Abstract
To examine the prevalence and incidence of diabetic eye disease (DED) among individuals with diabetes in Europe, a systematic review to identify all published European prevalence and incidence studies of DED in individuals with diabetes managed in primary health care was performed according to the MOOSE and PRISMA guidelines. The databases Medline, Embase and Web of Science were searched to 2 September 2017. Meta-analyses and meta-regressions were performed. The pooled prevalence estimates were applied to diabetes prevalence rates provided by the International Diabetes Foundation atlas and Eurostat population data, and extrapolated to the year 2050. Data of 35 prevalence and four incidence studies were meta-analyzed. Any diabetic retinopathy (DR) and diabetic macular edema (DME) were prevalent in 25.7% (95% CI 22.8–28.8%) and 3.7% (95% CI 2.2–6.2%), respectively. In meta-regression, the prevalence of DR in persons with type 1 diabetes was significantly higher compared to persons with type 2 diabetes (54.4% vs. 25.0%). The pooled mean annual incidence of any DR and DME in in persons with type 2 diabetes was 4.6% (95% CI 2.3–8.8%) and 0.4% (95% CI 0.5–1.4%), respectively. We estimated that persons with diabetes affected by any DED in Europe will increase from 6.4 million today to 8.6 million in 2050, of whom 30% require close monitoring and/or treatment. DED is estimated to be present in more than a quarter of persons with type 2 diabetes and half of persons with type 1 diabetes underlining the importance of regular monitoring. Future health services need to be planned accordingly.
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Finger RP, Fimmers R, Holz FG, Scholl HPN. Incidence of blindness and severe visual impairment in Germany: projections for 2030. Investig Ophthalmol Vis Sci. 2011;52:4381–9.
Bourne RRA, Jonas JB, Bron AM, Cicinelli MV, Das A, Flaxman SR, et al. Prevalence and causes of vision loss in high-income countries and in Eastern and Central Europe in 2015: magnitude, temporal trends and projections. Br J Ophthalmol. 2018;102:575–85. https://doi.org/10.1136/bjophthalmol-2017-31125.
Yau JWY, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35:556–64. https://doi.org/10.2337/dc11-1909.
Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis. 2015;2:17.
Wong TY, Sun J, Kawasaki R, Ruamviboonsuk P, Gupta N, van Lansingh C, et al. Guidelines on diabetic eye care: the international council of ophthalmology recommendations for screening, follow-up, referral, and treatment based on resource settings. Ophthalmology. 2018;125:1608–22.
International Diabetes Federation. IDF diabetes atlas. 8th ed. Brussels: International Diabetes Federation; 2017.
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA. 2000;283:2008–12.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.
Retinopathy Working Party. A protocol for screening for diabetic retinopathy in Europe. Diabet Med. 1991;8:263–7.
Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs—an extension of the modified airlie house classification. Ophthalmology. 1991;98:786–806. https://doi.org/10.1016/s0161-6420(13)38012-9.
Wilkinson CP, Ferris FL, Klein RE, Lee PP, Agardh CD, Davis M, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82. https://doi.org/10.1016/s0161-6420(03)00475-5.
Meurer P, Schluchter M. Wissenschaftliches Arbeiten mit Citavi 5. Hinweise zum Schreiben wissenschaftlicher Arbeiten mit der Software» Citavi–Literaturverwaltung und Wissensorganisation « 2015: Zugriff am.
Li JQ, Terheyden JH, Welchowski T, Schmid M, Letow J, Wolpers C, et al. Prevalence of retinal vein occlusion in Europe: a systematic review and meta-analysis. Ophthalmologica. 2018;49:1–7.
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology [STROBE] statement: guidelines for reporting observational studies. Gac Sanit. 2008;22:144–50.
R Core Team. R. A language and environment for statistical computing. 2015. https://www.R-project.org. Accessed 2 Sept 2017
Schwarzer G. Meta: an R package for meta-analysis. R News. 2007;7:40–5.
Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58. https://doi.org/10.1002/sim.1186.
Cochran WG. The comparison of percentages in matched samples. Biometrika. 1950;37:256–66.
United Nations Statistics Division. Standard Country and area codes for statistical use (M49). https://unstats.un.org/unsd/methodology/m49/. Accessed 3 May 2019.
Friberg E, Orsini N, Mantzoros CS, Wolk A. Diabetes mellitus and risk of endometrial cancer: a meta-analysis. New York: Springer; 2007.
Ben Q, Xu M, Ning X, Liu J, Hong S, Huang W, et al. Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer. 2011;47:1928–37. https://doi.org/10.1016/j.ejca.2011.03.003.
Eurostat. Population on 1 January. 2016. http://ec.europa.eu/eurostat/tgm/table.do?tab=table&init=1&plugin=1&language=en&pcode=tps00001. Accessed 11 May 2017.
Eurostat. People in the EU – population projections. http://ec.europa.eu/eurostat/statistics-explained/index.php/People_in_the_EU_%E2%80%93_population_projections (2015). Accessed 14 Jul 2017.
Eurostat. Population projections. http://ec.europa.eu/eurostat/tgm/table.do?tab=table&init=1&plugin=1&language=de&pcode=tps00002 (2016). Accessed 11 May 2017.
Lenoble P, Kheliouen M, Bourderont D, Klinger V, Nasica X, Benseddik Y, Holl P. Screening diabetic retinopathy using a telediagnosis system. Results of the upper Rhine survey. J Fr Ophtalmol. 2009;32:91–7. https://doi.org/10.1016/j.jfo.2009.01.006.
Schulze-Dobold C, Erginay A, Robert N, Chabouis A, Massin P. Ophdiat((R)): five-year experience of a telemedical screening programme for diabetic retinopathy in Paris and the surrounding area. Diabetes Metab. 2012;38:450–7. https://doi.org/10.1016/j.diabet.2012.05.003.
Soulie-Strougar M, Charles A, Metral P, Quercia P, Souchier M, Chirpaz L, et al. Screening diabetic retinopathy in Burgundy with an itinerant nonmydriatic camera. J Fr Ophtalmol. 2007;30:121–6.
Raum P, Lamparter J, Ponto KA, Peto T, Hoehn R, Schulz A, et al. Prevalence and cardiovascular associations of diabetic retinopathy and maculopathy: results from the Gutenberg Health Study. PLoS ONE. 2015;10:e0127188. https://doi.org/10.1371/journal.pone.0127188.
Zietz B, Kasparbauer A, Ottmann S, Spiegel D, Palitzsch KD. Diabetic retinopathy and associated risk factors in type-1 and type-2 diabetics in the Upper Palatinate. Dtsch Med Wochenschr. 2000;125:783–8. https://doi.org/10.1055/s-2007-1024518.
Giuffre G, Lodato G, Dardanoni G. Prevalence and risk factors of diabetic retinopathy in adult and elderly subjects: the Casteldaccia Eye Study. Graefes Arch Clin Exp Ophthalmol. 2004;242:535–40. https://doi.org/10.1007/s00417-004-0880-4.
Goldaracena MB, Escudero JM, Arrondo A, Villarrubia A, Aramendia B, Iturralde R. Prevalencia de retinopatía diabética en una población diabética registrada en atención primaria. Prevalence of diabetic retinopathy. A population based study in primary health care. 1998.
Hernández Mira G, Macarro Merino A, Fernández Perianes J, Fernández Vigo J. Prevalencia de retinopatía diabética en Extremadura. Av Diabetol. 1996;12:165–71.
Gil Hernández MA, Abreu Reyes P, Pareja Rios A, Martinez Piñero A. Estudio de la retinopatía diabética en la población de la isla de Hierro. Arch Soc Canar Oftal. 2000;11:23–6.
Lopez IM, Diez A, Velilla S, Rueda A, Alvarez A, Pastor CJ. Prevalence of diabetic retinopathy and eye care in a rural area of Spain. Ophthalmic Epidemiol. 2002;9:205–14.
Martinez RM, Moya MM, Bellot BA, Belmonte MJ. Diabetic retinopathy screening and teleophthalmology. Arch Soc Esp Oftalmol. 2012;87:392–5. https://doi.org/10.1016/j.oftal.2012.04.004.
Romero-Aroca P, Sagarra-Alamo R, Baget-Bernaldiz M, Fernández-Ballart J, Méndez-Marin I. Prevalence and relationship between diabetic retinopathy and nephropathy, and its risk factors in the North-East of Spain, a population-based study. Ophthalmic Epidemiol. 2010;17:251–65.
Romero-Aroca P, Fernandez-Alart J, Baget-Bernaldiz M, Mendez-Marin I, Salvat-Serra M. Diabetic retinopathy epidemiology in type II diabetic patients. Effect of the changes in the diagnostic criteria and stricter control of the diabetes between 1993 and 2005 on the incidence of diabetic retinopathy. Arch Soc Esp Oftalmol. 2007;82:209–18.
Bueso E, Fernandez-Vigo J, Perez C, Merino A, Perianes J. Prevalence of diabetic retinopathy in the Regional Community of Extremadura. 1997–2001 (Extremadura Project to Prevent Blindness). Arch Soc Esp Oftalmol. 2005;80:187–94.
Santos Bueso E, Macarro Merino A, Garrote Florencio T, Fernández-Vigo López J. Prevalencia de retinopatía diabética en el centro de salud de Torrejoncillo (Cáceres). Av Diabetol. 2002;18:203–7.
Santos-Bueso E, Fernandez-Perez C, Macarro A, Fernandez-Vigo J. Prevalence of diabetic retinopathy in the city of Badajoz 2002 (Extremadura project to prevent blindness). Arch Soc Esp Oftalmol. 2007;82:153–8.
Teruel MC, Fernandez-Real JM, Ricart W, Valent FR, Valles PM. Prevalence of diabetic retinopathy in the region of Girona. Study of related factors. Arch Soc Esp Oftalmol. 2005;80:85–91.
Vleming EN, Castro M, Lopez-Molina MI, Teus MA. Use of non-mydriatic retinography to determine the prevalence of diabetic retinopathy in diabetic patients. Arch Soc Esp Oftalmol. 2009;84:231–6.
Broadbent DM, Scott JA, Vora JP, Harding SP. Prevalence of diabetic eye disease in an inner city population: the Liverpool Diabetic Eye Study. Eye (London). 1999;13(Pt 2):160–5. https://doi.org/10.1038/eye.1999.43.
Ding J, Strachan MWJ, Reynolds RM, Frier BM, Deary IJ, Fowkes FGR, et al. Diabetic retinopathy and cognitive decline in older people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes. 2010;59:2883–9. https://doi.org/10.2337/db10-0752.
Ellis JD, Zvandasara T, Leese G, McAlpine R, Macewen CJ, Baines PS, et al. Clues to duration of undiagnosed disease from retinopathy and maculopathy at diagnosis in type 2 diabetes: a cross-sectional study. Br J Ophthalmol. 2011;95:1229–33. https://doi.org/10.1136/bjo.2010.196204.
Jones CD, Greenwood RH, Misra A, Bachmann MO. Incidence and progression of diabetic retinopathy during 17 years of a population-based screening program in England. Diabetes Care. 2012;35:592–6. https://doi.org/10.2337/dc11-0943.
Kohner EM, Aldington SJ, Stratton IM, Manley SE, Holman RR, Matthews DR, Turner RC. United Kingdom Prospective Diabetes Study, 30: diabetic retinopathy at diagnosis of non-insulin-dependent diabetes mellitus and associated risk factors. Arch Ophthalmol. 1998;116:297–303.
Leese GP, Morris AD, Swaminathan K, Petrie JR, Sinharay R, Ellingford A, et al. Implementation of national diabetes retinal screening programme is associated with a lower proportion of patients referred to ophthalmology. Diabet Med. 2005;22:1112–5. https://doi.org/10.1111/j.1464-5491.2005.01603.x.
Ling R, Ramsewak V, Taylor D, Jacob J. Longitudinal study of a cohort of people with diabetes screened by the Exeter Diabetic Retinopathy Screening Programme. Eye (London). 2002;16:140–5. https://doi.org/10.1038/sj/EYE/6700081.
Scanlon PH, Carter SC, Foy C, Husband RF, Abbas J, Bachmann MO. Diabetic retinopathy and socioeconomic deprivation in Gloucestershire. J Med Screen. 2008;15:118–21. https://doi.org/10.1258/jms.2008.008013.
Thomas RL, Dunstan FD, Luzio SD, Chowdhury SR, North RV, Hale SL, et al. Prevalence of diabetic retinopathy within a national diabetic retinopathy screening service. Br J Ophthalmol. 2015;99:64–8. https://doi.org/10.1136/bjophthalmol-2013-304017.
Younis N, Broadbent DM, Harding SP, Vora JR. Prevalence of diabetic eye disease in patients entering a systematic primary care-based eye screening programme. Diabet Med. 2002;19:1014–21.
Gunnlaugsdottir E, Halldorsdottir S, Klein R, Eiriksdottir G, Klein BE, Benediktsson R, et al. Retinopathy in old persons with and without diabetes mellitus: the Age, Gene/Environment Susceptibility-Reykjavik Study (AGES-R). Diabetologia. 2012;55:671–80. https://doi.org/10.1007/s00125-011-2395-y.
Hapnes R, Bergrem H. Diabetic eye complications in a medium sized municipality in southwest Norway. Acta Ophthalmol Scand. 1996;74:497–500.
Bertelsen G, Peto T, Lindekleiv H, Schirmer H, Solbu MD, Toft I, et al. Tromsø eye study: prevalence and risk factors of diabetic retinopathy. Acta Ophthalmol. 2013;91:716–21.
Kilstad HN, Sjølie AK, Gøransson L, Hapnes R, Henschien HJ, Alsbirk KE, et al. Prevalence of diabetic retinopathy in Norway: report from a screening study. Acta Ophthalmol. 2012;90:609–12.
Medeiros MD, Mesquita E, Papoila AL, Genro V, Raposo JF. First diabetic retinopathy prevalence study in Portugal: RETINODIAB Study—evaluation of the screening programme for Lisbon and Tagus Valley region. Br J Ophthalmol. 2015;99:1328–33. https://doi.org/10.1136/bjophthalmol-2015-306727.
Kuiv R, Tein P, Algvere PV, Bäcklund LB, Holm O. Photographic detection of retinopathy in insulin-treated diabetes. Acta Ophthalmol. 1997;75:447–56.
Larsson L, Alm A, Bergenheim T, Lithner F, Bergström R. Retinopathy in diabetic patients aged 15–50 years in the county of Umeå, Sweden. Acta Ophthalmol Scand. 1999;77:430–6.
Kernell A, Dedorsson I, Johansson B, Wickström CP, Ludvigsson J, Tuvemo T, et al. Prevalence of diabetic retinopathy in children and adolescents with IDDM A population-based multicentre study. Diabetologia. 1997;40:307–10.
Tóth G, Szabó D, Sándor GL, Szalai I, Lukács R, Pék A, et al. Diabetes and diabetic retinopathy in people aged 50 years and older in Hungary. Br J Ophthalmol. 2017;101:965–9. https://doi.org/10.1136/bjophthalmol-2016-309016.
Olafsdottir E, Andersson DKG, Dedorsson I, Stefansson E. The prevalence of retinopathy in subjects with and without type 2 diabetes mellitus. Acta Ophthalmol. 2014;92:133–7. https://doi.org/10.1111/aos.12095.
The Royal College of Ophthalmologists. Diabetic Retinopathy Guidelines December 2012; 2012.
Chakrabarti R, Harper CA, Keeffe JE. Diabetic retinopathy management guidelines. Expert Rev Ophthalmol. 2012;7:417–39.
Ponto KA, Koenig J, Peto T, Lamparter J, Raum P, Wild PS, et al. Prevalence of diabetic retinopathy in screening-detected diabetes mellitus: results from the Gutenberg Health Study (GHS). Diabetologia. 2016;59:1913–9.
Thomas RL, Dunstan F, Luzio SD, Roy CS, Hale SL, North RV, et al. Incidence of diabetic retinopathy in people with type 2 diabetes mellitus attending the Diabetic Retinopathy Screening Service for Wales: retrospective analysis. BMJ. 2012;344:e874. https://doi.org/10.1136/bmj.e874.
Younis N, Broadbent DM, Vora JP, Harding SP. Incidence of sight-threatening retinopathy in patients with type 2 diabetes in the Liverpool Diabetic Eye Study: a cohort study. Lancet. 2003;361:195–200. https://doi.org/10.1016/S0140-6736(03)12267-2.
Romero-Aroca P, de La Riva-Fernandez S, Valls-Mateu A, Sagarra-Alamo R, Moreno-Ribas A, Soler N. Changes observed in diabetic retinopathy: eight-year follow-up of a Spanish population. Br J Ophthalmol. 2016. https://doi.org/10.1136/bjophthalmol-2015-307689.
Salinero-Fort MA, San FJ, de Burgos-Lunar C, Arrieta-Blanco FJ, Gomez-Campelo P. Four-year incidence of diabetic retinopathy in a Spanish cohort: the MADIABETES study. PLoS ONE. 2013;8:e76417. https://doi.org/10.1371/journal.pone.0076417.
Younis N, Broadbent DM, Harding SP, Vora JP. Incidence of sight-threatening retinopathy in Type 1 diabetes in a systematic screening programme. Diabet Med. 2003;20:758–65.
Kempen JH, O’Colmain BJ, Leske MC, Haffner SM, Klein R, Moss SE, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122:552–63. https://doi.org/10.1001/archopht.122.4.552.
Centers for Disease Control and Prevention. Age-adjusted percentage of adults with diabetes using diabetes medication, by type of medication, United States, 1997–2011; 2015.
Ting DSW, Cheung GCM, Wong TY. Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: a review. Clin Exp Ophthalmol. 2016;44:260–77.
Schmidt-Erfurth U, Chong V, Loewenstein A, Larsen M, Souied E, Schlingemann R, et al. Guidelines for the management of neovascular age-related macular degeneration by the European Society of Retina Specialists (EURETINA). Br J Ophthalmol. 2014;98:1144–67.
Pasquel FJ, Hendrick AM, Ryan M, Cason E, Ali MK, Narayan KV. Cost-effectiveness of different diabetic retinopathy screening modalities. J Diabetes Sci Technol. 2016;10:301–7.
Higgins JP, Deeks JJ, Higgins J, Green S. 9.5. 4 Incorporating heterogeneity into random-effects models. Cochrane handbook for systematic reviews of interventions, Version. 2011;5.
Hocking A, Laurence C, Lorimer M. Patients’ knowledge of their chronic disease: the influence of socio-demographic characteristics. Aust Fam Physician. 2013;42:411.
Pastorino S, Richards M, Hardy R, Abington J, Wills A, Kuh D, Pierce M. Validation of self-reported diagnosis of diabetes in the 1946 British birth cohort. Prim Care Diabetes. 2015;9:397–400.
Diabetic Retinopathy Study Research Group. Report No. 7: a modification of the Airlie House classification of diabetic retinopathy. Investig Ophthalmol Vis Sci. 1981;21:210–26.
Massin P, Angioi-Duprez K, Bacin F, Cathelineau B, Cathelineau G, Chaine G, et al. Detection, monitoring and treatment of diabetic retinopathy. Recommendations of ALFEDIAM. Committee of above-mentioned experts and validated by the board of directors and scientific board of ALFEDIAM. Diabetes Metab. 1996;22:203–9.
Harding S, Greenwood R, Aldington S, Gibson J, Owens D, Taylor R, et al. Grading and disease management in national screening for diabetic retinopathy in England and Wales. Diabet Med. 2003;20:965–71.
Facey K, Cummins E, Macpherson K, Morris A, Reay L, Slattery J. Health technology assessment report 1: organisations of services for diabetic retinopathy screening. Glasgow: Health Technology Board for Scotland; 2002.
Klein R, Klein BEK, Magli YL, Brothers RJ, Meuer SM, Moss SE, Davis MD. An alternative method of grading diabetic retinopathy. Ophthalmology. 1986;93:1183–7.
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European Society of Retina Specialists (EURETINA) project grant, the Jackstaedt Stiftung, and the Else Kroehner Fresenius Stiftung. None of the funders were involved in the study design, in the collection, analysis, and interpretation of data, in the writing of the report, or in the decision to submit the article for publication. All researchers confirm their independence from funders. All authors, external and internal, had full access to all of the data (including statistical reports and tables) in the study and can take responsibility for the integrity of the data and the accuracy of the data analysis.
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RPF conceived and designed the study. JQL, JLe, CW, and IPC undertook the literature search, extracted data and performed quality assessment of the included studies. JQL, TW, and MS performed the data analysis. JQL, TW, MS, FGH, and RPF interpreted data. JQL and RPF wrote the first draft of the report. RPF as guarantor accepts full responsibility for the work and the conduct of the study, had access to the data, and controlled the decision to publish. All authors provided critical comments and approved the final version.
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Li, J.Q., Welchowski, T., Schmid, M. et al. Prevalence, incidence and future projection of diabetic eye disease in Europe: a systematic review and meta-analysis. Eur J Epidemiol 35, 11–23 (2020). https://doi.org/10.1007/s10654-019-00560-z
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DOI: https://doi.org/10.1007/s10654-019-00560-z