- Email: [email protected]
Diabetic retinopathy screening in a Canadian community pediatric diabetes clinic
Diabetic retinopathy screening in a Canadian community pediatric diabetes clinic Kedija Abdella, * Kylen D. McReelis, †,‡ M. Hermina Strungaru †,§ ABSTRACT ● Objective: To evaluate the screening rates for diabetic pediatric patients in a regional center according to the Canadian Diabetes Association guidelines. Design: Retrospective study. Participants: The study consisted of 82 patients seen in the pediatric diabetes clinic at Peterborough Regional Health Center. Methods: Medical records for all pediatric patients with diabetes were reviewed between July 2016 and February 2017. Parents and children were surveyed on details of their ocular examination history. Logistic regression analysis was conducted to evaluate if any characteristics were associated with noncompliance to Canadian Diabetes Association guidelines. Results: The average age of the patients in our study was 12 years old with a mean duration of diabetes of 4 years. The majority of patients had type 1 diabetes (n ¼ 79/82, 96.3%) and the mean HbA1c level was 9.1. Only 16 patients (19.5%) adhered to the Canadian Diabetes Association guidelines for diabetic retinopathy screening. Of the 66 patients who did not comply with the guidelines, 65 (98.5%) had received more exams than recommended under their respective screening guidelines. All dilated eye examinations were normal, and no diabetic retinopathy was found. Statistical analysis revealed that the duration of diabetes may be a predicting factor of noncompliance to the guidelines (–0.2488, 95% CI –0.505, –0.042). Conclusions: This study shows a low compliance rate with screening guidelines in our diabetic pediatric population. Of interest, the low compliance in this cohort was related to excessive eye exams. This study also found a low incidence rate of diabetic retinopathy despite poor management of diabetes, similar to previous studies of pediatric diabetic eye disease.
Diabetic retinopathy (DR) is the leading cause of new cases of legal blindness in adults1 and the third cause of blindness in Canada overall.2 The prevalence of retinopathy in the adult population with diabetes mellitus (DM) in the United States is 40.3% while the sight-threatening retinopathy prevalence is 8.2%.3 Diabetic retinopathy currently affects 500 000 Canadians.4 In type 1 DM patients, non-proliferative diabetic retinopathy is more likely to be found than proliferative diabetic retinopathy with a population frequency between 4%–16%5–7 for non-proliferative DR and 1.2%–9%8–10 for proliferative DR. Screening for DR is a crucial component of diabetes management as early detection of retinopathy can help prevent worsening of the sight threatening disease. Diabetic retinopathy screening generally consists of a dilated fundus examination from an experienced eye care professional, possible optical coherence tomography (OCT), and fluorescein angiography when indicated. While rates of DR in pediatric populations are low, various health organizations have still developed guidelines and screening regulations for such patients.11,12 The prevalence of DR in post-pubertal patients with type 1 diabetes increases dramatically after having DM for a period of 5 years,11 while 39% of similar patients with type 2 diabetes may have DR at the time of the diagnosis.13 Therefore, screening for DR in children with DM is dependent on the age of onset, the type of DM,
and the length of time the patient has had the disease. The Canadian Diabetes Association (CDA) recommends the initial retinopathy screening be at five years after the diagnosis of type 1 DM in all individuals aged 15 years and older or at age 15 if the patient has had type 1 DM for greater than 5 years.I In all individuals with type 2 DM, screening is recommended for at the time of diagnosis.12 Although type 1 DM pediatric patients should not be screened before the age of 15, we examined compliance of pediatric patients of all ages in terms of both underscreening as well as overscreening. Studies focusing on adult patients have shown a weak adherence to the screening recommendations outlined by the CDA.14 In 2008, 38% of a diabetic cohort across five provinces in Canada had never been screened for DR and another 30% had not been screened within the last two years.14 Lack of adherence to screening guidelines by underscreening of both pediatric and adult populations has been found in other countries as well, including in the United Kingdom and the United States.9,15,16 Factors that may predict noncompliance to the recommended guidelines include a lack of awareness of the potential consequences of DR, fear of laser treatment, and guilt over poor DM control.17 According to one study, the most significant predictor of getting screened was if the physician recommended a regular eye examination.18
& 2018 Canadian Ophthalmological Society. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jcjo.2018.03.012 ISSN 0008-4182/17 CAN J OPHTHALMOL — VOL. ], NO. ], ] 2018
1
Diabetic retinopathy screening—Abdella et al. Since compliance with DR screening guidelines has not been studied extensively in children, the objective of this study was to evaluate the diabetic retinopathy screening rates of pediatric patients with DM, and to determine the primary care physician’s adherence to the CDA guidelines. We believe this is the first study of such guideline compliance in Canada. We recognize that with the current health care climate in North America, quality improvement has become an important factor for physicians to consider. Since the age and gender distribution of children in Peterborough is comparable to Ontario, the largest province by population in Canada, we feel that our community clinic’s experience is translatable to other community clinics in Canada.19
Paent’s consent received
Study paent’s medical records and fill out quesonnaire
Assess paent’s compliance based on age and type of DM
Paent’s screening is compliant with CDA guidelines
Paent received too many eye exams (over-screened)
This study adhered to the tenets of the Declaration of Helsinki and was approved by the Peterborough Regional Health Center Research Ethics Board. Each subject provided informed consent. All patients who attended the diabetic pediatric clinic at Peterborough Regional Health Center between August 2016 and February 2017 were included. We identified 125 eligible children through the appointment schedule. Of these patients, 81 (64.8%) consented to participate after being approached in the clinic. For patients who missed their appointment, we sent consent forms and a questionnaire through mail, and 7.0% (n ¼ 3/43) responded, but only one was in time to be included in the study. Patients who did not respond were not included in the study. Clinical data was collected through the examination of patient records and through verbal clinical questionnaires to parents and guardians. Patients were assigned numbers to protect their privacy and ensure confidentiality. The parents and guardians were asked whether or not the patient was referred to and seen by an ophthalmologist or optometrist and when the first eye exam was given. They were also asked about how often the patient had been screened and whether or not the eye examination was negative for diabetic retinopathy. The responses to the questionnaire were used to determine compliance to the screening guidelines. Hospital records were used to determine the type of DM, date of DM diagnosis, systemic complications, and the most recent hemoglobin A1c (HbA1c). Compliance to CDA guidelines was assessed based on age and type of DM, as
outlined in Table 1. If patients received the right number of eye exams and screening was initiated at the recommended time, then they were deemed compliant. If one of these criteria was not followed, they were considered noncompliant. It was then determined whether non-compliant patients had received too many or too few eye exams compared with respective guidelines. This process is illustrated in Figure 1. Statistical analysis of the data was carried out using R Foundations for Statistical Computing 3.4.0 (The R Foundation, Vienna, Austria). Stepwise Akaike information criterion (AIC) variable selection for logistic regression was conducted to identify any predictors of noncompliance to the CDA screening guidelines with p ≤ 0.05 considered significant.
RESULTS The mean age of the 82 participants was 12 years of age (range 3–18 years), with 48 male patients (58.5%)and 79 Caucasian patients (96.3%) as seen in Table 2. Among the study participants, 79 patients (96.3%) had type 1 DM and 3 patients (3.7%) had type 2 DM. Mean age at diagnosis was 8 years (range 1–17 years), and the mean duration of DM was 4 years (range 0–15 years). HbA1c level 46.0 was in 81 participants (98.8%). We found that Table 2—Demographic characteristics of diabetic pediatric patients Features
Table 1—Screening guidelines for diabetic pediatric patients based on the Canadian Diabetes Association 415 o15
When yearly screening should be initiated Five years after diagnosis of T1DM In all individuals at diagnosis of T2DM At age 15 if duration of T1DM 45 years In all individuals at diagnosis of T2DM
T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus.
2
Paent received too few eye exams (under-screened)
Fig. 1 — Flowchart indicating process taken to recruit and consider patients for this study. CDA, Canadian Diabetes Association.
METHODS
Age (years)
Paent’s screening is not compliant with CDA guidelines
CAN J OPHTHALMOL — VOL. ], NO. ], ] 2018
Age (years) Mean Range Gender, No. (%) Female Male Ethnicity, No. (%) Asian Caucasian Mixed African-Caucasian
Data (n ¼ 82) 12.74 ± 3.50 3-18 34 (41.5) 48 (58.5) 1 (1.2) 79 (96.3) 2 (2.5)
Diabetic retinopathy screening—Abdella et al. Table 3—Diabetic characteristics of diabetic pediatric patients Feature Age at diagnosis (years) Mean age Range Duration of DM (years) Mean age Range Type of diabetes T1DM No. (%) T2DM No. (%) HbA1c Mean Range 4 6 No. (%) Systemic complications no (%) Insulin pump no (%)
Data (n ¼ 82)
Feature 8.41 ± 4.33 1–7 4.32 ± 3.64 0–15 79 (96.3) 3 (3.7) 9.12 ± 1.49 5.2–12.8 81 (98.8) 32 (39.0) 34 (41.4)
DM, diabetes mellitus; T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus; HbA1c, hemoglobin A variant (biomedical marker).
32 patients (39.0%) had systemic complications related to DM, such as diabetic ketoacidosis; and 34 patients (41.5%) in our cohort were on an insulin pump (Table 3). Of the 70 patients (85.4%) who had received an eye exam, 47 (67.1%) reported receiving a dilated comprehensive eye examination within the past 12 months, and 23 (32.9%) had an examination 4 12 months ago (Table 4). Of the patients who received eye exams, 53 (75.7%) saw an optometrist,8 (11.4%) saw an ophthalmologist, 6 (8.6%) saw both an optometrist and an ophthalmologist, and 3 (4.3%) did not know the type of the eye doctor they saw. None of the patients who had received an eye examination reported having DR, and no patients reported receiving treatment for DR (Table 4). Only 16 patients (19.5%) were screened for DR based on CDA guidelines (Table 5). Of the patients not following the guidelines, 65 received too many eye exams and only one received too few compared with CDA screening guidelines for their age and type of DM (Table 5). The data from all 82 patients was included in the logistic regression model to assess the predicting factors of the noncompliance with CDA guidelines. The model revealed that the only significant predicting factor of noncompliance was duration of DM (–0.249, 95% CI –0.505 to –0.042; p ¼ 0.0322), where shorter duration Table 4—Characteristics of diabetic pediatric patients who had an eye examination Characteristic Number of eye exams Mean Range Last eye examination within o 1 year no (%) Eye doctor MD No. (%) OD No. (%) Both No. (%) Unknown No. (%) DR treatment No. (%)
Table 5—Compliance with Canadian Diabetes Association guidelines for diabetic retinopathy screening in our cohort
Total (n ¼ 70) 3.43 ± 3.76 0–20 47 (67.1) 8 (11.4) 53 (75.7) 6 (8.6) 3 (4.3) 0 (0)
MD, doctor of medicine (ophthalmologist); OD, doctor of optometry; DR, diabetic retinopathy.
Data n ¼ 82 16 (19.5) 66 (80.5) n ¼ 66 65 (98.5) 1 (1.5)
Complying with CDA guidelines Yes No. (%) No No. (%) Reason for non-compliance Too many eye exam No. (%) Too few eye exam No. (%) CDA, Canadian Diabetes Association; DR, diabetic retinopathy.
predicts higher rates of noncompliance. Age and gender failed to predict noncompliance. Due to having only a small number of non-Caucasian patients and patients with Type 2 diabetes, race and type of diabetes were not evaluated as predicting variables. This patient background likely reflects the background ethnic variation in our local community. Our model-fitting process began with a logistic regression model, regressing non-compliance against age, sex, duration of DM, HbA1c level, and an indicator variable for systemic complications (true/false). Stepwise AIC variable selection was applied to this model and removed sex and then age. Of the remaining three predictors, only one was considered to be significant (Duration, p ¼ 0.0322), with results shown in Table 6. Removing the other two non-significant predictors did not result in improvements to the model (reduction of AIC by 0.497, and increase of residual deviance by 3.503, shown in Table 7); therefore, we concluded with a predictive model using duration, HbA1c, and systemic complications. The difference in coefficient of Duration of DM is minimal between the two models: -0.2488, 95% CI –0.505 to –0.042, p ¼ 0.0322 for the three-variable conclusion; and -0.2656, 95% CI –0.515 to –0.070), p¼0.0174 for the single. Accordingly, we have quoted the three-variable model in the rest of this manuscript, as it should have slightly better predictive powers.
DISCUSSION This study involving children seen in a community care pediatric diabetic clinic in Canada showed that compliance rate with screening guidelines was only 19.5% (n ¼ 16/82)with the large majority of children having too many eye examinations. While the nature of noncompliance in our pediatric community differs from the underscreening found in other studies, most populations have been found to be noncompliant to their respective Table 6—Stepwise AIC-reduced model output, residual deviance: 69.736 AIC: 77.736
(Intercept) Duration HbA1C Systemic Complications
Estimate
p-value
2.5%
97.5%
-2.9256 -0.2488 0.2880 -1.0512
0.1101 0.0322 0.1480 0.1637
-6.69405756 -0.50524443 -0.09759681 -2.71064193
0.57800248 -0.04210508 0.69322459 0.33192246
AIC, Akaike information criterion.
CAN J OPHTHALMOL — VOL. ], NO. ], ] 2018
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Diabetic retinopathy screening—Abdella et al. Table 7—Model reduced to only significant predictors, residual deviance: 73.239 AIC: 77.239
(Intercept) Duration
Estimate
p-value
2.5%
97.5%
-0.5237 -0.2656
0.2003 0.0174
-1.3510911 -0.5145967
0.26749403 -0.07039506
AIC, Akaike information criterion.
guidelines for DR screening. Rosenberg’s study in 2011 on children from the Bronx, an area of New York City, showed only 35% of patients with DM were referred for an eye examination.9 A screening rate of 52% in adult patients was found in another American study.16 Research conducted in the United Kingdom, where screening is recommended annually for both Type 1 and Type 2 DM after the age of 12, found that only 64% of diabetic patients were receiving screening accordingly.15 While the previous studies exhibit low compliance rates to national guidelines, the low compliance is due to lack of eye examinations for DR screening. The main reason for low compliance in these studies was the low rates of referrals for screening. These lower referral rates are a result of less frequent visits to their family physicians, lower education of patients, lower age of patients, and less practical knowledge of DM.9,14,16 However, the lack of compliance in our study was actually due to excessive eye examinations, in relation to the CDA guidelines. Our community diabetes clinics, pediatricians, and nursing and allied health staff place emphasis on system care for diabetes, often having checklists for lab renal, vascular, and other complications of diabetes. Perhaps in the pediatric cohort we need to educate these groups about the actual guidelines to avoid over-screening of certain groups. Our study showed that shorter duration of DM may predict noncompliance to the guidelines outlined by CDA with a relatively short duration of DM compared with previous studies. With shorter duration of DM, parents and guardians may not have been familiar yet with the screening guidelines. This predictor of noncompliance varies from the factors previously discussed in adult diabetic patients. Physician recommendations as a predictor should be further investigated in pediatric patients. In our study, no DR was found despite poor control of DM, as indicated by the high HbA1c levels (mean 9). The incidence of DR in our cohort was consistent with many other studies. In 2016, Beauchamp et al. analyzed 12 535 children in a type 1 DM Exchange Clinic Registry and found that no participants had received treatment for diabetic retinopathy, although it did not report the incidence of DR.20 The mean age, DM duration, and HbA1c of this previous study were very close to the demographics of our present cohort. Another study that reviewed the data of 2125 children with DM screened for the first time found that the incidence of DR was 4.7 per 1000 pediatric patients per year.21 However, some studies have shown that the incidence of DR in pediatric patients may be higher. One United Kingdom–based study, which
4
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reviewed care data on over 27 600 children with diagnosed DM, found that 13% of those who had been screened had at least background DR.15 According to Wang et al.,22 diabetic retinopathy developed in children under the age of 21 who had been newly diagnosed with DM at rates of 20.1% and 7.2% in type 1 and type 2 patients, respectively.22 These studies do not support the extremely low incidence of DR found in our study, but this may be due to a higher mean age in the cohorts. The low incidence of DR in our study is likely due to a short mean duration of DM, and a relatively small cohort size. The duration of diabetes is well known to be an important risk factor for the development of DR. Studies have shown a typical duration of 4 5 years before development of DR, with one reporting an incidence of DR of 17% in people with DM for o 5 years and 97.5% in those with 4 15 years with DM.11 Since DR incidence increases with duration, screening should remain consistent and compliant with the guidelines to ensure patients do not develop or exacerbate DR. Because of the risk of blindness from DR, it is important for any primary care physician to know when to refer a patient with DM for an eye examination. Only 13% of family physicians from Quebec were familiar with the guidelines23 for type 1 DM and 80% for type 2 DM. Kraft reported24 that 60% of primary care physician referred patients with type 1 DM and 40% referred patients with type 2 DM for eye exams. While surveying primary care physicians in the United States, Mukamel25 found that most of the patients were referred to an optometrist only when they had eye complaints, with only 16% being routinely referred. In our study, 55 of the patients which had received screenings saw an optometrist and only 8 saw an ophthalmologist. This is because the parents self-referred their children to an eye doctor, and optometrists are more accessible than ophthalmologists. One limitation in this study was that eye examination information was requested from the parents of the diabetic pediatric patients rather than from their eye care professionals. Another limitation is that there was no long-term follow-up of pediatric diabetic patients. Future studies should follow the cohort from this study to observe the screening rates compared with CDA guidelines as the cohort ages. The incidence of DR should also be examined in the follow-up of the cohort. Additionally, future studies should investigate the reasons behind low compliance rates in retinopathy screening and how those reasons differ between adults and children. The patients in our population were overscreened, and we have identified this as a significant quality improvement objective for our community clinic. We will be moving to a standardized referral form with tracking, as well as offering an educational program for local primary caregivers and the staff in our multidisciplinary clinic. In the future, it is important to not onlyeducate family physicians and pediatricians, but to also educate parents
Diabetic retinopathy screening—Abdella et al. and guardians about the screening guidelines for diabetic retinopathy so that they also can be proactive in assuring compliance with CDA guidelines.
APPENDIX A. SUPPLEMENTARY
MATERIAL
Supplementary data are available in the online version of this article at https://doi.org/10.1016/j.jcjo.2018.03.012. REFERENCES 1. Zhang X, Norris SL, Saadine J, et al. Effectiveness of interventions to promote screening for diabetic retinopathy. Am J Prev Med. 2007;33:318-35. 2. Cruess AF, Gordon KD, Bellan L, Mitchell S, Pezzullo ML. The cost of vision loss in Canada. 2. Results. Can J Ophthalmol. 2011;46:315-8. 3. Kempen JH, O'Colmain BJ, Leske MC, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122:552-63. 4. Eye connect: diabetic retinopathy. Canadian National Institute for the blind: seeing beyond vision loss website. Available from: www.cnib.ca/en/your-eyes/eye-conditions/eye-connect/DR/Pages/ default.aspx. Accessed March 10, 2017. 5. Johansen J, Sjolie AK, Eshoj O. Refraction and retinopathy in diabetic children below 16 years of age. Acta Ophthalmol (Copenh). 1994;72:674-7. 6. Holl RW, Lang GE, Grabert M, Heinze E, Lang GK, Debatin KM. Diabetic retinopathy in pediatric patients with type-1 diabetes: effect of diabetes duration, prepubertal and pubertal onset of diabetes, and metabolic control. J Pediatr. 1998;132:790-4. 7. Massin P, Erginay A, Mercat-Caudal I, et al. Prevalence of diabetic retinopathy in children and adolescents with type-1 diabetes attending summer camps in France. Diabetes Metab. 2007;33:284-9. 8. Hamouda B, Messaoud R, Grira S, et al. Prevalence and risk factors of diabetic retinopathy in children and young adults. J Fr Ophtalmol. 2001;24:367-70. 9. Rosenberg JB, Freidman IB, Gurland JE. Compliance with screening guidelines for diabetic retinopathy in a large academic children's hospital in the Bronx. Journal of Diabetes and Its Complications. 2011;25:222-6. 10. Tapley JL, McGwin G, Ashraf AP, et al. Feasibility and efficacy of diabetic retinopathy screening among youth with diabetes in a pediatric endocrinology clinic: a cross-sectional study. Diabetol Metab Syndr. 2015;7:56. 11. Klein R, Klein BE, 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;102:520-6. 12. Canadian Diabetes Association Clinical Practice Guideline Expert Committee. Canadian Diabetes Association clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes. 2008;32(Suppl 1):S1-201. 13. Kohner EM, Aldington SJ, Stratton IM, et al. United Kingdom prospective DM study, 30: diabetic retinopathy at diagnosis of noninsulin-dependent diabetes mellitus and associated risk factors. Arch Ophthalmol. 1998;116:297-303. 14. Boucher MC, Desroches G, Garcia-salinas R, et al. Teleophthalmology screening for diabetic retinopathy through mobile imaging units within Canada. Can J Ophthalmol. 2008;43:658-68. 15. Ibanez-bruron MC, Solebo AL, Cumberland PM, Rahi JS. Screening for diabetic retinopathy in children and young people in the UK: potential gaps in ascertainment of those at risk. Diabetic Medicine. 2017;34:1012-3.
16. Tseng VL, Greenberg PB, Scott IU, Anderson KL. Compliance with the American Academy of Ophthalmology preferred practice pattern for diabetic retinopathy in a resident ophthalmology clinic. Retina. 2010;30:787-94. 17. Lewis K, Patel D, Yorston D, Charteris D. A qualitative study in the United Kingdom of factors influencing attendance by patients with diabetes at ophthalmic outpatient clinics. Ophthalmic Epidemiol. 2007;14:375-80. 18. Dervan E, Lillis D, Flynn L, Staines A, O’Shea D. Factors that influence the patient uptake of diabetic retinopathy screening. Ir J Med Sci. 2008;177:303-8. 19. Census Profile, 2016 Census. Statistics Canada. Available from: www12.statcan.gc.ca/census-recensement/2016/dp-pd/prof/index. cfm?Lang=E. Published Accessed November 29, 2017. 20. Beauchamp G, Boyle CT, Tamborlane WV, et al. Treatable diabetic retinopathy is extremely rare among pediatric t1d exchange clinic registry participants. Diabetes Care. 2016;39:e218-9. 21. Scanlon PH, Stratton IM, Bachmann MO, Jones C, Leese GP. Risk of diabetic retinopathy at first screen in children at 12 and 13 years of age. Diabetic Medicine. 2016;33(12):1655-8. 22. Wang SY, Andrews CA, Herman WH, Gardner TW, Stein JD. Incidence and risk factors for developing diabetic retinopathy among youths with type 1 or type 2 diabetes throughout the United States. Ophthalmology. 2017;124:424-30. 23. Delorme C, Boisjoly HM, Baillargeon L, Turcotte P, Bernard PM. Screening for diabetic retinopathy. Do family physicians know the Canadian guidelines? Canadian Family Physician. 1998;44: 1473-9. 24. Kraft SK, Marrero DG, Lazaridis EN, Fineberg N, Qiu C, Clark CM Jr. Primary care physicians' practice patterns and diabetic retinopathy. Current levels of care Archives of Family Medicine. 1997;6:29-37. 25. Mukamel DB, Bresnick GH, Wang Q, Dickey CF. Barriers to compliance with screening guidelines for diabetic retinopathy. Ophthalmic Epidemiology. 1991;6:61-72.
Disclosure: The authors have no proprietary or commercial interest in any materials discussed in this article. Supported by: This research did not receive any specific grant from funding agencies in the public, commercial, or not-forprofit sectors. The authors thank Dr. Wesley Burr, PhD, professor of statistics at Trent University, for his help with our statistical analysis. From the ⁎Trent University, Peterborough, Ont.; †Peterborough Health Regional Center, Peterborough, Ont.; ‡Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ont.; §Department of Ophthalmology and Vision Sciences, University of Alberta, Edmonton, Alb. Originally received Nov. 19, 2017. Final revision Jan. 31, 2018. Accepted Mar. 13, 2018 Correspondence to: Dr. M. Hermina Strungaru, MD, PhD, FRCSC, Department of Ophthalmology and Vision Sciences, University of Alberta, 2319, 10240 Kingsway Avenue NW, Edmonton, Canada, T5H3V9; [email protected]
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Diabetic retinopathy (DR) is the leading cause of new cases of legal blindness in adults1 and the third cause of blindness in Canada overall.2 The prevalence of retinopathy in the adult population with diabetes mellitus (DM) in the United States is 40.3% while the sight-threatening retinopathy prevalence is 8.2%.3 Diabetic retinopathy currently affects 500 000 Canadians.4 In type 1 DM patients, non-proliferative diabetic retinopathy is more likely to be found than proliferative diabetic retinopathy with a population frequency between 4%–16%5–7 for non-proliferative DR and 1.2%–9%8–10 for proliferative DR. Screening for DR is a crucial component of diabetes management as early detection of retinopathy can help prevent worsening of the sight threatening disease. Diabetic retinopathy screening generally consists of a dilated fundus examination from an experienced eye care professional, possible optical coherence tomography (OCT), and fluorescein angiography when indicated. While rates of DR in pediatric populations are low, various health organizations have still developed guidelines and screening regulations for such patients.11,12 The prevalence of DR in post-pubertal patients with type 1 diabetes increases dramatically after having DM for a period of 5 years,11 while 39% of similar patients with type 2 diabetes may have DR at the time of the diagnosis.13 Therefore, screening for DR in children with DM is dependent on the age of onset, the type of DM,
and the length of time the patient has had the disease. The Canadian Diabetes Association (CDA) recommends the initial retinopathy screening be at five years after the diagnosis of type 1 DM in all individuals aged 15 years and older or at age 15 if the patient has had type 1 DM for greater than 5 years.I In all individuals with type 2 DM, screening is recommended for at the time of diagnosis.12 Although type 1 DM pediatric patients should not be screened before the age of 15, we examined compliance of pediatric patients of all ages in terms of both underscreening as well as overscreening. Studies focusing on adult patients have shown a weak adherence to the screening recommendations outlined by the CDA.14 In 2008, 38% of a diabetic cohort across five provinces in Canada had never been screened for DR and another 30% had not been screened within the last two years.14 Lack of adherence to screening guidelines by underscreening of both pediatric and adult populations has been found in other countries as well, including in the United Kingdom and the United States.9,15,16 Factors that may predict noncompliance to the recommended guidelines include a lack of awareness of the potential consequences of DR, fear of laser treatment, and guilt over poor DM control.17 According to one study, the most significant predictor of getting screened was if the physician recommended a regular eye examination.18
& 2018 Canadian Ophthalmological Society. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jcjo.2018.03.012 ISSN 0008-4182/17 CAN J OPHTHALMOL — VOL. ], NO. ], ] 2018
1
Diabetic retinopathy screening—Abdella et al. Since compliance with DR screening guidelines has not been studied extensively in children, the objective of this study was to evaluate the diabetic retinopathy screening rates of pediatric patients with DM, and to determine the primary care physician’s adherence to the CDA guidelines. We believe this is the first study of such guideline compliance in Canada. We recognize that with the current health care climate in North America, quality improvement has become an important factor for physicians to consider. Since the age and gender distribution of children in Peterborough is comparable to Ontario, the largest province by population in Canada, we feel that our community clinic’s experience is translatable to other community clinics in Canada.19
Paent’s consent received
Study paent’s medical records and fill out quesonnaire
Assess paent’s compliance based on age and type of DM
Paent’s screening is compliant with CDA guidelines
Paent received too many eye exams (over-screened)
This study adhered to the tenets of the Declaration of Helsinki and was approved by the Peterborough Regional Health Center Research Ethics Board. Each subject provided informed consent. All patients who attended the diabetic pediatric clinic at Peterborough Regional Health Center between August 2016 and February 2017 were included. We identified 125 eligible children through the appointment schedule. Of these patients, 81 (64.8%) consented to participate after being approached in the clinic. For patients who missed their appointment, we sent consent forms and a questionnaire through mail, and 7.0% (n ¼ 3/43) responded, but only one was in time to be included in the study. Patients who did not respond were not included in the study. Clinical data was collected through the examination of patient records and through verbal clinical questionnaires to parents and guardians. Patients were assigned numbers to protect their privacy and ensure confidentiality. The parents and guardians were asked whether or not the patient was referred to and seen by an ophthalmologist or optometrist and when the first eye exam was given. They were also asked about how often the patient had been screened and whether or not the eye examination was negative for diabetic retinopathy. The responses to the questionnaire were used to determine compliance to the screening guidelines. Hospital records were used to determine the type of DM, date of DM diagnosis, systemic complications, and the most recent hemoglobin A1c (HbA1c). Compliance to CDA guidelines was assessed based on age and type of DM, as
outlined in Table 1. If patients received the right number of eye exams and screening was initiated at the recommended time, then they were deemed compliant. If one of these criteria was not followed, they were considered noncompliant. It was then determined whether non-compliant patients had received too many or too few eye exams compared with respective guidelines. This process is illustrated in Figure 1. Statistical analysis of the data was carried out using R Foundations for Statistical Computing 3.4.0 (The R Foundation, Vienna, Austria). Stepwise Akaike information criterion (AIC) variable selection for logistic regression was conducted to identify any predictors of noncompliance to the CDA screening guidelines with p ≤ 0.05 considered significant.
RESULTS The mean age of the 82 participants was 12 years of age (range 3–18 years), with 48 male patients (58.5%)and 79 Caucasian patients (96.3%) as seen in Table 2. Among the study participants, 79 patients (96.3%) had type 1 DM and 3 patients (3.7%) had type 2 DM. Mean age at diagnosis was 8 years (range 1–17 years), and the mean duration of DM was 4 years (range 0–15 years). HbA1c level 46.0 was in 81 participants (98.8%). We found that Table 2—Demographic characteristics of diabetic pediatric patients Features
Table 1—Screening guidelines for diabetic pediatric patients based on the Canadian Diabetes Association 415 o15
When yearly screening should be initiated Five years after diagnosis of T1DM In all individuals at diagnosis of T2DM At age 15 if duration of T1DM 45 years In all individuals at diagnosis of T2DM
T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus.
2
Paent received too few eye exams (under-screened)
Fig. 1 — Flowchart indicating process taken to recruit and consider patients for this study. CDA, Canadian Diabetes Association.
METHODS
Age (years)
Paent’s screening is not compliant with CDA guidelines
CAN J OPHTHALMOL — VOL. ], NO. ], ] 2018
Age (years) Mean Range Gender, No. (%) Female Male Ethnicity, No. (%) Asian Caucasian Mixed African-Caucasian
Data (n ¼ 82) 12.74 ± 3.50 3-18 34 (41.5) 48 (58.5) 1 (1.2) 79 (96.3) 2 (2.5)
Diabetic retinopathy screening—Abdella et al. Table 3—Diabetic characteristics of diabetic pediatric patients Feature Age at diagnosis (years) Mean age Range Duration of DM (years) Mean age Range Type of diabetes T1DM No. (%) T2DM No. (%) HbA1c Mean Range 4 6 No. (%) Systemic complications no (%) Insulin pump no (%)
Data (n ¼ 82)
Feature 8.41 ± 4.33 1–7 4.32 ± 3.64 0–15 79 (96.3) 3 (3.7) 9.12 ± 1.49 5.2–12.8 81 (98.8) 32 (39.0) 34 (41.4)
DM, diabetes mellitus; T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus; HbA1c, hemoglobin A variant (biomedical marker).
32 patients (39.0%) had systemic complications related to DM, such as diabetic ketoacidosis; and 34 patients (41.5%) in our cohort were on an insulin pump (Table 3). Of the 70 patients (85.4%) who had received an eye exam, 47 (67.1%) reported receiving a dilated comprehensive eye examination within the past 12 months, and 23 (32.9%) had an examination 4 12 months ago (Table 4). Of the patients who received eye exams, 53 (75.7%) saw an optometrist,8 (11.4%) saw an ophthalmologist, 6 (8.6%) saw both an optometrist and an ophthalmologist, and 3 (4.3%) did not know the type of the eye doctor they saw. None of the patients who had received an eye examination reported having DR, and no patients reported receiving treatment for DR (Table 4). Only 16 patients (19.5%) were screened for DR based on CDA guidelines (Table 5). Of the patients not following the guidelines, 65 received too many eye exams and only one received too few compared with CDA screening guidelines for their age and type of DM (Table 5). The data from all 82 patients was included in the logistic regression model to assess the predicting factors of the noncompliance with CDA guidelines. The model revealed that the only significant predicting factor of noncompliance was duration of DM (–0.249, 95% CI –0.505 to –0.042; p ¼ 0.0322), where shorter duration Table 4—Characteristics of diabetic pediatric patients who had an eye examination Characteristic Number of eye exams Mean Range Last eye examination within o 1 year no (%) Eye doctor MD No. (%) OD No. (%) Both No. (%) Unknown No. (%) DR treatment No. (%)
Table 5—Compliance with Canadian Diabetes Association guidelines for diabetic retinopathy screening in our cohort
Total (n ¼ 70) 3.43 ± 3.76 0–20 47 (67.1) 8 (11.4) 53 (75.7) 6 (8.6) 3 (4.3) 0 (0)
MD, doctor of medicine (ophthalmologist); OD, doctor of optometry; DR, diabetic retinopathy.
Data n ¼ 82 16 (19.5) 66 (80.5) n ¼ 66 65 (98.5) 1 (1.5)
Complying with CDA guidelines Yes No. (%) No No. (%) Reason for non-compliance Too many eye exam No. (%) Too few eye exam No. (%) CDA, Canadian Diabetes Association; DR, diabetic retinopathy.
predicts higher rates of noncompliance. Age and gender failed to predict noncompliance. Due to having only a small number of non-Caucasian patients and patients with Type 2 diabetes, race and type of diabetes were not evaluated as predicting variables. This patient background likely reflects the background ethnic variation in our local community. Our model-fitting process began with a logistic regression model, regressing non-compliance against age, sex, duration of DM, HbA1c level, and an indicator variable for systemic complications (true/false). Stepwise AIC variable selection was applied to this model and removed sex and then age. Of the remaining three predictors, only one was considered to be significant (Duration, p ¼ 0.0322), with results shown in Table 6. Removing the other two non-significant predictors did not result in improvements to the model (reduction of AIC by 0.497, and increase of residual deviance by 3.503, shown in Table 7); therefore, we concluded with a predictive model using duration, HbA1c, and systemic complications. The difference in coefficient of Duration of DM is minimal between the two models: -0.2488, 95% CI –0.505 to –0.042, p ¼ 0.0322 for the three-variable conclusion; and -0.2656, 95% CI –0.515 to –0.070), p¼0.0174 for the single. Accordingly, we have quoted the three-variable model in the rest of this manuscript, as it should have slightly better predictive powers.
DISCUSSION This study involving children seen in a community care pediatric diabetic clinic in Canada showed that compliance rate with screening guidelines was only 19.5% (n ¼ 16/82)with the large majority of children having too many eye examinations. While the nature of noncompliance in our pediatric community differs from the underscreening found in other studies, most populations have been found to be noncompliant to their respective Table 6—Stepwise AIC-reduced model output, residual deviance: 69.736 AIC: 77.736
(Intercept) Duration HbA1C Systemic Complications
Estimate
p-value
2.5%
97.5%
-2.9256 -0.2488 0.2880 -1.0512
0.1101 0.0322 0.1480 0.1637
-6.69405756 -0.50524443 -0.09759681 -2.71064193
0.57800248 -0.04210508 0.69322459 0.33192246
AIC, Akaike information criterion.
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Diabetic retinopathy screening—Abdella et al. Table 7—Model reduced to only significant predictors, residual deviance: 73.239 AIC: 77.239
(Intercept) Duration
Estimate
p-value
2.5%
97.5%
-0.5237 -0.2656
0.2003 0.0174
-1.3510911 -0.5145967
0.26749403 -0.07039506
AIC, Akaike information criterion.
guidelines for DR screening. Rosenberg’s study in 2011 on children from the Bronx, an area of New York City, showed only 35% of patients with DM were referred for an eye examination.9 A screening rate of 52% in adult patients was found in another American study.16 Research conducted in the United Kingdom, where screening is recommended annually for both Type 1 and Type 2 DM after the age of 12, found that only 64% of diabetic patients were receiving screening accordingly.15 While the previous studies exhibit low compliance rates to national guidelines, the low compliance is due to lack of eye examinations for DR screening. The main reason for low compliance in these studies was the low rates of referrals for screening. These lower referral rates are a result of less frequent visits to their family physicians, lower education of patients, lower age of patients, and less practical knowledge of DM.9,14,16 However, the lack of compliance in our study was actually due to excessive eye examinations, in relation to the CDA guidelines. Our community diabetes clinics, pediatricians, and nursing and allied health staff place emphasis on system care for diabetes, often having checklists for lab renal, vascular, and other complications of diabetes. Perhaps in the pediatric cohort we need to educate these groups about the actual guidelines to avoid over-screening of certain groups. Our study showed that shorter duration of DM may predict noncompliance to the guidelines outlined by CDA with a relatively short duration of DM compared with previous studies. With shorter duration of DM, parents and guardians may not have been familiar yet with the screening guidelines. This predictor of noncompliance varies from the factors previously discussed in adult diabetic patients. Physician recommendations as a predictor should be further investigated in pediatric patients. In our study, no DR was found despite poor control of DM, as indicated by the high HbA1c levels (mean 9). The incidence of DR in our cohort was consistent with many other studies. In 2016, Beauchamp et al. analyzed 12 535 children in a type 1 DM Exchange Clinic Registry and found that no participants had received treatment for diabetic retinopathy, although it did not report the incidence of DR.20 The mean age, DM duration, and HbA1c of this previous study were very close to the demographics of our present cohort. Another study that reviewed the data of 2125 children with DM screened for the first time found that the incidence of DR was 4.7 per 1000 pediatric patients per year.21 However, some studies have shown that the incidence of DR in pediatric patients may be higher. One United Kingdom–based study, which
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reviewed care data on over 27 600 children with diagnosed DM, found that 13% of those who had been screened had at least background DR.15 According to Wang et al.,22 diabetic retinopathy developed in children under the age of 21 who had been newly diagnosed with DM at rates of 20.1% and 7.2% in type 1 and type 2 patients, respectively.22 These studies do not support the extremely low incidence of DR found in our study, but this may be due to a higher mean age in the cohorts. The low incidence of DR in our study is likely due to a short mean duration of DM, and a relatively small cohort size. The duration of diabetes is well known to be an important risk factor for the development of DR. Studies have shown a typical duration of 4 5 years before development of DR, with one reporting an incidence of DR of 17% in people with DM for o 5 years and 97.5% in those with 4 15 years with DM.11 Since DR incidence increases with duration, screening should remain consistent and compliant with the guidelines to ensure patients do not develop or exacerbate DR. Because of the risk of blindness from DR, it is important for any primary care physician to know when to refer a patient with DM for an eye examination. Only 13% of family physicians from Quebec were familiar with the guidelines23 for type 1 DM and 80% for type 2 DM. Kraft reported24 that 60% of primary care physician referred patients with type 1 DM and 40% referred patients with type 2 DM for eye exams. While surveying primary care physicians in the United States, Mukamel25 found that most of the patients were referred to an optometrist only when they had eye complaints, with only 16% being routinely referred. In our study, 55 of the patients which had received screenings saw an optometrist and only 8 saw an ophthalmologist. This is because the parents self-referred their children to an eye doctor, and optometrists are more accessible than ophthalmologists. One limitation in this study was that eye examination information was requested from the parents of the diabetic pediatric patients rather than from their eye care professionals. Another limitation is that there was no long-term follow-up of pediatric diabetic patients. Future studies should follow the cohort from this study to observe the screening rates compared with CDA guidelines as the cohort ages. The incidence of DR should also be examined in the follow-up of the cohort. Additionally, future studies should investigate the reasons behind low compliance rates in retinopathy screening and how those reasons differ between adults and children. The patients in our population were overscreened, and we have identified this as a significant quality improvement objective for our community clinic. We will be moving to a standardized referral form with tracking, as well as offering an educational program for local primary caregivers and the staff in our multidisciplinary clinic. In the future, it is important to not onlyeducate family physicians and pediatricians, but to also educate parents
Diabetic retinopathy screening—Abdella et al. and guardians about the screening guidelines for diabetic retinopathy so that they also can be proactive in assuring compliance with CDA guidelines.
APPENDIX A. SUPPLEMENTARY
MATERIAL
Supplementary data are available in the online version of this article at https://doi.org/10.1016/j.jcjo.2018.03.012. REFERENCES 1. Zhang X, Norris SL, Saadine J, et al. Effectiveness of interventions to promote screening for diabetic retinopathy. Am J Prev Med. 2007;33:318-35. 2. Cruess AF, Gordon KD, Bellan L, Mitchell S, Pezzullo ML. The cost of vision loss in Canada. 2. Results. Can J Ophthalmol. 2011;46:315-8. 3. Kempen JH, O'Colmain BJ, Leske MC, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122:552-63. 4. Eye connect: diabetic retinopathy. Canadian National Institute for the blind: seeing beyond vision loss website. Available from: www.cnib.ca/en/your-eyes/eye-conditions/eye-connect/DR/Pages/ default.aspx. Accessed March 10, 2017. 5. Johansen J, Sjolie AK, Eshoj O. Refraction and retinopathy in diabetic children below 16 years of age. Acta Ophthalmol (Copenh). 1994;72:674-7. 6. Holl RW, Lang GE, Grabert M, Heinze E, Lang GK, Debatin KM. Diabetic retinopathy in pediatric patients with type-1 diabetes: effect of diabetes duration, prepubertal and pubertal onset of diabetes, and metabolic control. J Pediatr. 1998;132:790-4. 7. Massin P, Erginay A, Mercat-Caudal I, et al. Prevalence of diabetic retinopathy in children and adolescents with type-1 diabetes attending summer camps in France. Diabetes Metab. 2007;33:284-9. 8. Hamouda B, Messaoud R, Grira S, et al. Prevalence and risk factors of diabetic retinopathy in children and young adults. J Fr Ophtalmol. 2001;24:367-70. 9. Rosenberg JB, Freidman IB, Gurland JE. Compliance with screening guidelines for diabetic retinopathy in a large academic children's hospital in the Bronx. Journal of Diabetes and Its Complications. 2011;25:222-6. 10. Tapley JL, McGwin G, Ashraf AP, et al. Feasibility and efficacy of diabetic retinopathy screening among youth with diabetes in a pediatric endocrinology clinic: a cross-sectional study. Diabetol Metab Syndr. 2015;7:56. 11. Klein R, Klein BE, 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;102:520-6. 12. Canadian Diabetes Association Clinical Practice Guideline Expert Committee. Canadian Diabetes Association clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes. 2008;32(Suppl 1):S1-201. 13. Kohner EM, Aldington SJ, Stratton IM, et al. United Kingdom prospective DM study, 30: diabetic retinopathy at diagnosis of noninsulin-dependent diabetes mellitus and associated risk factors. Arch Ophthalmol. 1998;116:297-303. 14. Boucher MC, Desroches G, Garcia-salinas R, et al. Teleophthalmology screening for diabetic retinopathy through mobile imaging units within Canada. Can J Ophthalmol. 2008;43:658-68. 15. Ibanez-bruron MC, Solebo AL, Cumberland PM, Rahi JS. Screening for diabetic retinopathy in children and young people in the UK: potential gaps in ascertainment of those at risk. Diabetic Medicine. 2017;34:1012-3.
16. Tseng VL, Greenberg PB, Scott IU, Anderson KL. Compliance with the American Academy of Ophthalmology preferred practice pattern for diabetic retinopathy in a resident ophthalmology clinic. Retina. 2010;30:787-94. 17. Lewis K, Patel D, Yorston D, Charteris D. A qualitative study in the United Kingdom of factors influencing attendance by patients with diabetes at ophthalmic outpatient clinics. Ophthalmic Epidemiol. 2007;14:375-80. 18. Dervan E, Lillis D, Flynn L, Staines A, O’Shea D. Factors that influence the patient uptake of diabetic retinopathy screening. Ir J Med Sci. 2008;177:303-8. 19. Census Profile, 2016 Census. Statistics Canada. Available from: www12.statcan.gc.ca/census-recensement/2016/dp-pd/prof/index. cfm?Lang=E. Published Accessed November 29, 2017. 20. Beauchamp G, Boyle CT, Tamborlane WV, et al. Treatable diabetic retinopathy is extremely rare among pediatric t1d exchange clinic registry participants. Diabetes Care. 2016;39:e218-9. 21. Scanlon PH, Stratton IM, Bachmann MO, Jones C, Leese GP. Risk of diabetic retinopathy at first screen in children at 12 and 13 years of age. Diabetic Medicine. 2016;33(12):1655-8. 22. Wang SY, Andrews CA, Herman WH, Gardner TW, Stein JD. Incidence and risk factors for developing diabetic retinopathy among youths with type 1 or type 2 diabetes throughout the United States. Ophthalmology. 2017;124:424-30. 23. Delorme C, Boisjoly HM, Baillargeon L, Turcotte P, Bernard PM. Screening for diabetic retinopathy. Do family physicians know the Canadian guidelines? Canadian Family Physician. 1998;44: 1473-9. 24. Kraft SK, Marrero DG, Lazaridis EN, Fineberg N, Qiu C, Clark CM Jr. Primary care physicians' practice patterns and diabetic retinopathy. Current levels of care Archives of Family Medicine. 1997;6:29-37. 25. Mukamel DB, Bresnick GH, Wang Q, Dickey CF. Barriers to compliance with screening guidelines for diabetic retinopathy. Ophthalmic Epidemiology. 1991;6:61-72.
Disclosure: The authors have no proprietary or commercial interest in any materials discussed in this article. Supported by: This research did not receive any specific grant from funding agencies in the public, commercial, or not-forprofit sectors. The authors thank Dr. Wesley Burr, PhD, professor of statistics at Trent University, for his help with our statistical analysis. From the ⁎Trent University, Peterborough, Ont.; †Peterborough Health Regional Center, Peterborough, Ont.; ‡Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ont.; §Department of Ophthalmology and Vision Sciences, University of Alberta, Edmonton, Alb. Originally received Nov. 19, 2017. Final revision Jan. 31, 2018. Accepted Mar. 13, 2018 Correspondence to: Dr. M. Hermina Strungaru, MD, PhD, FRCSC, Department of Ophthalmology and Vision Sciences, University of Alberta, 2319, 10240 Kingsway Avenue NW, Edmonton, Canada, T5H3V9; [email protected]
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