Diabetes mellitus (DM) is a growing epidemic worldwide and the Asia-Pacific is expected to experience the greatest burden of DM, where economies are moving from low- to middle-income levels.1,2 In China, a large-scale population-based study conducted on 46,239 adults reported a 14-fold rise in DM prevalence over the span of 30 years (0.67% in 1980 vs 9.7% in 2008).3 The Asia-Pacific is home to half of the people with diabetes in the world; specifically, 153 million and 78 million are from the Western Pacific and Southeast Asia, respectively.4 Populous countries, such as China and India, have achieved recent exponential economic success, and in turn, adopted dramatic lifestyle changes such as unhealthy diets and a lack of physical activity leading to obesity, high blood pressure (BP), and high cholesterol contributing to the rising prevalence of diabetes.5
With increasing prevalence of DM, prevalence of diabetic retinopathy (DR), a leading cause of blindness in adults, is also set to increase.6 Vision impairment from DR places a considerable burden on patients' quality of life (QoL).7 Globally in 2015, an estimated 36 million were blind and 216 million people had visual impairment.8 The largest number of blind and visually impaired people resided in the Asian region, namely, South Asia, followed by East Asia and Southeast Asia.8 Diabetic retinopathy caused 1.1% of all cases of blindness and 1.3% of all visual impairment in 2015.9 The percentage of blindness caused by DR varied in the Asia-Pacific, ranging from less than 1% in South Asia (0.16%), Oceania (0.32%), East Asia (0.51%), and Southeast Asia (0.59%) to more than 3% in Central Asia (3.60%), high-income Asia-Pacific countries (3.87%), and Australasia (4.48%).10 Prevalence of blindness and visual impairment due to DR decreased between 1990 and 2015 in Oceania and Central and Eastern Europe, yet increased in the high-income Asia-Pacific, North America, Australasia, and Asian regions.9
Vision loss from DR is almost entirely preventable.11 In a meta-analysis that included 27,120 diabetic participants, the pooled incidence of proliferative diabetic retinopathy (PDR) was found to be lower in participants from 1986-2008 (2.6%) compared with participants from 1975-1985 (19.5%).12 These findings highlight the benefits of having programs targeted at increasing awareness of DR-related risk factors, earlier identification and initiation of care for patients with retinopathy, and improved primary interventions through glycemic and BP control. The main limitation of the meta-analysis, however, is a lack of contributing data from countries within the Asia-Pacific. With diabetes13 and DR rapidly increasing in the Asia-Pacific, it is vital to ensure that ophthalmologists are adequately prepared. In this review, we describe the DR-related epidemiology, its risk factors, screening strategies, management, and public health challenges faced uniquely within the Asia-Pacific.
Prevalence of DR
Vision-threatening DR (VTDR) consists of the advanced stage of PDR or diabetic macular edema (DME).14,15Table 1 summarizes the prevalence of studies conducted within the last decade, organized by regions.16 A majority of prevalence studies from the Asia-Pacific focused on DR in type 2 diabetes because of the low prevalence of type 1 diabetes in these populations. Hence, comparison of DR prevalence between Asia-Pacific and global estimates14 will be restricted only to type 2 diabetes.
The prevalence of DR among type 2 diabetes from Singapore (30.4-35.0%),17-19 China (11.9-43.1%),20-25 Hong Kong (12.9-39.0%),26,27 Taiwan (25.0%),28 Pakistan (27.4%),29 Malaysia (39.8%),30 Sri Lanka (27.4%),31 Thailand (24.0-31.4%),32,33 and Australia (28.5-39.4%)34-36 is comparable to the United Kingdom37,38 and United States39 (28.5-39.1%). Studies from South Korea (15.8%),40 India (9.6-33.9%),41-50 and New Zealand (19.0-22.5%)51,52 revealed lower DR prevalence than Western countries, whereas Indonesia (43.1%)53 had significantly higher DR prevalence. The authors suggested that the low DR prevalence in South Korea40 may be a result of an effective diabetes program as evident by their high (80%) rates of diagnosed diabetes. The availability of good healthcare alone, however, cannot explain why Singapore has twice the prevalence of DR as compared with South Korea, as the healthcare systems in these countries are comparable in terms of their accessibility and proficiency. Moreover, Singapore also had high (89%) rates of diagnosed diabetes.17
Estimates on VTDR prevalence from Singapore (7.1-9.0%),17-19 China (4.4-13.8%),20-22 Hong Kong (9.8%),26 Nepal (14.4%),54 and Indonesia (26.3%)53 reported higher VTDR prevalence than the United Kingdom37,38 and the United States39 (1.4-4.4%). This implies that most DR cases may have been detected only when symptomatic or complications have occurred, or that these populations are genetically more susceptible to the severe form of DR. Countries such as South Korea (4.6%),40 Taiwan (2.8%),28 India (3.3-6.6%),42,46,50 Australia (non-Indigenous: 4.4%),34 and New Zealand (2.5%)52 reported similar VTDR prevalence as Western countries. Comparison of VTDR between Asia-Pacific and Western countries, however, should be interpreted with caution. A majority of the countries in the Asia-Pacific17-22,25,26,28,40,42,43,46,50,53 considered the severe form of nonproliferative DR (NPDR) as part of VTDR, whereas the global estimates only considered PDR and/or DME.14 Prevalence of DME in South Korea (2.8%),40 Singapore (5.7-7.2%),18,19 China (5.2-11.2%),21,25 Hong Kong (8.6%),26 Nepal (5.5%),55 Sri Lanka (5.3%),31 Australia (8.5%),35 and New Zealand (11.4%)51 is higher than the West (1.4-3.8%).38,39
Studies from Australia36,56 and Singapore17,57 reported that the frequency of type 2 DM varied by race/ethnicity but the frequency of DR prevalence did not. Within Australia, although the prevalence of DM in indigenous populations was 8 times higher than non-Indigenous Australians, the prevalence of DR was essentially similar between Indigenous and non-Indigenous Australians.36,56 Similarly in Singapore, although the prevalence of DM among Indians (21.6%) was 2-fold higher compared with Chinese (11.5%), the prevalence of DR did not vary greatly between them (Indians 36.5% and Chinese 30.3%).17,57 Rather, the differences may be attributed to different racial and cultural attitudes that favor practices that are considered risk factors for DM, such as alcohol consumption, cardiovascular disease prevalence, smoking, obesity, and hypertension.2,58
Indians living in Singapore had a higher DR prevalence than Indians living in an urban region of India (18%).46 The authors speculated that the higher DR prevalence observed in Singapore Indians may be a result of an increased acculturation to a Westernized lifestyle.59 This hypothesis is in line with the increased prevalence of DM and DR among second-generation Indian immigrants than first-generation Indian immigrants living in Singapore. Furthermore, the lower prevalence of DR may be a result of selective mortality of those with DR in urban India, leading to a lower prevalence.
Rapidly developing economies such as China and India are observing an urban-rural divide in terms of DR disease burden. In India, the less developed rural region demonstrated a marked lower prevalence of DR (10.3%42 vs 18.0%46) in the type 2 diabetes population. Similarly in China, the poorer southern regions experienced lower prevalence of DR and VTDR (27.6% and 11.9%) than the more affluent northern regions (33.1% and 15.5%).20 However, earlier studies from China (2008,60 2009,25 2011,61 2012,24 201523) consistently reported higher prevalence of DR among adults with type 2 diabetes living in rural regions (29.1-43.1%)24,25 compared with their urban counterparts (18.1%).24 One plausible explanation as suggested by the authors may be a lack of access to medical resources, resulting in higher rates of undiagnosed DM, which puts people living in the rural area at higher risk of developing severe forms of DR.20
MODIFIABLE RISK FACTORS
Table 2 summarizes the common modifiable risk factors for DR, namely, hyperglycemia, BP, dyslipidemia, and obesity, from studies conducted in the Asia-Pacific. Studies from the Asia-Pacific have reported consistent associations between hyperglycemia19,21,40,42,62-67 and systolic BP18,19,21,40,64-67 with DR but less consistent association with diastolic BP.18,40,42,65 Furthermore, conflicting findings have been reported between associations of lipid serum levels and obesity with DR.
Studies from China,62 South Korea,40 Singapore,18 and Australia68 did not find any significant associations between dyslipidemia with DR. However, a study from China found that a higher level of triglycerides was protective of DR [odds ratio (OR), 0.93; P = 0.01], whereas higher levels of low density lipoprotein (LDL) cholesterol were associated with DR (OR, 1.15; P < 0.001).21 Also, higher levels of total (and LDL) cholesterols were protective of any DR (P = 0.001) but not with VTDR among Singaporean Malays.19 In Australia, higher levels of total (and LDL) cholesterols were independently associated with clinically significant macular edema (CSME) but not with DR.68 The differential finding between low triglyceride21 (and cholesterol)19 levels with retinopathy remained unexplained and requires further exploration by other studies.
Asian studies reported either a nonsignificant or inverse association of body mass index (BMI) with DR. Studies from China21,69 reported no significance between BMI and DR, whereas those from South Korea40 and Singapore70-72 found an inverse relationship between BMI and the presence of DR.73 It is possible that lower BMI may reflect a more advanced, poorly controlled form of diabetes that results in both unintentional weight loss and DR, whereas those diabetics with higher BMI may have a shorter duration or milder stage of the disease that is less likely to cause DR. Another possible explanation for the protective effect of BMI could be that persons with DR could have adopted positive behavioral modifications that led to lower BMI levels. A study on Western individuals from Australia reported opposing results, where higher BMI was found to have increased the odds of having DR. A recent study from Singapore reported that, though a lower BMI was protective of DR, a higher waist-hip ratio (WHR), indicating abdominal obesity, was associated with an increase of DR in women.70 These findings suggest that WHR may be a more accurate indicator than BMI for monitoring for obesity in Asians.
A majority of Asia-Pacific studies have used an observational study design where temporality of diseases cannot be drawn. There is a need to assess the ethnic variations in DR risk factors using a longitudinal study design with uniform measurement methods to examine DR-related causal risk factors.
PREVENTION AND SCREENING
Controlling Risk Factors
Studies conducted in the Asia-Pacific region have supported a correlation between glycemic control and diabetes complications in type 2 diabetes patients.66,74,75 A clinical study from Australia showed that patients with poor BP or lipid control in addition to poor glucose control were at a greater risk of DR, compared with glucose control alone.74 In a recent clinical study from Singapore, a wider variability of systolic BP, even among those with good glycemic control, was associated with moderate DR among patients with type 2 diabetes.66 Good glycemic control is also important as it can lead to the regression of DR. In China, a 5-year community-based prospective study on patients with type 2 diabetes showed DR regression in 24% of patients (n = 110), which occurred mostly in patients with lower glucose and lower serum triglyceride levels.76 In Hong Kong, the regression rate was 13.2% and was also associated with lower glycated hemoglobin A1c (HbA1c) along with an absence of albuminuria.63
Data from the UK Prospective Diabetes Study and the Diabetes Control and Complications Trial, major clinical trial studies from the United Kingdom and United States involving white populations, showed that controlling blood glucose (HbA1c < 7%)77,78 and BP79,80 levels slowed the onset and progression of retinopathy. However, there is no clinical trial data from the Asia-Pacific. Thus, there is a need to have randomized controlled trials to test the benefit of lowering blood glucose and BP in populations within the Asia-Pacific.
Regular photographic screening of DR is an effective strategy to prevent vision loss from DR.81 There were regional variations in the methods of DR screening used. In India, most patients were diagnosed with DR in eye hospitals,82 which often used DR screening camps, as opposed to programs integrated into existing diabetes management clinics. Despite these efforts, however, the coverage of screening services in India was still limited, with the majority of programs reaching less than half of their targeted districts.82 In Cambodia, the majority of patients with diabetes presented to the eye hospital as walk-in cases.83 In China, DR screening among persons with diabetes has not been carried out nor has a systematic screening program for DR been established.
The nonmydriatic camera is an acceptable screening tool, used in studies from developed countries.84 The popularity of nonmydriatic cameras has increased because of 3 reasons; first, its lack of dilation makes screening easier to perform without ophthalmologist supervision; second, it is considered a safer option, particularly in Asia, where acute angle closure is a concern; third, it is a much preferred method by patients who travel long distances to return home. One study in China reported a sensitivity of 67% and specificity of 94% of 1-field fundus photographs taken with a nonmydriatic camera when compared with ophthalmoscopy in detecting VTDR; whereas for detecting any DR, the sensitivity and specificity of the nonmydriatic camera were 76% and 80%, respectively.85 Another study in China, using 2-field fundus photographs, found sensitivity and specificity to be 86% and 92%, respectively, in detecting VTDR and 91% and 80% in detecting any DR, compared with single-field.85 These numbers are comparable to a meta-analysis of nonmydriatic cameras, which reported 70% sensitivity and 87% specificity for detecting any DR (n = 1960).86
A growing body of evidence has shown the efficacy of remote DR screening programs, proving that telemedicine is able to improve rates of DR screening for patients in remote areas with limited access to ophthalmology services. In Australia, the Remote Outreach DR Screening (RODRS) Service was implemented to provide appropriate DR screening for remote communities. The RODRS service was highly successful as screening rates increased 4-fold from 16.3% to 66.3%.87 In India a trial estimated that 150 patients could be screened per day with only 1 ophthalmologist making final diagnoses from a separate location.88 Alternative models such as the Aravind Eye Care System of India89 and the Peking University Eli Lilly Diabetic Eye Disease Centre in China are emerging models for long-term and sustainable management of DR in large developing countries, whereas initiatives such as the delivery of effective eye care in rural India via a mobile van have been used.2
Given the exponential rise of DM globally, the manpower needed for DR screenings is likely to be outpaced. A study from Singapore demonstrated that trained nonphysician graders are able to provide good detection of DR and maculopathy (κ = 0.66) from fundus photographs.90 Recent studies from the United States91 and Singapore92 showed that automated detection of DR lesions from fundus photographs using deep-learning algorithms had high sensitivity and specificity for identifying DR using retinal images. Hence, software for automated detection of DR lesions from fundus photographs can reduce the workload for manual grading considerably by filtering out healthy eyes and identifying DR lesions to aid in quicker diagnosis and reduce human error. Digital retinal imaging screening on a telemedicine platform using an automated detection system may be a feasible and cost-effective public healthcare strategy for the surveillance and prevention of blindness due to DR in low-middle income countries in view of the lack of resources.
DR Screening Guidelines in the Asia-Pacific
Only less than a quarter of countries in the Asia-Pacific have nationally available DR screening guidelines. Of these, 5 countries, namely, Australia,93 New Zealand,94 China,95 India,96 and Malaysia,97 have guidelines written specifically on the care of DR, whereas the remaining 5 countries (Japan,98 Singapore,99 Hong Kong,100 the Philippines,101 and Sri Lanka102) incorporated their DR screening guidelines within diabetes guidelines. A recent systematic review of DR screening guidelines in Asia reported that most of these countries were in line with the International Council of Ophthalmology's standards on the time to commence initial DR screening and frequency of follow-up evaluations.103 However, guidelines are vague on the threshold for referrals to specialists based on disease severity as most are based on visual acuity. A situational analysis from India found that a significant portion of programs still refer patients to eye specialists for early DR.82 Although the effect of this practice has not been assessed, the current standards of practice recommend referring only VTDR to specialists and monitoring for other DR. A simple and more user-friendly standardized classification guideline would allow for better communication between ophthalmologists and primary care professionals.104
Effectiveness of any screening program depends on the adherence to the guidelines set. In Australia, a study found 77% of non-Indigenous Australians adhere to the screening guidelines compared with only 53% of Indigenous Australians.105 The examination rates among developing countries are considerably lower. Less than one third of diabetic patients from India106 and China107 had undergone an eye examination in the previous year. In South Korea, only a third of patients underwent an annual dilated fundus examination on a regular basis.108 Data from rural China suggest that use of eye care among those with diabetes may even be lower.25 Also, resource constraints in developing regions of the Asia-Pacific may be limited to the provision of screening services and lack the continuity of screening for DR, which is crucial for the management of diabetes-related complications.103
Management of DR in low-middle income countries faces major challenges due to lack of access to eye specialists, health care resources, and facilities. In India, 72% of the population live in rural areas, whereas the majority of ophthalmologists are based in urban centers.109 Hence, people living in remote and underserved areas may experience greater challenges in accessing specialized expert eye care. Even though the use of retinal photocoagulation has been the mainstay of DR treatment for the past few decades, a 2000 national survey in China showed that 90% of rural hospitals had no laser facilities.110 This may explain the finding from the Handan Eye Study, where less than 10% of patients in rural China requiring laser treatment for diabetic eye disease had received it.25 In Cambodia, a situational analysis on DR management reported a lack of optical coherence tomography and vitreoretinal operating machines in the eye hospital.83
Newer pharmacological developments have revolutionized DR treatment from vision stabilization to vision improvement.15 Xu et al111 reported good clinical efficacy using intravitreal ranibizumab and conbercept in 62 Chinese patients over a 12-month clinical study. Sato el al112 did a retrospective review of 56 eyes of Japanese patients with DME treated with intravitreal ranibizumab and reported predictors of good clinical outcomes included better baseline best corrected visual acuity and lower central retinal thickness; hence, this supports the early use of intravitreal anti-vascular endothelial growth factor (anti-VEGF) in DME. However, the high cost of treatment, travelling time, and lack of reimbursed healthcare may impair patient compliance; hence, the number of anti-VEGF injections might be suboptimal.113 Also, many patients in both developed and developing countries do not have sufficient resources to cover the long-term treatment costs for DME.114 As such, ophthalmologists in the Asian regions often select focal/grid laser photocoagulation as their mainstay of treatment and patients are only treated when DR has progressed to advanced stages.
IMPACT OF DIABETIC RETINOPATHY
Few studies in the Asia-Pacific have reported the cost of illness associated with DR. A large-scale longitudinal study in Taiwan reported increased healthcare costs associated with progressive DR.115 Specifically, individuals who progressed from early to advanced stages of DR experienced the greatest increase in cost compared with patients without progression, from US$2723 in 2000 to US$6204 in 2004.115 In Singapore, a study on 500 patients with type 2 diabetes found that in 2010, the annual direct medical cost associated with diabetes care was US$1575 per patient.116 They found that medications and presence of diabetes-related systemic complications were significantly associated with cost.116 In a recent study in Singapore, the presence and severity of DR were associated with increased direct medical costs in patients with type 2 diabetes, which suggested that preventing progression of DR may reduce the economic burden of DR.117 However, in the earlier study, the presence of DR was not a strong determinant of costs.116 As suggested by the authors, a possible reason is that the cost data were obtained from primary clinics,116 where conditions were less severe compared with those patients visiting a secondary hospital.117 This may have limited the analysis on the influence of DR on cost.
Systematic DR screening was cost-effective compared with opportunistic screening for DR. Rachapelle and co-workers118 examined the cost-effectiveness of the Sankara Nethralaya Medical Research Foundation telemedicine DR screening program in rural southern India. They found the program to be cost-effective at a frequency of screening for up to 2 years.118 However, yearly DR screening was no longer considered as cost-effective (defined as less than US$3183 per quality-adjusted life year gained). Furthermore, once household costs were included in the model, only screening once every 5 years was considered cost-effective. In Singapore, a cost-effectiveness analysis was performed for a telemedicine-based DR screening program, which calculated the total cost savings to be US$128 per person.119 Upon extrapolation to the large diabetic population in Singapore, its future cost savings to the healthcare system was projected to be US$21 million.119 In Japan, implementation of a DR screening program would result in an incremental cost of US$64 and estimates a significant reduction (-16%) in cases of adult blindness.120 However, costs varied depending on the capabilities of healthcare systems; hence, countries should evaluate strategies to make screening programs as sustainable and cost-effective as possible.
Visual impairment as a result of DR has a significant negative impact on the patient's QoL. In Singapore, a population-based study showed that VTDR and PDR are the DR severity levels at which functioning is compromised in Malay persons with diabetes.121 In addition, the 3 most difficult vision-dependent activities for people with DR were associated with reading small print, completing lottery forms, and reading newspapers, whereas the 3 least difficult activities were cooking, playing cards, or seeing stairs.121 In a clinical study from Australia, poor visual acuity from DR in the better eye was associated with decreased functioning and emotional well-being in patients with DR.122 In a recent study from Australia on patients with DR and DME, poorer self-reported vision in adults with DR was associated with emotional distress through limitations in daily living activities and social factors.123 Others have shown that there was a significant improvement in Japanese patients' quality of life after vitreous surgery for PDR even without significant corresponding improvements in visual acuity.124 These findings clearly demonstrate that the presence and severity of DR and vision impairment associated with DR are detrimental to patient functioning and QoL. However, such patient-centered research is absent from populous countries like India and China, which are expected to experience the greatest burden of DR.13
PUBLIC HEALTH CHALLENGES AND FUTURE DIRECTIONS
Patient awareness is alarmingly low and is significantly associated with poor health literacy, low socioeconomic status, and poor control of HbA1c and BP levels.1 Awareness of eye-related complications in the diabetic population varied, ranging from 28.8% to 84%, whereas specific knowledge about DR was less likely to be reported.125 For example in India, 45% of people with diabetes only accessed eye clinics after losing their vision.82 In South India, a study reported that only 1 in 10 people in the community are aware that DR is a possible sequela of diabetes.126 Also, 72% of informational sheets on diabetes in Indian clinics did not contain any mention of DR.125 In China, even among diabetic subjects who reported recent eye examinations, nearly half believed that regular eye examinations are unnecessary in the absence of visual symptoms.107 A similar misconception was reported in Myanmar, which showed that despite 92% of diabetic individuals being aware that they should visit an ophthalmologist, 34% felt the need to see an ophthalmologist only when they developed trouble with their eyesight.127
More targeted health education towards people with lower educational levels and socioeconomic status could potentially cover gaps in health knowledge and primary care physicians could closely monitor and counsel those with poorly controlled HbA1c and BP levels. Another recommendation would be to train health professionals to engage with newly diagnosed diabetic patients in discussions about diabetes control and management along with its complications, specifically potential blindness.128
Poor Control of Risk Factors
A major effort in DR prevention comes from optimizing diabetes care to reduce onset of DR. Optimal glycemic control varied among patients with DR, ranging from 17% in Singapore75 and 20% in India129 to 69% in Australia.74 Findings from these few Asia-Pacific74,75,129 studies demonstrate a poorer glycemic control among Asians than Australians. A number of interventional studies have been tested and demonstrated to improve diabetes self-management. These limited studies, namely, from South Korea,130 China,131-133 Malaysia,134 and India,135,136 found positive impacts on patients' glycemic control or positive behavioral change (eg, diet, exercise, self-monitoring of blood glucose). However, the small number of studies limits inferences about the Asia-Pacific population.137 More research is needed to evaluate the benefits of low-cost screening tools, along with the efficacy, cost-effectiveness, and sustainability of culturally appropriate interventions in such countries.
Scarce Data on Low-Middle Income Countries
We can only tackle DR-related visual impairment if we are able to see the full picture. As seen in Table 1, there remain countries without DR prevalence data, namely, Afghanistan, Brunei Darussalam, Bhutan, Cambodia, Lao People's Democratic Republic, Maldives, Myanmar, Philippines, Vietnam, countries within the central region of Asia (ie, Armenia, Azerbaijan, Georgia, Kazakhstan, Kyrgyzstan, Mongolia, Tajikistan, Turkmenistan, and Uzbekistan), and also countries within the Oceania region (ie, Kiribati, Marshall Islands, Micronesia, Papua New Guinea, Samoa, Tonga), where diabetes seems to be increasing rapidly.
Despite being the most common cause of DR-induced vision loss, even fewer countries in the Asia-Pacific region have provided DME data. For example, countries such as Taiwan, Bangladesh, India, Pakistan, Indonesia, Malaysia, Thailand, East Timor, and those in Oceania have mostly reported prevalence of VTDR or CSME but not specifically DME. Overall, epidemiological data on type 1 data and DME prevalence are relatively scarce.
Epidemiological studies of DR in low-income countries in the Asia-Pacific may be hindered by a lack of resources. The Rapid Assessment of Avoidable Blindness (RAAB) screening method may be adapted for monitoring DR prevalence in resource challenged areas such as developing countries of the Asia-Pacific.138-141 By minimizing the sample size and only screening high-risk individuals, RAAB+DR reduces screening costs while gathering fairly accurate prevalence estimates rapidly. Considering that there is inadequate data on DR prevalence in certain developing countries, RAAB+DR may be suitable for the collection of good quality epidemiological data, which is essential for planning and implementation of future public health policies.125
Adherence and Barriers to DR Screening
Adherence to screening has been hindered by lack of awareness of DR, lack of healthcare resources, and lack of accessibility.1 Despite high prevalence of diabetes and its complications, awareness of DR is low. This occurs with equal predilection in both developed and developing countries.1 Studies from China107 (n = 824) and Indonesia142 (n = 196) showed that diabetic patients with a better DR knowledge score tended to attend regular eye examinations. In rural China, a focus group study found that the top 3 patient-identified barriers to screening were forgetting appointments, feeling that physicians were not well-trained, and transportation costs.143 Medical cost, however, was not ranked as a major barrier to accessing eye care, which was in accordance with another study from China.107 However, in India, a clinical study on 233 patients with VTDR seen at tertiary referral center cited financial cost as the major reason for noncompliance with follow-up appointments.144 Country-specific barriers such as high costs, travelling time, inconvenience from screening or treatment, and lack of medical reimbursements may impede patient uptake.125,128
As this review shows, DR remains a significant major public health issue in the Asia-Pacific. A major concern is the more severe problem of VTDR, which could be a reflection of the lack of routine DR screening and timely treatment in the developing region, resulting in its late diagnosis only at the symptomatic stage. Awareness of DR remains alarmingly low and well-organized efforts are needed to educate patients, physicians, and policy makers. Use of low-cost screening technologies such as digital retinal imaging and remote grading may identify patients requiring ophthalmologist review. Telemedicine has increased access to screening for diabetics living in remote and hard-to-reach areas and has optimized screenings to be more cost-efficient and convenient in urban areas. Uptake of anti-VEGF therapy for treatment of DR is sluggish due to cost. A more cost-effective treatment strategy for DME is urgently needed for the Asia-Pacific. Management of DR in the Asia-Pacific requires establishing clear, specific guidelines that would serve as a foundation for structuring an effective public healthcare program.
A limitation of this review is the inclusion of English-only studies. Ideally, reviews should have included all studies conducted on the topic regardless of language. Even though this was applied for practical reasons, it means that a large number of relevant papers may have been excluded, especially as English is not the primary spoken language in most developing countries. Further research and initiatives to obtain prevalence data on DR and conduct randomized clinical trials for the Asia-Pacific are needed, which can further reduce the burden of blindness because of DR.
1. Sabanayagam C, Yip W, Ting DS, et al. Ten emerging trends in the epidemiology of diabetic retinopathy
. Ophthalmic Epidemiol.
2. Ruta LM, Magliano DJ, Lemesurier R, et al. Prevalence of diabetic retinopathy
in type 2 diabetes in developing and developed countries. Diabet Med.
3. Yang SH, Dou KF, Song WJ. Prevalence of diabetes among men and women in China. N Engl J Med.
2010;362:2425-2426; author reply, 2426.
4. Cho NH, Whiting D, Forouhi N, et al. IDF Diabetes Atlas
. 7th ed. International Diabetes Federation; 2015. Available at: http://www.diabetesatlas.org/component/attachments/?task=download&id=116
. Accessed September 1, 2017.
5. Murray CJ, Vos T, Lozano R, et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet.
6. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy
7. Fenwick EK, Pesudovs K, Rees G, et al. The impact of diabetic retinopathy
: understanding the patient's perspective. Br J Ophthalmol.
8. Bourne RRA, Flaxman SR, Braithwaite T, et al. Magnitude, temporal trends, and projections of the global prevalence of blindness and distance and near vision impairment: a systematic review and meta-analysis. Lancet Glob Health.
9. Flaxman SR, Bourne RRA, Resnikoff S, et al. Global causes of blindness and distance vision impairment 1990-2020: a systematic review and meta-analysis. Lancet Glob Health.
10. Leasher JL, Bourne RR, Flaxman SR, et al. Global estimates on the number of people blind or visually impaired by diabetic retinopathy
: a meta-analysis from 1990 to 2010. Diabetes Care.
11. Ferris FL 3rd. How effective are treatments for diabetic retinopathy
12. Wong TY, Mwamburi M, Klein R, et al. Rates of progression in diabetic retinopathy
during different time periods: a systematic review and meta-analysis. Diabetes Care.
13. Ramachandran A, Ma RC, Snehalatha C. Diabetes in Asia. Lancet.
14. Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy
. Diabetes Care.
15. Stewart MW. Treatment of diabetic retinopathy
: recent advances and unresolved challenges. World J Diabetes.
16. Bourne RR, Stevens GA, White RA, et al. Causes of vision loss worldwide, 1990-2010: a systematic analysis. Lancet Glob Health.
17. Huang OS, Tay WT, Ong PG, et al. Prevalence and determinants of undiagnosed diabetic retinopathy
and vision-threatening retinopathy in a multiethnic Asian cohort: the Singapore Epidemiology of Eye Diseases (SEED) Study. Br J Ophthalmol.
18. Zheng Y, Lamoureux EL, Lavanya R, et al. Prevalence and risk factors of diabetic retinopathy
in migrant Indians in an urbanized society in Asia: the Singapore Indian Eye Study. Ophthalmology.
19. Wong TY, Cheung N, Tay WT, et al. Prevalence and risk factors for diabetic retinopathy
: the Singapore Malay Eye Study. Ophthalmology.
20. Liu Y, Song Y, Tao L, et al. Prevalence of diabetic retinopathy
among 13473 patients with diabetes mellitus in China: a cross-sectional epidemiological survey in six provinces. BMJ Open.
21. Zhang G, Chen H, Chen W, et al. Prevalence and risk factors for diabetic retinopathy
in China: a multi-hospital-based cross-sectional study. Br J Ophthalmol.
August 30, 2017. [Epub ahead of print].
22. Pan CW, Wang S, Qian DJ, et al. Prevalence, awareness, and risk factors of diabetic retinopathy
among adults with known type 2 diabetes mellitus in an urban community in China. Ophthalmic Epidemiol.
23. Hu Y, Teng W, Liu L, et al. Prevalence and risk factors of diabetes and diabetic retinopathy
in Liaoning province, China: a population-based cross-sectional study. PLoS One.
24. Liu L, Wu X, Liu L, et al. Prevalence of diabetic retinopathy
in mainland China: a meta-analysis. PloS One.
25. Wang FH, Liang YB, Zhang F, et al. Prevalence of diabetic retinopathy
in rural China: the Handan Eye Study. Ophthalmology.
26. Lian JX, Gangwani RA, McGhee SM, et al. Systematic screening for diabetic retinopathy
(DR) in Hong Kong: prevalence of DR and visual impairment among diabetic population. Br J Ophthalmol.
27. Kung K, Chow KM, Hui EM, et al. Prevalence of complications among Chinese diabetic patients in urban primary care clinics: a cross-sectional study. BMC Fam Pract.
28. Lin JC, Shau WY, Lai MS. Sex- and age-specific prevalence and incidence rates of sight-threatening diabetic retinopathy
in Taiwan. JAMA Ophthalmol.
29. Mahar PS, Awan MZ, Manzar N, et al. Prevalence of type-II diabetes mellitus and diabetic retinopathy
: the Gaddap Study. J Coll Physicians Surg Pak.
30. Abougalambou SS, Abougalambou AS. Risk factors associated with diabetic retinopathy
among type 2 diabetes patients at teaching hospital in Malaysia. Diabetes Metab Syndr.
June 4, 2014. [Epub ahead of print].
31. Katulanda P, Ranasinghe P, Jayawardena R. Prevalence of retinopathy among adults with self-reported diabetes mellitus: the Sri Lanka Diabetes and Cardiovascular Study. BMC Ophthalmol.
32. Jongsareejit A, Potisat S, Krairittichai U, et al. The Thai DMS Diabetes Complications (DD.Comp.) Project: prevalence and risk factors of diabetic retinopathy
in Thai patients with type 2 diabetes mellitus. J Med Assoc Thai
33. Chetthakul T, Deerochanawong C, Suwanwalaikorn S, et al. Thailand diabetes registry project: prevalence of diabetic retinopathy
and associated factors in type 2 diabetes mellitus. J Med Assoc Thai.
34. Keel S, Xie J, Foreman J, et al. The prevalence of diabetic retinopathy
in Australian adults with self-reported diabetes: the National Eye Health Survey. Ophthalmology.
35. Kaidonis G, Mills RA, Landers J, et al. Review of the prevalence of diabetic retinopathy
in Indigenous Australians. Clin Exp Ophthalmol.
36. Xie J, Arnold AL, Keeffe J, et al. Prevalence of self-reported diabetes and diabetic retinopathy
in Indigenous Australians: the National Indigenous Eye Health Survey. Clin Exp Ophthalmol.
37. Mathur R, Bhaskaran K, Edwards E, et al. Population trends in the 10-year incidence and prevalence of diabetic retinopathy
in the UK: a cohort study in the Clinical Practice Research Datalink 2004-2014. BMJ Open.
38. Thomas RL, Dunstan FD, Luzio SD, et al. Prevalence of diabetic retinopathy
within a national diabetic retinopathy
screening service. Br Ophthalmol.
39. Zhang X, Saaddine JB, Chou CF, et al. Prevalence of diabetic retinopathy
in the United States, 2005-2008. JAMA.
40. Jee D, Lee WK, Kang S. Prevalence and risk factors for diabetic retinopathy
: the Korea National Health and Nutrition Examination Survey 2008-2011. Invest Ophthalmol Vis Sci.
41. Jonas JB, Nangia V, Khare A, et al. Prevalence and associated factors of diabetic retinopathy
in rural central India. Diabetes Care.
42. Raman R, Ganesan S, Pal SS, et al. Prevalence and risk factors for diabetic retinopathy
in rural India. Sankara Nethralaya Diabetic Retinopathy
Epidemiology and Molecular Genetic Study III (SN-DREAMS III), report no 2. BMJ Open Diabetes Res Care
43. Rani PK, Raman R, Chandrakantan A, et al. Risk factors for diabetic retinopathy
in self-reported rural population with diabetes. J Postgrad Med.
44. Ramavat PR, Ramavat MR, Ghugare BW, et al. Prevalence of diabetic retinopathy
in western Indian type 2 diabetic population: a hospital-based cross-sectional study. J Clin Diagn Res.
45. Gadkari SS, Maskati QB, Nayak BK. Prevalence of diabetic retinopathy
in India: the All India Ophthalmological Society Diabetic Retinopathy
Eye Screening Study 2014. Indian J Ophthalmol.
46. Raman R, Rani PK, Reddi Rachepalle S, et al. Prevalence of diabetic retinopathy
in India: Sankara Nethralaya Diabetic Retinopathy
Epidemiology and Molecular Genetics Study report 2. Ophthalmology.
47. Pradeepa R, Anitha B, Mohan V, et al. Risk factors for diabetic retinopathy
in a South Indian type 2 diabetic population—the Chennai Urban Rural Epidemiology Study (CURES) Eye Study 4. Diabetic Med.
48. Namperumalsamy P, Kim R, Vignesh TP, et al. Prevalence and risk factors for diabetic retinopathy
: a population-based assessment from Theni District, South India. Br J Ophthalmol.
49. Krishnaiah S, Das T, Nirmalan PK, et al. Risk factors for diabetic retinopathy
: findings from the Andhra Pradesh Eye Disease Study. Clin Ophthalmol.
50. Sunita M, Singh AK, Rogye A, et al. Prevalence of diabetic retinopathy
in urban slums: the Aditya Jyot Diabetic Retinopathy
in Urban Mumbai Slums Study-report 2. Ophthalmic Epidemiol.
April 12, 2017. [Epub ahead of print].
51. Papali'i-Curtin AT, Dalziel DM. Prevalence of diabetic retinopathy
and maculopathy in Northland, New Zealand: 2011-2012. N Z Med J.
52. Chang LY, Lee AC, Sue W. Prevalence of diabetic retinopathy
at first presentation to the retinal screening service in the greater Wellington region of New Zealand 2006-2015, and implications for models of retinal screening. N Z Med J.
53. Sasongko MB, Widyaputri F, Agni AN, et al. Prevalence of diabetic retinopathy
and blindness in Indonesian adults with type 2 diabetes. Am J Ophthalmol.
June 30, 2017. [Epub ahead of print].
54. Thapa R, Joshi DM, Rizyal A, et al. Prevalence, risk factors and awareness of diabetic retinopathy
among admitted diabetic patients at a tertiary level hospital in Kathmandu. Nepal J Ophthalmol.
55. Mishra SK, Pant BP, Subedi P. The prevalence of diabetic retinopathy
among known diabetic population in Nepal. Kathmandu Univ Med J.
56. Landers J, Henderson T, Abhary S, et al. Prevalence and associations of diabetic retinopathy
in Indigenous Australians within central Australia: the Central Australian Ocular Health Study. Clin Exp Ophthalmol.
57. Chiang PP, Lamoureux EL, Cheung CY, et al. Racial differences in the prevalence of diabetes but not diabetic retinopathy
in a multi-ethnic Asian population. Invest Ophthalmol Vis Sci.
58. Raymond NT, Varadhan L, Reynold DR, et al. Higher prevalence of retinopathy in diabetic patients of South Asian ethnicity compared with white Europeans in the community: a cross-sectional study. Diabetes Care.
59. Zheng Y, Lamoureux EL, Ikram MK, et al. Impact of migration and acculturation on prevalence of type 2 diabetes and related eye complications in Indians living in a newly urbanised society. PloS One.
60. Xie XW, Xu L, Wang YX, et al. Prevalence and associated factors of diabetic retinopathy
. The Beijing Eye Study 2006. Graefes Arch Clin Exp Ophthalmol
61. Liu L, Liu LM, Hu YD, et al. Epidemic studies of diabetic retinopathy
in China-a review. Int J Ophthalmol.
62. Xu J, Xu L, Wang YX, et al. Ten-year cumulative incidence of diabetic retinopathy
. The Beijing Eye Study 2001/2011. PLoS One
63. Tam VH, Lam EP, Chu BC, et al. Incidence and progression of diabetic retinopathy
in Hong Kong Chinese with type 2 diabetes mellitus. J Diabetes Complications.
64. Kajiwara A, Miyagawa H, Saruwatari J, et al. Gender differences in the incidence and progression of diabetic retinopathy
among Japanese patients with type 2 diabetes mellitus: a clinic-based retrospective longitudinal study. Diabetes Res Clin Pract.
65. Rajalakshmi R, Amutha A, Ranjani H, et al. Prevalence and risk factors for diabetic retinopathy
in Asian Indians with young onset type 1 and type 2 diabetes. J Diabetes Complications.
66. Foo V, Quah J, Cheung G, et al. HbA1c, systolic blood pressure variability and diabetic retinopathy
in Asian type 2 diabetics. J Diabetes.
67. Tapp RJ, Shaw JE, Harper CA, et al. The prevalence of and factors associated with diabetic retinopathy
in the Australian population. Diabetes Care.
68. Benarous R, Sasongko MB, Qureshi S, et al. Differential association of serum lipids with diabetic retinopathy
and diabetic macular edema. Invest Ophthalmol Vis Sci.
69. Pang C, Jia L, Jiang S, et al. Determination of diabetic retinopathy
prevalence and associated risk factors in Chinese diabetic and pre-diabetic subjects: Shanghai Diabetic Complications Study. Diabetes Metab Res Rev.
70. Man RE, Sabanayagam C, Chiang PP, et al. Differential association of generalized and abdominal obesity with diabetic retinopathy
in Asian patients with type 2 diabetes. JAMA Ophthalmol.
71. Rooney D, Lye WK, Tan G, et al. Body mass index and retinopathy in Asian populations with diabetes mellitus. Acta Diabetol.
72. Lim LS, Tai ES, Mitchell P, et al. C-reactive protein, body mass index, and diabetic retinopathy
. Invest Ophthalmol Vis Sci.
73. Dirani M, Xie J, Fenwick E, et al. Are obesity and anthropometry risk factors for diabetic retinopathy
? The Diabetes Management Project. Invest Ophthalmol Vis Sci
74. Fenwick EK, Xie J, Man REK, et al. Combined poor diabetes control indicators are associated with higher risks of diabetic retinopathy
and macular edema than poor glycemic control alone. PloS One.
75. Huang OS, Lamoureux EL, Tay WT, et al. Glycemic and blood pressure control in an Asian Malay population with diabetes and diabetic retinopathy
. Arch Ophthalmol.
76. Jin P, Peng J, Zou H, et al. The 5-year onset and regression of diabetic retinopathy
in Chinese type 2 diabetes patients. PloS One.
77. Mohamed Q, Gillies MC, Wong TY. Management of diabetic retinopathy
: a systematic review. JAMA.
78. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med.
79. Matthews DR, Stratton IM, Aldington SJ, et al. Risks of progression of retinopathy and vision loss related to tight blood pressure control in type 2 diabetes mellitus: UKPDS 69. Arch Ophthalmol.
80. Estacio RO, Jeffers BW, Gifford N, et al. Effect of blood pressure control on diabetic microvascular complications in patients with hypertension and type 2 diabetes. Diabetes Care.
81. Arun CS, Ngugi N, Lovelock L, et al. Effectiveness of screening in preventing blindness due to diabetic retinopathy
. Diabetic Med.
82. Indian Institute of Public Health. The emerging epidemic of diabetic retinopathy
in India: report of a situational analysis and evaluation of existing programmes for screening and treatment of diabetic retinopathy
83. Chakrabarti R, Ormsby GM, Muhfarriq S, et al. Situation analysis for managing diabetic retinopathy
in Takeo province, Cambodia. 2012. Available at: http://www.icoph.org/dynamic/attachments/resources/2012_dr_situation_analysisincambodia.pdf
84. Williams GA, Scott IU, Haller JA, et al. Single-field fundus photography for diabetic retinopathy
screening: a report by the American Academy of Ophthalmology. Ophthalmology.
85. Ding J, Zou Y, Liu N, et al. Strategies of digital fundus photography for screening diabetic retinopathy
in a diabetic population in urban China. Ophthalmic Epidemiol.
86. Shi L, Wu H, Dong J, et al. Telemedicine for detecting diabetic retinopathy
: a systematic review and meta-analysis. Br J Ophthalmol.
87. Glasson NM, Crossland LJ, Larkins SL. An innovative Australian outreach model of diabetic retinopathy
screening in remote communities. J Diabetes Res.
88. Bai VT, Murali V, Kim R, et al. Teleophthalmology-based rural eye care in India. Telemed J E Health.
89. Aravind Eye Care System. Guidelines for the comprehensive management of diabetic retinopathy
in India. https://www.iapb.org/wp-content/uploads/Guidelines-for-the-Comprehensive-Management-of-DR-in-India.pdf
. Published July 2008. Accessed October 20, 2017.
90. Bhargava M, Cheung CY, Sabanayagam C, et al. Accuracy of diabetic retinopathy
screening by trained non-physician graders using non-mydriatic fundus camera. Singapore Med J.
91. Gulshan V, Peng L, Coram M, et al. Development and validation of a deep learning algorithm for detection of diabetic retinopathy
in retinal fundus photographs. JAMA.
92. Ting DSW, Cheung CYL, Lim G, et al. Development and validation of a deep learning system for diabetic retinopathy
and related eye diseases using retinal images from multi-ethnic populations with diabetes. JAMA.
2017. In press.
93. Australian Diabetes Society for the Department of Health and Ageing. Guidelines for the management of diabetic retinopathy
. 2008. Accessed October 20, 2017.
94. New Zealand Ministry of Health. Diabetic retinal screening, grading, monitoring and referral guidance. Available at: https://www.health.govt.nz/system/files/documents/publications/diabetic-retinal-screening-grading-monitoring-referral-guidance-mar16.pdf
. 2016. Accessed October 20, 2017.
95. Group COSRW. Diagnosis and treatment guideline of diabetic retinopathy
. Zhonghua Yan Ke Za Zhi.
96. VISION 2020: The Right To Sight India. Guidelines for diabetic eye care in India. https://www.iapb.org/wp-content/uploads/ICO-Guidelines-for-Diabetic-Eye-Care-Adapted-to-India_VISION-2020-India.pdf
. Published January 2015. Accessed October 20, 2017.
97. Ministry of Health Malaysia. Screening of diabetic retinopathy
. Published June 2011. Accessed October 20, 2017.
98. The Japan Diabetes Society. Evidence-based practice guideline for the treatment for diabetes in Japan 2013. http://www.jds.or.jp/modules/en/index.php?content_id=44
. 2013. Accessed October 20, 2017.
100. Primary Care Office, Department of Health. Hong Kong reference framework for diabetes care for adults in primary care settings. http://www.pco.gov.hk/english/resource/files/RF_DM_full.pdf
. 2017. Accessed October 20, 2017.
101. Unite for Diabetes Philippines. Philippine practice guidelines for the diagnosis and management of diabetes: part 1- screening & diagnosis. https://www.diabetesphil.org/html/files/clinical_practice_guidelines_draft.pdf
. 2011. Accessed October 20, 2017.
102. Sri Lanka College of Obstetricians & Gynaecologists. Management of diabetes mellitus clinical practice guidelines. http://www.slcog.lk/img/guidelines/Other%20national%20Gidelines/Physicians/Book%201/Management%20of%20Diabetes%20Mellitus.pdf
. Accessed October 20, 2017.
103. Wang LZ, Cheung CY, Tapp RJ, et al. Availability and variability in guidelines on diabetic retinopathy
screening in Asian countries. Br J Ophthalmol.
March 14, 2017. [Epub ahead of print].
104. Ting DS, Cheung GC, Wong TY. Diabetic retinopathy
: global prevalence, major risk factors, screening practices and public health challenges: a review. Clin Exp Ophthalmol.
105. Foreman J, Keel S, Xie J, et al. Adherence to diabetic eye examination guidelines in Australia: the National Eye Health Survey. Med J Aust.
106. Dandona R, Dandona L, John RK, et al. Awareness of eye diseases in an urban population in southern India. Bull World Health Org.
107. Wang D, Ding X, He M, et al. Use of eye care services among diabetic patients in urban and rural China. Ophthalmology.
108. Lee JH, Song SJ. Current challenges in diabetic retinopathy
: are we really doing better? Endocrinol Metab (Seoul).
109. Prathiba V, Rema M. Teleophthalmology: a model for eye care delivery in rural and underserved areas of India. Int J Fam Med.
110. Xu H, Zhang W. Present condition of ophthalmology resource in China in 2000. Med Soc (Berkeley).
111. Xu Y, Rong A, Xu W, et al. Comparison of 12-month therapeutic effect of conbercept and ranibizumab for diabetic macular edema: a real-life clinical practice study. BMC Ophthalmol.
112. Sato S, Shinoda H, Nagai N, et al. Predictive factors of better outcomes by monotherapy of an antivascular endothelial growth factor drug, ranibizumab, for diabetic macular edema in clinical practice. Medicine (Baltimore).
113. Cheung GC, Yoon YH, Chen LJ, et al. Diabetic macular oedema: evidence-based treatment recommendations for Asian countries. Clin Exp Ophthalmol.
May 30, 2017. [Epub ahead of print].
114. Stewart MW. A review of ranibizumab for the treatment of diabetic retinopathy
. Ophthalmol Ther.
115. Woung LC, Tsai CY, Chou HK, et al. Healthcare costs associated with progressive diabetic retinopathy
among National Health Insurance enrollees in Taiwan, 2000-2004. BMC Health Serv Res.
116. CS Ng, Toh MP, Ko Y, et al. Direct medical cost of type 2 diabetes in Singapore. PloS One.
117. Zhang X, Low S, Kumari N, et al. Direct medical cost associated with diabetic retinopathy
severity in type 2 diabetes in Singapore. PloS One.
118. Rachapelle S, Legood R, Alavi Y, et al. The cost-utility of telemedicine to screen for diabetic retinopathy
in India. Ophthalmology.
119. Nguyen HV, Tan GS, Tapp RJ, et al. Cost-effectiveness of a national telemedicine diabetic retinopathy
screening program in Singapore. Ophthalmology.
120. Kawasaki R, Akune Y, Hiratsuka Y, et al. Cost-utility analysis of screening for diabetic retinopathy
in Japan: a probabilistic Markov modeling study. Ophthalmic Epidemiol.
121. Lamoureux EL, Tai ES, Thumboo J, et al. Impact of diabetic retinopathy
on vision-specific function. Ophthalmology.
122. Lamoureux EL, Hassell JB, Keeffe JE. The impact of diabetic retinopathy
on participation in daily living. Arch Ophthalmol.
123. Fenwick EK, Cheng GH, Man REK, et al. Inter-relationship between visual symptoms, activity limitation and psychological functioning in patients with diabetic retinopathy
. Br J Ophthalmol.
September 19, 2017. [Epub ahead of print].
124. Okamoto F, Okamoto Y, Fukuda S, et al. Vision-related quality of life and visual function following vitrectomy for proliferative diabetic retinopathy
. Am J Ophthalmol.
125. Lin S, Ramulu P, Lamoureux EL, et al. Addressing risk factors, screening, and preventative treatment for diabetic retinopathy
in developing countries: a review. Clin Exp Ophthalmol.
126. Rema M, Pradeepa R. Diabetic retinopathy
: an Indian perspective. Indian J Med Res.
127. Muecke JS, Newland HS, Ryan P, et al. Awareness of diabetic eye disease among general practitioners and diabetic patients in Yangon, Myanmar. Clin Exp Ophthalmol.
128. Lewis K. Improving patient compliance with diabetic retinopathy
screening and treatment. Community Eye Health.
129. Raman R, Gupta A, Kulothungan V, et al. Prevalence and risk factors of diabetic retinopathy
in subjects with suboptimal glycemic, blood pressure and lipid control. Sankara Nethralaya Diabetic Retinopathy
Epidemiology and Molecular Genetic Study (SN-DREAMS, report 33). Curr Eye Res
130. Song MS, Kim HS. Intensive management program to improve glycosylated hemoglobin levels and adherence to diet in patients with type 2 diabetes. Appl Nurs Res.
131. Liu S, Bi A, Fu D, et al. Effectiveness of using group visit model to support diabetes patient self-management in rural communities of Shanghai: a randomized controlled trial. BMC Public Health.
132. Shi Q, Ostwald SK, Wang S. Improving glycaemic control self-efficacy and glycaemic control behaviour in Chinese patients with type 2 diabetes mellitus: randomised controlled trial. J Clin Nurs.
133. Li G, Zhang P, Wang J, et al. The long-term effect of lifestyle interventions to prevent diabetes in the China Da Qing Diabetes Prevention Study: a 20-year follow-up study. Lancet.
134. Ahmad B, Md Zain AZ, Fatt QK. Type 2 diabetes patients are more amenable to change following a contextualised diabetes education programme in Malaysia. Diabetes Metab Syndr.
July 3, 2017. [Epub ahead of print].
135. Malathy R, Narmadha M, Ramesh S, et al. Effect of a diabetes counseling programme on knowledge, attitude and practice among diabetic patients in Erode district of South India. J Young Pharm.
136. Ramachandran A, Snehalatha C, Mary S, et al. The Indian Diabetes Prevention Programme shows that lifestyle modification and metformin prevent type 2 diabetes in Asian Indian subjects with impaired glucose tolerance (IDPP-1). Diabetologia.
137. Rawal LB, Tapp RJ, Williams ED, et al. Prevention of type 2 diabetes and its complications in developing countries: a review. Int J Behav Med.
138. Kuper H, Polack S, Limburg H. Rapid assessment of avoidable blindness. Community Eye Health.
139. Katibeh M, Behboudi H, Moradian S, et al. Rapid assessment of avoidable blindness and diabetic retinopathy
in Gilan Province, Iran. Ophthalmic Epidemiol.
April 19, 2017. [Epub ahead of print].
140. Zatic T, Bendelic E, Paduca A, et al. Rapid assessment of avoidable blindness and diabetic retinopathy
in Republic of Moldova. Br J Ophthalmol.
141. Polack S, Yorston D, Lopez-Ramos A, et al. Rapid assessment of avoidable blindness and diabetic retinopathy
in Chiapas, Mexico. Ophthalmology.
142. Adriono G, Wang D, Octavianus C, et al. Use of eye care services among diabetic patients in urban Indonesia. Arch Ophthalmol.
143. Yan X, Liu T, Gruber L, et al. Attitudes of physicians, patients, and village health workers toward glaucoma and diabetic retinopathy
in rural China: a focus group study. Arch Ophthalmol.
144. Vengadesan N, Ahmad M, Sindal MD, et al. Delayed follow-up in patients with diabetic retinopathy
in South India: social factors and impact on disease progression. Indian J Ophthalmol.
145. Fukushima S, Nakagami T, Suto C, et al. Prevalence of retinopathy and its risk factors in a Japanese population. J Diabetes Invest.
146. Akhter A, Fatema K, Ahmed SF, et al. Prevalence and associated risk indicators of retinopathy in a rural Bangladeshi population with and without diabetes. Ophthalmic Epidemiol.
147. Dawkins RC, Oliver GF, Sharma M, et al. An estimation of the prevalence of diabetes mellitus and diabetic retinopathy
in adults in Timor-Leste. BMC Res Notes.
148. Brian G, Fischer-Harder K, Sikivou B, et al. Diabetic eye disease among adults in Fiji with self-reported diabetes. Clin Exp Ophthalmol.
149. Win TST, Kenilorea G, Gadabu E, et al. The prevalence of diabetes complications and associated risk factors in Pacific Islands countries. Diabetes Res Clin Pract.