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Risk Factors for Late-Onset Infection Following Glaucoma Filtration Surgery
Henry D. Jampel, MD, MHS;
Harry A. Quigley, MD;
Lisa A. Kerrigan-Baumrind, MS;
B. Michele Melia, ScM;
David Friedman, MD, MPH;
Yolanda Barron, MS;
for the Glaucoma Surgical Outcomes Study Group
Arch Ophthalmol. 2001;119:1001-1008.
ABSTRACT
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Objective To determine the risk factors for late-onset infection following glaucoma
filtration surgery.
Methods We performed a case-control study comparing 131 cases of late-onset
infection collected from 27 surgeons at 10 centers with 500 controls matched
for date of surgery and surgeon. The criterion for the presence of infection
was severe anterior chamber reaction occurring later than 4 weeks after surgery.
An opaque bleb and positive culture results were not required for diagnosis.
Risk factors were identified by univariate and multivariate logistic regression
analyses.
Results Some of the risk factors that were statistically significant in the
multivariate model after adjusting for age, race, and sex were (1) performance
of a full-thickness rather than a guarded procedure (risk ratio [RR], 13.1;
95% confidence interval [CI], 2.12-80.9), (2) filtration surgery performed
without concurrent cataract surgery (RR, 2.25; 95% CI, 1.24-4.08), (3) use
of mitomycin (RR, 2.48; 95% CI, 1.06-5.83), (4) intermittent use of antibiotics
after surgery (RR, 2.10; 95% CI, 1.09-4.02), and (5) continuous use of antibiotics
after surgery (RR, 5.94; 95% CI, 2.09-16.9).
Conclusions Eyes undergoing full-thickness procedures or filtration surgery without
cataract extraction are at increased risk for late infection. Intraoperative
mitomycin and episodic or continuous antibiotic use after the postoperative
period are associated with an increased risk of infection.
INTRODUCTION
DURING THE past 3 decades there have been many reports of late-onset
infections in eyes with filtration blebs, including case series of endophthalmitis1-16
defined by vitreous involvement, and the more recently recognized entity of
blebitis in which the vitreous is not involved.2, 5, 14-18
These reports span the period during which full-thickness glaucoma procedures5, 7, 9, 11-14,16-21
were replaced by partial-thickness procedures1-2,4-6,8-9,12-13,15, 18, 20-21
and fluorouracil was introduced4, 9, 13-14,16-18
followed by mitomycin.1-2,4-6,13-15,18
These reports also include eyes with inadvertent filtration blebs following
cataract surgery.3, 9, 11, 14, 21
The prognosis for eyes with late-onset endophthalmitis associated with
filtration surgery is poor,5, 12
with a recent study reporting a median visual acuity after endophthalmitis
of 20/200.22 Furthermore, it has been suggested
that the incidence of late-onset endophthalmitis is increasing.23
There has been much speculation as to what risk factors are associated with
late-onset infection after filtration surgery. We report the results of a
large multicenter case-control study of late-onset infection after glaucoma
filtration surgery that investigated many possible risk factors.
METHODS
The Joint Committee on Clinical Investigation of The Johns Hopkins Hospital
(Baltimore, Md) approved the research. Each case and each control was assigned
an identifying number and all patient identifiers were removed from the database.
We sought the participation of glaucoma surgeons who had observed the
development of late-onset infection in their patients and were willing to
have the medical records reviewed. We aimed for geographic diversity among
the study sites.
CASE SELECTION
Surgeons were asked to recall the names of patients on whom they had
performed glaucoma filtration surgery and who subsequently developed a late-onset
infection. In several instances, surgeons had been keeping a list of such
cases. Other sources of cases included hospital International
Classification of Diseases, Ninth Revision (ICD-9) discharge codes and the records of vitreoretinal specialists who
treated cases of late-onset infection after glaucoma filtration surgery. Some
of the cases had previously been included in other reports of glaucoma surgical
results.2, 6, 9, 14, 22
Cases had to have been operated on at the participating study center to ensure
that preoperative and operative information could be obtained and so that
appropriate controls could be selected. Only eyes operated on after January
1, 1980, were considered. Eyes were considered potential cases if they developed
a hypopyon or an anterior chamber reaction recorded as greater than or equal
to 2+ cell and 2+ flare at least 4 weeks after a glaucoma
filtration operation, either alone or combined with cataract extraction. Eyes
that had undergone drainage device surgery or trabeculotomy were excluded.
Eyes with a previous history of inflammation or eyes that had persistent inflammation
since the time of surgery were excluded unless there was a positive bacteriologic
culture.
CONTROL SELECTION
For each case, a list was made of all trabeculectomies, full-thickness
procedures, and combined cataract and glaucoma operations performed by the
same surgeon within the 6 months before and the 6 months after surgery. This
stipulation on the controls minimized the chance that the cases and controls
would differ in terms of indications for surgery, surgical technique, and
postoperative care. The list was derived from databases maintained by the
surgeon, appointment books listing the names of patients undergoing surgery,
and operating room logs.
The operations were ranked using a random number table. Starting with
the operation ranked first, the medical records were sequentially examined
for suitability as controls until up to 4 controls had been identified. The
principal reason for excluding a potential control was that the length of
follow-up after surgery for the control may have been less than 90% of the
duration of follow-up for the case prior to the episode of endophthalmitis
(otherwise, the "control" might really be a "case" that had simply not been
followed up for long enough). Other reasons for excluding potential controls
included incomplete medical records and incorrect identification of previous
glaucoma surgery. If a patient had undergone glaucoma surgery in both eyes
during this time frame, only the eye operated on closest to the date of surgery
of the case was used. One hundred fifteen cases had 4 controls, 9 cases had
3 controls, 6 cases had 2 controls, and 1 case had 1 control. Some cases had
less than 4 controls because of our inability to locate controls with follow-up
comparable to the cases.
DATA ABSTRACTION AND ENTRY
A single study coordinator (L.A.K.-B.) who traveled to the glaucoma
surgeons' offices abstracted the information from the medical records. The
information abstracted on a standardized data collection form included (1)
patient characteristics, such as age, race, sex, history of systemic diseases,
use of systemic corticosteroids and aspirin use; (2) ocular characteristics,
including refractive error, previous ocular surgery, and type and severity
of glaucoma; (3) intraoperative characteristics such as technique of glaucoma
surgery, combination with cataract surgery, use of antifibrosis agents, tenonectomy,
and antibiotic administration at the end of surgery; (4) postoperative characteristics
such as wound leak, flat anterior chamber, and suprachoroidal hemorrhage,
as well as blepharitis, dellen, trauma, leaking bleb, position and description
of bleb, and record of intraocular pressures (IOPs); and (5) history of antibiotic
treatment, contact lens use, use of eye drops in the operated or unoperated
eye, use of artificial tears, and performance of bleb revision surgery.
DATA ANALYSIS
A univariate conditional logistic regression analysis using the PHREG
procedure in SAS (SAS Institute Inc, Cary, NC) was performed to investigate
the relationship between case status and each of the potential risk factors.
Potential risk factors associated with case status with P values of .20 or less in the univariate analysis were entered into
a conditional multiple logistic regression model. Both forwards and backwards
stepwise regression procedures that retained variables with P values of .05 or less were performed. Only risk factors for which
data were present for 95% or more of cases and controls were included. For
example, although the variable "high bleb" was a strong risk factor in the
univariate analysis, a description of the bleb as high or low was present
in fewer than half of the cases and controls, and would have limited the model
to a small percentage of the total cases and controls available. Age, race,
and sex were included in the multivariate models regardless of level of statistical
significance. Table 1 presents
the variables from the univariate analysis that were included or excluded
from the initial stepwise model. A P value of .05
or less was considered statistically significant in the conditional multiple
logistic regression model.
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Table 1. Variable Selection for the Conditional Multiple Logistic Regression
Model Evaluating Risk Factors for Late-Onset Bleb-Related Endophthalmitis
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RESULTS
The complete medical records of 131 patients with and 500 patients without
late-onset infection following glaucoma filtration surgery, matched for surgeon
and date of surgery, were identified. Glaucoma filtration surgery was performed
by 27 experienced surgeons at 10 centers (Table 2). The dates of surgery ranged from August 12, 1980, to December
16, 1997 (Figure 1). The median
length of time between the date of surgery and the diagnosis of infection
was 1.7 years (range, 29 days to 10.9 years) (Figure 2). The length of time from symptoms to diagnosis in 7 full-thickness
cases was 4.1 ± 4.6 (mean ± SD) days and in 123 partial-thickness
procedures was 3.4 ± 11.6 (mean ± SD) days (P = .17, Wilcoxon signed rank test). Fifty percent of patients were
aged between 60 and 76 years (range, 3-97 years), 53% were of European ancestry,
25% of African ancestry, and 22% were of unknown racial origin. Other demographic
features of the cases and controls are presented in Table 3.
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Table 2. Distribution of Cases of Late-Onset Bleb-Related Infections
and Controls by Practice
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Figure 1. Distribution of the dates of glaucoma
filtration surgery.
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Figure 2. Length of time between glaucoma
filtration surgery and the diagnosis of infection.
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Table 3. Demographics of Cases of Late-Onset Bleb-Related Infection
and Their Controls*
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Vitreous involvement was present in 123 (94%) cases; 82 (63%) had an
opaque bleb, 89 (68%) had a hypopyon, and 58 (44%) had all 3 findings (Table 4). Using the presence of vitreous
involvement as the distinguishing feature between blebitis and endophthalmitis,
there were 123 cases of endophthalmitis and 8 cases of blebitis. At the last
visit prior to the diagnosis of late-onset bleb-related infection, the visual
acuity of the cases was 20/50.
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Table 4. Key Clinical Findings in Eyes With Late-Onset Bleb-Related
Infection*
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The mean ± SD age of the cases was 63.4 ± 16.7 years and
that of the controls was 66.9 ± 14.6 years. In the univariate analysis,
younger age was a risk factor for infection, with a conditional risk of 1.08
for every 5 years of decreasing age (95% confidence interval [CI], 1.02-1.16; P = .01). Postoperative IOPs were 10.7 ± 4.3 (mean
± SD) mm Hg for the cases and 12.7 ± 5.0 mm Hg for the controls.
The conditional risk of developing an infection increased by 50% for every
3 mm Hg decrease in IOP (odds ratio, 1.50; 95% CI, 1.28-1.76; P<.001).
Univariate-matched analyses for discrete variables are presented in Table 5. Strong risk factors for the occurrence
of late-onset, bleb-related infection included a history of prior intraocular
surgery, full-thickness filtration surgery, and the use of mitomycin; wound
leak, flat anterior chamber, or suprachoroidal hemorrhage in the early postoperative
period; and the presence of bleb leak or a high bleb. In addition, the use
of antibiotics beyond the immediate postoperative period, either intermittently
or continuously, was a strong risk factor. Other possible risk factors (risk
ratio,  2.0) included the use of systemic corticosteroid use, juvenile
glaucoma, silk conjunctival sutures, pale-colored bleb, contact lens wear,
bleb revision surgery, and use of epinephrine eye drops in the operative eye.
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Table 5. Univariate Matched Analyses of Risk Factors For Late-Onset
Infection After Glaucoma Filtration Surgery
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Combined cataract and glaucoma surgery, the presence of a superiorly
located bleb, and the use of any glaucoma medications in the fellow eye were
protective against the development of infection in the univariate analysis
(Table 5). Additional univariate-matched
analyses that excluded the 8 cases of blebitis in one, and excluded the 17
cases diagnosed between 1 and 3 months after surgery in another, yielded the
same results (data not shown).
The initial conditional multiple logistic regression model identified
statistically significant associations between previous surgery, full-thickness
surgery, glaucoma surgery without concurrent cataract surgery, lower postoperative
IOP, episodic or continuous postoperative use of antibiotics, and lack of
use of glaucoma medications in the fellow eye (Table 6). Mitomycin was not associated with late-onset infection
in this initial model.
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Table 6. Conditional Multiple Regression Model of Risk Factors of Late-Onset,
Bleb-Related Infection Following Glaucoma Filtration Surgery*
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When we excluded variables from the model that might be related to the
use of mitomycin, such as previous intraocular surgery, the presence of a
bleb leak, the episodic or continuous use of antibiotics postoperatively,
and the average IOP during the postoperative period, the use of mitomycin
became strongly associated with the development of an infection. Furthermore,
the use of mitomycin remained in the model as all variables were added back
to the model except for previous surgery (Table 7). The use of fluorouracil was not statistically significant
(P = .23), although its effect was in the direction
of a risk factor.
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Table 7. Modified Conditional Multiple Regression Model of Risk Factors
for Late-Onset Bleb-Related Infection (History of Prior Ocular Surgery Excluded)*
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COMMENT
The risk factors for late-onset infection following glaucoma filtration
surgery have not been well characterized. Most reports in the literature are
small case series, and hence are not amenable to a case-control analysis necessary
for identifying risk factors. The recent publication of a case-control study
of infection after glaucoma filtration surgery is an important addition to
the literature.22 However, the number of cases
enrolled was relatively small, and controls were matched to cases by the use
of antifibrosis agents, eliminating the possibility of determining whether
antifibrosis agents were associated with an increased risk of late-onset bleb-related
infection. We set out to design a study with numbers of cases and controls
sufficient to allow the identification of statistically significant associations.
This involved pooling the experiences of many practices, which allowed us
to assemble what we believe to be the largest number of cases of late-onset
infection after glaucoma filtration surgery to date.
We used the univariate analysis to point out risk factors that might
be important, but whose representation in the medical records were so incomplete
(bleb description), or occurrence so infrequent (use of systemic corticosteroids),
that they could not be entered into a multivariate model (Table 1). Furthermore, the univariate analysis could point out risk
factors, such as bleb leak, that may not have been significant in the multivariate
model owing to close association with other variables.
Our univariate analysis confirms the findings of others that inferiorly
located blebs are associated with a high incidence of late-onset infection.
The univariate analysis also suggests an association between the notation
of a high bleb and the presence of blepharitis with the development of an
infection. A high bleb may be more susceptible to penetration by pathogens
in the conjunctiva, while eyes with blepharitis may have a greater load of
bacteria, thus predisposing them to infection.
Another important potential association detected in our univariate analysis,
but not in the multivariate analysis, is between a history of bleb leak and
the subsequent development of an infection (risk ratio, 3.7; 95% CI, 2.19-6.25).
Soltau et al22 recently reported on 55 consecutive
cases of bleb-related infection occurring at 2 institutions. Some of their
cases and controls were included in our study. They found that eyes with bleb-related
infections were 26 times as likely to have a bleb leak detected at the time
of infection than eyes without a bleb-related infection. They found a nearly
significant association (P = .07) between a history
of a preexisting bleb leak and the subsequent development of an infection.
It seems biologically plausible that a bleb with a visible breach in its wall
would be at greater risk for infection than one whose surface was intact.
Multivariate analyses are critical because they adjust for the presence
of many related variables. However, multivariate models can be influenced
by the choice of variables that are included in the model. When 2 variables
that are closely associated are placed in a model, sometimes only 1 will remain
significant. Furthermore, including a variable that is in the causal pathway
will remove a true association. A classic example of this would be a regression
model looking for an association with skin cancer that includes both freckles
and sun exposure. Keeping freckles in the model may falsely remove the association
between skin cancer and sun exposure.
In our multivariate analysis, we found that a history of prior surgery,
but not the use of mitomycin, was significantly associated with infection.
One possible explanation for this is that a history of previous surgery led
the surgeons to use mitomycin, which then produced a thin bleb, followed by
a bleb leak, and ultimately an infection. This pathway to infection is supported
by the findings of Greenfield et al,24 who
demonstrated that the use of mitomycin predisposes to wound leaks. When mitomycin
did not seem to be a risk factor in our initial model, we removed variables
that we speculated might lie along the same causal pathway to infection and
ran the model again. We found that when a history of previous surgery was
not included in the model, mitomycin became a significant risk factor, with
a risk ratio of 2.48. Our decision to remove the association of previous surgery
is supported by the study of Soltau et al.22
When they matched their cases and controls for antifibrosis use, they did
not find an association between late-onset bleb-related infection and a history
of previous surgery.
In our study, there were no preoperative characteristics of either patients
or eyes that were risk factors. In terms of variables occurring at the time
of surgery, the performance of a full-thickness rather than a guarded filtration
procedure was a strong risk factor, with a risk ratio of 13.1. This confirms
the findings of Sastry et al,25 who in analyzing
the Medicare database for hospital admissions for endophthalmitis following
glaucoma surgery, found a history of a full-thickness procedure disproportionately
represented. On the other hand, the performance of combined cataract and glaucoma
surgery vs glaucoma surgery alone seemed to be protective against the development
of infection most likely because the glaucoma portion of the combined procedure
results in thicker blebs than glaucoma surgery alone. The observation by Greenfield
et al6 that the blebs in eyes that have undergone
combined cataract and glaucoma surgery are thicker than those that undergo
trabeculectomy alone supports this hypothesis.
Some studies have suggested that mitomycin is a risk factor,6 whereas others have concluded that it is not.8, 13, 26 Others have suggested
fluorouracil to be a risk factor,16 contrary
to our findings. The limitations of our medical record review precluded an
analysis by dose, duration, or route of administration of the antifibrosis
agent.
The notation of any of the early postoperative complications of flat
anterior chamber, wound leak, and suprachoroidal hemorrhage was associated
with the development of late-onset infection. Mochizuki et al26
found early wound leak to be a risk factor in their study of 11 infections
developing after 632 trabeculectomies. Perhaps these complications are associated
with problems with the filtration operation that later manifest themselves
in a bleb that is more prone to late-onset infection. For example, eyes with
a flat anterior chamber owing to overfiltration may more often develop a thin
bleb that could in turn predispose to late-onset infection.
The association of antibiotic use postoperatively and late-onset infection
is a provocative finding. To interpret the significance of this association,
it is necessary to clarify that because we performed a conditional analysis,
cases were matched with controls who had the same surgeon. Therefore, the
association we found between antibiotic use and late-onset infection means
that individual surgeons must have used antibiotics postoperatively in certain
patients but not others. However, the multivariate analysis demonstrates that
antibiotic use is associated with the development of infection, independent
of the other variables that we examined, such as blepharitis or bleb leak.
Then why would a surgeon use antibiotics in some patients and not others?
Perhaps they were used in response to some other variable that we did not
consider or that was not noted in the medical record.
Given this caveat, our finding of a strong association between the use
of antibiotics after surgery and late-onset infection raises the possibility
that the use of antibiotics, particularly in a continuous fashion, could increase
the likelihood of an infection. Lamping et al20
reported that in 4 cases of late-onset endophthalmitis, 3 were receiving continuous
prophylactic antibiotics at the time of infection. It could be that the antibiotics
select for virulent bacteria that cause serious infection. However, the study
by Wand et al27 does not support this hypothesis.
They performed conjunctival cultures in eyes that had been treated with antibiotics
after filtration surgery and found no difference from the untreated, unoperated
fellow eye in the bacterial flora. Unfortunately, we did not capture information
about the antibiotic sensitivities of the organisms cultured from the cases
to test this hypothesis. Even if we had such information, case-control studies
such as this can establish associations, but not cause and effect. Thus, we
cannot prove that the use of antibiotics increases the risk of infection.
However, these data suggest that further study is needed to justify the use
and safety of postoperative antibiotics.
Our study design does not shed any light on the prevalence of late-onset
infection after glaucoma filtration surgery. To determine this definitively,
a prospective observational study of thousands of glaucoma operations annually
would be needed. Two retrospective studies of endophthalmitis following trabeculectomy
with mitomycin have recently been published. In the first, 6 cases occurred
following 229 trabeculectomies with mitomycin, with a mean follow-up of 18
months, an approximate rate of 1.8% per year.8
In the second, bleb-associated endophthalmitis developed in 13 cases, an average
of 18.5 months following 609 trabeculectomies with mitomycin, a rate of 1.4%
per year.6
There are limitations to our analysis. Because we only studied the patients
of glaucoma specialists, our study may not be generalizable to glaucoma surgery
performed by nonspecialists. Also, our study design depended on surgeon recall
of cases of endophthalmitis that occurred during a long period. There were
undoubtedly cases that were not recalled, and the effect of not including
these forgotten cases in our analysis cannot be determined. Finally, statistical
analysis using linear regression models merely determine whether outcomes
and covariates are statistically related, and not whether they are causally
related.
On the basis of our analyses, we recommend that full-thickness filtration
procedures and trabeculectomies performed at locations other than the superior
limbus be performed only if the indications are compelling. The possibility
that mitomycin could increase the risk of late-onset endophthalmitis should
be factored into the risk/benefit equation determining its use in an individual
eye. Surgeons ought to think carefully before embarking on an intermittent
or chronic course of antibiotics as prophylaxis against blebitis or endophthalmitis.
Patients whose eyes have received mitomycin had a serious complication in
the immediate postoperative period, have a bleb that appears high or thin,
have a bleb leak, or have tempted the surgeon to consider or initiate antibiotic
therapy need to be monitored particularly closely for the earliest signs of
infection. It seems that the most successful filtration operations, in eyes
with low IOP and receiving no medication, are at greatest risk. All patients,
but particularly the patients just described, should be provided with specific
instructions on how to obtain emergency care and instructed to inform their
surgeon immediately of the signs and symptoms of possible infection. We believe
that detection at the earliest stages of infection will result in better outcomes,
but this assumption also merits further study.
AUTHOR INFORMATION
Accepted for publication January 10, 2001.
This study was supported by the Glaucoma Research Foundation, San Francisco,
Calif.
We would like to acknowledge Sandra Wilson for her help in data collection.
Glaucoma Surgical Outcomes Study Group*
Baltimore, Md: Harry Quigley, MD, Henry Jampel,
MD, David Friedman, MD, Wilmer Eye Institute, Alan Robin, MD;
Chevy Chase, Md: Arthur Schwartz, MD; Philadelphia, Pa: Jay Katz, MD, George Spaeth, MD, Richard
Wilson, MD, Marlene Moster, MD, Wills Eye Hospital; New
York, NY: Jeffrey Liebmann, MD, Robert Ritch, MD, Kevin Greenidge,
MD, Alyson Hall, MD, New York Eye and Ear Infirmary; Miami,
Fla: Steven Gedde, MD, Douglas Anderson, MD, Paul Palmberg, MD, Richard
Parrish, MD, Elizabeth Hodapp, MD, Donald Budenz, MD, Bascom Palmer Eye Institute;
Boston, Mass: John Thomas, MD, Richard Simmons,
MD, Bradford Shingleton, MD, Claudia Richter, MD, A. Robert Bellows, MD, B.
Thomas Hutchinson, MD; Detroit, Mich: Dong Shin,
MD, PhD, Kresge Eye Institute; Ann Arbor, Mich: Paul
Lichter, MD, Kellogg Eye Institute; Seattle, Wash:
Murray Johnstone, MD.
*Not all study investigators contributed cases.
Corresponding author and reprints: Henry D. Jampel, MD, MHS, Wilmer
Eye Institute, Maumenee B-110, 600 N Wolfe St, Baltimore, MD 21287-9205 (e-mail: hjampel{at}jhmi.edu).
From the Wilmer Eye Institute, Baltimore, Md.
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