When should screening for diabetic retinopathy begin for children with type 1 diabetes?

Figures & data

Table 1. Previous publications reporting prevalence of DR in children with T1DM.

Publication	Study setting/population characteristics	Screening details	Clinical parameters measured	Prevalence of DR	Significant findings	Conclusions
Kubin 2011 [17]	Finland Population-based 297 persons with T1DM Mean age: 11.9 years Mean duration of diabetes: 4.9 years	Fundus photographs following dilation Canon CF 60 1 × 60° image per eye captured	Duration of diabetes, gender, stage of puberty (using Tanner classification), relative height for age, relative weight for height, blood pressure, HbA1c, urinary albumin content, and lipids	Prevalence of DR: 11.8%, all had mild BDR Prevalence of DR in males: 7.6%, females: 16.5% Youngest age at which DR was found was 8 years	DR was associated with older age, a longer duration of diabetes, a higher HbA1c, and gender.	Signs of DR in childhood may act as a risk marker for florid DR in early adulthood. Pinpointing those people at risk for intensified treatment and close follow-up are crucial in preventing visual impairment and blindness
Kernell 1997 [18]	Sweden Population-based 780 persons aged <15 years at diagnosis with a duration of diabetes <12 years from 8 different regions 557 persons were photographed Median age: 14.6 years Duration of diabetes: 8 years	Fundus photographs 3 × 45° fields per eye. Graded using modified Airlie house protocol (KROC study) by 3 ophthalmologists	Weight, height, insulin dose (IU/kg), body weight, number of insulin doses per day	Prevalence of DR: 14.5% 11.8% had BDR, 2.2% PPDR, and 0.2% PDR. Youngest age at which PPDR was found was 11.8 years and PDR 21.5 years. Prevalence of DR by age 8–10 years: 5% 23–25 years: 71% Pubertal stage 1 6% Pubertal stage 5 18%	More advanced stages of DR (40–65) were associated with a longer duration of DM	BDR and PPDR were found in children before puberty. Our recommendation would be to begin screening for DR from the age of 10 years. Although these early retinal changes do not need photocoagulation, it is important to diagnose DR as soon as possible in order to intensify treatment and normalize metabolic control. If screening is performed annually from age 10 instead of biennially from age 15, it could prevent blindness in at least one patient with a cost-benefit of more than £200,000 for the society.
Donaghue 1997 [19]	Diabetes clinics Australia Study A—38 prepubertal persons and 140 pubertal persons with T1DM aged 10–14 years with a duration of diabetes of 3–12 years. Study B—193 persons with T1DM aged 15–22 years with prepubertal-onset diabetes	Fundus photography 7 fields per eye captured using a Topcon camera following dilation. Grading was performed using an adaption of the ETDRS protocol	HbA1c, albumin excretion rate	Prevalence of DR, Study A Prepubertal: 27% Pubertal: 29% Study B Prepubertal 15–22 years 52%	No significant difference for DR between the 2 groups
Kullberg 2002 [20]	Sweden Hospital clinics 440 persons with T1DM aged <36 years at diagnosis 224 persons aged <15 years at onset and 216 persons aged 15–36 years. Fundus photos on 390 patients	Color fundus photography 3 ×  45° 35 mm films per eye following dilation. Images graded by 2 ophthalmologists using the modified Airlie house protocol	Data on HbA1c, blood pressure, antihypertensive treatments, insulin use, urinary albumin concentration, body weight, and height were collected from medical records.	Prevalence of DR: 29% Youngest age of DR: 9 years, Youngest age of DR with more than Ma’s or Hm’s: 18 years. Prevalence with DR by age at onset of DM 0–19 years: 27% 20–35 years: 32.6%		Risk of DR varies with different age at onset, independently of differences in the duration of glycemic control.
Maguire 2005 [21]	Australia Children’s hospital 668 children and adolescents with T1DM. Analysis divided by age at screening 50 persons aged <11 years Median HbA1c: 8.5% 618 persons aged ≥11 years median HbA1c: 8.7%	Fundus photography 7 field stereoscopic following dilation with a Topcon camera. Graded using the ETDRS protocol		Prevalence of DR <11 years: 16% ≥11 years: 22% No PDR and no laser
LeCaire 2006 [22]	Wisconsin, USA Population-based 474 persons with T1DM	Fundus photographs 30° 7 field imaging following dilation Graded using WESDR protocol	Height, weight, waist:hip circumference, blood pressure, and HbA1c	Prevalence of DR Min-severe NPDR: 43% Prevalence of DR by duration of DM 4 years: 6%, 7 years: 23%, 9 years: 47% 14 years: 73%	Risk of DR increased with increasing duration of diabetes and HbA1c levels
Flack 1996 [23]	Finland Population-based 182 children			Prevalence of DR increased from 10.8% to 28% during a follow-up of 2.5 years. DR diagnosed at a mean age of 15.3 years and duration of DM 8.9 years.	Increased HbA1c levels during puberty was the only factor that differentiated these patients from age, sex, puberty, and duration of diabetes matched controls.
Geloneck 2015 [24]	Philadelphia, USA Hospital-based 370 children aged <18 years with T1DM or T2DM Mean age: 11.2 years, duration: 5.2 years	Dilated fundoscopy performed by pediatric ophthalmologists		No DR seen in 338 persons with T1DM and 32 persons with T2DM Mean age at first eye exam: 11.2 years		DR is rare in children regardless of duration and control of DM. Screening examinations for T1DM could begin at the age of 15 years or at 5 years after the diagnosis of DM, whichever occurs later, unless the child is judged by the endocrinologist as being at unusually high risk. We think that the value of screening for such mild disease is questionable, considering the large number of normal examinations being performed. A more reasonable screening target may be identification of sight-threatening DR, which might be close to requiring treatment.
Cahill 2000 [25]	Republic of Ireland Hospital clinic 34 persons with juvenile-onset diabetes of ≥10 years	Fundus photography 7 field following dilation. Graded in a retinal grading center by ETDRS protocols	Age at diagnosis of DM, duration of DM, recent HbA1c, hypertension treatment, and microalbuminuria obtained from medical records.	Prevalence of DR: 44%, all minimal-mod BDR	Those with DR had significantly higher HbA1c levels. No other differences found	Due to coincident lifestyle changes and the probability of long duration of disease, accurate detection of early DR in juvenile-onset diabetes with disease duration of 10 years or more is important
Demirel 2013 [26]	Turkey Pediatric hospital clinic 155 persons with T1DM for 2 years aged ≥11 years Mean age: 14.4 (2.1) years, duration: 6.3 (2.9) years, mean HbA1c: 8.4%	Fundus examination performed by an ophthalmologist following mydriasis. Fundus imaging carried out in suspected cases.	Presence of DR, nephropathy, and peripheral neuropathy, duration of diabetes, HbA1c, BMI, dyslipidemia, total cholesterol, triglycerides, LDL-cholesterol, HDL-cholesterol, microalbuminuria, and hypertension	No DR found		Persons with poor metabolic control, dyslipidemia, and hypertension should be screened 2 years after diagnosis of DM or after 11 years of age. Those with good metabolic control without hypertension or dyslipidemia screening could be postponed to 5 years after a diagnosis of DM.
Dujic 2009 [27]	Serbia Ophthalmology clinic 33 persons with juvenile-onset DM 1992–2007 Mean age: 23.1 (6.4) years, duration: 17.4 (7.4) years.	After dilation direct and indirect ophthalmoscopy performed by ophthalmologists	Age, age at diagnosis of DM, time when eye complications occurred, and treatment modalities.	Prevalence of DR NPDR: 41.4%, PDR: 13.1%, 10.1% had macula involvement 11 of 66 eyes had a vitreous Hm, 2 persons had neovascular glaucoma, and 1 person had rubeosis iridis		Screening for DR should begin at age 10.
Florkowski 2001 [28]	New Zealand Population-based 286 persons with T1DM and age at onset <20 years	Fundoscopy through dilated pupils by an experienced observer		Prevalence of DR was 37.4%	Those with DR were older, and had diabetes for longer, with higher HbA1c levels compared to those without DR.	The association between age at diagnosis and the effects of extended duration of exposure to diabetes suggests that targeting of resources to younger patients is appropriate.
Holl 1998 [29]	Germany Ophthalmology clinic 441 children with T1DM Median age: 15.5 years Duration of diabetes: 6.3 years.	Fundus examination in the ophthalmology department following dilation 2 × 60° fields per eye captured using a Canon 60 degree camera (Canon, Ota, Tokyo, Japan) and Kodak 64 ASA film (Kodak, Rochester, New York, New Jersey, USA)		Prevalence of mild NPDR: 16.3% Moderate NPDR: 0.9% Shortest duration of DM when DR seen was 2.2 years Youngest age when DR seen was 5.5 years		Screening could be conducted biennially in children, provided there are no other risk factors.
Olsen 2004 [30]	Denmark Prospective nation-wide study 339 children and adolescents with T1DM 304 had prepubertal onset diabetes <11.7 years in girls and <12.9 years in boys	Fundus photography with central grading	Demographic data, HbA1c, albumin excretion rate	Prevalence of DR: 57.6% Prevalence of DR in those aged 12–15 years: 17.7%, 16–20 years: 45.4% >20 years: 67.6%	DR was significantly associated with poor long-term metabolic control and duration of DM	Prepubertal diabetes duration contributes to the overall risk of developing microvascular injury but is modest compared to post-pubertal duration.

ETDRS: early treatment of diabetic retinopathy study; DR: diabetic retinopathy; BDR: backrground diabetic retinopathy; PDR: proliferative diabetic retinopathy; PPDR: pre-proliferative diabetic retinopathy; DM: diabetes mellitus; Ma's: microaneurysms; Hm's: haemorrhages; T1DM: type 1 diabetes mellitus; T2DM: type 2 diabetes mellitus; WESDR: Wisconsin epidemiological study of diabetic retinopathy; NPDR: non-proliferative diabetic retinopathy; LDL: low density lipoprotein; HDL: high density liproprotein.

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