[Skip to Content]
[Skip to Content Landing]
Download PDF
Figure 1.
Types of Diabetic Retinopathy (DR) in Either Eye
Types of Diabetic Retinopathy (DR) in Either Eye

Percentage of the sample with various levels of diabetic retinopathy in either eye stratified by site and overall.

Figure 2.
Types of Other Ocular Findings in Either Eye
Types of Other Ocular Findings in Either Eye

Percentage of the sample having other ocular findings in either eye stratified by site. AMD indicates age-related macular degeneration; Cat, cataract; CWS, cotton-wool spots; Glau ON, glaucomatous/optic nerve findings; Hyp Ret, hypertensive retinopathy; Misc, miscellaneous; and Ptrgm, pterygium.

Table 1.  
Classifications Used to Grade DR Presence and Severity Based on the National Health Service Grading Classification Systema
Classifications Used to Grade DR Presence and Severity Based on the National Health Service Grading Classification Systema
Table 2.  
Other Characteristics of Sample Stratified by Site and Overall
Other Characteristics of Sample Stratified by Site and Overall
Table 3.  
Number and Percentage of Patients With Other Ocular Findings
Number and Percentage of Patients With Other Ocular Findings
1.
Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United States. Atlanta, GA: US Dept of Health and Human Services; 2014. http://www.cdc.gov/diabetes/pubs/statsreport14.htm. Accessed October 10, 2014.
2.
Boyle  JP, Honeycutt  AA, Narayan  KM,  et al.  Projection of diabetes burden through 2050. Diabetes Care. 2001;24(11):1936-1940.
PubMedArticle
3.
Saaddine  JB, Honeycutt  AA, Narayan  KM, Zhang  X, Klein  R, Boyle  JP.  Projection of diabetic retinopathy and other major eye diseases among people with diabetes mellitus. Arch Ophthalmol. 2008;126(12):1740-1747.
PubMedArticle
4.
Zhang  X, Saaddine  JB, Chou  C-F,  et al.  Prevalence of diabetic retinopathy in the United States, 2005-2008. JAMA. 2010;304(6):649-656.
PubMedArticle
5.
Rein  DB, Zhang  P, Wirth  KE,  et al.  The economic burden of major adult visual disorders in the United States. Arch Ophthalmol. 2006;124(12):1754-1760.
PubMedArticle
6.
Mohamed  Q, Gillies  MC, Wong  TY.  Management of diabetic retinopathy: a systematic review. JAMA. 2007;298(8):902-916.
PubMedArticle
7.
Basch  CE, Walker  EA, Howard  CJ, Shamoon  H, Zybert  P.  The effect of health education on the rate of ophthalmic examinations among African Americans with diabetes mellitus. Am J Public Health. 1999;89(12):1878-1882.
PubMedArticle
8.
Sloan  FA, Grossman  DS, Lee  PP.  Effects of receipt of guideline-recommended care on onset of diabetic retinopathy and its progression. Ophthalmology. 2009;116(8):1515-1521.
PubMedArticle
9.
American Academy of Ophthalmology Retina Panel. Preferred Practice Pattern Guidelines Diabetic Retinopathy. San Francisco, CA: American Academy of Ophthalmology; 2012. http://one.aao.org/preferred-practice-pattern/diabetic-retinopathy-ppp--2014. Accessed October 15, 2014.
10.
Cavallerano  J. Optometric Clinical Practice Guideline, Care of the Patient with Diabetes Mellitus, Reference Guide for Clinicians. St Louis, MO. American Optometric Association; 2009. http://www.aoa.org/documents/CPG-3.pdf. Accessed October 7, 2014.
11.
American Diabetes Association.  Standards of medical care in diabetes—2013. Diabetes Care. 2013;36(suppl 1):S11-S66.
PubMedArticle
12.
Saaddine  JB, Engelgau  MM, Beckles  GL, Gregg  EW, Thompson  TJ, Narayan  KM.  A diabetes report card for the United States: quality of care in the 1990s. Ann Intern Med. 2002;136(8):565-574.
PubMedArticle
13.
Maclennan  PA, McGwin  G  Jr, Heckemeyer  C,  et al.  Eye care use among a high-risk diabetic population seen in a public hospital’s clinics. JAMA Ophthalmol. 2014;132(2):162-167.
PubMedArticle
14.
Pérez  CM, Febo-Vázquez  I, Guzmán  M, Ortiz  AP, Suárez  E.  Are adults diagnosed with diabetes achieving the American Diabetes Association clinical practice recommendations? P R Health Sci J. 2012;31(1):18-23.
PubMed
15.
Paz  SH, Varma  R, Klein  R, Wu  J, Azen  SP; Los Angeles Latino Eye Study Group.  Noncompliance with vision care guidelines in Latinos with type 2 diabetes mellitus: the Los Angeles Latino Eye Study. Ophthalmology. 2006;113(8):1372-1377.
PubMedArticle
16.
Baker  RS, Watkins  NL, Wilson  MR, Bazargan  M, Flowers  CW  Jr.  Demographic and clinical characteristics of patients with diabetes presenting to an urban public hospital ophthalmology clinic. Ophthalmology. 1998;105(8):1373-1379.
PubMedArticle
17.
Centers for Disease Control and Prevention. Improving the nation’s vision health: a coordinated public health approach. http://www.cdc.gov/visionhealth/pdf/improving_nations_vision_health.pdf. Accessed October 7, 2014.
18.
Owsley  C, McGwin  G, Scilley  K, Girkin  CA, Phillips  JM, Searcey  K.  Perceived barriers to care and attitudes about vision and eye care: focus groups with older African Americans and eye care providers. Invest Ophthalmol Vis Sci. 2006;47(7):2797-2802.
PubMedArticle
19.
Maclennan  PA, McGwin  G  Jr, Searcey  K, Owsley  C.  A survey of Alabama eye care providers in 2010-2011. BMC Ophthalmol. 2014;14:44.
PubMedArticle
20.
Rask  KJ, Williams  MV, Parker  RM, McNagny  SE.  Obstacles predicting lack of a regular provider and delays in seeking care for patients at an urban public hospital. JAMA. 1994;271(24):1931-1933.
PubMedArticle
21.
Chou  C-F, Sherrod  CE, Zhang  X,  et al.  Barriers to eye care among people aged 40 years and older with diagnosed diabetes, 2006-2010. Diabetes Care. 2014;37(1):180-188.
PubMedArticle
22.
Stefánsson  E, Bek  T, Porta  M, Larsen  N, Kristinsson  JK, Agardh  E.  Screening and prevention of diabetic blindness. Acta Ophthalmol Scand. 2000;78(4):374-385.
PubMedArticle
23.
Forster  AS, Forbes  A, Dodhia  H,  et al.  Changes in detection of retinopathy in type 2 diabetes in the first 4 years of a population-based diabetic eye screening program: retrospective cohort study. Diabetes Care. 2013;36(9):2663-2669.
PubMedArticle
24.
Garg  S, Jani  PD, Kshirsagar  AV, King  B, Chaum  E.  Telemedicine and retinal imaging for improving diabetic retinopathy evaluation. Arch Intern Med. 2012;172(21):1677-1678.
PubMedArticle
25.
Kirkizlar  E, Serban  N, Sisson  JA, Swann  JL, Barnes  CS, Williams  MD.  Evaluation of telemedicine for screening of diabetic retinopathy in the Veterans Health Administration. Ophthalmology. 2013;120(12):2604-2610.
PubMedArticle
26.
Zimmer-Galler  IE, Zeimer  R.  Telemedicine in diabetic retinopathy screening. Int Ophthalmol Clin. 2009;49(2):75-86.
PubMedArticle
27.
Silva  PS, Cavallerano  JD, Aiello  LM, Aiello  LP.  Telemedicine and diabetic retinopathy. Arch Ophthalmol. 2011;129(2):236-242.
PubMedArticle
28.
Wilson  RR, Silowash  R, Anthony  L, Cecil  RA, Eller  A.  Telemedicine process used to implement an effective and functional screening program for diabetic retinopathy. J Diabetes Sci Technol. 2008;2(5):785-791.
PubMedArticle
29.
Mansberger  SL, Gleitsmann  K, Gardiner  S,  et al.  Comparing the effectiveness of telemedicine and traditional surveillance in providing diabetic retinopathy screening examinations. Telemed J E Health. 2013;19(12):942-948.
PubMedArticle
30.
Li  HK, Horton  M, Bursell  S-E,  et al.  Telehealth practice recommendations for diabetic retinopathy, second edition. Telemed J E Health.2011;17(10):1-24.Article
31.
Lin  DY, Blumenkranz  MS, Brothers  RJ, Grosvenor  DM.  The sensitivity and specificity of single-field nonmydriatic monochromatic digital fundus photography with remote image interpretation for diabetic retinopathy screening. Am J Ophthalmol. 2002;134(2):204-213.
PubMedArticle
32.
Massin  P, Erginay  A, Ben Mehidi  A,  et al.  Evaluation of a new non-mydriatic digital camera for detection of diabetic retinopathy. Diabet Med. 2003;20(8):635-641.
PubMedArticle
33.
Bragge  P, Gruen  RL, Chau  M, Forbes  A, Taylor  HR.  Screening for presence or absence of diabetic retinopathy: a meta-analysis. Arch Ophthalmol. 2011;129(4):435-444.
PubMedArticle
34.
Ogunyemi  O, Terrien  E, Eccles  A,  et al.  Teleretinal screening for diabetic retinopathy in six Los Angeles urban safety-net clinics: initial findings. AMIA Annu Symp Proc.2011;2011:1027-1035.
35.
Gibson  DM.  Eye care availability and access among individuals with diabetes, diabetic retinopathy, or age-related macular degeneration. JAMA Ophthalmol. 2014;132(4):471-477.
PubMedArticle
36.
Nathoo  N, Ng  M, Rudnisky  CJ, Tennant  MTS.  The prevalence of diabetic retinopathy as identified by teleophthalmology in rural Alberta. Can J Ophthalmol. 2010;45(1):28-32.
PubMedArticle
37.
Arora  S, Kurji  AK, Tennant  MTS.  Dismantling sociocultural barriers to eye care with tele-ophthalmology: lessons from an Alberta Cree community. Clin Invest Med. 2013;36(2):E57-E63.
PubMed
38.
Cavallerano  AA, Conlin  PR.  Teleretinal imaging to screen for diabetic retinopathy in the Veterans Health Administration. J Diabetes Sci Technol. 2008;2(1):33-39.
PubMedArticle
39.
Maberley  D, Morris  A, Hay  D, Chang  A, Hall  L, Mandava  N.  A comparison of digital retinal image quality among photographers with different levels of training using a non-mydriatic fundus camera. Ophthalmic Epidemiol. 2004;11(3):191-197.
PubMedArticle
40.
Jones  S, Edwards  RT.  Diabetic retinopathy screening: a systematic review of the economic evidence. Diabet Med. 2010;27(3):249-256.
PubMedArticle
41.
Rein  DB, Wittenborn  JS, Zhang  X,  et al; Vision Cost-Effectiveness Study Group.  The cost-effectiveness of three screening alternatives for people with diabetes with no or early diabetic retinopathy. Health Serv Res. 2011;46(5):1534-1561.
PubMedArticle
42.
Harding  S, Greenwood  R, Aldington  S,  et al; Diabetic Retinopathy Grading and Disease Management Working Party.  Grading and disease management in national screening for diabetic retinopathy in England and Wales. Diabet Med. 2003;20(12):965-971.
PubMedArticle
43.
American Academy of Ophthalmology Preferred Practice Patterns Committee. Preferred Practice Pattern Guidelines: Comprehensive Adult Medical Eye Evaluation. San Francisco, CA: American Academy of Ophthalmology; 2010. http://one.aao.org/preferred-practice-pattern/comprehensive-adult-medical-eye-evaluation--octobe. Accessed October 7, 2014.
44.
Zimmer-Galler  I, Zeimer  R.  Results of implementation of the DigiScope for diabetic retinopathy assessment in the primary care environment. Telemed J E Health. 2006;12(2):89-98.
PubMedArticle
45.
Cavallerano  AA, Cavallerano  JD, Katalinic  P,  et al; Joslin Vision Network Research Team.  A telemedicine program for diabetic retinopathy in a Veterans Affairs Medical Center—the Joslin Vision Network Eye Health Care Model. Am J Ophthalmol. 2005;139(4):597-604.
PubMedArticle
46.
An  J, Nichol  MB.  Multiple medication adherence and its effect on clinical outcomes among patients with comorbid type 2 diabetes and hypertension. Med Care. 2013;51(10):879-887.
PubMedArticle
47.
Krapek  K, King  K, Warren  SS,  et al.  Medication adherence and associated hemoglobin A1c in type 2 diabetes. Ann Pharmacother. 2004;38(9):1357-1362.
PubMedArticle
48.
Gregg  EW, Geiss  LS, Saaddine  J,  et al.  Use of diabetes preventive care and complications risk in two African-American communities. Am J Prev Med. 2001;21(3):197-202.
PubMedArticle
49.
Flavin  NE, Mulla  ZD, Bonilla-Navarrete  A,  et al.  Health insurance and the development of diabetic complications. South Med J. 2009;102(8):805-809.
PubMedArticle
50.
Sivaprasad  S, Gupta  B, Gulliford  MC,  et al.  Ethnic variations in the prevalence of diabetic retinopathy in people with diabetes attending screening in the United Kingdom (DRIVE UK). PLoS One. 2012;7(3):e32182. doi:10.1371/journal.pone.0032182.
PubMedArticle
51.
Kempen  JH, O’Colmain  BJ, Leske  MC,  et al; Eye Diseases Prevalence Research Group.  The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122(4):552-563.
PubMedArticle
52.
Wong  TY, Klein  R, Islam  FM,  et al.  Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006;141(3):446-455.
PubMedArticle
53.
Shin  P, Finnegan  B.  Assessing the need for on-site eye care professionals in community health centers. Policy Brief George Wash Univ Cent Health Serv Res Policy. 2009;(2):1-23.
PubMed
54.
Tielsch  JM, Sommer  A, Katz  J, Royall  RM, Quigley  HA, Javitt  J.  Racial variations in the prevalence of primary open-angle glaucoma: the Baltimore Eye Survey. JAMA. 1991;266(3):369-374.
PubMedArticle
55.
Javitt  JC, McBean  AM, Nicholson  GA, Babish  JD, Warren  JL, Krakauer  H.  Undertreatment of glaucoma among black Americans. N Engl J Med. 1991;325(20):1418-1422.
PubMedArticle
56.
Liu  L, Wu  J, Geng  J, Yuan  Z, Huang  D.  Geographical prevalence and risk factors for pterygium: a systematic review and meta-analysis. BMJ Open. 2013;3(11):e003787.
PubMedArticle
57.
Saw  SM, Tan  D.  Pterygium: prevalence, demography and risk factors. Ophthalmic Epidemiol. 1999;6(3):219-228.
PubMedArticle
58.
Olayiwola  JN, Sobieraj  DM, Kulowski  K, St Hilaire  D, Huang  JJ.  Improving diabetic retinopathy screening through a statewide telemedicine program at a large federally qualified health center. J Health Care Poor Underserved. 2011;22(3):804-816.
PubMedArticle
59.
Jiménez-Ramírez  F, Pérez  R.  Diabetic retinopathy education and screening at the community pharmacy in Puerto Rico. P R Health Sci J. 2011;30(3):139-144.
PubMed
Original Investigation
Journal Club
February 2015

Diabetes Eye Screening in Urban Settings Serving Minority PopulationsDetection of Diabetic Retinopathy and Other Ocular Findings Using Telemedicine

Author Affiliations
  • 1Department of Ophthalmology, School of Medicine, University of Alabama at Birmingham
  • 2Department of Epidemiology, School of Public Health, University of Alabama at Birmingham
  • 3Department of Public Health Sciences, Miller School of Medicine, University of Miami, Miami, Florida
  • 4Bascom Palmer Eye Institute, Miller School of Medicine, University of Miami, Miami, Florida
  • 5Wilmer Eye Institute, Dana Center for Preventive Ophthalmology, The Johns Hopkins School of Medicine, Baltimore, Maryland
  • 6Department of Epidemiology, Wake Forest School of Medicine, Winston-Salem, North Carolina
  • 7Department of Ophthalmology, Wake Forest School of Medicine, Winston-Salem, North Carolina
  • 8Wills Eye Hospital, Thomas Jefferson University, Philadelphia, Pennsylvania
  • 9Vision Health Initiative, Division of Diabetes Translation, Centers for Disease Control and Prevention, Atlanta, Georgia
JAMA Ophthalmol. 2015;133(2):174-181. doi:10.1001/jamaophthalmol.2014.4652
Abstract

Importance  The use of a nonmydriatic camera for retinal imaging combined with the remote evaluation of images at a telemedicine reading center has been advanced as a strategy for diabetic retinopathy (DR) screening, particularly among patients with diabetes mellitus from ethnic/racial minority populations with low utilization of eye care.

Objective  To examine the rate and types of DR identified through a telemedicine screening program using a nonmydriatic camera, as well as the rate of other ocular findings.

Design, Setting, and Participants  A cross-sectional study (Innovative Network for Sight [INSIGHT]) was conducted at 4 urban clinic or pharmacy settings in the United States serving predominantly ethnic/racial minority and uninsured persons with diabetes. Participants included persons aged 18 years or older who had type 1 or 2 diabetes mellitus and presented to the community-based settings.

Main Outcomes and Measures  The percentage of DR detection, including type of DR, and the percentage of detection of other ocular findings.

Results  A total of 1894 persons participated in the INSIGHT screening program across sites, with 21.7% having DR in at least 1 eye. The most common type of DR was background DR, which was present in 94.1% of all participants with DR. Almost half (44.2%) of the sample screened had ocular findings other than DR; 30.7% of the other ocular findings were cataract.

Conclusions and Relevance  In a DR telemedicine screening program in urban clinic or pharmacy settings in the United States serving predominantly ethnic/racial minority populations, DR was identified on screening in approximately 1 in 5 persons with diabetes. The vast majority of DR was background, indicating high public health potential for intervention in the earliest phases of DR when treatment can prevent vision loss. Other ocular conditions were detected at a high rate, a collateral benefit of DR screening programs that may be underappreciated.

Introduction

There are approximately 29.1 million persons with diabetes mellitus in the United States,1 with the prevalence expected to increase dramatically in future decades.2 A common diabetes complication is diabetic retinopathy (DR).1,3 Approximately 4.4% of Americans older than 40 years have DR.4 The personal and economic burdens of DR are noteworthy. Diabetic retinopathy is the leading cause of new blindness among working-age adults in the United States,1 with an estimated economic burden of $493 million per year.5 Prevention and optimal management of DR consist of tight glycemic and blood pressure control, routine dilated comprehensive eye examination, timely treatment, and patient education.68 The American Academy of Ophthalmology, American Optometric Association, and American Diabetes Association recommend routine, annual dilated eye examination for persons with diabetes. This examination should be instituted for type 1 diabetes 5 years after diagnosis and, for type 2 diabetes, at the time of diagnosis and annually thereafter.911 The percentage of Americans with diabetes receiving dilated eye care annually is low. Data analysis of the Behavioral Risk Factor Surveillance System revealed a dilated examination annual rate of 63.3% in persons with self-reported diabetes.12 Among ethnic/racial minority populations with diabetes, the annual eye examination rate is even lower: approximately 32% to 49% among African Americans and Hispanics.1316 Common barriers to care for minority populations are lack of accessibility (scarcity of eye care professionals in communities and transportation challenges) and cost.1721

Quiz Ref IDThe implementation of DR screening programs is associated with an increase in the percentage of people with diabetes receiving retinal screenings, a lower rate of those with sight-threatening DR detected at subsequent screenings, and a lower incidence and prevalence of blindness in the population.2225 The use of a nonmydriatic camera for retinal imaging combined with the remote evaluation of images at a telemedicine reading center has been advanced as a strategy for DR screening and is used widely in national screening programs.2630 Studies3133 show that DR screening results using nonmydriatic cameras via telemedicine agree with the criterion standard of dilated fundus photography. This screening strategy may be particularly relevant for people with diabetes who face barriers due to transportation and cost in seeking comprehensive dilated eye care from an ophthalmologist or optometrist.34,35 Screenings are brief compared with those using dilated examination, less burdensome since dilation is not required, and take place in the primary care setting or in novel settings, such as pharmacies. Patients express satisfaction with this screening approach.3638 Clinic personnel can be trained to operate the camera and upload images to a reading center.33,39 There is growing evidence25,40,41 that DR screening programs, combined with telemedicine, are cost-effective interventions.

In the present study, we sought to examine the feasibility and effectiveness of noninvasive DR screening using a nonmydriatic camera combined with a telemedicine reading center. We focused on screening settings accessible to patients with diabetes in 4 cities in the United States, namely, primary care clinics and pharmacies providing services to largely uninsured and/or minority populations.

Methods

The Innovative Network for Sight (INSIGHT) study was approved by the institutional review boards of The Johns Hopkins University, University of Alabama at Birmingham, University of Miami, Wake Forest University, and Wills Eye Hospital (WEH) and followed the tenets of the Declaration of Helsinki. Participants provided informed consent, written at some sites and oral at other sites. Participants did not receive financial compensation. The protocol has been described in detail (A. Murchison, MD, MPH, written communication, October 8, 2014); our focus in the present study was on the rates of DR and other ocular findings identified through the screening. Of the 4 study sites, 3 were based in outpatient clinics serving uninsured or underinsured populations with high representation of persons from ethnic/racial minorities. The fourth site was an outpatient pharmacy setting in an urban environment. Persons aged 18 years or older with a diagnosis of diabetes mellitus (type 1 or 2) were invited to participate in a DR screening. Birmingham, Alabama (University of Alabama at Birmingham), was one clinical site. The Cooper Green Mercy Health Service’s internal medicine clinic is a county-operated safety-net clinic serving county residents regardless of their ability to pay or insurance status. English-speaking patients with diabetes were invited to participate from January 26 to July 24, 2012. The second clinic site was in Miami, Florida (University of Miami). The Jessie Trice Community Health Center is a federally qualified health center serving the uninsured or underinsured population in the county. Participants were recruited via flyers and by referral from local physicians. Participants spoke English, Spanish, or Creole. Screening was conducted from March 2, 2012, to April 11, 2013. The third clinic site was in Winston-Salem, North Carolina (The Johns Hopkins University). The Downtown Health Plaza, affiliated with Wake Forest School of Medicine, serves low-income persons residing in the downtown area. Physicians and staff invited English-speaking individuals with diabetes to participate in the screening, which was conducted from May 5, 2013, to November 14, 2014. The pharmacy site was in Philadelphia, Pennsylvania (WEH). The outpatient pharmacy at Thomas Jefferson University Hospital is located in an urban environment. English- or Spanish-speaking persons with diabetes were invited for screening by pharmacy personnel when picking up medications for diabetes, by family practice physicians in nearby offices, and with flyers or advertisements in newspapers. The screening program took place from December 5, 2011, to March 29, 2013.

Participants completed a questionnaire providing contact information, demographics, age when first told by a physician that they had diabetes, whether they knew their hemoglobin A1c level, when they had received their most recent dilated eye examination, smoking status, and health insurance status. They were asked if they needed assistance in making an eye appointment once their DR screening results were available.

Ocular imaging was performed by trained technicians using a nonmydriatic camera with autofocus (model AFC-230, Nidek Inc). Dark fabric was draped over the participant’s head and/or the room was darkened. Technicians were trained in camera use by the WEH telemedicine reading center staff and followed the manufacturer’s standard operating instructions. Three photos were taken per eye: anterior segment, nasal fundus, and temporal fundus. If the images were blurry, additional images were taken to achieve satisfactory quality. Images were generated using NAVIS-Lite software (Nidek Inc) and uploaded to a Health Insurance Portability and Accountability Act (HIPAA)–compliant secure website at WEH.

Trained/certified readers at WEH read the images. A HIPAA-compliant proprietary software program (Diabetic Retinopathy Disease Management, version OTM1; Ocular Telehealth Management) was used for image management and report generation. Readers evaluated images using the National Health Service’s DR grading classification system (Table 1).42 Cataracts were graded according to a protocol using anterior segment photographs. Established algorithms were used to identify other ocular disease including hypertensive retinopathy, age-related macular degeneration, and glaucoma. A 10% random sample of images labeled normal by the readers was reviewed by an ophthalmologist; none was found to have signs of ocular pathology (A. Murchison, MD, MPH, written communication, October 8, 2014). The intrarater κ coefficient for readers with respect to DR findings was 0.72 with 88.8% agreement. The intergrader κ coefficient for DR findings was 0.62 (95% CI, 0.51-0.73) with agreement of 84.1%. Readers assigned preliminary grades within 48 hours of image upload. Ocular pathology other than DR was recorded. A retina specialist from the INSIGHT group (including J.A.H.) reviewed images showing signs of DR or other ocular findings.

Results from the reading center’s review of images were summarized in a screening report sent electronically to the participant’s site. The coordinator mailed a letter to participants describing the results and recommended follow-up care based on the findings; the recommendations were derived from the American Academy of Ophthalmology’s guidelines43 for DR follow-up and were based on the presence and degree of DR (Table 1). The letter to participants whose reports recommended normal (nonurgent) referral or follow-up (grades R0, R1, or P) encouraged them to seek an appointment for a dilated eye examination on an annual basis. For abnormal results for grade R1 or P DR, the letter encouraged the participant to seek an appointment for a dilated eye examination “within the next few months.” For individuals whose reports recommended prompt referral to an eye care professional owing to DR or maculopathy (grades R2, R3, or M), the coordinator telephoned the participant within 48 hours of receiving the report from the reading center, informed the participant of the recommendation, and offered to schedule an appointment with an ophthalmologist. Up to 5 telephone attempts were made to reach a participant. A letter was also mailed to the participant with results and recommendations. Patients with images deemed to be ungradable due to poor quality were advised to return for a dilated examination. Results were sent to the patient’s primary care physician upon patient request.

Data Management and Statistical Analysis

Each site oversaw its own data entry and securely transmitted the information to the data coordinating center at the University of Alabama at Birmingham, where a multisite database was constructed and data analysis was performed. Analysis of variance and χ2 tests were used to compare continuous and categorical data, respectively, across groups. P ≤ .05 (unpaired, 2-tailed test) was considered statistically significant.

Results

A total of 1894 persons participated in screening (Table 2), with 31.7% of the sample from Birmingham, 32.1% from Miami, 26.7% from Philadelphia, and 9.5% from Winston-Salem. The participants’ mean age at each site was similar, ranging from 53 to 55 years. There were more women (63.1%) than men (36.9%). Most individuals screened were of ethnic/racial minorities (88.0%); however, there were site differences. In Birmingham, most participants were African American (84.3%); in Philadelphia and Winston-Salem, approximately 68% of the participants were African American with a larger percentage of whites than in Birmingham, whereas in Miami 63.6% were Hispanic, Haitian, or Cuban American and 33.9% were African American, with very few whites screened.

The mean age at diabetes diagnosis by self-report was 44.5 years (Table 2). The mean duration of diabetes was approximately 8 to 10 years in Birmingham, Miami, and Philadelphia but longer (14.6 years) in Winston-Salem. Approximately 25% of the sample reported smoking or using other tobacco products. The percentage of patients with health insurance was wide, ranging from 22.6% in Miami to 79.2% in Philadelphia. There was site variability for when participants reported receiving their last dilated eye examination. About half of the Birmingham participants reported having a dilated eye examination within the past year, but at other sites, those reporting eye care within the past year ranged from 25.5% to 32.4%. In Miami, almost half (45.0%) of the participants reported receiving a dilated examination 2 or more years ago, and 11.2% reported never having a dilated examination. Approximately 30% to 42% of the participants at Miami, Philadelphia, and Winston-Salem indicated that they knew their hemoglobin A1c level compared with only 13.5% in Birmingham.

Across the sample, 21.7% of the participants had DR (background, preproliferative, proliferative, and/or maculopathy) in either eye: Birmingham, 23.5%; Miami, 24.1%; Philadelphia, 15.8%; and Winston-Salem, 24.3%. Figure 1 shows the percentage of participants with specific types of DR in either eye. At Birmingham, Miami, and Winston-Salem, background DR was present in 22.2% to 23.7% of the participants, but the percentage was lower in Philadelphia (14.4%). Among patients with DR, the vast majority had background DR (94.1%), with rates of preproliferative and proliferative DR ranging from 0% to 11.4% depending on the site. The proportion of participants with maculopathy in the overall sample was 9.3%. The rate of maculopathy was similar in Birmingham, Miami, and Winston-Salem, ranging from 9% to 11%, but was approximately half that rate in Philadelphia (5.4%). Depending on the site, no or very few participants displayed evidence of having had photocoagulation treatment. Twelve percent of the patients had at least 1 ungradable image in 1 or both eyes.

Quiz Ref IDThe prevalence of DR (regardless of type) was similar for whites vs the combined ethnic/racial minority groups (22.6% vs 21.6%, P = .74) and was unrelated to time since the last dilated eye examination (P = .44), smoking or other tobacco product use (P = .40), health insurance status (P = .21), or knowledge of hemoglobin A1c level (P = .82). Participants with DR had a longer duration of diabetes than did those without DR (mean [SD], 13.7 years [9.8] vs 8.8 [10.4], P < .001).

Quiz Ref IDAlmost half of the participants (44.2%) had ocular findings other than DR, with variability across the sites. Miami had double the prevalence of other ocular findings (61.1%) compared with Birmingham (29.7%), with Philadelphia and Winston-Salem falling between the 2 extremes. Table 3 lists the percentage of other ocular findings in either eye by type in the overall sample. The most common other finding was cataract, present in almost one-third of the participants. Hypertensive retinopathy, followed by cotton-wool spots, glaucomatous or optic nerve findings, and age-related macular degeneration, were also noted. Pterygium notations were much less common, and nevus was rare. Figure 2 displays the types of other ocular findings stratified by site.

Discussion

One in 5 patients with diabetes screened positive for DR using a telemedicine screening program in 4 urban settings in the United States serving predominantly ethnic/racial minority populations. This rate is similar to that reported in 2 previous US studies also using telemedicine reading centers.44,45 Three of our sites based at primary care clinics had very similar rates of DR (23.5%-24.3%), but the Philadelphia site (a pharmacy) was lower (15.8%), which could result from many factors. Patients who fill prescriptions may be more medically adherent and less likely to have diabetes complications.46,47 Philadelphia had a higher percentage of participants with health insurance (79.2%) compared with other sites (34.6%). Patients with diabetes having health insurance are more likely to have better glycemic control and lower rates of diabetic eye disease compared with those lacking health insurance.16,48,49 Given the lower DR rate in the pharmacy cohort, it may be that screening in this setting will have lower yield than in outpatient clinics, which is an issue for further study.

The majority (94.1%) of persons with DR had background DR, which is similar to the percentage determined in screening programs in primary care settings in the United States and Canada.28,29,34,36,44,45 Patients with proliferative disease were rare at all sites. From a public health perspective, our finding that most patients with DR had background DR, with almost 10% of persons with diabetes screened having maculopathy, indicates a high potential for intervention in DR’s earliest phases when treatment can prevent vision loss. In contrast to a UK report,50 the rate of DR detected in our program was not higher among ethnic/racial minorities compared with the rate in whites of European origin. At first glance, this finding may seem paradoxical since the prevalence of DR among African Americans and Hispanics in the United States is higher than that in whites of European descent.51,52 However, only 12% of the participants in our study were white; this small sample size may have made it difficult to evaluate white vs ethnic/racial minority differences in our screening program.

Diabetic retinopathy was unrelated to smoking status, health insurance status, and knowledge of one’s hemoglobin A1c level. These findings highlight the potential benefit of a DR screening program for the general population of people with diabetes rather than a more narrow approach for a selected subpopulation. However, DR was more likely to be present in persons with longer durations of diabetes, which is a well-established risk factor. This finding underscores the importance for screening programs to target individuals with long-standing diabetes.

The rate of self-reported dilated eye care use in the past year was low for the overall sample (32.2%), suggesting that DR screening in these settings could fulfill a critical role for patients with diabetes not routinely accessing annual dilated eye examination care. There were interesting differences across sites in the reported dilated examination rates. In Birmingham, more than half (52.8%) of the participants reported having a dilated examination within the past year, whereas at the other sites, the dilated examination rate was considerably lower (25.5%-32.4%). Unlike the other sites, Birmingham’s county-operated health system has an ophthalmology clinic. The other primary care sites did not have on-site eye services. This distinction may have contributed to a higher eye care utilization rate among Birmingham patients since care was accessible on site.53 The situation was inverted in Miami, where almost half (45.0%) of those screened reported not having a dilated eye examination in 2 or more years, and 11.2% reporting never having one. Previously, the clinic had an on-site optometrist, but that service was closed prior to the start of the present study. It remains to be determined whether these factors influenced the lower rate of eye care utilization.

Almost half of the participants had other ocular findings. This finding is an important collateral benefit of DR screening programs since many ocular findings detected are potentially sight-threatening conditions (eg, cataract, glaucoma, and macular degeneration) that are amenable to vision-preserving treatments. The most common other ocular finding was cataract. Glaucomatous/optic nerve findings were the most commonly noted conditions in Birmingham, which is not surprising given the high percentage of African Americans in the sample (84.3%), who have a 4- to 5-times greater risk for glaucoma-associated disorders compared with whites.54,55 Pterygium occurred in more than 10% of the persons screened in Miami but was rare at other sites, which may reflect the higher risk of pterygium for persons residing closer to the equator or with prolonged UV light exposure.56,57

The rate of other ocular findings differed substantially among sites, with Miami having the highest rate at greater than 60%. In contrast, Birmingham had half the rate (approximately 30%). Although DR screening has the additional benefit of identifying other potentially sight-threatening conditions, the particular lesion types and their frequency in the population screened depends on demographics, lifestyle, and utilization of comprehensive eye services.

Study strengths include a focus on evaluating a DR screening program in urban settings that predominantly serve patients with diabetes from ethnic/racial minorities and uninsured or underinsured populations, an approach receiving only scant attention previously.58,59 Our target populations have among the lowest comprehensive eye care utilization rates in the United States, thus being at high risk for undetected DR. Screening incorporated a nonmydriatic camera that is rapid and less burdensome and a central reading center through telemedicine. Multiple sites allowed us to implement the program in diverse geographic locations. Study limitations include selection bias during enrollment; it is unknown whether those who participated vs those who did not were systemically different. Information is unavailable on the percentage of persons who declined participation. Although inclusion of 4 different sites enhances generalizability, the sites differed in many ways; factors contributing to site differences cannot be precisely determined but can be addressed in future research. One site had fewer participants than the others because of delayed start-up. Although we have not focused on patient follow-up for recommended eye appointments, acuity screening, and patient satisfaction in this article, these issues will be addressed in subsequent reports.

Conclusions

Quiz Ref IDIn a DR telemedicine screening program in urban clinic and pharmacy settings in the United States serving predominantly ethnic/racial minority populations, 1 in 5 persons with diabetes screened positive for DR. Most had background DR, suggesting a high potential for intervention in DR’s earliest phases when management can prevent vision loss. Other ocular conditions were detected in almost 50% of the patients screened, a potentially underappreciated feature of DR screening programs for preventing vision loss.

Back to top
Article Information

Submitted for Publication: July 8, 2014; final revision received September 19, 2014; accepted September 23, 2014.

Corresponding Author: Cynthia Owsley, PhD, Department of Ophthalmology, School of Medicine, University of Alabama at Birmingham, 700 S 18th St, Ste 609, Birmingham, AL 35294 (owsley@uab.edu).

Published Online: November 13, 2014. doi:10.1001/jamaophthalmol.2014.4652.

Author Contributions: Drs Owsley and McGwin had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Owsley, McGwin, Lee, Friedman, Gower, Haller, Hark, Saaddine.

Acquisition, analysis, or interpretation of data: Owsley, McGwin, Lam, Friedman, Gower, Haller, Hark, Saaddine.

Drafting of the manuscript: Owsley, McGwin, Friedman, Hark, Saaddine.

Critical revision of the manuscript for important intellectual content: Owsley, Lee, Lam, Friedman, Gower, Haller, Hark.

Statistical analysis: Owsley, McGwin, Saaddine.

Obtained funding: Owsley, Lee, Friedman, Hark, Saaddine.

Administrative, technical, or material support: Owsley, Lam, Haller, Hark.

Study supervision: Owsley, Gower, Haller, Hark, Saaddine.

Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Friedman has consulted for Nidek Inc about devices unrelated to this project. No other disclosures are reported.

Funding/Support: This research was supported through Centers for Disease Control and Prevention (CDC) cooperative agreements with The Johns Hopkins University, University of Alabama at Birmingham, University of Miami, and Wills Eye Hospital (5U58DP002651, 5U58DP002652, 5U58DP002653, and 5U58DP002655). The grantees received additional support directly from Alcon Research Institute (The Johns Hopkins University), the EyeSight Foundation of Alabama (University of Alabama at Birmingham), Research to Prevent Blindness (University of Alabama at Birmingham), and the Buck Trust (University of Alabama at Birmingham). Nidek provided the cameras and operator training free of charge.

Role of the Funder/Sponsor: The CDC participated in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, and approval of the manuscript; and decision to submit the manuscript for publication.

Group Information: The Innovative Network for Sight (INSIGHT) Research Group members are listed in the eAppendix in the Supplement.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC.

Correction: This article was corrected on March 27, 2015, to add the group information to the Article Information section.

References
1.
Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United States. Atlanta, GA: US Dept of Health and Human Services; 2014. http://www.cdc.gov/diabetes/pubs/statsreport14.htm. Accessed October 10, 2014.
2.
Boyle  JP, Honeycutt  AA, Narayan  KM,  et al.  Projection of diabetes burden through 2050. Diabetes Care. 2001;24(11):1936-1940.
PubMedArticle
3.
Saaddine  JB, Honeycutt  AA, Narayan  KM, Zhang  X, Klein  R, Boyle  JP.  Projection of diabetic retinopathy and other major eye diseases among people with diabetes mellitus. Arch Ophthalmol. 2008;126(12):1740-1747.
PubMedArticle
4.
Zhang  X, Saaddine  JB, Chou  C-F,  et al.  Prevalence of diabetic retinopathy in the United States, 2005-2008. JAMA. 2010;304(6):649-656.
PubMedArticle
5.
Rein  DB, Zhang  P, Wirth  KE,  et al.  The economic burden of major adult visual disorders in the United States. Arch Ophthalmol. 2006;124(12):1754-1760.
PubMedArticle
6.
Mohamed  Q, Gillies  MC, Wong  TY.  Management of diabetic retinopathy: a systematic review. JAMA. 2007;298(8):902-916.
PubMedArticle
7.
Basch  CE, Walker  EA, Howard  CJ, Shamoon  H, Zybert  P.  The effect of health education on the rate of ophthalmic examinations among African Americans with diabetes mellitus. Am J Public Health. 1999;89(12):1878-1882.
PubMedArticle
8.
Sloan  FA, Grossman  DS, Lee  PP.  Effects of receipt of guideline-recommended care on onset of diabetic retinopathy and its progression. Ophthalmology. 2009;116(8):1515-1521.
PubMedArticle
9.
American Academy of Ophthalmology Retina Panel. Preferred Practice Pattern Guidelines Diabetic Retinopathy. San Francisco, CA: American Academy of Ophthalmology; 2012. http://one.aao.org/preferred-practice-pattern/diabetic-retinopathy-ppp--2014. Accessed October 15, 2014.
10.
Cavallerano  J. Optometric Clinical Practice Guideline, Care of the Patient with Diabetes Mellitus, Reference Guide for Clinicians. St Louis, MO. American Optometric Association; 2009. http://www.aoa.org/documents/CPG-3.pdf. Accessed October 7, 2014.
11.
American Diabetes Association.  Standards of medical care in diabetes—2013. Diabetes Care. 2013;36(suppl 1):S11-S66.
PubMedArticle
12.
Saaddine  JB, Engelgau  MM, Beckles  GL, Gregg  EW, Thompson  TJ, Narayan  KM.  A diabetes report card for the United States: quality of care in the 1990s. Ann Intern Med. 2002;136(8):565-574.
PubMedArticle
13.
Maclennan  PA, McGwin  G  Jr, Heckemeyer  C,  et al.  Eye care use among a high-risk diabetic population seen in a public hospital’s clinics. JAMA Ophthalmol. 2014;132(2):162-167.
PubMedArticle
14.
Pérez  CM, Febo-Vázquez  I, Guzmán  M, Ortiz  AP, Suárez  E.  Are adults diagnosed with diabetes achieving the American Diabetes Association clinical practice recommendations? P R Health Sci J. 2012;31(1):18-23.
PubMed
15.
Paz  SH, Varma  R, Klein  R, Wu  J, Azen  SP; Los Angeles Latino Eye Study Group.  Noncompliance with vision care guidelines in Latinos with type 2 diabetes mellitus: the Los Angeles Latino Eye Study. Ophthalmology. 2006;113(8):1372-1377.
PubMedArticle
16.
Baker  RS, Watkins  NL, Wilson  MR, Bazargan  M, Flowers  CW  Jr.  Demographic and clinical characteristics of patients with diabetes presenting to an urban public hospital ophthalmology clinic. Ophthalmology. 1998;105(8):1373-1379.
PubMedArticle
17.
Centers for Disease Control and Prevention. Improving the nation’s vision health: a coordinated public health approach. http://www.cdc.gov/visionhealth/pdf/improving_nations_vision_health.pdf. Accessed October 7, 2014.
18.
Owsley  C, McGwin  G, Scilley  K, Girkin  CA, Phillips  JM, Searcey  K.  Perceived barriers to care and attitudes about vision and eye care: focus groups with older African Americans and eye care providers. Invest Ophthalmol Vis Sci. 2006;47(7):2797-2802.
PubMedArticle
19.
Maclennan  PA, McGwin  G  Jr, Searcey  K, Owsley  C.  A survey of Alabama eye care providers in 2010-2011. BMC Ophthalmol. 2014;14:44.
PubMedArticle
20.
Rask  KJ, Williams  MV, Parker  RM, McNagny  SE.  Obstacles predicting lack of a regular provider and delays in seeking care for patients at an urban public hospital. JAMA. 1994;271(24):1931-1933.
PubMedArticle
21.
Chou  C-F, Sherrod  CE, Zhang  X,  et al.  Barriers to eye care among people aged 40 years and older with diagnosed diabetes, 2006-2010. Diabetes Care. 2014;37(1):180-188.
PubMedArticle
22.
Stefánsson  E, Bek  T, Porta  M, Larsen  N, Kristinsson  JK, Agardh  E.  Screening and prevention of diabetic blindness. Acta Ophthalmol Scand. 2000;78(4):374-385.
PubMedArticle
23.
Forster  AS, Forbes  A, Dodhia  H,  et al.  Changes in detection of retinopathy in type 2 diabetes in the first 4 years of a population-based diabetic eye screening program: retrospective cohort study. Diabetes Care. 2013;36(9):2663-2669.
PubMedArticle
24.
Garg  S, Jani  PD, Kshirsagar  AV, King  B, Chaum  E.  Telemedicine and retinal imaging for improving diabetic retinopathy evaluation. Arch Intern Med. 2012;172(21):1677-1678.
PubMedArticle
25.
Kirkizlar  E, Serban  N, Sisson  JA, Swann  JL, Barnes  CS, Williams  MD.  Evaluation of telemedicine for screening of diabetic retinopathy in the Veterans Health Administration. Ophthalmology. 2013;120(12):2604-2610.
PubMedArticle
26.
Zimmer-Galler  IE, Zeimer  R.  Telemedicine in diabetic retinopathy screening. Int Ophthalmol Clin. 2009;49(2):75-86.
PubMedArticle
27.
Silva  PS, Cavallerano  JD, Aiello  LM, Aiello  LP.  Telemedicine and diabetic retinopathy. Arch Ophthalmol. 2011;129(2):236-242.
PubMedArticle
28.
Wilson  RR, Silowash  R, Anthony  L, Cecil  RA, Eller  A.  Telemedicine process used to implement an effective and functional screening program for diabetic retinopathy. J Diabetes Sci Technol. 2008;2(5):785-791.
PubMedArticle
29.
Mansberger  SL, Gleitsmann  K, Gardiner  S,  et al.  Comparing the effectiveness of telemedicine and traditional surveillance in providing diabetic retinopathy screening examinations. Telemed J E Health. 2013;19(12):942-948.
PubMedArticle
30.
Li  HK, Horton  M, Bursell  S-E,  et al.  Telehealth practice recommendations for diabetic retinopathy, second edition. Telemed J E Health.2011;17(10):1-24.Article
31.
Lin  DY, Blumenkranz  MS, Brothers  RJ, Grosvenor  DM.  The sensitivity and specificity of single-field nonmydriatic monochromatic digital fundus photography with remote image interpretation for diabetic retinopathy screening. Am J Ophthalmol. 2002;134(2):204-213.
PubMedArticle
32.
Massin  P, Erginay  A, Ben Mehidi  A,  et al.  Evaluation of a new non-mydriatic digital camera for detection of diabetic retinopathy. Diabet Med. 2003;20(8):635-641.
PubMedArticle
33.
Bragge  P, Gruen  RL, Chau  M, Forbes  A, Taylor  HR.  Screening for presence or absence of diabetic retinopathy: a meta-analysis. Arch Ophthalmol. 2011;129(4):435-444.
PubMedArticle
34.
Ogunyemi  O, Terrien  E, Eccles  A,  et al.  Teleretinal screening for diabetic retinopathy in six Los Angeles urban safety-net clinics: initial findings. AMIA Annu Symp Proc.2011;2011:1027-1035.
35.
Gibson  DM.  Eye care availability and access among individuals with diabetes, diabetic retinopathy, or age-related macular degeneration. JAMA Ophthalmol. 2014;132(4):471-477.
PubMedArticle
36.
Nathoo  N, Ng  M, Rudnisky  CJ, Tennant  MTS.  The prevalence of diabetic retinopathy as identified by teleophthalmology in rural Alberta. Can J Ophthalmol. 2010;45(1):28-32.
PubMedArticle
37.
Arora  S, Kurji  AK, Tennant  MTS.  Dismantling sociocultural barriers to eye care with tele-ophthalmology: lessons from an Alberta Cree community. Clin Invest Med. 2013;36(2):E57-E63.
PubMed
38.
Cavallerano  AA, Conlin  PR.  Teleretinal imaging to screen for diabetic retinopathy in the Veterans Health Administration. J Diabetes Sci Technol. 2008;2(1):33-39.
PubMedArticle
39.
Maberley  D, Morris  A, Hay  D, Chang  A, Hall  L, Mandava  N.  A comparison of digital retinal image quality among photographers with different levels of training using a non-mydriatic fundus camera. Ophthalmic Epidemiol. 2004;11(3):191-197.
PubMedArticle
40.
Jones  S, Edwards  RT.  Diabetic retinopathy screening: a systematic review of the economic evidence. Diabet Med. 2010;27(3):249-256.
PubMedArticle
41.
Rein  DB, Wittenborn  JS, Zhang  X,  et al; Vision Cost-Effectiveness Study Group.  The cost-effectiveness of three screening alternatives for people with diabetes with no or early diabetic retinopathy. Health Serv Res. 2011;46(5):1534-1561.
PubMedArticle
42.
Harding  S, Greenwood  R, Aldington  S,  et al; Diabetic Retinopathy Grading and Disease Management Working Party.  Grading and disease management in national screening for diabetic retinopathy in England and Wales. Diabet Med. 2003;20(12):965-971.
PubMedArticle
43.
American Academy of Ophthalmology Preferred Practice Patterns Committee. Preferred Practice Pattern Guidelines: Comprehensive Adult Medical Eye Evaluation. San Francisco, CA: American Academy of Ophthalmology; 2010. http://one.aao.org/preferred-practice-pattern/comprehensive-adult-medical-eye-evaluation--octobe. Accessed October 7, 2014.
44.
Zimmer-Galler  I, Zeimer  R.  Results of implementation of the DigiScope for diabetic retinopathy assessment in the primary care environment. Telemed J E Health. 2006;12(2):89-98.
PubMedArticle
45.
Cavallerano  AA, Cavallerano  JD, Katalinic  P,  et al; Joslin Vision Network Research Team.  A telemedicine program for diabetic retinopathy in a Veterans Affairs Medical Center—the Joslin Vision Network Eye Health Care Model. Am J Ophthalmol. 2005;139(4):597-604.
PubMedArticle
46.
An  J, Nichol  MB.  Multiple medication adherence and its effect on clinical outcomes among patients with comorbid type 2 diabetes and hypertension. Med Care. 2013;51(10):879-887.
PubMedArticle
47.
Krapek  K, King  K, Warren  SS,  et al.  Medication adherence and associated hemoglobin A1c in type 2 diabetes. Ann Pharmacother. 2004;38(9):1357-1362.
PubMedArticle
48.
Gregg  EW, Geiss  LS, Saaddine  J,  et al.  Use of diabetes preventive care and complications risk in two African-American communities. Am J Prev Med. 2001;21(3):197-202.
PubMedArticle
49.
Flavin  NE, Mulla  ZD, Bonilla-Navarrete  A,  et al.  Health insurance and the development of diabetic complications. South Med J. 2009;102(8):805-809.
PubMedArticle
50.
Sivaprasad  S, Gupta  B, Gulliford  MC,  et al.  Ethnic variations in the prevalence of diabetic retinopathy in people with diabetes attending screening in the United Kingdom (DRIVE UK). PLoS One. 2012;7(3):e32182. doi:10.1371/journal.pone.0032182.
PubMedArticle
51.
Kempen  JH, O’Colmain  BJ, Leske  MC,  et al; Eye Diseases Prevalence Research Group.  The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122(4):552-563.
PubMedArticle
52.
Wong  TY, Klein  R, Islam  FM,  et al.  Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006;141(3):446-455.
PubMedArticle
53.
Shin  P, Finnegan  B.  Assessing the need for on-site eye care professionals in community health centers. Policy Brief George Wash Univ Cent Health Serv Res Policy. 2009;(2):1-23.
PubMed
54.
Tielsch  JM, Sommer  A, Katz  J, Royall  RM, Quigley  HA, Javitt  J.  Racial variations in the prevalence of primary open-angle glaucoma: the Baltimore Eye Survey. JAMA. 1991;266(3):369-374.
PubMedArticle
55.
Javitt  JC, McBean  AM, Nicholson  GA, Babish  JD, Warren  JL, Krakauer  H.  Undertreatment of glaucoma among black Americans. N Engl J Med. 1991;325(20):1418-1422.
PubMedArticle
56.
Liu  L, Wu  J, Geng  J, Yuan  Z, Huang  D.  Geographical prevalence and risk factors for pterygium: a systematic review and meta-analysis. BMJ Open. 2013;3(11):e003787.
PubMedArticle
57.
Saw  SM, Tan  D.  Pterygium: prevalence, demography and risk factors. Ophthalmic Epidemiol. 1999;6(3):219-228.
PubMedArticle
58.
Olayiwola  JN, Sobieraj  DM, Kulowski  K, St Hilaire  D, Huang  JJ.  Improving diabetic retinopathy screening through a statewide telemedicine program at a large federally qualified health center. J Health Care Poor Underserved. 2011;22(3):804-816.
PubMedArticle
59.
Jiménez-Ramírez  F, Pérez  R.  Diabetic retinopathy education and screening at the community pharmacy in Puerto Rico. P R Health Sci J. 2011;30(3):139-144.
PubMed
×