Diabetic retinopathy is one of the most prevalent but preventable blinding diseases in the United States. This article reviews the pathophysiology of diabetic retinopathy, the evidence for its primary and secondary prevention, and both traditional and emerging strategies for its assessment.

Diabetic retinopathy is the leading cause of blindness among adults aged 20-74 years in the United States, which notably includes the working-age population. With early detection, diabetic retinopathy can be treated with modalities that have been proven to decrease the risk of severe vision loss by > 90%.

Given the proven benefits of early detection, guidelines for screening for diabetic retinopathy have been established by national professional organizations such as the American Diabetes Association (ADA) and the American Academy of Ophthalmology (AAO). Unfortunately, on average, < 50% of diabetic patients in the United States meet these recommendations.1-3  In fact, 60% of patients who require vision-preserving laser surgery do not receive treatment.4  The barriers to recommended eye examinations are numerous and include insufficient referrals, socioeconomic factors, and poor geographical access to care.

Recent advances in digital imaging have opened new avenues for assessing retinopathy, which may provide better access to diagnosis and management for this treatable, but often blinding, condition. This article will provide an overview of the epidemiology of diabetic retinopathy, its pathophysiology and classification, and the multicenter prospective clinical trials that have provided rigorous evidence for its screening and treatment. The technological advances relevant to screening will be discussed, and finally, the important role of primary care providers in retinal screening for patients with diabetes will be examined.

Approximately 8% of the U.S. population has diabetes, which equates to > 23.6 million children and adults.5  The prevalence of diabetes varies among ethnicities: 5.2% for European Americans, 9% for Native Americans, 11% for African Americans, and 10.4% for Mexican Americans.6  The World Health Organization estimates that > 180 million people worldwide have diabetes. This number is likely to more than double by the year 2030. At least 10% will likely develop visual impairment secondary to diabetic retinopathy.7 

The prevalence of diabetic retinopathy is high; 20 years after diagnosis, > 90% of patients with type 1 diabetes and > 60% of those with type 2 diabetes will have some degree of retinopathy.8,9  The major risk factors for developing diabetic retinopathy are duration of diabetes8,9  and severity of hyperglycemia.10-14  Other important factors include hypertension15,16  and elevated serum lipid levels.17,18 

The natural history of diabetic retinopathy typically follows an orderly and predictable pattern. Long-term hyperglycemia causes vascular endothelial dysfunction resulting in loss of endothelial cells and pericytes. The retina then develops micro-aneurysms, intraretinal hemorrhages, and focal areas of retinal ischemia (cotton-wool spots). At this point, the retinopathy is classified as nonproliferative diabetic retinopathy (NPDR).

As the retinopathy progresses, the vessels become further damaged, resulting in retinal nonperfusion and more widespread ischemia. Clinically, the retina can have signs of vascular damage including venous beading, intraretinal microvascular abnormalities, and more severe hemorrhages (Figure 1). At this point, the retinopathy is classified as severe NPDR. Even at this stage, most patients are asymptomatic.

With further ischemic injury, compensatory chemical mediators, most notably vascular endothelial growth factor, induce the growth of fragile new blood vessels at the inner surface of the retina.19  This stage, called proliferative diabetic retinopathy (PDR), is characterized by neovascularization of the optic disc and neovascularization elsewhere. When these fragile vessels bleed, the vitreous hemorrhage causes symptoms of “floaters” or, if severe, loss of vision. Over time, the new vessels fibrose and can contract, resulting in tractional retinal detachments, which can cause significant vision loss.

Macular edema, the leading cause of vision loss among patients with diabetes, can occur at any stage of diabetic retinopathy. Damaged retinal vessels result in increased vascular permeability, causing an accumulation of intraretinal fluid and/or lipid, which is clinically apparent with direct ophthalmoscopy. The retina appears thickened and may contain yellow hard exudates (lipid). Macular edema may cause symptoms of blurry vision, or it may cause no symptoms at all.

Several multicenter randomized controlled clinical trials have demonstrated that diabetic retinopathy can be prevented or that its natural course can be altered. The landmark Diabetes Control and Complications Trial (DCCT) involved 1,441 subjects with type 1 diabetes, ages 13-39 years, at 29 medical centers in the United States and Canada. Study participants had either no disease or early diabetic retinopathy and were randomized to either intensive blood glucose control (mean A1C 7.2%) or conventional blood glucose control (mean A1C 9.1%). The study demonstrated that intensive blood glucose control reduced the risk of progression of diabetic retinopathy by 54%, reduced the development of severe NPDR or PDR by 47%, reduced the need for laser surgery by 56%, and reduced the risk of diabetic macular edema by 23%.10,11 

The U.K. Prospective Diabetes Study (UKPDS) confirmed the protective effect of intensive blood glucose control in patients with type 2 diabetes and also evaluated the effect of hypertension. A total of 1,148 patients with type 2 diabetes and hypertension were enrolled and treated with either an angiotensin-converting enzyme inhibitor (captopril) or a β-blocker (atenolol). This study demonstrated that patients with tight blood pressure control (< 150/85 mmHg) compared to patients with blood pressure less tightly controlled (< 180/95 mmHg) were found to have a 37% risk reduction in microvascular changes, 34% risk reduction in the need for laser treatment, and 47% risk reduction in decreased vision.12,13,15 

Several randomized trials have also demonstrated the value of surgical treatments to minimize the complications of diabetic retinopathy. In the Diabetes Retinopathy Study (DRS) of more than 1,700 patients at 15 medical centers, panretinal photocoagulation (PRP; laser treatment to the peripheral retina) reduced the risk of severe (defined as 5/200 or worse) vision loss from PDR from 15.9% in untreated eyes to 6.4% in treated eyes.20  Once a patient reached the PDR stage (fragile new blood vessels), it was observed that argon laser treatment of the retina resulted in regression of the neovascularization.

The Early Treatment of Diabetic Retinopathy Study (ETDRS) enrolled 3,711 patients and provided valuable information regarding management of diabetic retinopathy. First, it demonstrated that PRP can reduce the risk of severe vision loss to < 2% if administered at the appropriate stage (severe NPDR or PDR). Second, focal laser treatment (treatment to the macular area with an argon laser) was found to reduce moderate visual loss (doubling of the visual angle) by 50%. Finally, it was found that aspirin did not alter rates of progression of diabetic retinopathy and did not increase the risk of vitreous hemorrhage.21-23 

The Diabetic Retinopathy Vitrectomy Study (DRVS) showed that there was a benefit to early vitrectomy (surgical removal of vitreous) in very severe PDR in patients with type 1 diabetes. Two years after surgery, 36% of the early vitrectomy group and 12% of the late vitrectomy group had visual acuity of 20/40 or better.24,25 

These landmark studies have demonstrated that the blinding complications from diabetes can be largely prevented medically, by glycemic and blood pressure control, as well as by early detection and timely treatment of diabetic retinopathy with photocoagulation/surgical techniques. Therefore, screening guidelines have been developed by national professional organizations such as the ADA26  and AAO.27 

Adults and children > 10 years of age with type 1 diabetes should have an initial dilated examination by an ophthalmologist within 5 years of the onset of diabetes. Because people may already have type 2 diabetes before they are aware of symptoms and up to 20% of patients with type 2 diabetes have retinopathy at the time of diagnosis, they should have an initial dilated examination by an ophthalmologist at the time of their diabetes diagnosis.9  Subsequent examinations should be yearly or more frequently if retinopathy is progressing. Pregnant women with preexisting diabetes should have a dilated eye examination early in the first trimester of pregnancy because pregnancy can potentiate rapid progression of retinopathy. Close follow-up should continue throughout pregnancy and 1 year postpartum. Current recommended screening guidelines are summarized in Table 1.

The retinopathy screening paradigm is based on clinical trials that have demonstrated the benefits of screening. However, current care falls far below these recommendations. Insufficient screening may be partially related to lack of access to eye care specialists. The advent of retinal imaging and digital technology may provide an avenue for greater compliance with screening recommendations.

In 2004, the American Telemedicine Association established consensus recommendations that provided guidelines for clinical, technical, and operational performance standards for diabetic retinopathy screening. The development of retinal imaging and, more recently, digital retinal photography may help address the barriers to access for retinopathy screening. Telehealth (telecommunication to promote health) or telemedicine (telecommunication for diagnostic and therapeutic intervention) programs based on retinal imaging with or without remote interpretation may facilitate early diagnosis of diabetic retinopathy and timely treatment, hence preserving vision.28 

Methods of screening for diabetic retinopathy include direct and indirect ophthalmoscopy, stereoscopic color film fundus photography, mydriatic or nonmydriatic digital color (Figure 2), and monochromatic photography. Traditionally, ophthalmologists have screened for diabetic retinopathy by dilating the pupil and performing indirect ophthalmoscopy, in which the entire retina is examined. This method of screening is successful where access to eye care is sufficient. However, the increasing rate of patients with diabetes will soon outpace the supply of eye care providers, both in the United States and worldwide. At present, some communities have poor or even no access to ophthalmologic care. In these settings, remote interpretation of film-based or digital photographs of the retina may be employed.

The gold standard for the detection of diabetic retinopathy consists of 30-degree stereoscopic photography of seven standard fields on color film, as developed for the ETDRS—Classification of Diabetic Retinopathy.29  This has a sensitivity and specificity for the detection of diabetic retinopathy that is superior to direct30  and indirect31  ophthalmoscopy by ophthalmologists. The efficacy of trained readers has been demonstrated in a systematic review, in which the interpretation of mydriatic (dilated) retinal photography provided the most sensitive screening and monitoring test for sight-threatening retinopathy, with sensitivities > 80%.32  However, this technique is labor intensive, has a long turnaround time, and requires expensive equipment and trained retinal photographers and readers. From a patient's perspective, it can be time-consuming, and the required pupillary dilation may be uncomfortable. Thus, seven-field stereoscopic fundus photography is an ideal gold standard but is not ideal for widespread implementation.

The development of digital retinal photography has facilitated rapid acquisition and interpretation of fundus images, quantitative analysis of data for documentation and progression of retinopathy, and the rapid deployment of retinal imaging worldwide. Currently, there are no universally accepted criteria for the detection of diabetic retinopathy using digital imaging. However, several systems are being studied and validated. Retinal imaging can be performed using digital retinal photographs with (mydriatic) or without (nonmydriatic) dilating the pupil. The digital photographs may be interpreted by trained readers or forwarded to a reading center for interpretation and grading (“store and forward”).

Several studies have examined the sensitivity and specificity of digital imaging. Two-field mydriatic33  and two-field nonmydriatic34  digital photography performed favorably compared to ophthalmoscopy and seven-field stereophotography.

Because of their ease of use and associated patient comfort, nonmydriatic cameras have facilitated retinal imaging for patients with diabetes in primary care settings, including family practice, internal medicine, and endocrinology offices. The cameras do not require operation by a trained retinal photographer and their use has been validated.35,36  Furthermore, an AAO meta-analysis determined that there was sufficient evidence from randomized clinical trials (Level 1) that single-field digital fundus photography can serve as a screening tool for diabetic retinopathy to identify patients with retinopathy for referral for ophthalmologic evaluation and management.37  Another study evaluated single-field 45-degree nonmydriatic monochromatic images and found them to be highly correlated (κ = 0.97, P = 0.0001) to the gold standard of the stereoscopic seven-field mydriatic images.38 

As an alternative to a single field, some cameras can photograph three 45-degree fields. A recent report evaluated single-field versus three-field nonmydriatic images compared to the seven-field gold standard and concluded that three color 45-degree nonmydriatic images had a sensitivity and specificity of 82 and 92%, respectively, and may also be an effective tool in a screening setting to determine levels of diabetic retinopathy for specialist referral.39 

Recognizing the importance of diabetic retinal imaging, several countries have implemented national screening programs such as the National Plan for Screening in the United Kingdom and the OPHDIAT program in France. The OPHDIAT telemedicine system comprises 11 screening centers equipped with nonmydriatic cameras. Fundus photographs are acquired by technicians, with remote interpretation by ophthalmologists who grade the images. In 28 months, 15,307 diabetic retinopathy screening examinations were performed, and diabetic retinopathy was detected in 3,350 patients (23.4%).40  It was found that the rates of diabetic retinopathy screening improved from 50% before to more than 70% after the implementation of OPHDIAT.41 

Acquisition of digitized retinal images allow for novel image analysis methods and Web-based connectivity to create models of remote, computer-assisted, or even automated diagnosis and management of diabetic retinopathy. Several systems are in development and are currently being clinically validated.42,43 

Although retinal imaging programs are important in improving access to care and identifying patients who need further evaluation, they do not replace comprehensive eye exams by ophthalmologists. A full evaluation is required when a screening retinal photograph is unreadable and for follow-up of abnormalities detected by the screening system. In addition, non—diabetes-related ocular conditions such as cataract, hypertensive retinopathy, and glaucoma are optimally evaluated during a comprehensive eye exam.

The importance of systemic factors such as glycemic and blood pressure control in preventing and slowing the progression of diabetic retinopathy was conclusively demonstrated in the DCCT and UKPDS clinical trials. Primary care physicians play a significant role in optimizing glycemic control and managing other risk factors such as hypertension and hyperlipidemia, which can potentially affect eye health.

Appropriate referral by primary care providers at recommended intervals for diabetic retinopathy eye examinations is crucial, because timely treatment with panretinal and focal laser photocoagulation surgery has been proven in the ETDRS, DRS, and DRVS trials to decrease vision loss from diabetes. Primary care physicians can educate their patients with diabetes about the importance of retinal examinations, as diabetic retinopathy is often asymptomatic. Encouragement by primary care providers may increase the likelihood that patients will keep their ophthalmology appointments.

In addition, primary care providers can communicate with ophthalmologists to convey the reason for referrals and supply patient information such as A1C results and presence of any other comorbid conditions. (A sample communication form is provided by Sinclair et al.44 ) After patients get eye examinations, primary care providers can expect to receive assessments from the eye care providers and then can reinforce to patients any recommendations for ophthalmological follow-up care.

Finally, as telehealth and telemedicine programs are implemented, the role of primary care providers may become even more encompassing, as screening retinal photographs may be obtained directly in the primary care office, and, perhaps in the future, primary care providers may even be trained to evaluate retinal photographs.45 

1.
Brechner
RJ
,
Cowie
CC
,
Howie
LJ
,
Herman
WH
,
Will
JC
,
Harris
MI
:
Ophthalmic examination among adults with diagnosed diabetes mellitus
.
JAMA
270
:
1714
-
1718
,
1993
2.
Lee
PP
,
Feldman
ZW
,
Ostermann
J
,
Brown
DS
,
Sloan
FA
:
Longitudinal rates of annual eye examinations of persons with diabetes and chronic eye diseases
.
Ophthalmology
110
:
1952
-
1959
,
2003
3.
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
113
:
1372
-
1377
,
2006
4.
Ferris
FL
 3rd
,
Davis
MD
,
Aiello
LM
:
Treatment of diabetic retinopathy
.
N Engl J Med
341
:
667
-
678
,
1999
5.
American Diabetes Association
:
All about diabetes [article online]
. Available from http://www.diabetes.org/about-diabetes.jsp.
Accessed 22 May 2009
6.
Cowie
CC
,
Rust
KF
,
Byrd-Holt
DD
,
Eberhardt
MS
,
Flegal
KM
,
Engelgau
MM
,
Saydah
SH
,
Williams
DE
,
Geiss
LS
,
Gregg
EW
:
Prevalence of diabetes and impaired fasting glucose in adults in the U.S. population: National Health and Nutrition Examination Survey 1999-2002
.
Diabetes Care
29
:
1263
-
1268
,
2006
7.
World Health Organization
:
What is diabetes? [article online]
Available from http://www.who.int/mediacentre/factsheets/fs312/en/index.html.
Accessed 22 May 2009
8.
Klein
R
,
Klein
BE
,
Moss
SE
,
Davis
MD
,
DeMets
DL
:
The Wisconsin Epidemiologic Study of Diabetic Retinopathy. IX. Four-year incidence and progression of diabetic retinopathy when age at diagnosis is less than 30 years
.
Arch Ophthalmol
107
:
237
-
243
,
1989
9.
Klein
R
,
Klein
BE
,
Moss
SE
,
Davis
MD
,
DeMets
DL
:
The Wisconsin Epidemiologic Study of Diabetic Retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years
.
Arch Ophthalmol
102
:
527
-
532
,
1984
10.
DCCT Research Group
:
Progression of retinopathy with intensive versus conventional treatment in the Diabetes Control and Complications Trial
.
Ophthalmology
102
:
647
-
661
,
1995
11.
DCCT Research Group
:
The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the Diabetes Control and Complications Trial
.
Diabetes
44
:
968
-
983
,
1995
12.
UK Prospective Diabetes Study Group
:
Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33)
.
Lancet
352
:
837
-
853
,
1998
13.
Kohner
EM
,
Stratton
IM
,
Aldington
SJ
,
Holman
RR
,
Matthews
DR
UK Prospective Diabetes Study (UKPDS) Group
:
Relationship between the severity of retinopathy and progression to photocoagulation in patients with type 2 diabetes mellitus in the UKPDS (UKPDS 52)
.
Diabet Med
18
:
178
-
184
,
2001
14.
Wong
TY
,
Liew
G
,
Tapp
RJ
,
Schmidt
MI
,
Wang
JJ
,
Mitchell
P
,
Klein
R
,
Klein
BE
,
Zimmet
P
,
Shaw
J
:
Relation between fasting glucose and retinopathy for diagnosis of diabetes: three population-based cross-sectional studies
.
Lancet
371
:
700
-
702
,
2008
15.
UK Propspective Diabetes Study Group
:
Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38
.
BMJ
317
:
703
-
713
,
1998
16.
Snow
V
,
Weiss
KB
,
Mottur-Pilson
C
Clinical Efficacy Assessment Subcommittee of the American College of Physicians
:
The evidence base for tight blood pressure control in the management of type 2 diabetes mellitus
.
Ann Intern Med
138
:
587
-
592
,
2003
17.
van Leiden
HA
,
Dekker
JM
,
Moll
AC
,
Nijpels
G
,
Heine
RJ
,
Bouter
LM
,
Stehouwer
CD
,
Polak
BC
:
Blood pressure, lipids, and obesity are associated with retinopathy: the Hoorn study
.
Diabetes Care
25
:
1320
-
1325
,
2002
18.
Klein
R
,
Sharrett
AR
,
Klein
BE
,
Moss
SE
,
Folsom
AR
,
Wong
TY
,
Brancati
FL
,
Hubbard
LD
,
Couper
D
ARIC Group
:
The association of atherosclerosis, vascular risk factors, and retinopathy in adults with diabetes: the Atherosclerosis Risk in Communities study
.
Ophthalmology
109
:
1225
-
1234
,
2002
19.
Boulton
M
,
Foreman
D
,
Williams
G
,
McLeod
D
:
VEGF localisation in diabetic retinopathy
.
Br J Ophthalmol
82
:
561
-
568
,
1998
20.
Diabetic Retinopathy Study Research Group
:
Photocoagulation treatment of proliferative diabetic retinopathy: clinical application of Diabetic Retinopathy Study (DRS) findings, DRS Report Number 8
.
Ophthalmology
88
:
583
-
600
,
1981
21.
ETDRS Research Group
:
Early photocoagulation for diabetic retinopathy (ETDRS report number 9)
.
Ophthalmology
98
(
5 Suppl.
):
766
-
785
,
1991
22.
ETDRS Study Research Group
:
Photocoagulation for diabetic macular edema (ETDRS report number 1)
.
Arch Ophthalmol
103
:
1796
-
1806
,
1985
23.
ETDRS Study Group
:
Effects of aspirin treatment on diabetic retinopathy (ETDRS report number 8)
.
Ophthalmology
. 
98
(
5 Suppl.
):
757
-
765
,
1991
24.
DRVS Research Group
:
Early vitrectomy for severe proliferative diabetic retinopathy in eyes with useful vision: results of a randomized trial (DRVS report number 3)
.
Ophthalmology
95
:
1307
-
1320
,
1988
25.
DRVS Research Group
:
Early vitrectomy for severe vitreous hemorrhage in diabetic retinopathy: four year results of a randomized trial (DRVS report number 5)
.
Arch Ophthalmol
108
:
958
-
964
,
1990
26.
American Diabetes Association
:
Standards of medical care in diabetes—2009
.
Diabetes Care
32
(
Suppl. 1
):
S13
-
S61
,
2009
27.
American Academy of Ophthalmology Retina Panel
:
Preferred practice pattern guidelines: diabetic retinopathy
.
San Francisco
,
American Academy of Ophthalmology
,
2008
. Available online from http://one.aao.org/CE/PracticeGuidelines/PPP_Content.aspx?cid=d0c853d3-219f-487b-a524-326ab3cecd9a
28.
Davis
RM
,
Fowler
S
,
Bellis
K
,
Pockl
J
,
Al Pakalnis
V
,
Woldorf
A
:
Telemedicine improves eye examination rates in individuals with diabetes: a model for eye-care delivery in underserved communities
.
Diabetes Care
26
:
2476
,
2003
29.
ETDRS Research Group
:
Grading diabetic retinopathy from stereoscopic color fundus photographs: an extension of the modified Airlie House classification (ETDRS report number 10)
.
Ophthalmology
98
(
5 Suppl.
):
786
-
806
,
1991
30.
Harding
SP
,
Broadbent
DM
,
Neoh
C
,
White
MC
,
Vora
J
:
Sensitivity and specificity of photography and direct ophthalmoscopy in screening for sight threatening eye disease: the Liverpool Diabetic Eye Study
.
BMJ
311
:
1131
-
1135
,
1995
31.
Kalm
H
,
Egertsen
R
,
Blohmé
G
:
Nonstereo fundus photography as a screening procedure for diabetic retinopathy among patients with type II diabetes: compared with 60D enhanced slit-lamp examination
.
Acta Ophthalmol (Copenh)
67
:
546
-
553
,
1989
32.
Hutchinson
A
,
McIntosh
A
,
Peters
J
,
O'Keeffe
C
,
Khunti
K
,
Baker
R
,
Booth
A
:
Effectiveness of screening and monitoring tests for diabetic retinopathy: a systematic review
.
Diabet Med
17
:
495
-
506
,
2000
33.
Scanlon
PH
,
Malhotra
R
,
Greenwood
RH
,
Aldington
SJ
,
Foy
C
,
Flatman
M
,
Downes
S
:
Comparison of two reference standards in validating two field mydriatic digital photography as a method of screening for diabetic retinopathy
.
Br J Ophthalmol
87
:
1258
-
1263
,
2003
34.
Boucher
MC
,
Gresset
JA
,
Angioi
K
,
Olivier
S
:
Effectiveness and safety of screening for diabetic retinopathy with two nonmydriatic digital images compared with the seven standard stereoscopic photographic fields
.
Can J Ophthalmol
38
:
557
-
568
,
2003
35.
Bursell
SE
,
Cavallerano
JD
,
Cavallerano
AA
,
Clermont
AC
,
Birkmire-Peters
D
,
Aiello
LP
,
Aiello
LM
Joslin Vision Network Research Team
:
Stereo nonmydriatic digital-video color retinal imaging compared with Early Treatment Diabetic Retinopathy Study seven standard field 35-mm stereo color photos for determining level of diabetic retinopathy
.
Ophthalmology
108
:
572
-
585
,
2001
36.
Cavallerano
AA
,
Cavallerano
JD
,
Katalinic
P
,
Tolson
AM
,
Aiello
LP
,
Aiello
LM
Joslin Vision Network Clinical Team
:
Use of Joslin Vision Network digital-video nonmydriatic retinal imaging to assess diabetic retinopathy in a clinical program
.
Retina
23
:
215
-
223
,
2003
37.
Williams
GA
,
Scott
IU
,
Haller
JA
,
Maguire
AM
,
Marcus
D
,
McDonald
HR
:
Single-field fundus photography for diabetic retinopathy screening: a report by the American Academy of Ophthalmology
.
Ophthalmology
111
:
1055
-
1062
,
2004
38.
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: a comparison with ophthalmoscopy and standardized mydriatic color photography
.
Am J Ophthalmol
134
:
204
-
213
,
2002
39.
Vujosevic
S
,
Benetti
E
,
Massignan
F
,
Pilotto
E
,
Varano
M
,
Cavarzeran
F
,
Avogaro
A
,
Midena
E
:
Screening for diabetic retinopathy: 1 and 3 nonmydriatic 45-degree digital fundus photographs vs 7 standard Early Treatment Diabetic Retinopathy Study fields
.
Am J Ophthalmol
148
:
111
-
118
,
2009
40.
Massin
P
,
Chabouis
A
,
Erginay
A
,
Viens-Bitker
C
,
Lecleire-Collet
A
,
Meas
T
,
Guillausseau
PJ
,
Choupot
G
,
André
B
,
Denormandie
P
:
OPHDIAT: a telemedical network screening system for diabetic retinopathy in the Ile-de-France
.
Diabetes Metab
34
:
227
-
234
,
2008
41.
Chabouis
A
,
Berdugo
M
,
Meas
T
,
Erginay
A
,
Laloi-Michelin
M
,
Jouis
V
,
Guillausseau
PJ
,
M'bemba
J
,
Chaine
G
,
Slama
G
,
Cohen
R
,
Reach
G
,
Marre
M
,
Chanson
P
,
Vicaut
E
,
Massin
P
:
Benefits of OPHDIAT, a telemedical network to screen for diabetic retinopathy: a retrospective study in five reference hospital centres
.
Diabetes Metab
35
:
228
-
232
,
2009
42.
Rudnisky
CJ
,
Tennant
MT
,
Weis
E
,
Ting
A
,
Hinz
BJ
,
Greve
MD
:
Web-based grading of compressed stereoscopic digital photography versus standard slide film photography for the diagnosis of diabetic retinopathy
.
Ophthalmology
114
:
1748
-
1745
,
2007
43.
Chaum
E
,
Karnowski
TP
,
Govindasamy
VP
,
Abdelrahman
M
,
Tobin
KW
:
Automated diagnosis of retinopathy by content-based image retrieval
.
Retina
28
:
1463
-
1477
,
2008
44.
Sinclair
SH
,
Delvecchio
C
:
The internist's role in managing diabetic retinopathy: screening for early detection
.
Cleve Clin J Med
71
:
151
-
159
,
2004
45.
Farley
TF
,
Mandava
N
,
Prall
FR
,
Carsky
C
:
Accuracy of primary care clinicians in screening for diabetic retinopathy using single-image retinal photography
.
Ann Fam Med
6
:
428
-
434
,
2008