Review

Incidence and progression of diabetic retinopathy:

a systematic review
Charumathi Sabanayagam, Riswana Banu, Miao Li Chee, Ryan Lee, Ya Xing Wang, Gavin Tan, Jost B Jonas, Ecosse L Lamoureux, Ching-Yu Cheng,
Barbara E K Klein, Paul Mitchell, Ronald Klein, C M Gemmy Cheung, Tien Y Wong

Diabetic retinopathy is a leading cause of vision impairment and blindness. We systematically reviewed studies Lancet Diabetes Endocrinol 2018
published from Jan 1, 1980, to Jan 7, 2018, assessed the methodological quality, and described variations in incidence Published Online
of diabetic retinopathy by region with a focus on population-based studies that were conducted after 2000 (n=8, July 10, 2018
http://dx.doi.org/10.1016/
including two unpublished studies). Of these eight studies, five were from Asia, and one each from the North
S2213-8587(18)30128-1
America, Caribbean, and sub-Saharan Africa. The annual incidence of diabetic retinopathy ranged from 2∙2% to
Singapore Eye Research
12∙7% and progression from 3∙4% to 12∙3%. Progression to proliferative diabetic retinopathy was higher in Institute, Singapore National
individuals with mild disease compared with those with no disease at baseline. Our Review suggests that more Eye Centre, Singapore
high-quality population-based studies capturing data on the incidence and progression of diabetic retinopathy with (C Sabanayagam PhD,
R Banu DipSci,
stratification by age and sex are needed to consolidate the evidence base. Our data is useful for conceptualisation and
M L Chee BSc, R Lee MBBS,
development of major public health strategies such as screening programmes for diabetic retinopathy. G Tan PhD,
Prof E L Lamoureux PhD,
Introduction the review in accordance with the Preferred Reporting C-Y Cheng PhD,
C M G Cheung MD,
Diabetes affected an estimated 415 million people Items for Systematic Reviews and Meta-analysis guide­
Prof T Y Wong PhD);
worldwide in 2015, with the number expected to rise to lines.18 A comprehensive search of PubMed was Ophthalmology and Visual
642 million by 2040.1 With the rising prevalence of diabetes conducted to identify studies published from Jan 1, 1980, Sciences Academic Clinical
and increasing numbers of people with diabetes living until Jan 7, 2018. Keywords in title and abstract were Program, Duke-NUS Medical
School, Singapore
longer, the number of people with diabetic retinopathy and combined using “OR”/“AND” operators and included (C Sabanayagam, G Tan,
visual impairment due to this disease is rising worldwide.2 the following: “incidence”, “development”, “progression”, Prof E L Lamoureux, C-Y Cheng,
Although there have been many studies on the and “diabetic retinopathy”. Studies with­ out full-text C M G Cheung, Prof T Y Wong);
prevalence of diabetic retinopathy, with systemic reviews articles and duplicates were discarded. In order not to Duke-NUS Medical School,
National University of
summarising global estimates of prevalence across miss out on potentially useful articles, references cited Singapore, Singapore
regions,3 there are fewer studies reporting on the inci­ in key articles were also searched manually. After the (C Sabanayagam, G Tan,
dence. In particular, there is no systematic review of initial search was performed, studies were screened for Prof E L Lamoureux, C-Y Cheng,
incidence or progression of diabetic retinopathy despite eligibility. Relevance of studies was assessed at first using Prof T Y Wong); Yong Loo Lin
School of Medicine, National
multiple individual studies.4−16 Interpreting incidence their titles and abstracts and finally by full review of University of Singapore,
data from such different studies is challenging because the articles. Searching and eligibility were carried out Singapore (Prof E L Lamoureux,
of wide variation in estimates between countries and independently by two investigators (RL and RB), and C-Y Cheng, Prof T Y Wong);
regions, due to differences in study methods, type of inclusion was discussed with the first author (CS). Beijing Institute of
Ophthalmology, Beijing
diabetes, and time trends. A systematic review previously Studies were eligible for inclusion if they were original Tongren Eye Center, Beijing
examining the progression of diabetic retinopathy to research reports describing incidence or progression Tongren Hospital, Capital
proliferative diabetic retinopathy and severe visual loss, of diabetic retinopathy, or both. Additional criteria for Medical University, and Beijing
showed declining progression since 1980 in high-income inclusion based on full-text review were as follows: Ophthalmology & Visual
Sciences Key Laboratory,
countries.17 However, little is known about the incidence (1) prospective or retrospective cohort studies that Beijing, China (Y X Wang MD,
and progression of the disease in other parts of the world, provided estimates of incidence or progression or pro- Prof J B Jonas MD); Department
which now bear the major burden of diabetes, such as vided data from which incidence or progression could be of Ophthalmology, Medical
Faculty Mannheim of the
China7,16 and India.11 Robust data on incidence and calculated in a defined population (population or clinic-
Ruprecht-Karls-University
progression of diabetic retinopathy are important for based) with diabetes, (2) follow-up duration of at least Heidelberg, Mannheim,
development of major public health strategies such as 2 years, (3) a sample size of at least 100 participants at Germany (Prof J B Jonas);
screening programmes. baseline, and (4) studies published in English language Department of Ophthalmology
and Visual Sciences, University
To address this gap, we conducted a systematic review only. Studies were excluded if: (1) they were clinical
of Wisconsin School of Medicine
to estimate the global incidence of diabetic retinopathy, trials, (2) they did not report original data (eg, reviews, and Public Health, Madison, WI,
and to describe variations by region, study characteristics, editorials), (3) full-text was not available, (4) the study USA (Prof B E K Klein MD,
and time period in which the studies were conducted. population was dynamic (where participants enter and Prof R Klein MD); Centre for
Vision Research, University of
We assessed progression as a secondary outcome. leave the cohort at various points in time—eg, most
Sydney, Sydney, NSW, Australia
of the diabetic retinopathy screening studies), and (Prof P Mitchell PhD)
Methods (5) reported incidence (>70%) was markedly out of the Correspondence to:
Search strategy and selection criteria range of previously reported data. Wherever possible, if Prof Tien Y Wong, Singapore
For this Review, we conducted a systematic search of the published estimates were inadequate or did not fit National Eye Centre,
Singapore 168751
the literature on incidence and progression of diabetic into our reporting scheme (eg, Beijing Eye Study), we
ophwty@nus.edu.sg
retinopathy using the PubMed database. We conducted contacted the study investigators to clarify the estimates.

www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1 1

 Review
(1a) Study characteristics
Study setting
Study location
Authorship
Study period
(1b) Population characteristics
Age at baseline
Sex
Race or ethnicity
Type of diabetes
Duration of diabetes
(1c) Methodological characteristics
Incidence estimates
Follow-up duration
Method of DR diagnosis
Classification system used to
define DR
Severity levels of incident DR
DR=diabetic retinopathy.
Table 1: Data extraction elements from the included studies
See Online for appendix
Besides the published studies, we included data from
two of our recently completed studies: the Singapore
Malay Eye Study (SiMES),19 and the Singapore Indian Eye
2 www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1
Study (SINDI).20 Incidence of diabetic retinopathy in
Elements
SiMES and SINDI has not been published before. Brief
methods of the SiMES and SINDI cohort studies have
Population, clinic been detailed in the appendix.
North America, Europe, Asia, Africa, Caribbean, and Australia
First author Data extraction and quality assessment
Year of publication A data extraction spreadsheet was used to collect
information on study and participant characteristics
Mean age (years) from each of the included studies (table 1). We assessed
Male, female the quality of the included studies, using a modified
White, black, Asian, and Hispanic version of the Risk of Bias tool developed by Hoy and
Type 1, type 2, unspecified colleagues.21 The domains assessed included study
Mean (years) setting, study design, study population, method of
ascertainment of diabetic retinopathy, demonstration
Number at risk at baseline, number of cases (including severity) at follow-up that the outcome of interest was not present at the start
Year of baseline exam, and year of diagnosis of the study, reporting of outcome in sex subgroups, and
Fundus photography, ophthalmoscopy, slit-lamp biomicroscopy information on severity level of incident cases (table 2).
Early Treatment of Diabetic Retinopathy Study (ETDRS), International Clinical Scores ranged from 0 to 8, with 0 representing good
Diabetic Retinopathy and Diabetic Macular Edema (DME) Severity Scale quality. Based on the total score, studies were classified to
Mild, moderate, severe, and proliferative have lower (scores 0–2) or higher risk of bias (scores ≥5).
Since treatment strategies have changed over the
years and public health efforts to curtail the burden of
diabetic retinopathy have evolved since the year 2000,
we stratified the studies by study period (before 2000 vs
after 2000) to make comparisons more robust and to
Low risk of bias High risk of bias
obtain contemporary incidence data that are crucial to
decide interventions.
Study setting
Population or community 0 ∙∙
Assessment of diabetic retinopathy from retinal
Clinic or hospital ∙∙ 1
photographs
Study design
Most of the studies9,15,16,22 graded retinal photographs for
Prospective cohort 0 ∙∙ diabetic retinopathy according to the Early Treatment of
Retrospective cohort ∙∙ 1 Diabetic Retinopathy Study (ETDRS) protocol.15 The
Diabetes type Nakuru Eye study4 graded disease based on the UK national
Specified as type 1 or type 2 0 ∙∙ guidelines on screening for diabetic retinopathy.23 The
Combined or unspecified ∙∙ 1 Sankara Nethralaya-Diabetic Retinopathy Epidemiology
Ascertainment of DR and Molecular Genetics Study II (SN-DREAMS-II),11 and
Retinal photographs 0 ∙∙ the Beixinjing Community study7 used the International
Ophthalmoscopy, slit-lamp ∙∙ 1 Clinical Diabetic Retinopathy and Diabetic Macular Edema
biomicroscopy
(DME) Severity Scale.24
Exclusion of prevalent DR
Documented excluding those with 0 ∙∙ ETDRS protocol
prevalent DR at baseline
For each eye, retinopathy severity score was assigned
Not documented ∙∙ 1
according to the ETDRS adaptation of the modified Airlie
Sex subgroups
House Classification System (table 3).25 Retinopathy
Reported 0 ∙∙
severity was categorised as minimal (level 20), mild
Not reported ∙∙ 1
(level 35), moderate (level 43 to 47), or severe (level 53)
Severity of incident cases
non-proliferative diabetic retinopathy, and proliferative
Reported 0 ∙∙
diabetic retinopathy (level >60). On the basis of the
Not reported ∙∙ 1
severity score of the worse eye, incident disease was
DR=diabetic retinopathy. defined as development of any new diabetic retinopathy
(defined as score level 20 and above in at least one eye) at
Table 2: Risk of bias items assessed in the included studies
the follow-up among those who had no retinopathy at
baseline25 (ETDRS level 10/10 in both eyes) at baseline. All
those with some form of diabetic retinopathy (ETDRS
level ≥20) but without proliferative disease (level ≥60)
were included for assessing progression. For assessing

progression, the retinopathy level of each participant was
derived by concatenating the levels for the two eyes,
giving the eye with the higher level greater weight. This
scheme provides a 15-step scale (10/10, 14–15/10,
14–15/14–15, 20/<20, 20/20, 35/<35, 35/35, 43/<43, 43/43,
47/<47, 47/47, 53/<53, 53/53, 60+/<60+, 60+/60+), with all
levels of proliferative disease grouped as one step. For the
purposes of this study, an increase of two or more steps
on the 15-step scale at the follow-up assessment from
the baseline examination was considered to indicate
disease progression. To assess whether those with mild
retinopathy had higher prevalence of progression to
proliferative diabetic retinopathy compared with those
with no retinopathy at baseline, we defined incident
proliferative disease as development of new proliferative
diabetic retinopathy (level 60 and above) in either eye
among those with no retinopathy at baseline in either eye
and progression from mild disease to proliferative disease
as progression from minimal–mild diabetic retinopathy
(level 20–35) in the worse eye at baseline to proliferative
diabetic retinopathy (level ≥60) at follow-up.26,27 Few
studies, however, included those with “no retinopathy” at
baseline for defining progression.26,27 To standardise our
definition, we recalculated progression in these studies
according to our definition.
Under the International Clinical Diabetic Retinopathy
and DME Severity Scale24 and the UK national Guidelines
on Screening for Diabetic Retinopathy,23 diabetic
retinopathy was graded according to the following levels
of retinopathy: no diabetic retinopathy, mild, moderate,
or severe non-proliferative diabetic retinopathy, and
proliferative diabetic retinopathy. Incidence was defined
as those who showed no diabetic retinopathy at baseline
but developed some retinopathy during follow-up.
Progression was defined as those who showed some
diabetic retinopathy at baseline with subsequent increase
in the severity of disease, as two-step progression (prog-
ression of diabetic retinopathy from mild to severe
non-proliferative diabetic retinopathy and moderate
non-proliferative disease to proliferative disease). Lesions
characteristic of each level are detailed in the appendix.
Incidence was calculated as cumulative incidence—
ie, incidence proportion. Because studies varied in
length of follow-up, we subsequently calculated annual
incidence on the basis of exponential assumption using
the formula −ln (1−S)/t, where S is the proportion of new
cases (number of new cases at follow-up divided by
number at risk at baseline) over t years and t is the time
of follow-up.28 Similar to the incidence estimates, we
calculated the cumulative progression (over the entire
follow-up period) and the annual progression.
We classified studies as before 2000 if the study period
ended before the end of Dec 31, 1999, irrespective of the
publication date. This is because some studies were
conducted before 2000, but published their findings
several years later. For example, the Diabetes Incidence
Study in Sweden (DISS)6 was conducted between 1987 and
www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1 3
Review
Severity Lesions
10 No retinopathy No retinopathy
14–15 Questionable DR >1 haemorrhage present but microaneurysms absent
20 Minimal NPDR Microaneurysms only
35 Mild NPDR Hard exudates; cotton wool spots or mild retinal haemorrhages, or both
43 Moderate NPDR Moderate haemorrhages in four fields or severe in one field, or mild
intraretinal microvascular abnormalities (IRMA) in one to three fields
47 Moderately Both characteristics from level 43 or IRMA in four fields, or both, severe
severe NPDR haemorrhages in two to three fields, and venous beading in one field
53 Severe NPDR Two or more characteristics from level 47 or severe retinal haemorrhages in
four fields, or both; moderate to severe IRMA in one field; and venous
beading in at least two fields
61 Mild PDR NVE, 0∙5 disk area in at least one field, or presence of laser scars in the
periphery consistent with panretinal photocoagulation
65 Moderate PDR NVE, 0∙5 disk area in at least one field or NVD, or both, graded less than
standard photo 10A
71 Severe PDR VH or PRH, or both equal to or exceeding one disk area; NVE equal to or
exceeding half disk area with VH or PRH, or both; NVD less than standard
photo 10A with VH or PRH, or both; and NVD equal to or exceeding
standard photo 10A
81 and 85 Advanced PDR Macula obscured by VH or PRH; or retina detached at the centre of the
macula, or all of these
ETDRS=Early Treatment of Diabetic Retinopathy Study. DR=diabetic retinopathy. NPDR=non-proliferative DR.
NVD=new vessels on disk. NVE=new vessels everywhere. PDR=proliferative DR. PRH=preretinal haemorrhage.
VH=vitreous haemorrhage.
Table 3: Adaptation from ETDRS classification of diabetic retinopathy level25
1988 (baseline) and 1994 (follow-up), the Atherosclerosis
Risk in Communities study (ARIC)29 between 1993 and
1996, and the first follow-up of the Barbados Incidence
Study of Eye Diseases (BISED-I)8 between 1987−1992 and
1992−1997. All these studies, however, published their
findings after 2000. To obtain contemporary data on
incidence, we focused our review on investigations
conducted after 2000, but included the data in table 4 as
historical data. Within the group of studies conducted
after 2000, we estimated and compared the annual
incidence of diabetic retinopathy by study region, type of
diabetes, duration of diabetes, follow-up duration, and
method of ascertain­ment of diabetic retinopathy. We also
assessed the effect of major risk factors for diabetic
retinopathy including age, sex, ethnicity, duration of
diabetes, glycaemic control (as established by the level of
HbA1c), and hypertension wherever data were available.
Results
We identified 561 studies with our initial strategy
(figure 1) and excluded 495 that were not relevant. We
reviewed the full text of 66 articles and, of these, 24 met
our inclusion criteria. Including two additional studies
that had individual-level data, we included 26 articles in
total for the outcome, incident diabetic retinopathy, of
which we included 14 articles for the outcome,
progression of diabetic retinopathy. Of the 26 studies,
14 studies were conducted in general populations or
communities4,6−9,11,14−16,26,27,29 and 12 studies in clinic or
hospital settings.5,10,12,13,30−37 We initially included both
 Review

Region Follow-up Diabetes Diabetes Age at Ethnicity Number Number at Cumulative Annual Year of Year of
duration, type duration, baseline, of risk (cases) incidence, incidence, baseline follow-up
years years years fundus % % exam exam
fields
Studies conducted after 2000
SN-DREAMS-II, Raman et al, India, South Asia 4 2 5∙3 55∙4 Indian 2 757 (70) 9∙2% 2∙4% 2003–06 2007–11
201711
Nakuru Eye Disease Cohort Study, Sub-Saharan 6 1 and 2 NA 50 Africans 2 44 (31) 18∙6% 3∙4% 2007–08 2012–14
Bastawrous et al, Kenya, 20174 Africa
BES, Xu et al, China, 201416 East Asia 10 1 and 2 5∙7 62∙1 Chinese 2 117 (23) 19∙7% 2∙2% 2001 2011
Beixinjing community, Jinet et al, East Asia 5 2 11∙0 66∙1 Chinese 2 322 (151) 46∙9% 12∙7% 2007 2012
China, 20147
LALES, Varma et al, USA, 201015 North 4 1 and 2 ≥10 years 30 Mexican 7 535 (182) 34∙0% 10∙4% 2000–03 2004–08
America =47% American
Barbados Incidence Study of Eye Caribbean 9 2 7∙3 57∙6 Black, white, 2 324 (128) 39∙5% 5∙6% 1987–92 1997–03
Diseases (BISED-II), Leske et al, others
Caribbean, 20069
SiMES, Singapore, unpublished South east 6 2 4∙2 58∙9 Malay 2 334 (62) 18∙6% 3∙4% 2004–06 2011–13
(2004–07) Asia
SINDI, Singapore, unpublished South east 6 2 5∙4 58∙2 Indian 2 492 (93) 18∙9% 3∙5% 2007–09 2013–15
(2007–09) Asia
Studies conducted before 2000
BISED-I, Leske et al, Caribbean, 20038 Caribbean 4 2 6∙5 57∙6 Black, white, 2 306 (92) 30∙1% 9∙0% 1987–92 1992–97
others
ARIC study, Wong et al, USA, 200829 North 3 1 and 2 NA Black, white 2 119 (12) 10∙1% 3∙6% 1993–95 1996
America
DISS, Henricsson et al, Sweden, 20036 Western 10 1 10∙0 35∙3 White 2 627 (247) 39∙4% 5∙0% 1987–88 1994
Europe
San Luis Valley Diabetes Study, North 4 2 4∙8 58∙1 Hispanic or 3 169 (47) 27∙8% 8∙1% 1984–88 1988–92
Tudor et al, Colorado, 199814 America non-Hispanic
whites
WESDR <30 years, Klein et al, USA, North 4 1 13∙8 28∙3 White 7 271 (160) 59∙0% 22∙3% 1980–82 1984–86
198927 America
WESDR ≥30 years, Klein et al, USA, North 4 2 14∙5 63∙1 White 7 474 (183) 38∙6% 12∙2% 1980–82 1984–86
198926 America

SN-DREAMS-II=Sankara Nethralaya-Diabetic Retinopathy Epidemiology and Molecular Genetics Study II. NA=not applicable. BES=Beijing Eye Study. LALES=Los Angeles Latino Eye Study. BISED-II=Barbados
Incidence Study of Eye Diseases, second follow-up. SiMES=Singapore Malay Eye Study. SINDI=Singapore Indian Eye Study. ARIC=Atherosclerosis Risk in Communities. DISS=Diabetes Incidence Study in Sweden.
WESDR=Wisconsin Epidemiologic Study of Diabetic Retinopathy.

Table 4: Description of studies included in the systematic review stratified by study period

population-based and clinic-based studies in the Review.
However, since the quality of clinic-based studies was
lower (nine of 12 had scores ≥3) compared with
population-based studies (ten of 14 studies had scores of
0 or 1), to minimise bias, we excluded clinic-based
studies from further review. In general, clinic studies
with lower quality scores had retrospective study design,
used ophthalmoscopy for assessing diabetic fundus
changes, and did not include information on the type of
diabetes, severity of disease, and sex-specific estimates.
Information on the study characteristics of the 12 clinic-
based studies are included in the appendix.
Characteristics of studies conducted after 2000
Among the 14 population-based studies (table 4),
eight were conducted after 2000: SN-DREAMS-II,11 the
Nakuru Eye Disease Cohort Study,4 the Beijing Eye
Study (BES),16 the Beixinjing community study,7 the
Los Angel-es Latino Eye Study (LALES),15 the Barbados
Incidence Study of Eye Diseases, second follow-up
(BISED-II),9 SiMES, and SINDI. The mean age of the
study participants at baseline ranged from 30 years in
LALES to 66∙1 years in the Beixinjing study.7 Ethnicity of
the study population included white, black, Hispanic,
African, and Asian (Chinese, Malay, and Indian). Sample
sizes ranged from 117 in BES16 to 757 in SN-DREAMS-II.11
Study population included type 2 diabetes in five studies
and an unspecified type in three studies.4,15,16 Whereas
seven studies included those with newly diagnosed
diabetes, the Beixinjing study in China7 included
those with previously diagnosed diabetes only. Annual
incidence ranged from 2∙2% in BES16 to 12∙7% in the
Beixinjing study.7
Incidence by region
Figure 2 shows the annual incidence of diabetic
retinopathy stratified by region and by period of study.
Of the eight studies conducted after 2000, five were from

4 www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1


Asia, and one each from North America (LALES),15
the Caribbean (BISED-II),9 and sub-Saharan Africa
(Nakuru study).4 Asian studies included: SN-DREAMS-II
(India),11 BES (China),16 the Beixinjing community study
(China),7 and SiMES and SINDI (Singapore). Annual
incidence was 10∙4% in LALES, 5∙6% in BISED-II, and
3∙4% in the Nakuru Study. Within Asia, annual incidences
were 2∙4% in SN-DREAMS-II, 2∙2% in BES, 12∙7% in
the Beixinjing study, 3∙4% in SiMES, and 3∙5% in SINDI.
Incidence by type of diabetes
None of the studies conducted after 2000 reported
incidence in type 1 diabetes. Five studies included
participants with type 2 diabetes,7,9,11 whereas three did
not identify the type of diabetes (mixed).4,15,16 Incidence in
those involving type 2 diabetes ranged from 2∙4% in
SN-DREAMS-II to 12∙7% in the Beixinjing community
study in China.7 The three studies including both
participants with type 1 and type 2 diabetes had annual
incidences of 2∙2% (BES), 3∙4% (Nakuru study), and
10∙4% (LALES).
Incidence by duration of diabetes
Mean duration of diabetes ranged from 4 to 6 years in
SN-DREAMS-II, BES, SiMES, and SINDI, to 7∙3 years in
BISED-II9, and to 11∙0 years in the Beixinjing community
study.7 Annual incidence in the studies with a mean
diabetes duration of 4–6 years ranged from 2∙2% in BES
to 3∙5% in SINDI. Incidence was higher in studies
with a higher duration of diabetes such as BISED-II
(incidence 5∙6%, mean duration of diabetes 7∙3 years),
the Beixinjing study (12∙7%, 11 years), and LALES (10∙4%,
and 47% had 10 years and above diabetes duration).
Incidence by follow-up duration
The duration of follow-up was 4 years in SN-DREAMS-II
and LALES, 5–6 years in the Beixinjing community
study, Nakuru, SiMES, and SINDI, and 9–10 years in
BISED-II and BES. Annual incidence in studies with
4 years of follow-up was 2∙4% (SN-DREAMS-II) and
10∙4% (LALES), and the incidence in 5–6 years of
follow-up ranged from 3∙4% (Nakuru, SiMES) to
12∙7% in the Beixinjing community study in China.7
Incidence in studies with 9–10 years of follow-up was
2∙2% in BES and 5∙6% in BISED-II.
Incidence by method of diagnosis
All studies used two-field fundus photography to
detect diabetic retinopathy, except LALES, which used
seven-field photography. The annual incidence in studies
that used two-field photo and ETDRS classification9,16
ranged from 2∙2% in BES16 to 5∙6% in BISED-II.9 The
incidence in LALES,15 which used a seven-field photo and
ETDRS scheme, was 10∙4%. Incidence in studies that
used other systems of classification was 3∙4% in the
Nakuru study, 2∙4% in SN-DREAMS-II,11 and 12∙7% in
the Beixinjing study.7
www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1 5
Review
Identification 896 articles searched from PubMed with key terms
Screening 561 titles and abstracts screened after applying filters
495 studies were not relevant
Eligibility 66 full-text articles for eligibility evaluation
45 articles excluded
27 dynamic population
5 small sample size
6 overwhelming incidence
2 trial
1 unable to get full-text
4 numbers not does given
Included 24 included studies from the search
2 unpublished with individual-level data
26 total studies included in the review
12 clinical studies excluded
14 population studies included
Figure 1: Selection process of articles in the Review (n=14)
Incidence in studies conducted before year 2000
Six population-based studies were conducted before year
2000, four of which were from the USA (the ARIC
study,29 the San Luis Valley Diabetes Study,14 the
Wisconsin Epidemiologic Study of Diabetic Retinopathy
(WESDR) <30 years,27 and the WESDR ≥30 years),26 and
one study each from the Caribbean (BISED-I)8 and
western Europe (Diabetes Incidence Study in Sweden
[DISS]).6 The follow-up assessment period ranged from
1984–86 in the WESDR studies to 1992–97 in BISED-I.
The annual incidence of diabetic retinopathy ranged
from 3∙6% in ARIC (type 1 and 2 diabetes) to 22∙3% in
WESDR<30 years. The annual incidence in studies
including type 1 diabetes was 5∙0% (DISS) and
22∙3% (WESDR<30 years); in studies with type 2
diabetes, incidence was 9∙0% in BISED-1 and 8∙1% in
the San Luis study.14 In the San Luis Study, 4-year
incidence was similar in Hispanic and non-Hispanic
white people with no significant difference (p=0∙38).
Risk factors and incident disease in contemporary
studies
Table 5 shows the incidence of diabetic retinopathy within
risk factor groups or association of risk factors with
incident disease in the eight population-based studies.
 Review

Before 2000 After 2000 (SN-DREAMS-II, Beixinjing community study, SiMES,

25 and SINDI) that assessed HbA1c as a risk factor. Effect
22·3 estimates ranged from 1∙1 to 1∙4.
20 Four studies assessed hypertension as a risk factor
(Nakuru, Beixinjing study, SiMES, and SINDI). However,
15
hypertension was significantly associated with incident
Incidence (%)

diabetic retinopathy in the Beixinjing study only.

12·2 12·7
Incidence of diabetic retinopathy increased with
10 10·4
9·0 increasing duration of diabetes in SN-DREAMS-II,
8·1
LALES, and SiMES. In BISED-II, incidence increased
5·6
5 5·0 4·8 from under 4 years until 14 years, after which a significant
3·5 3·4 3·5
2·4 2·2 decline was noted. In the Beixinjing study, incidence
0 was highest in those with less than 10 years duration
and decreased after 10 years. Incidence by duration of
WESDR <30, 1984–86

WESDR ≥30, 1984–86

San Luis, 1988–92

ARIC, 1996

DISS, 1994

BISED-I, 1992–97

SN-DREAMS-II, 2007–11

BES, 2011

Beixinjing, 2012

SiMES, 2011–13

SINDI, 2013–15

LALES, 2004–08

BISED-II, 1997–2003

Nakuru study, 2012–14

diabetes was not significant in BES and SINDI.
Five studies conducted after 2000 documented pro-
gression (any progression), of which three were from
Asia (SN-DREAMS-II, SiMES, and SINDI), and one each
from the USA (LALES) and sub-Saharan Africa (Nakuru)
(figure 3). Annual progressions in the Asian studies were
Asia US Other
pe

US
rs

3∙4%, 5∙0%, and 5∙3%. Annual progression was 4∙1% in

he
ro
Eu

Ot

the Nakuru study and 12∙3% in LALES.

Figure 2: Trends in the annual incidence of diabetic retinopathy in population-based studies
*Within each region, the studies are arranged by the year of ascertainment of diabetic retinopathy status (earliest
to latest). Progression to proliferative disease
Table 6 shows incident proliferative diabetic retinopathy
versus progression from mild to proliferative diabetic
The incidence of diabetic retinopathy decreased with retinopathy (in those with any diabetic retinopathy at
increasing age in several studies, including Nakuru baseline) stratified by study period. In studies published
study, BES, LALES, SiMES, and SINDI. The trend was after 2000, data on incident proliferative disease were
significant only in LALES (p<0∙001) and SINDI available in six studies and progression to proliferative
(p=0∙04). On the other hand, increasing age from diabetic retinopathy was available in five studies.
60 years to 80 years showed increasing incidence Annual incidence of proliferative disease ranged from
(p=0∙04) in the Beixinjing community study.7 In 0∙03% in SINDI to 0∙72% in the Nakuru Study.4 Annual
BISED-II, the incidence estimates were higher in the progression from mild to proliferative diabetic retin-
youngest and the oldest age groups.9 The incidences opathy ranged from 0% in the Nakuru Eye Study4
across age groups were not significant in the Nakuru to 1∙5% in SN-DREAMS-II. Progression from mild to
study4 and SN-DREAMS-II.11 proliferative diabetic retinopathy was higher than
Incidence was significantly higher in men compared in-cident proliferative diabetic retinopathy in four of the
with women in SINDI (22∙1% vs 13∙3%, p=0∙01). five studies that had data (SN-DREAMS-II, BISED-II,
A similar observation was made in SiMES, but the differ­ SiMES, and SINDI). The Nakuru Study had higher
ence was not statistically significant (20∙0% vs 14∙6%, incident proliferative disease than progression from mild
p=0∙2). The incidence was higher in women than in men disease. However, as acknowledged by the authors, the
in BES (24∙6% vs 15∙0%), BISED-II (41.8% vs 35.3%), and sample size in the Nakuru study with diabetic retinopathy
the Beixinjing community study (42∙4% vs 48∙3%), but at both timepoints was too small (n=23) to draw
the difference was not statistically significant in any study. meaningful conclusions.
Incidence was reported to be similar between men and
women in the Nakuru study.4 Discussion
Within Asian ethnic groups, the annual incidence was In this systematic review, estimating the incidence and
similar in Malays (3∙4%) and Indians (3∙5%) living in progression of diabetic retinopathy in eight population-
Singapore. Ethnicity-specific information was not available based studies conducted after 2000, the main findings
in other studies as the majority were based on a single are as follows: first, of the eight studies, five were
ethnic group—eg, BES including Chinese and BISED-II from Asia, and one each from the North America,
including people of predominantly African-American the Caribbean, and sub-Saharan Africa; second, all
ancestry. Ethnicity-specific incidence in the Nakuru Study studies included those with type 2 diabetes or unspecified
was too small to make meaningful conclusions. diabetes and none exclusively included participants with
Poor glycaemic control was significantly associated type 1 diabetes; third, the annual incidence of diabetic
with incident diabetic retinopathy in all four studies retinopathy ranged from 2∙2% in the BES to 12∙7% in

6 www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1

 Review

Age Sex Hypertension HbA1c Duration of diabetes

SN-DREAMS-II11 Age-specific estimates for age groups
40–49, 50–59, 60–69, ≥70 years:
9∙5%, 8∙4%, 10%, 9∙5% (p=0∙8)
Nakuru Eye Age-specific estimates for age groups
Disease Cohort 50–59, 60–69, 70–79, ≥80 years:
Study4 27∙3%, 28∙6%, 16∙7%, 0%, (ptrend=0∙5)
BES16 Age-specific estimates for age groups
40–49, 50–59, 60–69, ≥70 years: 37∙5%,
29∙6%, 16∙1%, 10∙0% (p=0∙09)
Beixinjing Age-specific estimates in age groups of
community7 <60, 60–70, 70–80, >80 years: 13∙3%,
32∙5%, 44∙4%, 9∙9% (p=0∙04)
LALES15 Age-specific estimates for age groups
40–49, 50–59, 60–69, ≥70 years: 45∙5%,
39∙2%, 22∙0%, 24∙3% (p<0∙001)
BISED-II9 Age-specific estimates for age groups
40–49, 50–59, 60–69, ≥70 years: 47∙0%,
38∙6%, 30∙0%, 62∙3%
SiMES Age-specific estimates for age groups
40–49, 50–59, 60–69, ≥70 years: 24∙6%,
19∙3%, 13∙8%, 18∙8% (p=0∙2)
SINDI Age-specific estimates for age groups
40–49, 50–59, 60–69, ≥70 years: 27∙6%,
19∙9%, 11∙2%, 20∙3% (p=0∙04)
NA NA Multivariable OR per unit increase 0–4, 5–9, 10–14, ≥15 years:
1∙16 (95% CI 1∙02–1∙34) 6∙1%, 7∙8%, 11∙5%, 20∙2%
(ptrend< 0∙0001).
Male vs female, age-adjusted No vs yes, NA NA
RR 0∙50 (95% CI 0∙20–1∙50) age-adjusted RR 1∙20
(95% CI 0∙40–3∙60)
Male vs female, 15% vs 24∙6% NA NA 1–4, 5–9, 10–14, ≥15 years:
(p=0∙2) 23∙8%, 12∙9%, 6∙7%, 38∙5%
(ptrend=0∙8)
Male vs female, 42∙4% vs No vs yes, multivariable Multivariable OR per unit increase <10, 10–20, 20–30, >30 years:
48∙3% (p=0∙6) OR 1∙80 (95% CI 1∙12 (95% CI 1∙01–1∙24) 51∙7%, 27∙2%, 20∙5%, 0∙7% (p=0∙9)
1∙14–2∙86)
NA NA NA New, 1–4, 5–9, 10–14, ≥15 years:
20∙4%, 34∙2%, 39∙8%, 55∙1%, 39∙5%
(p<0∙001)
Male vs female, 35∙3% vs NA NA ≤4, 5–9, 10–14, ≥15 years:
41∙8% (p=0∙3) 31∙7%, 58∙2%, 60∙0%, 38∙4%
(ptrend=0∙006)
Incidence in male vs female, No vs yes, multivariable Multivariable RR per unit increase New, 1–5, 5–10, ≥10 years=14∙7%,
20% vs 14∙6% (p=0∙2) RR 1∙26 (95% CI 1∙30 (95% CI 1∙19–1∙42), p<0∙001 13∙1%, 26∙5%, 24∙1% (ptrend=0∙04)
0∙72–2∙21), p=0∙9
Incidence in male vs female, No vs yes, multivariable Multivariable RR per unit increase New, 1–5, 5–10, ≥10 years: 15∙7%,
22∙1% vs 13∙3% (p=0∙01) RR 0∙84 (95% CI 1∙42 (95% CI 1∙29–1∙55), p<0∙001 16∙8%, 23∙1%, 19∙0% (ptrend=0∙3)
0∙56–1∙27), p=0∙5

SN-DREAMS-II=Sankara Nethralaya-Diabetic Retinopathy Epidemiology and Molecular Genetics Study II. NA=not applicable. OR=odds ratio. RR=risk ratio. BES=Beijing Eye Study. LALES=Los Angeles Latino Eye
Study. BISED-II=Barbados Incidence Study of Eye Diseases, second follow-up. SiMES=Singapore Malay Eye Study. SINDI=Singapore Indian Eye Study.

Table 5: Established risk factors and incidence of diabetic retinopathy in the eight studies conducted after year 2000

the Beixinjing community study and annual progression

Before 2000 After 2000
estimates ranged from 3∙4% in SN-DREAMS-II to 30
12∙3% in the LALES study; fourth, the progression to
proliferative disease was higher in individuals with mild 25·5
25
disease compared with those with no diabetic retinopathy
at baseline; finally, most of the studies document
20
decreasing incidence of diabetic retinopathy with
Progression (%)

increasing age, but did not find significant difference by

sex and did not identify hypertension as a risk factor. 15
Poor glycaemic control was consistently associated with 12·3
10·5
increased risk of diabetic retinopathy. 10 9·6
We found that contemporary studies include no data
from developed countries and countries with excellent 5·0 5·3
4·1
5 3·4
health-care systems such as Norway, Sweden, Australia,
Canada, and Japan. Further, all studies from the USA
were published before 2000, except LALES, and no recent 0
WESDR <30, 1984–86

WESDR ≥30, 1984–86

San Luis, 1988–92

LALES, 2004–08

SN-DREAMS, 2007–11

SiMES, 2011–13

SINDI, 2013–15

Nakuru study, 2012–14

study estimating incidence in white and black people

from the USA is available. The majority of con-temporary
studies were from Asia (five of eight). This recent surge
in Asian studies could be motivated by the excess burden
of diabetes in Asia. Around 80% of people with diabetes
are in developing countries, of which China and India
contribute to a large proportion.38 US US Asia Others
The annual incidence of diabetic retinopathy was highest
Figure 3: Annual progression of diabetic retinopathy stratified by study period and region
in the Beixinjing community study (12∙7%)7 followed *Within each region, the studies are arranged by the year of ascertainment of diabetic retinopathy status
by LALES (10∙4%)15 and BISED-II (5∙6%).9 The incidence (earliest to latest). †Progression refers to exponential progression.
was similar across the other four Asian studies, ranging
from 2∙2% to 3∙5%, although a slightly higher incidence
was found in Singapore compared with India and China.

www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1 7

 Review

Diabetes Follow-up, Incident PDR Progression from mild DR to PDR

type years
Number at Number Incidence Annual Number Number Cumulative Annual
risk of cases incidence at risk of cases progression progression
Conducted after 2000
SN-DREAMS-II11 2 4 757 11 1∙5% 0∙38% 119 7 5∙9% 1∙5%
Nakuru Eye Study4 1 and 2 6 167 7 4∙2% 0∙72% 9 0 0∙0% 0∙00%
BES16 1 and 2 10 113 6 5∙3% 0∙54% ∙∙ ∙∙ ∙∙ ∙∙
BISED-II9 2 9 324 8 2∙6% 0∙29% 109 9 8∙2% 0∙96%
SiMES 2 6 371 3 1∙0% 0∙17% 85 2 2∙0% 0∙40%
SINDI 2 6 512 1 0∙2% 0∙03% 175 2 1∙1% 0∙19%
Conducted before 2000
BISED-I8 2 4 306 6 2∙0% 0∙51% 101 7 6∙9% 1∙8%
DISS6 1 10 627 11 1∙8% 0∙18% ∙∙ ∙∙ ∙∙ ∙∙
WESDR <30 years27 1 4 271 1 0∙4% 0∙10% 303 37 12∙2% 3∙3%
WESDR ≥30 years26 2 4 474 2 0∙4% 0∙10% 293 7 2∙4% 0∙60%

DR=diabetic retinopathy. PDR=proliferative diabetic retinopathy. SN-DREAMS-II=Sankara Nethralaya-Diabetic Retinopathy Epidemiology and Molecular Genetics Study II.
BES=Beijing Eye Study. BISED-II=Barbados Incidence Study of Eye Diseases, second follow-up. SiMES=Singapore Malay Eye Study. SINDI=Singapore Indian Eye Study.
BISED-I=Barbados Incidence Study of Eye Diseases. DISS=Diabetes Incidence Study in Sweden. WESDR=Wisconsin Epidemiologic Study of Diabetic Retinopathy.

Table 6: Incident PDR and progression from mild DR to PDR in the included studies (n=10)

This finding could be due to the increased detection of
cases from the comprehensive screening programmes and
also due to the high-income lifestyle in Singapore. The
Beixinjing study had a significantly higher incidence
compared with other studies. This difference could be
attributed to the inclusion of individuals with previously
diagnosed diabetes in this study as opposed to other
studies which included those with new as well as known
diabetes. This is also evidenced by the long mean
duration of diabetes in the Beixinjing study (11 years).
The increase in the annual incidence in LALES could be
explained by the application of seven-field photographs
as well as the longer duration of diabetes in the study
population (47% with ≥10 years of duration).
Our data showed that the annual incidence was higher
in studies published before 2000 (four of six from
the USA) compared with those published after 2000.
This finding is in agreement with the results of a previous
meta-analysis, in which a decrease in the incidence of
blindness related to diabetic retinopathy was observed,
which was potentially due to concerted public health
efforts including improvement in metabolic control and
improvement in screening modalities.17 Two studies
conducted before 2000 assessed the incidence of
type 1 diabetes (DISS and the WESDR <30 years) with
incidence estimates of 5% and 22∙3%. None of the
contemporary studies assessed incidence of diabetic
retinopathy in participants with type 1 diabetes.
We found that studies with a shorter follow-up
(4–6 years) had a higher annual incidence compared with
those with a longer follow-up (9–10 years). A plausible
explanation for the difference could be that in studies
with a longer duration of follow-up, participants with a
higher incidence and a higher progression of diabetic
retinopathy might have had a higher mortality. As
expected, although incidence increased with duration of
diabetes, in general, incidence declined with duration of
more than 15 years. This trend could also be due to
selective mortality of those with longer duration of
diabetes.
The majority of the studies found a decreasing trend
(although not significant in some) in the incidence of
diabetic retinopathy with increasing age. This reverse
trend with a higher incidence in younger patients with
diabetes could represent a selective mortality of elderly
patients with diabetes and diabetic retinopathy. Alter­
natively, younger patients with diabetes might prioritise
personal and career development rather than their health
and are usually diagnosed after a long-term history of
hyperglycaemia. When stratified by sex, except for
SINDI, which found a higher incidence in men, the
remaining studies did not report a significant difference
in incidence by sex. The incidence did not differ by
ethnicity in the Singapore studies, which provided
ethnicity specific estimates. This finding is also in
agreement with the earlier-conducted San Luis Study
in the USA,14 which found no significant difference in
incidence between white and black people. The majority
of the studies (except the Beixinjing study) did not find
hypertension to be a risk factor for incident diabetic
retinopathy, whereas all four studies that assessed HbA1c
found a consistent positive association between HbA1c
and incident diabetic retinopathy.
Similar to the incidence estimates, progression
estimates were higher in the LALES study compared
with the other four studies. Progression estimates were
not available in the Beixinjing study and BISED-II,
which documented higher incident diabetic retinopathy.

8 www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1


We observed that the annual incidence of proliferative
disease was highest in the Nakuru study (0∙72%)
compared with other studies (0∙03–0∙54%). This finding
is in accordance with a previous report on global
estimates of blindness due to diabetic retinopathy by
Leasher and co-workers that found the prevalence of
blindness due to diabetic retinopathy was highest in
African regions including west sub-Saharan, north, and
east sub-Saharan Africa (0∙14–0∙19%) compared with
0∙1% or less in other regions.3 Our findings also suggest
that the onset of proliferative disease was more prevalent
in individuals with mild diabetic retinopathy at baseline
compared with those with no retinopathy at baseline.
In a recent report on patients with type 1 diabetes
with 30 years of follow-up, the Diabetes Control and
Complications Trial (DCCT)–EDIC study group estimated
that the prevalence of progression to proliferative disease
in 4 years was 2∙9% in patients with no retinopathy and
5∙7% in those with mild diabetic retinopathy at baseline.
Limiting the probability of progression to proliferative
disease to less than 5% between retinal screening
examinations, the group suggested an evidence-based
schedule for time to the next examination to be 4 years in
those with no retinopathy and 3 years in those with mild
diabetic retinopathy at baseline.39 Our data showing
prevalence of progression to proliferative diabetic retino­
pathy of less than 1% in individuals with no retinopathy
support the notion of extending the screening interval to
4 years in patients with diabetes and no retinopathy
(table 6).
On the basis of this review of contemporary studies, we
recommend some areas for future research: first, to
obtain precise estimates of incident diabetic retinopathy,
more contemporary studies representative of developed
countries with accessible and high-quality health-care
systems such as in western Europe, Australia, and high-
income Asia (eg, Japan, South Korea), and countries with
a high prevalence of diabetes are needed; second, more
studies including type 1 diabetes across all regions are
needed; third, to avoid heterogeneity across studies and
facilitate meta-analysis, future studies should follow a
uniform method, such as estimating incidence in those
with diabetes only (some studies estimated diabetic
retinopathy incidence in the overall population including
both diabetes and non-diabetes, which might dilute the
estimates), including information on severity of incident
diabetic retinopathy and, importantly, should report their
results by age and sex.
Our study has limitations. Although we used an annual­
ised incidence to compare estimates across studies, the
heterogeneity in the methods, the differences in the
population characteristics, the access to health care, the
availability of systematic screening programmes, and the
difference in the study periods limit the scope for
generalisations and comparisons. Therefore, differences
between regions and studies need to be interpreted
with caution.
www.thelancet.com/diabetes-endocrinology Published online July 10, 2018 http://dx.doi.org/10.1016/S2213-8587(18)30128-1 9
Review
In summary, this systematic Review provides a global
overview of the incidence and progression of diabetic
retinopathy published over the past few decades across
several regions. In our review of contemporary studies,
we found that even well developed economies do not
include contemporary data on incidence or progression
of diabetic retinopathy and no contemporary study
estimated the incidence in type 1 diabetes. Our review
suggests that more high-quality population-based
studies capturing data on the incidence and progression
of diabetic retinopathy with stratification by age, sex,
and severity of disease are needed to consolidate the
evidence base. Our data is useful for conceptualisation
and development of major public health strategies such
as screening programmes for diabetic retinopathy.
Contributors
CS and TYW designed the study. RL and RB performed the literature
review. CS supervised literature review and study selection and wrote
the initial draft. MLC performed the analysis for SiMES and SINDI,
and YXW recalculated the estimates for the BES. GT, JBJ, ELL, C-YC,
BEKK, PM, RK, CMGC, and TYW provided essential corrections to
the manuscript. Final version of the paper has been seen and approved
by all the authors.
Declaration of interests
We declare no competing interests.
Acknowledgments
Supported by the National Medical Research Council (NMRC),
Singapore. BES was supported by the State Natural Sciences Fund
(81041018) and the Natural Sciences Fund of the Beijing government
(7092021; 7112031).
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