Does patient education improve compliance to routine diabetic retinopathy screening?

Abstract

Introduction

Diabetic retinopathy (DR) screening relies on adherence to follow-up eye care. This article assesses if a model of patient education and tele-retina screening among high-risk patients with DR can achieve increased rates of compliance within a one-year follow-up.

Methods

Between May 2014 and May 2016, DR screening was conducted in a cohort of 101 patients with diabetes in Southern Ontario. Optical coherence tomography and fundus photography images were used to visualize the retina remotely. Enrolled patients participated in an educational seminar at the screening site with the expressed purpose of enhancing patient understanding of DR. A chi-squared test was used to assess patient compliance to follow-up examinations within 6–12 months, while pre-to post-screening HbA1c levels were compared using a dependent t-test.

Results

Of 101 patients who completed the study, 33 patients (32.6%) have never previously been screened for DR. Baseline compliance to annual screening increased from 36 patients (35.6%) to 51 patients (50.5%) after the tele-retina programme (p = 0.03). Eighty-nine patients (88%) were referred to an optometrist for ongoing care compared with 12 patients (11.9%) to an ophthalmologist for management of DR. Overall, 100 patients (99.0%) were satisfied with the tele-retina screening. There was no significant change in pre- to-post screening HbA1c levels (p = 0.91).

Discussion

Patient education-focused tele-retina screening for DR significantly increased compliance to follow-up in a high-risk, non-compliant patient population. Management of diabetes as captured by HbA1c levels remain unchanged in the cohort indicating a need for ongoing inter-professional collaboration in education and vision screening.

Keywords

Tele-retina screening follow-up patient education diabetes diabetic retinopathy

Introduction

The prevalence of diabetes has increased significantly in Ontario since the turn of the millennium.^1,2 From 1996 to 2009, the number of adults with either type 1 or type 2 diabetes over the age of 20 years has collectively risen from 439,123 to 1,140,248 while the population as a whole has increased by approximately 1.2 million over the same period.² This epidemic is observed internationally with the global prevalence of diabetes anticipated to climb above 500 million adults by 2030.³

Diabetic retinopathy (DR) is a leading cause of blindness in the working-age population and a common cause of visual impairment in Canada.^4–6 While DR treatment is available, the success of such interventions relies on early detection through regular screening and timely referrals for treatment.⁷ Although screening for DR is covered in most Canadian provinces, including Ontario, only two-thirds of Ontarians with diabetes over 20 years of age were screened in 2015.⁸ Despite national tele-ophthalmology initiatives to bridge the gap to access to care by establishing screening camps closer to communities, ongoing reasons for non-compliance include a lack of education around the importance of DR screening.^9,10 A National Health and Nutrition Examination Survey indicate that people at ‘highest risk’ are people without a high school diploma or people at lower income levels with significantly higher rates of DR.¹¹ This survey implies that a lack of knowledge of diabetic complications may lead to negligence and non-compliance to screening. Other existing barriers include travel considerations, socioeconomic barriers, and health system barriers.⁹

Tele-retina, a new branch of telemedicine that delivers eye care through digital equipment and telecommunications technology,¹² has the potential to address some of these barriers. By providing access to specialist care from remote sites, a reduction in wait and travel times to the ophthalmologist is cost-effective for patients and enables sharing of health information with multiple members of the healthcare team remotely.¹³ However, long-term screening goals still remain elusive. Keenum and colleagues (2015)¹⁴ proposed that DR screening programmes will not meet national screening goals without the incorporation of eye health education initiatives. Literature has shown that handouts and telephone reminders were helpful,^15,16 but an education session comprised of a visual-oral presentation has not been explored to date.

Herein this study aims to address these key factors: patient education and access to care, which can influence compliance to screening, particularly in a ‘high-risk’ patient population. We defined ‘high-risk’ as patients with diabetes who are previously non-compliant with screening examinations or have not had examinations within at least one year or who were not scheduled for a follow-up exam. A tele-retina screening programme with an education component was implemented in the Hamilton-Niagara-Haldimand Brant Local Health Integration Network (HNHB LHIN) to implement a model for ongoing care and education around DR. We aimed to determine the effect of compliance to follow-up through implementation of a visual-oral presentation by an eye-care professional at each screening site.

Methods

This prospective cohort study enrolled patients from nine sub-urban community sites in the HNHB LHIN and their surrounding catchment area, between May 2014 and May 2016. Patients were included in this study if they were over 18 years old, were literate in English, competent to give informed consent, and diagnosed with type 1 or 2 diabetes. Patients were excluded from the study if they presented with narrow angles at screening, had a history of angle-closure glaucoma for which they could not be dilated or were unwilling or unable to complete all parts of the screening examination. The study was carried out following the tenets of the Declaration of Helsinki and the Good Clinical Practice guidelines and was approved by the Hamilton Integrated Research Ethics Board (REB #14-661). Informed consent was obtained prior to enrolling patients in the study.

The screening programme was organized and advertised in collaboration with LHIN. Advertisement of the programme using posters, email communication, and discussion with local representatives also helped to engage local physicians and nurses. For each patient, demographics including age, gender, highest level of education, occupation, and marital status, were obtained at each screening site. Most recent pre-screening HbA1c levels were obtained from the patients’ referring physician or nurse practitioner. Corrected visual acuity (VA) was measured by a research fellow using a four-meter Early Treatment of Diabetic Retinopathy Study (ETDRS) chart. Intraocular pressure (IOP) were measured using a Tonopen (AVIA®, Reichert). Prior to imaging, pupils were dilated using Mydfrin (Phenylephrine Hydrochloride) 2.5% ophthalmic solution and Mydriacyl (Tropicamide) 1% ophthalmic solution.

At each site, the ophthalmic technician used Cirrus HD-Optical Coherence tomography (OCT) (Cirrus HD-OCT 4000, Carl Zeiss Meditec, Dublin, CA), to acquire five-line horizontal scans and macular cube scans as well as two fundus images, one centred on the macula and one on the optic nerve head. These images were uploaded by the ophthalmic technician to a secure database hosted by the Ontario Telemedicine Network (OTN) and transferred to the retina specialist for assessment using the OTN platform. Results and follow-up recommendations were communicated back to the screening sites. Patients without retinal pathology or with mild non-proliferative DR were referred to optometrists for follow-up within six months to one year as per the 2017 International Council of Ophthalmology guidelines.¹⁷ Patients requiring further investigations or management were seen by an ophthalmologist within one month. Compliance with follow-up appointments was assessed within 6–12 months. HbA1c levels were obtained from the patient’s referring physician or nurse to assess objective changes post-screening.

Education: During the screening, a 12-slide basic DR presentation including images, made by the retina specialist (VC), was presented to patients by an eye-care professional. The presentation described how diabetes can impact the eye, why vision loss might take place, and possible treatment options. It also addresses risk factors and importance of regular annual screening.

Patients were administered two 35-question surveys: a pre- and post-education seminar questionnaire (Appendix A). The DR knowledge assessment questions were identical in both questionnaires. The first questionnaire was administered at the time of registration. The final questionnaire was administered within 15 minutes of the completion of the education seminar, immediately following all the vision assessments. The post-education seminar survey also included a set of additional questions to assess overall satisfaction with the tele-retina programme and to identify patient-specific barriers to screening. Patient satisfaction with the tele-retina screening programme was assessed using a Likert scale, which has previously been demonstrated to be a valid approach of assessing satisfaction with care in an ophthalmology setting.¹⁸

All analyses were performed on SPSS Software (IBM, Version 22.0). Continuous variables were reported as means and standard deviations. Categorical data was summarized as frequency values and percentages. A chi-squared test was used to compare the proportion of patients compliant to follow-up to those who were already compliant with DR screening prior to the tele-retina session. Change in HbA1c levels pre-to-post tele-retina screening was compared using a dependent t-test. All tests were two-tailed and a p-value < 0.05 was considered significant.

Results

The DR screening was completed by 101 patients from nine sites in Southern Ontario (Figure 1). Of these, 22 patients (21.7%) were recruited from a long-term psychiatric inpatient hospital facility. High-risk patients accounted for 65 (64.4%) of the patient cohort; more specifically, 34 patients (33.7%) had not had any form of eye examinations within at least the past five years. Thirty-three patients (32.6%) highlighted that this was their first DR screening. Further demographic information is available in Table 1. Baseline diabetic examination results are displayed in Table 2.

Figure 1.

Patient recruitment plot.

Table 1.

Patient demographics.

Gender – N patients (%)
Male	44 (43.6)
Female	57 (56.4)
Age in years – Mean (SD)	58.0 (11.8)
Intra-ocular pressure (mmHg) – Mean (SD)
OD	17.8 (3.1)
OS	17.8 (3.3)
Race – N patients (%)
Caucasian	88 (87.1%)
Black	2 (2.0)
Asian	3 (3.0)
Hispanic	2 (2.0)
Other	6 (5.9)
Education completed – N patients (%)
Did not complete high school	21 (20.8)
High school	41 (40.6)
College and university bachelor’s degree	30 (29.7)
Professional and graduate degree	8 (7.9)
Information missing	1 (1.0)
Average income below the estimated poverty line
Yes	52 (51.5)
No	34 (33.7)
Unknown	15 (14.5)

SD: standard deviation; OD: Oculus dextrus (right eye); OS: Oculus sinister (left eye).

Table 2.

Baseline diabetic examination.

Type of diabetes – N patients (%)
Type 1	8 (7.9)
Type 2	92 (91.1)
Information missing	1 (1.0)
Uses insulin – N patients (%)
No	63 (62.4)
Yes	38 (37.6)
Pre-screening HbA1c
Mean (SD)	8.1 (2.1)
HbA1c level after follow-up
Mean (SD)	8.2 (2.1)
Years with diabetes at screening
Mean (SD)	9.0 (10.0)
Visual acuity (ETDRS Letters)
OD, Mean (SD)	74.6 (15.9)
OS, Mean (SD)	74.1 (16.1)
Checks blood glucose at home – N patients (%)
No	17 (16.8)
Yes	83 (82.2)
Information missing	1 (1.0)
Self-reported hypertension – N patients (%)
No	39 (38.6)
Yes	59 (58.4)
Information missing	3 (3.0)
Most recent eye exam – N patients (%)
Within a year	36 (35.6)
Within 2 years	23 (22.7)
Other	42 (35.8)
Average daily blood glucose levels (mmol/L) – N patients (%)
4–8.9	47 (46.5)
9–12.9	21 (20.7)
13-17.9	15 (14.9)
≥18	4 (4.0)

SD: standard deviation; OD: Oculus dextrus (right eye);OS: Oculus sinister (left eye).

Baseline knowledge of DR was collected from the pre-screening questionnaires. Prior to the education session, 59 patients (58.4%) did not know diabetes could affect vision compared with 14 patients (13.9%) post screening (p = 0.001). Sixty-four patients (63.3%) correctly identified the recommended interval to follow-up for DR screening before the education seminar compared with 98 patients (97.0%) post-seminar (p = 0.001). However, although nearly 63% of patients knew the recommended screening guidelines, only 36 patients (35.4%) were compliant with follow-ups. Moreover, 64 patients (63.3%) did not know of any conservative or medical managements of diabetes compared with 16 (15.8%) post screening (p = 0.0001; Table 3). Following the education seminar at the screening sites, 95 patients (94.1%) reported to have understood the importance of annual eye exams and indicated that the education seminar made them more likely to attend their follow-up examinations. Compliance to follow-up post screening was 50.5% (51 patients), contributing to a significant increase in compliance compared with baseline (35.6%, p = 0.032) in a high-risk cohort. The primary motivation for follow-up among 56 patients (55.4%) was fear of losing vision. The remaining patients indicated that their motivation was either because ‘the doctor says so’ (20 patients (19.8%)) or because they were now more aware that annual screening was recommended (15 patients (14.7%)).

Table 3.

Knowledge assessment of diabetic retinopathy. These pre- and post-education questions were used to evaluate patients’ awareness of diabetic retinopathy.

Knowledge assessment survey
Questions	Pre-education answer	Pre-education answer	Post-education answer	Post-education answer
Questions	Correct answer (%)	Incorrect answer (%)	Correct answer (%)	Incorrect answer (%)
What are the complications of diabetic retinopathy?	59 (58.4)	42 (41.6)	87 (86.1)	14 (13.8)
Do you know how often your eyes should be examined?	65 (64.4)	36 (35.6)	98 (97.0)	3 (3.0)
The first sign that your diabetes may be affecting your eyes is:	41 (40.6)	56 (55.4)	55 (54.5)	24 (23.8)
Diabetes that affect the back of the eye can always be reversed (true/false).	66 (65.3)	30 (29.7)	55 (55.4)	41 (40.6)
Do you know what types of treatments are currently available for diabetic retinopathy?	4 (3.9)	92 (91.0)	78 (77.2)	16 (15.8)
Common causes of blindness in people under 50 years of age:	66 (65.2)	32 (31.6)	86 (85.1)	15 (14.9)
Diabetes can affect all the following organs:	14 (13.9)	56 (55.4)	51 (50.5)	41 (40.6)

Overall, there was high patient satisfaction with the screening programme. Ninety-eight patients (97.3%) reported that the education seminar was helpful; 78 patients (77.5%) were very satisfied with the tele-retina programme while 20 patients (20.7%) were satisfied, and two patients (1.8%) were ambivalent. Most patients (99.0%) acknowledged that they understood the information provided to them through the presentation and the recommendations for future screening (Table 4). Self-reported factors that contributed to patient satisfaction were location close to home (93.1%), free service (100.0%), and a telephone reminder one week prior to visit (98.0%). Most patients also strongly agreed that the need for an eye exam was explained to them in a way they could understand (99.0%) and were reassured that they could speak to the ophthalmologist regarding their vision if desired (83.0%).

Table 4.

Factors that determined satisfaction with tele-retina technology.

Satisfaction with tele-retina technology
Questions	Strongly disagree (%)	Disagree (%)	Neutral (%)	Agree (%)	Strongly agree (%)
The need for an eye screening exam was explained to me in a way I could understand.	1 (1.0)	0 (0)	0 (0)	26 (25.7)	74 (73.3)
The machine used for my eye exam was explained to me in a way I could understand.	0 (0)	0 (0)	1 (1.0)	40 (40.0)	59 (59.0)
The use of tele-retina communication between the site where I received screening and Hamilton Health Sciences was explained to me.	0 (0)	1 (1.0)	4 (4.0)	40 (39.6)	56 (55.4)
I understand that I can request to speak to the ophthalmologist (eye doctor) who evaluates the eye scans in Hamilton.	2 (2.0)	1 (1.0)	14 (14.0)	37 (37.0)	46 (46.0)
The screening nurse or technician gave me easy-to-understand information about the need for a follow up eye examination.	0 (0)	0 (0)	2 (2.0)	37 (36.6)	62 (61.4)
It's important to me that most of the eye exams were done close to my home and that I did not travel or stay at a large centre (Hamilton).	0 (0)	0 (0)	2 (2.0)	26 (25.7)	73 (72.3)

A longitudinal assessment of diabetic control was assessed via serum HbA1c levels at 12-month’s post screening. In total, 63 patients completed their blood work after screening. Remaining patients either did not follow-up as scheduled or did not complete any further blood work at the time of data collection. The mean HbA1c levels pre and post screening were 8.1% ± 2.1% and 8.2 ± 2.2% respectively (p = 0.91). A total of 89 patients (88.1%) were referred to community optometrists and 12 patients (11.9%) were referred to an ophthalmologist for further management. The mean time to follow up was 4.12 ± 1.4 months with either an ophthalmologist or optometrist.

Discussion

By 20 years after diabetes onset, approximately 60% of type 2 patients and virtually all of type 1 patients with diabetes will have some degree of retinopathy.¹⁹ Despite increasing efforts to make DR screening programmes more available in rural sites, only 67% of Ontarians with diabetes meet the current guidelines; this still falls short of the provincial target of 80%.⁸ It is important to identify ‘high-risk’ patients, those who at baseline, are non-compliant with the current Canadian screening recommendations. Similar to findings of Zhang et al. (2012),¹¹ our study also demonstrated that high-risk patients also fall within a low-income bracket (Table 1).²⁰ Household income below the low-income bracket can present barriers in transportation, lack of access to resources or information, and poor compliance.¹¹ Another major challenge now is that there is no existing province-wide database to identify high-risk patients. Thus, innovative solutions are necessary to increase compliance to DR screening and follow-up in ‘high-risk’ groups. This study used a patient education model combined with a tele-screening programme to reach high-risk, non-compliant patients to successfully increase compliance to follow-up. The programme was very well received with overall high patient satisfaction. Further, compliance to follow-up was significantly increased post screening in the high-risk cohort.

Although access to care has improved tremendously in recent years through tele-ophthalmology initiatives, a lack of awareness of diabetic complications remains as a gap in literature that hinders compliance to routines examinations.^19,21–24 We hoped to fill the gap by implementing an educational seminar as a component to tele-retina to provide a basic level of understanding of diabetes and its ocular complications. Our findings also revealed that most patients lack in awareness of the effect of diabetes on their vision. Our study did not show that illiteracy was a cofounding factor because nearly 78% of patients in our cohort (79 patients; Table 1) were at least high-school graduates. Lack of knowledge in this case can be attributed to a lack of education around diabetes. In our group, although a majority of patients (82.2%) reported monitoring blood glucose on a weekly basis, the majority (58.4%) did not know any of the complications of elevated blood glucose levels on vision. The purpose of monitoring daily blood glucose levels is to ensure appropriate actions are taken to prevent complications. However, if a majority of patients are lacking knowledge of the adverse effects, the importance of routine assessments can be undermined. This is why we believe that although nearly 64% of patients were aware that annual diabetic screening examinations are recommended, compliance to follow-up was half that (34.6%) at baseline. However, within one-year post screening, compliance to follow-up increased to 50.5%. A systematic review by Zhang et al. also found that, among other interventions, increasing patient and provider awareness of DR improved screening uptake by patients.⁹ Further, counselling newly diagnosed patients and patients with uncontrolled blood glucose on the importance of annual eye examinations can increase compliance.²⁵ Our study showed a significant improvement in compliance to follow-up eye screening following the provision of information about DR, its complications, and available treatments in a presentation format. Although we conducted an oral presentation with diagrams, Basch and colleagues (1999) showed that education in the format of booklet, pamphlet, or telephone counselling can also be useful.¹⁵

A study done by Tang et al. also reported that health literacy and patient awareness scores were negatively correlated to diabetic control.²⁶ Therefore, our study focused on HbA1c levels to assess longitudinal blood glucose control. Tight glycemic control with an HbA1c ≤7% is associated with favourable DR outcomes, delaying development or progression of microvascular complications.²⁷ Changes in Hb1c values can also affect vision and sensitivity at the central 10° of the macula.²⁸ However, there was no improvement in the systemic control of diabetes among patients in our study. The average HbA1c prior to screening was 8.1%, without any significant change after screening. Despite highlighting the importance of tight blood glucose levels to prevent DR, the HbA1c levels remained unaffected in our patient populations. Diabetes is a multisystem disorder and its management is complex; this warrants multidisciplinary support to achieve diabetic goals.⁹ While greater awareness of DR and access to appropriate resources serves as a foundation for better patient outcomes, continued patient education on self-management and self-efficacy is needed from all health care providers.^9,29

We also aimed to connect patients with local optometrists to facilitate ongoing care and compliance. Within one-year after screening, compliance to follow-up increased significantly from 35.4% to 50.5%. A key aspect of increased compliance using tele-retina is the ability to connect patients to long-term follow-up (optometry or ophthalmology). All patients in our study were referred to a vision care specialist; 88% of patients were referred to an optometrist close to home. In high-risk patient populations, where nearly 33% of patients have not had any formal DR screening, providing the basic knowledge and access to resources (via optometrists or ophthalmologists) can improve compliance to screening.

While the vast majority of patients reported that the educational seminar was helpful and made them feel more likely to attend follow-up appointments (96% and 94.1%, respectively), only 50.5% actually attended. This is comparable to the results of Basch’s group, which showed that eye health educational resources doubled retinal examinations (27.3% to 54.7%) but patient compliance was still only around 50%.¹⁵ For those unable to attend, we believe that factors such as inability to take time off work, inconvenience, or forgetfulness may be contributing to failure to comply despite advance notice of their follow-up.³⁰ Boucher et al.’s telemedicine initiative showed that patients were aware of the implications of diabetes but 28% were still noncompliant with follow-up due to negligence.³¹ Graham-Rowe et al. (2018) also showed that barriers of screening attendance were identified within the person with diabetes, such as confusion between retinopathy screening and routine follow-up, healthcare factors (i.e. lack of recommendations for screening and inaccurate registers) and lack of media coverage.³²

Our study is not without limitations. Longitudinal studies with a larger cohort are warranted to accurately assess the impact of an educational seminar. A 6–12-month duration for follow-up on HbA1 levels may be inadequate to identify a significant change in management practices. In addition, the questionnaire used in this study was not validated as there were no single published surveys addressing the objectives highlighted in our presentation. Further, the questionnaire included medical terms that lay patients may not be familiar with, which may be reflected in some of their responses rather than a true lack of knowledge of DR. Finally, an ongoing challenge for tele-retina initiatives is the inability to identify those individuals at highest risk – namely patients who do not seek any medical care from any other healthcare professional (i.e. general practitioner, diabetes education nurse, foot nurse, optometrist, etc.). Therefore, inter-professional outreach and collaboration is required to spread the word in to remote communities.

In conclusion, this pilot initiative demonstrates that patient compliance to screening can be improved through ongoing education around diabetes and eye diseases at screening sites and follow-up examinations. A written, visual, or oral format of education establishes a definite and measurable impact on patient understanding of eye diseases. These programmes are well received by high-risk patients who otherwise had poor compliance to screening. Reminders for upcoming appointments from the screening programme and/or referring doctors’ offices can be helpful. Finally, arranging follow-up with a local optometrist or ophthalmologist close to home, after the initial screening, can be effective in increasing compliance, accountability, and ensuring an inter-professional team approach to patient care.

Footnotes

Acknowledgements

We thank our on-site technicians, Myrna Fronda and Amanda Weaver, who travelled to every site and committed their time to register patients and acquire images, to make the screenings possible.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Financial support for the research from the Ministry of Health and Long-Term Care and Local Health Integration Network.

Appendix A

References

Lipscombe

Hux

Trends in diabetes prevalence, incidence, and mortality in Ontario, Canada 1995–2005: A population-based study.

Lancet 2007; 369: 750–756.

Lind

Garcia-Rodriguez

Booth

, et al. Mortality trends in patients with and without diabetes in Ontario, Canada and the UK from 1996–2009: A population-based study. Diabetologia 2013; 56: 2601–2608.

Whiting

Gauriguata

Weil

, et al. IDF diabetes atlas: Global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 2011; 94: 311–321.

Frank

Diabetic retinopathy.

N Engl J Med 2004; 350: 48–58.

Hirari

Tielsch

Klein

, et al. Ten-year change in vision-related quality of life in type I diabetes: Wisconsin epidemiologic study of diabetic retinopathy. Ophthalmology 2011; 118: 353–358.

Maberley

Hallands

Chuo

, et al. The prevalence of low vision and blindness in Canada. Eye 2006; 20: 341–346.

Lawrenson

Graham-Rowe

Lorencatto

, et al. Interventions to increase attendance for diabetic retinopathy screening. Cochrane Database Syst Rev 2018; 1: CD012054.

Health Quality Ontario. Measuring up: A yearly report on how Ontario’s health system is performing. Report, Toronto: Queen’s Printer for Ontario, 2015.

Zhang

Norris

Saaddine

, et al. Effectiveness of interventions to promote screening for diabetic retinopathy. Am J Prev Med 2007; 33: 318–335.

10.

Serpas

Genter

, et al. Divergent perceptions of barriers to diabetic retinopathy screening among patients and care providers, Los Angeles, California, 2014–2015. Prev Chronic Dis 2016; 13: E140.

11.

Zhang

Cotch

Ryskulova

, et al. Vision health disparities in the United States by race/ethnicity, education, and economic status: Findings from two nationally representative surveys. Am J Ophthalmol 2012; 154: S53–S62.

12.

Kanagasingam

Kumar

Goldschmidt

, et al. Teleophthalmology. Berlin: Springer-Verlag Berlin Heidelberg, 2006, https://www.springer.com/gp/book/9783540337140.

13.

Gupta

The economics of telemedicine for vitreoretinal diseases.

Curr Opin Ophthalmol 2011; 22: 194–198.

14.

Keenum

McGwin

Jr Witherspoon

, et al. Patients’ adherence to recommended follow-up eye care after diabetic retinopathy screening in a publicly funded county clinic and factors associated with follow-up eye care use. JAMA Ophthalmol 2016; 134: 1221–1228.

15.

Basch

Walker

Howard

, et al. The effect of health education on the rate of ophthalmic examinations among African Americans with diabetes mellitus. Am J Public Health 1999; 89: 1878–1882.

16.

Walker

Schechter

Caban

, et al. Telephone intervention to promote diabetic retinopathy screening among the urban poor. American Am J Prev Med 2008; 34; 185–191.

17.

International Council of Ophthalmology. ICO Guidelines for Diabetic Eye Care. San Francisco, CA: International Council of Ophthalmology, 2017.

18.

Ziaei

Katibeh

Eskandari

, et al. Determinants of patient satisfaction with ophthalmic services. BMC Res Notes 2011; 4:1–4.

19.

Singer

Nathan

Fogel

, et al. Screening for diabetic retinopathy. Ann Intern Med 1992; 116: 660–671.

20.

Statistics Canada. Low income cut-offs (LICOs) before and after tax by community and family size in current dollars, https://www150.statcan.gc.ca/t1/tbl1/en/tv.action?pid=1110024101 (2015, accessed 9 July 2018).

21.

Bursell

Cavallerano

, et al. Stereo nonmydriatic digital-video color retinal imaging compared with early treatment diabetic retinopathy study seven standard field 35-mm stereo color photos for determining level of diabetic retinopathy. Ophthalmology 2001; 108: 572–585.

22.

Maclennan

McGwin

Jr Searcey

, et al. A survey of Alabama eye care providers in 2010–2011. BMC Ophthalmol 2014; 14: 44.

23.

Pasagian-Macaulay

Basch

Zybert

, et al. Ophthalmic knowledge and beliefs among women with diabetes. Diabetes Educ 1997; 23: 433–437.

24.

Muba

Hall

Lewallen

Compliance with eye screening examinations among diabetic patients at a Tanzanian referral hospital.

Ophthalmic Epidemiol 2007; 14: 306–310.

25.

Sheppler

Lambert

Gardiner

, et al. Predicting adherence to diabetic eye examinations: development of the compliance with annual diabetic eye exams survey. Ophthalmology 2014; 121: 1212–1219.

26.

Tang

Pang

Chan

, et al. Health literacy, complication awareness, and diabetic control in patients with type 2 diabetes mellitus. J Adv Nurs 2008; 62: 74–83.

27.

Axer-Siegel

Herscovici

Gabbay

, et al. The relationship between diabetic retinopathy, glycemic control, risk factor indicators and patient education. Isr Med Assoc J 2006; 8: 523–526.

28.

Kaure

Ismail

Mutalib

, et al. HbA1c and retinal sensitivity in diabetics using microperimetry. J Optom . 2019; 12: 174–179. DOI: 10.1016/j.optom.2018.03.007

29.

Cavan

Makaroff

Fernades

, et al. The diabetic retinopathy barometer study: Global perspectives on access to and experience of diabetic retinopathy screening and treatment. Diabetes Res Clin Pract 2017; 129: 16–24.

30.

Willis

Doan

Gleeson

, et al. Self-reported healthcare utilization by adults with diabetic retinopathy in the United States. Ophthalmic Epidemiol. 2018; 25: 365–372. DOI: 10.1080/09286586.2018.1489970.

31.

Boucher

Nguyen

Angioi

Mass community screening for diabetic retinopathy using nonmydriatic camera with telemedicine.

Can J Ophthalmol 2005; 40: 734–742.

32.

Graham-Rowe

Lorencatto

Lawrenson

, et al. Barriers to and enablers of diabetic retinopathy screening attendance: a systematic review of published and grey literature. Diabet Med. 2018; 35: 1308–1319. DOI: 10.1111/dme.13686.