Development and Progression of Diabetic

Retinopathy 12 Months after

Phacoemulsification Cataract Surgery
Thomas Hong, BAppSci,1 Paul Mitchell, MD, PhD,1 Tania de Loryn, MA, DipClinPsych,1
Elena Rochtchina, MAppStat,1 Sudha Cugati, MBBS, MS,1 Jie Jin Wang, MMed, PhD1,2
Objective: To assess whether phacoemulsification cataract surgery exacerbates the development and
progression of diabetic retinopathy (DR) in a cataract surgical cohort.
Design: Clinic-based cohort study.
Participants: Patients aged 65⫹ years undergoing cataract surgery at an eye clinic in Sydney, Australia,
between 2004 and 2006.
Methods: Digital retinal photography was performed after pupil dilation preoperatively and at 1-, 6-, and
12-month postoperative visits. DR was assessed using the modified Early Treatment Diabetic Retinopathy Study
(ETDRS) classification. Preoperative and 1-month postoperative (baseline) photographs were compared side-
by-side with 12-month postoperative photographs. Odds ratios (ORs) and 95% confidence intervals (CIs) were
calculated for DR progression in operated (pseudophakic) compared with nonoperated (phakic) eyes, adjusted
for age, sex, diabetes duration, and preoperative glycosylated hemoglobin level.
Main Outcome Measures: Incident DR was defined in eyes without DR at baseline in which DR was
detected at 12-month postoperative visits. DR progression was defined as an increase of 1 or more ETDRS steps
during the same period, including incident cases.
Results: Of 1994 surgical patients recruited, 190 (9.53%) with diabetes and complete data and thus were
included. There were 56 patients with unilateral surgery performed before baseline (mean postoperative duration
3.3⫾3.3 years). The prevalence of DR at baseline was higher in these 56 pseudophakic eyes than in 324 phakic eyes
(71.4% vs. 48.2%, respectively, adjusted OR 2.16; 95% CI, 1.16 – 4.03). Of the 190 patients, 169 were followed for
12⫹ months postoperatively; 278 eyes were pseudophakic, and 60 eyes remained phakic at 12 months. During the
12-month postoperative period, incident DR developed in 28.2% of pseudophakic eyes and 13.8% of phakic eyes
(adjusted OR 2.65; 95% CI, 1.06 – 6.61). In a paired-eye comparison of 45 patients who remained unilaterally
pseudophakic at 12 months and were at risk of DR progression, 35.6% of pseudophakic eyes exhibited DR
progression compared with 20.0% of the fellow phakic eyes (adjusted OR 2.21; 95% CI, 0.85–5.71).
Conclusions: Diabetic patients undergoing phacoemulsification cataract surgery appear to have a doubling
of DR progression rates 12 months after surgery. This outcome, however, represents less progression than was
previously documented with intracapsular and extracapsular cataract surgical techniques.
Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed
in this article. Ophthalmology 2009;116:1510 –1514 © 2009 by the American Academy of Ophthalmology.

During the late 1970s to early 1990s, more rapid progres-
sion of diabetic retinopathy (DR) after cataract surgery was
consistently documented when using the 2 most common
surgical techniques at that time, intracapsular and extracap-
sular cataract extraction.1– 4 The phacoemulsification surgi-
cal technique was developed by Kelman in 1967, inspired
by dental ultrasonic techniques, and popularized in the early
1980s. However, it was not widely accepted until 1996,
when phacoemulsification was used for 97% of cataract
procedures in the United States.5 This new technique rap-
idly replaced the older methods and is currently the most
common surgical procedure for cataract surgery, in view of
the small incisions, reduced procedure time, and minimal
damage to ocular structures. The visual outcome after
phacoemulsification does not differ from that after extra-
capsular extraction.6 Phacoemulsification, however, was re-
ported to have less complications, particularly inflamma-
tion7,8 and postoperative astigmatism.
Whether eyes operated using the phacoemulsification
technique still have more rapid progression of DR in pa-
tients with diabetes remains to be clarified,9,10 because few
small studies that assessed DR progression after phacoemul-
sification surgery included nonoperated eyes as con-
trols.11–13 We aimed to assess this question in a cohort study
of cataract surgical patients with diabetes, including paired
controls between operated and nonoperated eyes of the
same patients.
Materials and Methods
Patients aged 65 years or older undergoing phacoemulsification
cataract surgery at Westmead Hospital, Sydney, Australia, from

1510 © 2009 by the American Academy of Ophthalmology ISSN 0161-6420/09/$–see front matter
Published by Elsevier Inc. doi:10.1016/j.ophtha.2009.03.003
 Hong et al 䡠 Progression of Diabetic Retinopathy after Phacoemulsification

Table 1. Modified Early Treatment Diabetic Retinopathy Study betes. DR was graded by a single grader (TH) using the modified
Classification System ETDRS classification system, with DR levels ranging from levels
20 to 90 (Table 1). Questions about the lesions graded were
Diabetic Retinopathy Level adjudicated, and all cases exhibiting progression were confirmed
both by a senior grader who assessed images for the field study and
DR absent 10
Questionable 14 and 15
by a retinal specialist (PM).
Minimal NPDR 20 Both the preoperative and the 1-month postoperative visits
Mild NPDR 35 were considered baseline status, given the impaired quality of the
Moderate NPDR 43 preoperative photos in some patients, because of cataract. Side-
Moderately severe NPDR 47 by-side grading of the baseline or 1-month photographs with the
Severe NPDR 53 12-month postoperative visit photographs was performed to assess
Mild PDR 61 DR progression, defined as a worsening by 1 or more levels on the
Moderate PDR 65 ETDRS scale at the postoperative visits. This included progression
Severe PDR 71 from no DR to minimal DR (level 20). Incident DR was defined in
Advanced PDR 81 eyes without DR at baseline (level 10) in which DR developed
End-stage PDR 85 postoperatively and is a subgroup of the cases that progressed. We
Inactive PDR 90 defined patients who had panretinal laser treatment before baseline
Ungradable 99 as DR level 90 (inactive PDR) at baseline. These patients could not
progress any further and were therefore excluded from the analysis
DR ⫽ diabetic retinopathy; NPDR ⫽ nonproliferative diabetic retinopa- for progression of DR (n ⫽ 32).
thy; PDR ⫽ proliferative diabetic retinopathy. SAS (V9.13, SAS Institute, Cary, NC) was used for all analy-
ses. We assessed differences in DR prevalence between operated
and nonoperated eyes before the study baseline, and the incidence
2004 to 2006, were recruited into a cohort study, aiming to assess and progression of DR in operated compared with nonoperated
surgical outcomes, including the risk of age-related macular de- eyes 12 months after surgery. Generalized estimating equation
generation and DR after cataract surgery. The Study was approved models14 were used to estimate odds ratios (ORs) and 95% con-
by the University of Sydney and Sydney West Area Health Service fidence intervals (CIs) after adjusting for age, sex, baseline HbA1c
Human Research Ethics Committees and adhered to the tenets of level, and duration of diabetes.
the Declaration of Helsinki. Written, informed consent was ob-
tained from all study participants. In this report, we included a
subset of this cataract surgical cohort of 1994 patients, 169 of 190 Results
patients with diabetes (type I or II) who were followed for at least
12 months after surgery. All 190 participants with diabetes underwent standard phacoemul-
Participants were examined and had retinal photography per- sification surgery at the time of recruitment or shortly after recruit-
formed at preoperative and 1-, 6-, 12-, and 24-month postoperative ment to the study, including 90 women and 100 men with a mean
visits. Before surgery, participants were interviewed using stan- age of 74.1 (⫾5.7) years. The mean duration since diagnosis of
dardized questionnaires to obtain information on medical and diabetes was 13.2 (⫾10.1) years, and the preoperative average
ocular conditions. Data collected included age, sex, race, and type, HbA1c level was 7.4% (⫾1.4%) at baseline (Table 2). Only 2
duration, and treatment for diabetes. Glycosylated hemoglobin patients were on insulin alone for 30 or more years. Of the 190
(HbA1c) values were collected preoperatively as a measure of patients, 3 had ungradable images at either the baseline or follow-
objective glycemic control. At each visit, a self-reported average up visits, 187 were followed at 6 months, but 18 were lost to
blood glucose level range was also collected. Snellen visual acuity follow-up after this time, leaving 169 followed for at least 12
and intraocular pressure were measured. Digital retinal photo- months postoperatively. Of these 169 participants, 278 eyes were
graphs of both eyes were taken after dilation, using a Canon pseudophakic and 60 eyes remained phakic up to the 12-month
CF-60DSi Digital Fundus Camera (Canon Inc, Tokyo, Japan). visit. Of these 60 phakic eyes, 45 were at risk of DR progression,
Photographs including Early Treatment Diabetic Retinopathy because 15 eyes had an ETDRS level of 90 (inactive PDR) at
Study (ETDRS) standard field 1 (optic disc), field 2 (macula), field baseline. There were a total of 32 eyes with ETDRS level 90
4 (superotemporal), field 5 (inferotemporal), and a nasal field, at baseline; 23 of these eyes were the study eyes of interest (to
including the optic disc, were taken on all participants with dia- undergo surgery at the study baseline). Apart from capsular tears,

Table 2. Baseline Characteristics of Study Participants by Diabetic Retinopathy Progression Status

(Progression Defined as an Increase of ⱖ1 Early Treatment Diabetic Retinopathy Study Steps)

By Status of DR in the Study Eye

Baseline Characteristics All (n ⴝ 190) Progressed (n ⫽ 48) No Progression (n ⫽ 102) P Value
Mean age, yrs (SD) 74.1 (5.7) 72.5 (4.8) 75.2 (5.9) 0.007
Female, % 47.4 45.8 54.9 0.30
Current smoker, % 12.2 10.6 13.7 0.59
Hypertension, % 76.8 72.9 77.4 0.54
Mean body mass index (SD) 28.5 (5.4) 28.5 (5.2) 28.8 (5.4) 0.83
Duration of diabetes, yrs (SD) 13.2 (10.0) 13.5 (10.0) 11.3 (9.8) 0.20
HbA1c, mean % (SD) 7.4 (1.4) 8.0 (1.5) 7.0 (1.5) 0.0001

DR ⫽ diabetic retinopathy; HbA1c ⫽ glycosylated hemoglobin; SD ⫽ standard deviation.

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 Ophthalmology Volume 116, Number 8, August 2009
Figure 1. Odds ratios and 95% CIs for the prevalence, incidence, and
progression of DR after cataract surgery: operated compared with nonop-
erated eyes of patients with diabetes who had cataract surgery at least 12
months earlier, adjusted for age, sex, diabetes duration, and preoperative
HbA1c level. DR prevalence at baseline comparing pseudophakic (n ⫽
56) with phakic (n ⫽ 324) eyes before study baseline (OR 2.16; 95% CI,
1.16 – 4.03; P ⫽ 0.02). DR incidence after cataract surgery, comparing
pseudophakic (n ⫽ 78) with phakic (n ⫽ 29) eyes at 12-month postop-
erative visits (OR 2.65; 95% CI, 1.06 – 6.61; P ⫽ 0.04). DR progression
after cataract surgery, comparing pseudophakic (n ⫽ 150) with phakic
(n ⫽ 45) eyes at 12-month postoperative visits (OR 1.82; 95% CI,
0.89 –3.72; P ⫽ 0.10). Paired-eye comparison of DR progression 12 months
after cataract surgery among 45 patients who had unilateral surgery at least
12 months prior (OR 2.21; 95% CI, 0.85–5.71; P ⫽ 0.10).
which led to vitrectomy in 2 patients (1 eye each), there were no
major surgical complications in this cohort.
At baseline, 56 of the 190 patients had already undergone
cataract surgery on 1 eye before recruitment into the study, with a
mean postoperative duration of 3.3⫾3.3 years. These 56 eyes were
classified as pseudophakic before baseline. DR was present in
71.4% of these 56 pseudophakic eyes, compared with 48.2% of
324 phakic eyes before baseline. After adjusting for age, sex,
duration of diabetes, and baseline HbA1c level, pseudophakic eyes
had significantly higher odds of presenting with DR (OR 2.16;
95% CI, 1.16 – 4.03) (Fig 1).
We observed DR progression in 81 eyes (both surgical and
nonsurgical) during the 6- to 12-month follow-up period after
entering the study; of these eyes, 33 (40.7%) progressed by 1
ETDRS step (Table 1), 12 (14.8%) progressed by 2 ETDRS steps,
and 36 (44.4%) progressed by 3 or more ETDRS steps. After
excluding the 56 baseline pseudophakic eyes, we compared DR
incidence between all operated and nonoperated eyes among pa-
tients without DR at baseline. During the 12-month postoperative
period, DR developed in 28.2% (n ⫽ 22) of the operated (study)
eyes and 20.0% (n ⫽ 12) of the baseline nonoperated (nonstudy)
eyes (adjusted OR for DR incidence in operated eyes, 1.86; 95%
CI, 0.97–3.58). This association was stronger after excluding base-
line nonoperated eyes that had surgery during the follow-up period
(some patients had second eye surgery during the 12-month pe-
riod). In other words, we compared eyes that had surgery at least
12 months prior (DR incidence 28.2%) with eyes that remained
phakic for the same period of time (DR incidence 13.8%). The risk
of developing DR was more than doubled in the operated eyes
(adjusted OR 2.65; 95% CI, 1.06 – 6.61) (Fig 1).
Similarly, DR progression 12 months after surgery was ob-
served in 32.0% (n ⫽ 48) of baseline-operated eyes and 26.5%
(n ⫽ 26) of baseline nonoperated eyes (adjusted OR 1.34; 95% CI,
0.80 –2.25). Of the 48 operated eyes that progressed, 20 (41.7%)
1512
progressed by 1 step, 8 (16.7%) progressed by 2 steps, and 20
(41.7%) progressed by 3 or more steps. After excluding eyes that
had surgery during the follow-up period, DR progression in non-
surgical eyes after 12 months was 22.9% (n ⫽ 11; adjusted OR
1.82; 95% CI, 0.89 –3.72, after adjusting for age, sex, duration of
diabetes, and baseline HbA1c level) (Fig 1). For each year increase
in diabetes duration, there was a 3.0% higher odds of DR progres-
sion (OR 1.03; 95% CI, 1.00 –1.07), after adjusting for age, sex,
baseline HbA1c level, and the postsurgical state.
There were 45 participants who had only unilateral surgery
performed during the 12-month follow-up period and were at risk
of DR progression (baseline DR level ⬍90). Paired-eye compari-
son of DR progression in this group of patients showed that the
proportion of eyes with DR progression was higher in the pseu-
dophakic eyes than in the fellow phakic eyes of the same patients
during the 12-month postoperative period (35.6% vs. 20.0%, re-
spectively; OR 2.21; 95% CI, 0.85–5.71) (Fig 1).
Discussion
Although phacoemulsification surgery is less disruptive
than intracapsular cataract extraction and extracapsular cat-
aract extraction,6,7 in this surgical cohort of patients with
diabetes, we found that those undergoing phacoemulsifica-
tion showed nearly a doubling of the progression rates for
DR 12 months after surgery. This increased progression rate
was lower than previously reported DR progression rates
using older cataract surgical techniques. Our paired com-
parison of operated and nonoperated eyes of the same
patients also suggested a higher progression rate of DR in
operated eyes, although this difference was marginally
nonsignificant.
The DR progression rate of 32.0% in eyes after phaco-
emulsification surgery shown in our sample is consistent
with previously reported progression rates ranging from
21% to 25%4,9,15 12 months after surgery, or 25%16 6
months after surgery. Only 3 previous studies have con-
ducted comparisons of operated versus nonoperated eyes to
assess DR progression after phacoemulsification sur-
gery.11–13 Krepler et al11 reported a 12.0% DR progression in
operated eyes versus 10.8% in nonoperated eyes among 42
patients who completed 1-year postoperative follow-up.11
Squirrell et al12 reported 20.0% versus 16.0% among 50
patients with type II diabetes undergoing unilateral phaco-
emulsification surgery during a 12-month period. Liao and
Ku13 reported that DR progression rates were 29.4% and
39.2% of 51 operated eyes at 1- and 3-year postoperative
visits, respectively, compared with 26.1% and 34.7% of 32
nonoperated eyes, respectively.13 The 2 studies conducted
by Krepler et al and Squirrell et al were paired-eye com-
parisons of the same patients. However, fellow eyes that had
surgery performed during the study follow-up periods were
included as controls in both studies.11,12 The study by Liao
and Ku13 was a comparison between any operated and
nonoperated eyes (not paired-eye comparisons of the same
subjects). All these studies did not find a significant differ-
ence in DR progression rates between operated and nonop-
erated eyes, although the reported progression rates were
consistently and slightly higher in operated compared with
nonoperated eyes.11–13 Our findings from the comparison of
any operated versus nonoperated eyes (regardless of
 Hong et al 䡠 Progression of Diabetic Retinopathy after Phacoemulsification
whether subsequent surgery was performed on some so-
called nonoperated eyes) showed findings similar to those
reported previously (32.0% in operated and 26.5% in non-
operated eyes; OR 1.34; 95% CI, 0.80 –2.25).
The advantage of our study over these previous studies is
its relatively large sample size (n ⫽ 169 patients), providing
information for comparison between any operated versus
nonoperated eyes. We also compared operated eyes with
those that remained nonoperated for the entire 12-month
follow-up period and conducted a paired-eye comparison in
45 patients who had unilateral surgery for at least 12 months
prior; the only difference between the 2 eyes was that one
had undergone surgery and one had not. We therefore
consider our findings for DR progression from the paired-
eye comparison of the same subjects less likely to be biased
than findings from comparison of any operated versus non-
operated eyes at baseline. The latter comparison may have
incorporated differences between study subjects in the risk
estimates. In addition, using eyes that were nonoperated at
baseline but had had surgery during the follow-up period as
controls may have led to misclassification of operated and
nonoperated eyes, resulting in a bias toward the null.
Our study sample has characteristics similar to those in
other reported study samples. The mean ages at cataract
surgery were similar across all the studies.11–13 Mean
HbA1c levels at preoperative visits were also similar across
these studies, including ours. Some previous studies found
that poor diabetic control contributed to DR progression
after surgery.17,18 Paired-eye comparisons of the same pa-
tients who had unilateral surgery eliminates the confound-
ing effect from poor diabetic control and is therefore the
most efficient way to investigate the effect of surgery on DR
incidence and progression.
In keeping with our study findings, other studies have
reported an increased risk of DR progression after phaco-
emulsification surgery in patients with more advanced pre-
operative stages of DR.9,10,19 The blood–aqueous barrier
has been found to be impaired more severely in patients
with proliferative DR than in patients without diabetes or in
those with nonproliferative DR, as indicated by substan-
tially higher levels of aqueous flare after surgery in eyes
with proliferative DR.10 We had few patients with active
proliferative DR in our sample and so were not able to
assess whether the detrimental effect of surgery was greater
in patients with proliferative DR. Given the previously
documented rapid DR progression after cataract surgery
using older surgery techniques, there is coherence in the
evidence relating to DR progression after cataract surgery.
One possibility that this study cannot easily address is
the concern that both DR and cataract are complications of
diabetes, and therefore the presence of cataract may be a
marker for greater severity or increased likelihood of pro-
gression of DR. Our study findings might, in part, reflect
this. A second concern is that there might be an “early
worsening” effect during the first 12 months, which may
potentially reflect efforts to tighten blood glucose control
before or after the surgery. Our paired-eye comparison of 45
subjects does account, at least partly, for both possibilities.
It is now well-accepted clinical practice that preoperative
laser treatment should be considered to adequately control
active DR features, particularly signs of macular edema,
even when not yet clinically significant, and to reduce the
risk of progression to proliferative DR or iris neovascular-
ization in patients with significant DR8 undergoing cataract
surgery. The number of patients who reported previous laser
treatment in our study sample was small (n ⫽ 32). Eyes that
had previous panretinal laser treatment were no longer
considered at risk of DR progression or development and
were thus excluded from the analyses in this report.
When comparing the reported DR progression rates after
phacoemulsification surgery with the rates after extracapsu-
lar cataract extraction surgery, the magnitude of the differ-
ences between operated and nonoperated eyes appears to
have been reduced substantially. Jaffe et al2 reported 37%
and Pollack et al20 reported 38.2% progression rates 12 to
18 months after surgery, compared with progression rates of
approximately 30% or less after phacoemulsification sur-
gery reported by recent studies,2,20 including ours.
Study Limitations
Limitations of our study should be noted. First, the assess-
ment of DR in nonoperated eyes may have been hampered
by lens opacity, so that we may have missed recognizing
mild DR lesions in nonoperated eyes. However, eyes that
remained unoperated for 12 months would have been
unlikely to have advanced cataract. For eyes with mod-
erate cataract, although a few microaneurysms may have
been undetected, this would not be as likely for retinal
hemorrhages.
Second, the fellow eyes may not be entirely comparable.
Although the decision for surgery was not made randomly,
factors including the duration of diabetes and glycemic,
blood pressure, and blood lipid control would be likely to
affect both eyes similarly. So in this regard, we have made
the best and most feasible comparison. It must be acknowl-
edged, however, that (1) local factors can result in asym-
metry of DR between the 2 eyes; and (2) decisions about
which eye is operated may reflect differences in DR
levels between the 2 eyes, of which we have no specific
knowledge.
Third, eyes that underwent cataract surgery may already
be at a greater risk of DR progression than nonsurgical
fellow eyes, regardless of their surgical status. The devel-
opment of cataract in people with diabetes is strongly re-
lated to poor glycemic control, which can also accelerate
DR. Although a randomized controlled trial is an ideal study
design for this study question, it would not be feasible or
ethical. A longitudinal observational study is a feasible
design with evidence quality close to that from random-
ized controlled trials, and paired-eye comparison of the
same patients is the most comparable analysis that we can
conduct.
We did not collect renal function data in our study
sample or complete surgical data on the types of intraoc-
ular lens, width of the incision, and skill level of the
surgeons. Although these factors are unlikely to have had
a major effect on DR progression, they may have had
minor influences.
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 Ophthalmology Volume 116, Number 8, August 2009
In conclusion, we found that phacoemulsification surgery
may still exacerbate the development and progression of DR
in older patients with diabetes, compared with fellow eyes
of the same patients that had not undergone phacoemulsi-
fication surgery during a 12-month period. The risk magni-
tude for DR progression after phacoemulsification surgery
was found to be substantially lower than the progression
rates previously documented after surgery using older sur-
gical techniques. Although these findings should not argue
against performing cataract surgery in older people with
diabetes, it is important for clinicians to recognize this
residual risk and to take appropriate precautions (closer
monitoring or preoperative laser for at-risk eyes).
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Footnotes and Financial Disclosures
Originally received: September 2, 2008.
Final revision: February 26, 2009.
Accepted: March 3, 2009.
Available online: June 5, 2009. Manuscript no. 2008-1050.
1
Centre for Vision Research, Department of Ophthalmology and West-
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Wales, Australia.
2
Centre for Eye Research Australia, Department of Ophthalmology, Uni-
versity of Melbourne, Melbourne, Victoria, Australia.
Presented at: Association for Research in Vision and Ophthalmology
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Financial Disclosure(s):
The author(s) have no proprietary or commercial interest in any materials
discussed in this article.
Supported by the Australian National Health and Medical Research Coun-
cil, Canberra, Australia (Grant No 302010). The funding organization had
no role in the design or conduct of this research.
Correspondence:
Jie Jin Wang, MMed, PhD, Centre for Vision Research, Department of
Ophthalmology, University of Sydney, Westmead Hospital, Hawkesbury
Road, Westmead, New South Wales, Australia, 2145. E-mail: jiejin_
wang@wmi.usyd.edu.au.