Use of Eye Care Services among Type 2 Diabetic Patients in Laguna

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Original Article Philippine Journal of OPHTHALMOLOGY Use of Eye Care Services among Type 2 Diabetic Patients in Laguna Glenn Carandang, MD, MPH, 1,2, Maria Victoria Rondaris, MD, MPH, 3, and Genejane Adarlo, MD, MEMME, PhD Candidate 4 1 San Pablo Colleges Medical Center, San Pablo City, Philippines 2 International Eye Institute, St Luke s Medical Center, Quezon City, Philippines 3 Department of Health Eye Center, East Avenue Medical Center, Quezon City, Philippines 4 Ateneo de Manila University Office of the Loyola Schools Health Services, Health Sciences Program, Quezon City, Philippines Correspondence: Glenn Vincent Carandang, MD, MPH St. Luke s Medical Center 279 E. Rodriguez Sr. Blvd., Quezon City, 1102, Philippines Email: carandang@ces.com.ph Disclaimer: Top Ophthalmic Products & Services Corporation (Makati City, Metro Manila, Philippines) provided the Topcon TRC-NW8F Non-Mydriatic Retinal Camera. ABSTRACT Objective: The aim of the study was to determine the prevalence of diabetic patients seeking an ophthalmic evaluation for. Specific objectives were to describe the prevalence and risk factors for diabetic retinopathy (DR) in a group of diabetic patients referred for retinal evaluation from different internists in Laguna by screening using digital retinal photography. Methods: The study was a hospital-based mixed method study involving two portions: quantitative (cross-sectional) and qualitative. The cross-sectional portion involved patients diagnosed with type 2 diabetes by internists from San Pablo Colleges Medical Center referred for retinal evaluation using a non-mydriatic retinal camera. Retinal photographs were categorised for the presence and severity of according to the international clinical DR severity scales recommended by the Global Diabetic Retinopathy Project Group. The qualitative portion involved a focus group discussion among diabetic patients and a short key informant interview with the referring internists. Results: Sixty-seven (67) diabetic patients were evaluated for (DR) using digital retinal photography. The overall prevalence of any DR was 26% (n=18): 55% mild NDPR, 33% moderate NDPR, 6% severe NPDR and 6% PDR. Diabetic macular edema (DME) was present in 22% of patients with any form of DR. The focus group discussion reported the following reasons for consulting an ophthalmologist: presence of blurring of vision, availability of budget, knowledge of the need for ophthalmic evaluation, and order for evaluation by the internist. Interviews among the referring internists revealed three primary reasons for referring: history of visual disturbances, uncontrolled diabetes and finances of the patient. Conclusion: This study presented a lower prevalence rate of among patients who underwent digital retinal photography compared to that of other studies published in the Philippines. Nevertheless, it is important to continue patient education with regards to diabetic complications in the eye, and improve the referral system among medical practitioners. Keywords: diabetes,, screening, patient education, referral system Philipp J Ophthalmol 2016;41:39-44 July - December 2016 39

Diabetic retinopathy (DR) is a leading cause of blindness, responsible for 4.8% of the 37 million cases of blindness worldwide, according to the World Health Organization (WHO) estimates. 1 In the United States, the estimated prevalence of and vision-threatening diabetic retinopathy was 28.5% and 4.4%, respectively. 2 While in Singapore, the prevalence of was 38.1% and of vision-threatening retinopathy was 11.8%. 3 In the Philippines, diabetes falls within the top 10 causes of mortality according to the Department of Health. In a hospital-based study done at the Philippine General Hospital using dilated fundus examination and fluorescein angiography revealed a clinical and angiographic DR prevalence of 61.8% and 83.6%, respectively. 4 Another study done in PGH, to determine the complications and cardiovascular risk factors among newly diagnosed Type 2 diabetics, showed a DR prevalence of 12%. 5 Despite advances in diagnosis and treatment of DR, there remain several barriers to screening for among patients and attending doctors, both in developed and developing countries. In the United States, one study revealed that no perceived need for screening (39.7%) and cost of an eye examination (32.3%) were the top reasons for not getting screened for DR. 6 In Indonesia, the lack of knowledge for the need of eye care and financial constraints were common reasons given by patients. 7 In China, the main reasons were lack of knowledge, no apparent symptoms and lack of advice for regular examinations from their medical provider. 8 Among physicians attending to diabetic patients, several studies showed varying practice patterns for screening and referring patients for ophthalmic evaluation. In the 1990s, studies showed that in Australia, about 53% of general practitioners do not perform fundus examination or screened only less than half of their patients using undilated fundoscopy 9 ; while two studies in the United States showed contrasting results. In the first study about 70% 10 would perform undilated fundoscopy while in the other, less than half would. 11 Interestingly, these two studies also showed similar referral practice patterns among doctors. In the first study about 35% of doctors never referred patients for ophthalmic evaluation while 26% referred all patients, and the remaining 39% referred on a case-to-case basis 12. In the second study 35% referred their Type 2 diabetic patients for ophthalmic evaluation. 13 More recent practice pattern studies reported that in Brazil, only 21.4% performed fundoscopy but 86.9% of them would refer patients to ophthalmologists for screening. 14 While in Canada, 19.4% of doctors felt there was no need to routinely perform fundus examination on all diabetics, but about 80.6% of them regularly referred all diabetics to an ophthalmologist; 86.1% of the participants felt there was no need to worry about retinopathy if blood sugar levels were controlled. 15 Interestingly, two studies reported that physicians who have recently graduated (less than 5 years in practice) tend to refer more to an ophthalmologist compared to those who had been practicing for 20 or more years. 11,12 A focused group discussion among primary care providers cited the most common barriers for referral: poor communication from eye care providers, finances, and availability of an eye specialist. Suggestions from the group to improve the referral system included: implementing electronic medical records, enhancing communications within the referral network, having a regular ophthalmologist and a retinal camera in the primary care clinics. 16 Multiple prevalence studies around the world used non-mydriatic ultrawide field retinal photography as a screening method. The images compared favourably with dilated ETDRS photography and dilated fundus examination in determining DR and DME severity. 15,16 Digital retinal photographs were also acquired more rapidly compared to the latter two methods, and proved beneficial in DR evaluation to a broader population. Vision loss from DR is preventable. Evidencebased treatment is available to reduce significantly the risk for moderate vision loss and blindness by more than 90%. 1 The rapidness of these new methods screening may create a paradigm shift in the referral system across medical specialties. And data from this study may reinforce the referral system as well as influence policy-making in the health sector. Objective The aim of the study was to determine the prevalence of diabetic patients seeking an ophthalmic evaluation for. Specific objectives were to describe the prevalence and risk factors for (DR) in a group of diabetic 40 Philippine Academy of Ophthalmology

Philippine Journal of OPHTHALMOLOGY patients referred for retinal evaluation from different internists in Laguna by screening using digital retinal photography. Methodology The study was a hospital-based mixed method study involving two portions: quantitative (crosssectional) and qualitative. The cross-sectional study involved 67 patients, aged 30 to 91, diagnosed with type 2 diabetes mellitus (DM) by three (3) internists and referred for retinal evaluation at San Pablo Colleges Medical Center. After obtaining an informed consent, patients underwent a standardized interview to obtain their age, gender, hypertension history, managing/referring physician, diabetes medications, and duration of their DM; as well as a review of their latest glycosylated hemoglobin (HBA1C). Visual acuity assessment using the Early Treatment Diabetic Retinopathy Study (ETDRS) chart (Figure 1), and a one-field nonmydriatic 45 degree retinal photography using Topcon TRC-NW8F Non-Mydriatic Retinal Camera (Topcon Corporation, Tokyo, Japan) were performed (Figure 2). The screening of all patients was done on August 8, 2013. Figure 1. Visual Acuity Assessment using ETDRS Chart From the digital photographs obtained, the presence and severity of were categorised according to the international clinical DR severity scales (Table 1 and 2) recommended by the Global Diabetic Retinopathy Project Group 8 as: (1) no (No DR), (2) mild/moderate/ severe non-proliferative (NPDR), (3) proliferative (PDR), and (4) for presence of diabetic macular edema (DME). (Table 2) Patients were categorised based on the worse eye. Results of the quantitative study were tabulated. Table 1. Diabetic Macular Edema Disease Severity Scale 8 Proposed Disease Severity Level Diabetic macular edema apparently absent Diabetic macular edema apparently present Findings Observable on Dilated Ophthalmoscopy No apparent retinal thickening or hard exudates in posterior pole Some apparent retinal thickening or hard exudates in posterior pole Table 2. Diabetic Retinopathy Disease Severity Scale 8 Proposed Disease Severity Level No apparent retinopathy Mild nonproliferative Moderate nonproliferative Severe nonproliferative Proliferative diabetic retinopathy Findings Observable on Dilated Ophthalmoscopy No abnormalities Microaneurysms only More than just microaneurysms but less than severe nonproliferative Any of the following: more than 20 intraretinal hemorrhages in each of 4 quadrants; definite venous beading in 2 quadrants; Prominent intraretinal microvascular abnormalities in 1 quadrant And no signs of proliferative retinopathy One or more of the following: neovascularization, vitreous/ preretinal hemorrhage The qualitative study involved two approaches conducted by a third party. The first approach was a focus group discussion (FGD) with 8 diabetic patients answering the question - what are the reasons for seeing an eye doctor? The second approach was through a short key informant interview among the 3 referring internists answering the question - what are the reasons for referring to an eye doctor? Figure 2. Digital Fundus Photography July - December 2016 41

Results In this study, the overall prevalence of any DR was 26% (n=18): 55% mild NDPR, 33% moderate NDPR, 6% severe NPDR and 6% PDR (Figure 4). DME was present in 22% of patients with any form of DR. Figure 5 shows the sample photos obtained from the non-mydriatic camera during the study. Figure 4. Prevalence of Diabetic Retinopathy Table 3. Clinical Characteristics of Patients with No DR, NPDR, PDR and DME. Overall No DR NPDR PDR DME N (%) 67 (100) 49 (73.1) 17 (25.4) 1 (1.5) 4 (6) Sex, Male 26 (38.8) 16 (32.7) 9 (52.9) 1 4 (100) Female 41 (61.2) 33 (67.3) 8 (47.1) 0 0 Age (Years) 60.8 (12) 62.1 (12.7) 57.2 (9.2) 59 59.8 (4.3) Diabetes Duration 7.5 (6.2) 7.2 (6.3) 8.4 (6.3) 10 7 (2.5) (Years) Age at Diabetes 53.3 (11.2) 54.9 (10.9) 48.8 (11.3) 49 52.8 (3.8) Diagnosis HBA1C (%) 7.5 (2.1) 7.5 (2.2) 7.8 (1.8) 6.5 7.9 (1.1) Insulin Treatment, 18 (26.9) 9 (18.4) 9 (52.9) 0 1 (25) Hypertension, 32 (47.8) 20 (40.8) 12 (70.6) 0 3 (75) Seen by an Ophthalmologist, 22 (32.8) 14 (28.6) 8 (47.1) 0 0 Note: Values are expressed as and mean (SD). Table 4. Diabetes Severity and Ophthalmic Consultation No Non-Proliferative Proliferative Diabetic Diabetic Diabetic Retinopathy Retinopathy Retinopathy Figure 5. Sample Photos depicting the level of diabetic retinopathy. Table 3 shows the clinical characteristics of the 67 participants. Most of the patients were female (61.2%). Mean age was 60.8 (±12) years, mean duration of diabetes was 7.5 (±6.2) years and mean HBA1C level was 7.5 (±2.1)%. Compared to patients without DR, those with some form of DR were younger, had longer duration of diabetes, had a higher mean HBA1C level and most had hypertension. Insulin use was also higher among patients with DR. Table 4 shows that only a third of all participants are seen by an ophthalmologist. Similar results were seen in No DR patients, of whom a third consulted an ophthalmologist for screening. Among NPDR patients, less than half saw an ophthalmologist. No one had been examined in the sub-group of NPDR patients with DME. No DR NPDR PDR DME Total Consulted an Ophthalmologist, 14 (28.6) 8 (47.1) 0 0 22 (32.8) No Ophthalmologist, 35 (71.4) 9 (52.9) 1 4 45 (67.2) Total 49 17 1 4 67 Note: DME patients is a sub-group of the NPDR patients. The focus group discussion reported the following reasons for consulting an ophthalmologist: presence of blurring of vision (6 out of 8 participants), availability of budget (4 out of 8), knowledge of the need for ophthalmic evaluation (2 out of 8), and order for evaluation by the internist (2 out of 8). Interviews among the referring internists revealed three primary reasons for referring: history of visual disturbances, uncontrolled diabetes and finances of the patient. 42 Philippine Academy of Ophthalmology

Philippine Journal of OPHTHALMOLOGY Discussion This study presents data on the prevalence of diabetic patients examined for, and the prevalence and severity of DR among diabetic patients treated at San Pablo Colleges Medical Center, who were screened each eye using a non-mydriatic retinal digital photographs. Twenty-six percent (26%) of participants had some form of DR. This prevalence rate is lower compared to 61.8% and 83.6% noted in the PGH study. The difference can probably be attributed to the different socio-economic status of both populations, influencing the control of their diabetes and early access to healthcare. Patients found to have DR tend to have longer duration of DM, poorer glycemic control based on their HBA1C level and have a history of hypertension. In this study, the two-thirds of participants were not screened for DR by an ophthalmologist since their diabetes diagnosis. These findings were similar with the results from a paper by Dandan Wang, et al in China where nearly a third of patients did not follow the annual eye evaluations and half did not have any form of examination 8 ; and with results reported in a poster presentation by Lee GD at the 2016 American Society of Retina Specialists (ASRS) in San Francisco, where out of the 149 patients, only 43 (29%) had a documented eye exam, and about 28% of those examined had. 18 The most common reasons cited for not seeking eye care were a lack of symptoms or a lack of perceived need for an eye examination, availability of budget, and a lack of knowledge about. These reasons were consistent with the findings of the studies done in China, Indonesia and the United States. 7-9 The interviews from referring internists revealed similar responses compared to the reports done in Canada and the United States, such as lack of a perceived need for referral (no visual disturbances or controlled blood glucose levels) and the lack of finances. 14-15 There is a paucity of information about factors influencing eye care-seeking behaviour and practice patterns with regards to screening among diabetic Filipino patients and primary care physicians, respectively. Clinical epidemiological information in the Philippines for DR is also far from comprehensive. Therefore, a large sample survey with long-term follow-up results is needed as well as a more comprehensive study on the knowledge, attitudes and practices among Filipino patients and doctors as well as a review of the feedback mechanisms vis-a-vis the referral system among medical practitioners. While the ophthalmologist can provide specialized eye care for the DR patient, prevention and control of diabetes and its complications lie primarily in the hands of their attending physician. Thus, results from such studies may help tailor recommendations to control the prevalence of and help strengthen partnership among primary care physicians and eye care specialists in preventing vision loss among these diabetic patients. Conclusion There is a need to strengthen awareness among diabetic patients with regards to complications in the eye and improve the referral system among medical practitioners. This study presented a lower prevalence rate of among patients who underwent digital retinal photography compared to that of other studies published in the Philippines. Nevertheless, it is important to continue patient education and good control of risk factors to lower further the prevalence of DR. References 1) World Health Organization. Prevention of blindness from diabetes mellitus: report of a WHO consultation in Geneva, Switzerland, 9-11 November 2005: http://www.who.int/ iris/handle/10665/43576 (accessed date: June 12, 2013). 2) Zhang X, Saaddine JB, Chou CF, et al. Prevalence of in the United States, 2005-2008. JAMA. 2010;304:649-56. 3) Lim MC, Lee SY, Cheng BC, et al. Diabetic retinopathy in diabetics referred to a tertiary centre from a nationwide screening programme. Ann Acad Med Singapore. 2008;37:753-9. 4) Fajardo-Gomez MF, Uy HS. Prevalence of diabetic retinopathy among diabetic patients in a tertiary hospital. Philipp J Ophthalmol. 2005;30:178-180. 5) Fojas, MC, Lantion-Ang, FL, Jimeno, CA, et al. Complications and cardiovascular risk factors among newly-diagnosed type 2 diabetics in Manila. Philipp J. Int Med 2009;47:99-105. 6) Chou CF, Sherrod CE, Zhang X, et al. Barriers to eye care July - December 2016 43

among people aged 40 years and older with diagnosed diabetes, 2006-2010. Diabetes Care 2014;37:180-188. 7) Adriono G, Wang D, Octavianus C, Congdon N. Use of eye care services among diabetic patients in urban Indonesia. Arch Ophthalmol. 2011;129:930-5. 8) Wang D, Ding X, He M, et al. Use of eye care services among diabetic patients in urban and rural China. Ophthalmology 2010;117:1755-1762. 9) Dickson PR, McCarty CA, Keeffe JE, et al. Diabetic retinopathy: examination practices and referral patterns of general practitioners. Med J Aust. 1996;164:341-4. 10) Yung CW, Boyer MM, Marrero DG, Gavin TC. Patterns of diabetic eye care by primary care physicians in the State of Indiana. Ophthalmic Epidemiol. 1995;2:85-91. 11) Kraft SK, Marrero DG, Lazaridis EN, et al. Primary care physicians practice patterns and : current levels of care. Arch Fam Med. 1997;6:29-37. 12) Preti RC, Saraiva F, Junior JA, et al. How much information do medical practitioners and endocrinologists have about? Clinics (Sao Paulo) 2007;62:273-8. 13) Khan, IA, Sadiqulla M. Practice patterns of diabetic retinopathy referral among doctors in a tertiary hospital. Int J Med Sci Public Health. 2014;3:233-235 14) Holley CD, Lee PP. Primary care provider views of the current referral-to-eye-care process: focus group results. Invest Ophthalmol Vis Sci 2010;51:1866-1872. 15) Williams GA, Scott IU, Haller JA, et al. Single-field fundus photography for screening: a report by the American Academy of Ophthalmology. Ophthalmology. 2004;111:1055-62. 16) Silva PS, Cavallerano JD, Sun JK, et al. Nonmydriatic ultrawide field retinal imaging compared with dilated standard 7-field 35-mm photography and retinal specialist examination for evaluation of. Am J Ophthalmol. 2012;154:549-559. 17) Wilkinson CP, Ferris FL III, Klein RE, et al. Proposed international clinical and diabetic macular edema disease severity scales. Ophthalmology 2003;110:1677-82. 18) Lee GD, et al. Referral rates are hurting people at risk for vision-threatening. Poster presentation at 34th Annual Scientific Meeting of the American Society of Retina Specialists (ASRS 2016) San Francisco, California, August 2016. 44 Philippine Academy of Ophthalmology