative diabetic retinopathy. Acta Ophthalmologica 2010;88(4):449-52. - PubMed
Voigt 2018 {published data only}
    1. Voigt M, Schmidt S, Lehmann T, Kohler B, Kloos C, Voigt UA, et al. Prevalence and progression rate of diabetic retinopathy in type 2 diabetes patients in correlation with the duration of diabetes. Experimental and Clinical Endocrinology and Diabetes 2018;126(9):570-6. - PubMed
WESDR {published data only}
    1. Cruickshanks KJ, Moss SE, Klein R, Klein BE. Physical activity and the risk of progression of retinopathy or the development of proliferative retinopathy. Ophthalmology 1995;102(8):1177-82. - PubMed
    1. Klein BE, Klein R, Moss SE, Palta M. A cohort study of the relationship of diabetic retinopathy to blood pressure. Archives of Ophthalmology 1995;113(5):601-6. [Klein 1995a] - PubMed
    1. Klein R, Klein BE, Jensen SC, Moss SE. The relation of socioeconomic factors to the incidence of proliferative diabetic retinopathy and loss of vision. Ophthalmology 1994;101(1):68-76. [Klein 1994a] - PubMed
    1. Klein R, Klein BE, Moss SE, Cruickshanks KJ. Relationship of hyperglycemia to the long-term incidence and progression of diabetic retinopathy. Archives of Internal Medicine 1994;154(19):2169-78. [Klein 1994c] - PubMed
    1. Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XVII. The 14-year incidence and progression of diabetic retinopathy and associated risk factors in type 1 diabetes. Ophthalmology 1998;105(10):1801-15. - PubMed
Yokoyama 1994 {published data only}
    1. Yokoyama H, Uchigata Y, Otani T, Aoki K, Maruyama A, Maruyama H, et al. Development of proliferative retinopathy in Japanese patients with IDDM: Tokyo Women's Medical College Epidemiologic Study. Diabetes Research and Clinical Practice 1994;24(2):113-9. - PubMed
Zavrelova 2011 {published data only}
    1. Zavrelova H, Hoekstra T, Alssema M, Welschen LM, Nijpels G, Moll AC, et al. Progression and regression: distinct developmental patterns of diabetic retinopathy in patients with type 2 diabetes treated in the diabetes care system West-Friesland, the Netherlands. Diabetes Care 2011;34(4):867-72. - PMC - PubMed

References to studies excluded from this review

Abougalambou 2015 {published data only}
    1. Abougalambou SS, Abougalambou AS. Risk factors associated with diabetic retinopathy among type 2 diabetes patients at teaching hospital in Malaysia. Diabetes and Metabolic Syndrome 2015;9(2):98-103. - PubMed
Adderley 2020 {published data only}
    1. Adderley NJ, Subramanian A, Toulis K, Gokhale K, Taverner T, Hanif W, et al. Obstructive sleep apnea, a risk factor for cardiovascular and microvascular disease in patients with type 2 diabetes: findings from a population-based cohort study. Diabetes Care 2020;43(8):1868-77. - PubMed
Adnitt 1970 {published data only}
    1. Adnitt PI, Taylor E. Progression of diabetic retinopathy. Relationship to blood-sugar. Lancet 1970;1(7648):652-4. - PubMed
Advance Collaborative Group 2008 {published data only}
    1. Advance Collaborative Group: Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, et al . Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. New England Journal of Medicine 2008;358(24):2560-72. - PubMed
Alattas 2022 {published data only}
    1. Alattas K, Alsulami DW, Alem RH, Alotaibi FS, Alghamdi BA, Baeesa LS. Relation between lipid profile, blood pressure and retinopathy in diabetic patients in King Abdulaziz University hospital: a retrospective record review study. International Journal of Retina and Vitreous 2022;8(1):20. - PMC - PubMed
Altaf 2013 {published data only}
    1. Altaf Q, Dodson P, Ali A, Raymond NT, Wharton H, Fellows H, et al. Obstructive sleep apnoea is associated with sight threatening retinopathy and predicts the development of preproliferative and proliferative retinopathy in patients with Type 2 diabetes: a longitudinal analysis. Diabetic Medicine 2013;30(1 Suppl):E5.
    1. Altaf QA, Dodson P, Ali A, Raymond NT, Wharton H, Fellows H, et al. Obstructive sleep apnoea predicts the development of preproliferative and proliferative retinopathy in patients with type 2 diabetes: a longitudinal analysis. Diabetologia 2013;56(Suppl 1):S490.
Ashakiran 2011 {published data only}
    1. Ashakiran S, Krishnamurthy N, Navin S, Patil S. Behaviour of serum uric acid and lipid profile in relation to glycemic status in proliferative and non-proliferative diabetic retinopathy. Current Neurobiology 2011;2(1):57-61.
Askarishahi 2011 {published data only}
    1. Askarishahi M, Hajizadeh E, Afkhami-Ardakani M. Factors affecting retinopathy in patients with type 2 diabetes by analyzing the current status data. Tehran University Medical Journal 2011;68(11):674-80.
Barr 2001 {published data only}
    1. Barr CC. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive insulin therapy, by The Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. N. Engl. J. Med 342:381-9, 2000. Survey of Ophthalmology 2001;45(5):459-60. - PubMed
Beulens 2009 {published data only}
    1. Beulens JW, Patel A, Vingerling JR, Cruickshank JK, Hughes AD, Stanton A, et al. Effects of blood pressure lowering and intensive glucose control on the incidence and progression of retinopathy in patients with type 2 diabetes mellitus: a randomised controlled trial. Diabetologia 2009;52(10):2027-36. - PubMed
Borch‐Johnsen 1987 {published data only}
    1. Borch-Johnsen K, Nissen H, Henriksen E, Kreiner S, Salling N, Deckert T, et al. The natural history of insulin-dependent diabetes mellitus in Denmark: 1. Long-term survival with and without late diabetic complications. Diabetic Medicine 1987;4(3):201-10. - PubMed
Bresnick 1987 {published data only}
    1. Bresnick GH, Palta M. Predicting progression to severe proliferative diabetic retinopathy. Archives of Ophthalmology 1987;105(6):810-4. - PubMed
Brinchmann‐Hansen 1985 {published data only}
    1. Brinchmann-Hansen O, Dahl-Jorgensen K, Hanssen KF, Sandvik L. Effects of intensified insulin treatment on various lesions of diabetic retinopathy. American Journal of Ophthalmology 1985;100(5):644-53. - PubMed
    1. Brinchmann-Hansen O, Dahl-Jorgensen K, Sandvik L, Hanssen KF. Blood glucose concentrations and progression of diabetic retinopathy: the seven year results of the Oslo study. BMJ 1992;304(6818):19-22. - PMC - PubMed
    1. Dahl-Jorgensen K, Brinchmann-Hansen O, Hanssen KF, Sandvik L, Aagenaes O. Rapid tightening of blood glucose control leads to transient deterioration of retinopathy in insulin dependent diabetes mellitus: the Oslo study. BMJ 1985;290(6471):811-5. - PMC - PubMed
Burton 2000 {published data only}
    1. Burton AJ, Reynolds A, O'Neill D. Sildenafil (Viagra) a cause of proliferative diabetic retinopathy? Eye 2000;14(5):785-6. - PubMed
Cantagallo 1989 {published data only}
    1. Cantagallo A. Epidemiology of diabetic retinopathy. Annali di Igiene : Medicina Preventiva e di Comunita 1989;1(3-4):591-620. - PubMed
Chahal 1985 {published data only}
    1. Chaha P, Inglesby DV, Sleightholm M, Kohner EM. Blood pressure and the progression of mild background diabetic retinopathy. Hypertension 1985;7(6 Pt 2):II79-83. - PubMed
Chaturvedi 1998 {published data only}
    1. Chaturvedi N, Sjolie AK, Stephenson JM, Abrahamian H, Keipes M, Castellarin A, et al. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes. Lancet 1998;351(9095):28-31. - PubMed
Chawla 2015 {published data only}
    1. Chawla A, Chawla R. Correlation between diabetic retinopathy microalbuminuria and other modifiable risk factors. International Journal of Diabetes in Developing Countries 2015;35(4 Suppl):S587-90.
Chen 2017 {published data only}
    1. Chen YT, Huon LK, Liu SY. Sleep apnea does not increase risk of diabetic retinopathy: a nationwide population-based study. Sleep Medicine 2017;40(1 Suppl):e57-8.
Chen 2020 {published data only}
    1. Chen DJ, Kuo J, Wright AJ, Chuang A, Crowell EL. Estimating progression and effect of HbA1C in nonproliferative diabetic retinopathy. Investigative Ophthalmology and Visual Science 2020;61(7):ARVO E-abstract 277.
Chew 2014 {published data only}
    1. 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. - PMC - PubMed
Chittimoju 2013 {published data only}
    1. Chittimoju VK, Pasula S. Study of serum magnesium, HBA1c and microalbuminuria in diabetic retinopathy. International Journal of Pharma and Bio Sciences 2013;4(3):B501-9.
Chung 2019 {published data only}
    1. Chung YR, Ha KH, Kim HC, Park SJ, Lee K, Kim DJ. Dipeptidyl peptidase-4 inhibitors versus other antidiabetic drugs added to metformin monotherapy in diabetic retinopathy progression: a real world-based cohort study. Diabetes and Metabolism Journal 2019;43(5):640-8. - PMC - PubMed
Cikamatana 2007 {published data only}
    1. Cikamatana L, Mitchell P, Rochtchina E, Foran S, Wang JJ. Five-year incidence and progression of diabetic retinopathy in a defined older population: the Blue Mountains Eye Study. Eye 2007;21(4):465-71. - PubMed
Cohen 1991 {published data only}
    1. Cohen DL, Neil HA, Thorogood M, Mann JI. A population‐based study of the incidence of complications associated with type 2 diabetes in the elderly. Diabetic Medicine 1991;8(10):928-33. - PubMed
Colin 2012 {published data only}
    1. Colin TS, Kiong NW, Wong HK, Yang FP. New insights into diabetic retinopathy-risk factors for prevalence, incidence and progression in Asians. Annals of the Academy of Medicine Singapore 2012;41(9 Suppl 1):S111.
Cuadras 2017 {published data only}
    1. Cuadras UD, Dominguez BY, Riano CR, Jimenez-Sierra JM, Hernandez-Zimbron LF, Rojas OV. Quantification of VEGF in peripheral blood as a marker of activity in diabetic retinopathy. Investigative Ophthalmology and Visual Science 2017;58(8):ARVO E-abstract 5027.
Danielsen 1983 {published data only}
    1. Danielsen R, Helgason T, Jonasson F. Prognostic factors and retinopathy in type 1 diabetics in Iceland. Acta Medica Scandinavica 1983;213(5):323-6. - PubMed
DCCT 1993 {published data only}
    1. Diabetes Control and Complications Trial Research Group, Nathan DM, Genuth S, Lachin J, Cleary P, Crofford O, et al . The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. New England Journal of Medicine 1993;329(14):977-86. - PubMed
    1. Diabetes Control and Complications Trial Research Group. Progression of retinopathy with intensive versus conventional treatment in the Diabetes Control and Complications Trial. Ophthalmology 1995;102(4):647-61. - PubMed
    1. Diabetes Control and Complications Trial Research Group. The effect of intensive diabetes treatment on the progression of diabetic retinopathy in insulin dependent diabetes mellitus. Archives of Ophthalmology 1995;113(1):36-51. - PubMed
Ding 2020 {published data only}
    1. Ding Y, Zhao J, Liu G, Li Y, Jiang J, Meng Y, et al. Total bilirubin predicts severe progression of diabetic retinopathy and the possible causal mechanism. Journal of Diabetes Research 2020;2020:[7 p.]. [DOI: 10.1155/2020/7219852] - DOI - PMC - PubMed
Dizdarevic 2012 {published data only}
    1. Dizdarevic A, Alikadic-Husovic A, Jusufovic V. Risk factors and diabetic retinopathy. Medicinski Glasnik 2012;9(1):104-6. - PubMed
Duckworth 2009 {published data only}
    1. Duckworth W, Abraira C, Moritz T, Reda D, Emanuele N, Reaven PD, et al. Glucose control and vascular complications in veterans with type 2 diabetes. New England Journal of Medicine 2009;360(2):129-39. - PubMed
Dujic 1998 {published data only}
    1. Dujic M, Misailovic K, Nikolic LJ, Ignjacev M. Occurrence of changes in the eye in diabetic retinopathy with significant myopia. Srpski Arhiv za Celokupno Lekarstvo 1998;126(11-12):457-60. - PubMed
Elshafei 2011 {published data only}
    1. Elshafei M, Gamra H, Khandekar R, Al Hashimi M, Pai A, Ahmed MF. Prevalence and determinants of diabetic retinopathy among persons >= 40 years of age with diabetes in Qatar: a community-based survey. European Journal of Ophthalmology 2011;21(1):39-47. - PubMed
Estacio 2000 {published data only}
    1. Estacio RO, Jeffers BW, Gifford N, Schrier RW. Effect of blood pressure control on diabetic microvascular complications in patients with hypertension and type 2 diabetes. Diabetes Care 2000;23 (2 Suppl):B54-64. - PubMed
ETDRS 1991c {published data only}
    1. Davis MD, Fisher MR, Gangnon RE, Barton F, Aiello LM, Chew EY, et al. Risk factors for high-risk proliferative diabetic retinopathy and severe visual loss: Early Treatment Diabetic Retinopathy Study report number 18. Investigative Ophthalmology and Visual Science 1998;39(2):233-52. - PubMed
    1. Early Treatment Diabetic Retinopathy Study Research Group. Effects of aspirin treatment on diabetic retinopathy. ETDRS report number 8. Ophthalmology 1991;98(5 Suppl):757-65. - PubMed
    1. Early Treatment Diabetic Retinopathy Study Research Group. Fluorescein angiographic risk factors for progression of diabetic retinopathy. ETDRS report number 13. Ophthalmology 1991;98(5 Suppl):834-40. - PubMed
    1. Early Treatment Diabetic Retinopathy Study Research Group. Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Ophthalmology 1991;98(5 Suppl):823-33. - PubMed
Foshati 2019 {published data only}
    1. Foshati S, Sabeti M, Zamani A. Predicting retinopathy risk among diabetic patients: a data mining approach. Biomedical Engineering - Applications, Basis and Communications 2019;31(2):1950015.
Friberg 1985 {published data only}
    1. Friberg TR, Rosenstock J, Sanborn G, Vaghefi A, Raskin P. The effect of long-term near normal glycemic control on mild diabetic retinopathy. Ophthalmology 1985;92(8):1051-8. - PubMed
Fung 2011 {published data only}
    1. Fung MM, Yap MK, Cheng KK. Community-based diabetic retinopathy screening in Hong Kong: ocular findings. Clinical and Experimental Optometry 2011;94(1):63-6. - PubMed
Fusi‐Rubiano 2015 {published data only}
    1. Fusi-Rubiano WJ, Ramsamy G, Gillani S, Bhatnagar A, Singh B, Raghavan R. Evaluation of medically treatable risk factors in subjects with significant diabetic retinopathy from a local health economy area in the UK. Diabetologia 2015;58(1 Suppl 1):S521.
Gallagher 2018 {published data only}
    1. Gallagher JR, Luckett JP, Reinoso M. Diabetic retinopathy: trends of posterior pole and peripheral involvement. Investigative Ophthalmology and Visual Science 2018;59(9):ARVO E-abstract 1888.
Gao 2014 {published data only}
    1. Gao X, Gauderman WJ, Marjoram P, Torres M, Chen YD, Taylor KD, et al. Native American ancestry is associated with severe diabetic retinopathy in Latinos. Investigative Ophthalmology and Visual Science 2014;55(9):6041-5. - PMC - PubMed
Garcia‐Medina 2011 {published data only}
    1. Garcia-Medina JJ, Pinazo-Duran MD, Garcia-Medina M, Zanon-Moreno V, Pons-Vazquez S. A 5-year follow-up of antioxidant supplementation in type 2 diabetic retinopathy. European Journal of Ophthalmology 2011;21(5):637-43. - PubMed
Garmo 2018 {published data only}
    1. Garmo V, Abbass I, Sheinson D, Ghanekar A, Moshfeghi A. Factors associated with progression among newly diagnosed untreated mild and moderate diabetic retinopathy in a real-world setting from a large U.S. claims database. Journal of Managed Care and Specialty Pharmacy 2018;24(10A):S59.
Geetha 2019 {published data only}
    1. Geetha P, Shanmugasundaram P. A prospective observational study on assessment of risk factor associated with diabetic retinopathy in patients diagnosed with type 2 diabetes mellitus in South Indian population. Research Journal of Pharmacy and Technology 2019;12(2):595-9.
González‐Villalpando 1994 {published data only}
    1. González-Villalpando ME, González-Villalpando C, Arredondo Pérez B, Stern MP. Diabetic retinopathy in Mexico. Prevalence and clinical characteristics. Archives of Medical Research 1994;25(3):355-60. - PubMed
    1. Gonzalez-Villalpando C, Gonzalez-Villalpando ME, Rivera Martinez D, Stern MP. Incidence and progression of diabetic retinopathy in low income population of Mexico City. Revista de Investigacion Clinica 1999;51(3):141-50. - PubMed
Grauslund 2011 {published data only}
    1. Grauslund J. Eye complications and markers of morbidity and mortality in long-term type 1 diabetes. Acta Ophthalmologica 2011;89(Thesis 1):1-19. [DOI: 10.1111/j.1755-3768.2010.02105.x] - DOI - PubMed
Gupta 2019 {published data only}
    1. Gupta M, Shukla R, Shukla S, Bajpai A, Yagnik D. Longitudinal follow up for the association of microvascular complications in type 1 diabetes (T1DM). Pediatric Diabetes 2019;20(28 Suppl):119. [DOI: 10.1111/pedi.12924] - DOI
Haffner 1993 {published data only}
    1. Haffner SM, Klein R, Moss SE, Klein BE. Sex hormones and the incidence of severe retinopathy in male subjects with type I diabetes. Ophthalmology 1993;100(12):1782-6. - PubMed
Hamman 1989 {published data only}
    1. Hamman RF, Mayer EJ, Moo-Young GA, Hildebrandt W, Marshall JA, Baxter J. Prevalence and risk factors of diabetic retinopathy in non-Hispanic whites and Hispanics with NIDDM. San Luis Valley Diabetes Study. Diabetes 1989;38(10):1231-7. - PubMed
Hautala 2018 {published data only}
    1. Hautala N, Siiskonen M, Hannula V, Jarvinen K, Falck A. Early glycaemic control for maintaining visual function in type 1 diabetes: the Oulu cohort study of diabetic retinopathy. European Journal of Ophthalmology 2018;28(6):684-9. - PubMed
Henricsson 1997 {published data only}
    1. Henricsson M, Nilsson A, Janzon L, Groop L. The effect of glycaemic control and the introduction of insulin therapy on retinopathy in non-insulin-dependent diabetes mellitus. Diabetic Medicine 1997;14(2):123-31. - PubMed
Hoang 2020 {published data only}
    1. Hoang A, Sohn JH, Foster A. Association between diabetic retinopathy and diabetic foot ulcer in South Texas. Investigative Ophthalmology and Visual Science 2020;61(7):ARVO E-abstract 4838.
Holman 2008 {published data only}
    1. Holman RR, Paul SK, Bethel MA, Matthews DR, Neil H, Andrew W. 10-year follow-up of intensive glucose control in type 2 diabetes. New England Journal of Medicine 2008;359(15):1577-89. - PubMed
Holt 2019 {published data only}
    1. Holt CB, Hoffmann-Petersen IT, Ostergaard JA, Parving H-HD, Thiel S, Hovind P, et al. Association between complement and severe retinal complications in type 1 diabetes: an 18-year follow-up study. Diabetes 2019;68(1 Suppl):40-LB. [DOI: 10.2337/db19-40-LB] - DOI
Hwang 2019 {published data only}
    1. Hwang TS, You Q, Wang J, Guo Y, Flaxel CJ, Bailey ST, et al. Optical coherence tomography angiography-quantified avascular area is associated with diabetic retinopathy severity and predicts one-year treatment requirement and disease progression. Investigative Ophthalmology and Visual Science 2019;60(9):ARVO E-abstract 4774.
Jacobsen 2003 {published data only}
    1. Jacobsen N, Kjer BE, Goldschmidt E, Andersen OO, Thorsteinsson B. Diabetic retinopathy in type 1 diabetics in the county of Frederiksborg. Ugeskrift for Laeger 2003;165(30):2953-6. - PubMed
Janka 1989 {published data only}
    1. Janka HU, Warram JH, Rand LI, Krolewski AS. Risk factors for progression of background retinopathy in long-standing IDDM. Diabetes 1989;38(4):460-4. - PubMed
Jin 2018 {published data only}
    1. Jin G, Xiao W, Ding X, Xu X, An L, Congdon N, et al. Prevalence of and risk factors for diabetic retinopathy in a rural Chinese population: the Yangxi eye study. Investigative Ophthalmology and Visual Science 2018;59(12):5067-73. - PubMed
Jonas 2017 {published data only}
    1. Jonas JB, Wu SL, Wang YX, Xiulan Z, Ma K, Zhang W, et al. Diabetic retinopathy in China: Population-based studies and clinical and experimental investigations. Lancet 2017;390(Special issue):S30. [DOI: 10.1016/S0140-6736(17)33168-9] - DOI
Kawasaki 2005 {published data only}
    1. Kawasaki R, Yamashita H. Risk factors for incidence and progression of diabetic retinopathy. Nihon Rinsho 2005;63 (6 Suppl ):178-82. - PubMed
Keech 2007 {published data only}
    1. Keech AC, Mitchell P, Summanen PA, O'Day J, Davis TM, Moffitt MS, et al. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): a randomised controlled trial. Lancet 2007;370(9600):1687-97. - PubMed
Kingsley 1988 {published data only}
    1. Kingsley LA, Dorman JS, Doft BH, Orchard TJ, LaPorte RE, Kuller LH, et al. An epidemiologic approach to the study of retinopathy: the Pittsburgh diabetic morbidity and retinopathy studies. Diabetes Research and Clinical Practice 1988;4(2):99-109. - PubMed
Klein 1988 {published data only}
    1. Klein BE, Moss SE, Klein R, Surawicz TS. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. XIII. Relationship of serum cholesterol to retinopathy and hard exudate. Ophthalmology 1991;98(8):1261-5. - PubMed
    1. Klein R, Moss SE, Klein BE, Davis MD, DeMets DL. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: VIII. The incidence of retinal photocoagulation. Journal of Diabetic Complications 1988;2(2):79-87. [PMID: Klein 1988b] - PubMed
Kohner 1986 {published data only}
    1. Kohner EM, Sleightholm M. Does microaneurysm count reflect severity of early diabetic retinopathy? Ophthalmology 1986;93(5):586-9. - PubMed
Kornerup 1955 {published data only}
    1. Kornerup T. Studies in diabetic retinopathy: an investigation of 1,000 cases of diabetes. Acta Medica Scandinavica 1955;153(2):81-101. - PubMed
Kroc Collaborative Study 1984 {published data only}
    1. Kroc Collaborative Study Group. Blood glucose control and the evolution of diabetic retinopathy and albuminuria. A preliminary multicenter trial. New England Journal of Medicine 1984;311(6):365-72. - PubMed
    1. Kroc Collaborative Study Group. Diabetic retinopathy after two years of intensified insulin treatment. Follow-up of the Kroc Collaborative Study. JAMA 1988;260(1):37-41. - PubMed
Krolewski 1986 {published data only}
    1. Krolewski AS, Warram JH, Rand LI, Christlieb AR, Busick EJ, Kahn CR. Risk of proliferative diabetic retinopathy in juvenile-onset type I diabetes: a 40-yr follow-up study. Diabetes Care 1986;9(5):443-52. - PubMed
Kulenovic 2006 {published data only}
    1. Kulenovic I, Rasic S, Karcic S. Development of microvascular complications in type 1 diabetic patients 10 years follow-up. Bosnian Journal of Basic Medical Sciences 2006;6(2):47-50. - PMC - PubMed
Kyari 2014 {published data only}
    1. Kyari F, Tafida A, Sivasubramaniam S, Murthy GV, Peto T, Gilbert CE, et al. Prevalence and risk factors for diabetes and diabetic retinopathy: results from the Nigeria national blindness and visual impairment survey. BMC Public Health 2014;14(100968562):1299. - PMC - PubMed
Lamoureux 2018 {published data only}
    1. Lamoureux EL, Li LJ, Win W, Gan AT, Man R, Nguyen QD, et al. Are person-and areal-level [sic] socio-economic status asoosciated [sic] with the onset and progression of diabetic retinopathy? Investigative Ophthalmology and Visual Science 2018;59(9):ARVO E-abstract 2601.
LaPorte 1986 {published data only}
    1. LaPorte RE, Dorman JS, Tajima N. Pittsburgh insulin-dependent diabetes mellitus morbidity and mortality study: physical activity and diabetic complications. Pediatrics 1986;78(6):1027-33. - PubMed
Lauritzen 1983 {published data only}
    1. Lauritzen T, Frost-Larsen K, Larsen HW, Deckert T. Effect of 1 year of near-normal blood glucose levels on retinopathy in insulin-dependent diabetics. Lancet 1983;1(8318):200-4. - PubMed
    1. Lauritzen T, Frost-Larsen K, Larsen HW, Deckert T. Two-year experience with continuous subcutaneous insulin infusion in relation to retinopathy and neuropathy. Diabetes 1985;34(3 Suppl):74-9. - PubMed
Lee 2010 {published data only}
    1. Lee CC, Stolk RP, Adler AI, Patel A, Chalmers J, Neal B, et al. Association between alcohol consumption and diabetic retinopathy and visual acuity - the AdRem Study. Diabetic Medicine 2010;27(10):1130-7. - PubMed
Lee 2011 {published data only}
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Leese 2004 {published data only}
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