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Trabeculectomy function after cataract extraction1
Trabeculectomy Function after Cataract Extraction Philip P. Chen, MD,1 Yaffa K. Weaver, MD,2 Donald L. Budenz, MD,2 William J. Feuer, MS,2 Richard K. Parrish II, MD2 Objective: To examine the effect of cataract extraction (CE) after trabeculectomy on intraocular pressure (IOP) control. Design: Retrospective noncomparative case series. Participants: A total of 115 consecutive patients who underwent extracapsular CE (N ⫽ 58) or phacoemulsification (N ⫽ 57) with intraocular lens (IOL) placement after trabeculectomy were studied. Intervention: Cataract extraction with IOL after trabeculectomy was performed. Main Outcome Measures: Preoperative, intraoperative, and postoperative factors were evaluated for association with loss of IOP control requiring additional medications, bleb needling, or further glaucoma surgery, using Kaplan–Meier survival analysis and Cox multivariate proportional hazards survival regression. Results: After mean postoperative follow-up of 21.1 ⫾ 14.3 months, additional glaucoma medication or needling of the filtering bleb to maintain IOP control was required in 35 eyes (30.4%) and was significantly associated with intraoperative iris manipulation and early postoperative peak IOP greater than 25 mmHg. Additional glaucoma surgery was eventually required in 11 eyes (9.6%) and was significantly associated with age of 50 years or younger, preoperative IOP greater than 10 mmHg, and early postoperative peak IOP greater than 25 mmHg. The cumulative proportion of patients who did not require reoperation for glaucoma was 93% and 90% at 1 and 2 years, respectively. The mean IOP at last visit had increased 1.6 mmHg above the pre-CE level and did not vary significantly after the first postoperative month. The median interval from CE to the addition of glaucoma medication or bleb needling was 1.6 months (within 3 months in 20 of 33 eyes) and that from nonsurgical intervention to further glaucoma surgery was 3.6 months (before the 7th postoperative month in 6 of 11 eyes). Of 19 eyes with hypotony (IOP 聿 6 mmHg) before CE, 11 eyes remained hypotonous after CE despite an increase in the mean IOP from 4.6 to 7.5 mmHg. Conclusions: When CE is performed after trabeculectomy, age of 50 years or younger, preoperative IOP greater than 10 mmHg, intraoperative iris manipulation, and early postoperative IOP greater than 25 mmHg are associated with worsened postoperative IOP control. Most bleb failures occur soon after CE. Resolution of pre-existing hypotony after CE is unpredictable. Ophthalmology 1998;105:1928 –1935 Glaucoma-filtering surgery may accelerate cataract formation in eyes with postoperative hypotony, shallow anterior chamber, or excessive inflammation.1– 4 Cataract extraction (CE) after glaucoma-filtering surgery may decrease bleb size and function and result in higher intraocular pressure (IOP); previous studies have reported 10% to 38% of eyes require additional medication or further glaucoma surgery
Originally received: November 24, 1997. Revision accepted: April 10, 1998. Manuscript no. 97810. 1 Department of Ophthalmology, University of Washington, Seattle, Washington. 2 Department of Ophthalmology, University of Miami School of Medicine, Bascom Palmer Eye Institute, Miami, Florida. Supported in part by an unrestricted grant from Research to Prevent Blindness, Inc, New York, New York; and Public Health Service Research Grant EY10410, Department of Health and Human Services, National Institutes of Health, National Eye Institute, Bethesda, Maryland. None of the authors have any proprietary interest in any of the products mentioned in this article. Reprint requests to Philip P. Chen, MD, Department of Ophthalmology, University of Washington, Box 356485, Seattle, WA 98195.
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to maintain IOP control after extracapsular cataract extraction (ECCE) with intraocular lens (IOL) placement.5–9 Minimizing intraoperative tissue trauma and postoperative inflammation may play a role in maintaining bleb function after CE.10,11 Uncomplicated phacoemulsification (PE) has been shown to result in significantly lower aqueous flare and cells after surgery than ECCE12,13 and fewer filtering bleb failures.14,15 Other authors have noted resolution of posttrabeculectomy hypotony after CE.16,17 We retrospectively examined preoperative, intraoperative, and postoperative factors to identify risk factors associated with loss of IOP control after ECCE or PE with IOL placement. We also investigated the resolution of post-trabeculectomy hypotony after CE.
Methods Before medical records were reviewed, approval for this study was given by the Medical Sciences Subcommittee for the Protection of Human Subjects in Research at the University of Miami School of Medicine. A computerized search using surgical current proce-
Chen et al 䡠 Cataract Extraction after Trabeculectomy Table 1. Outcomes of Trabeculectomy Function after Cataract Extraction Outcome
Definition
Complete success Qualified success Failure
No additional medications,* bleb needling, or further glaucoma surgery Additional medication* or bleb needling needed for IOP control Further glaucoma surgery needed for IOP control
IOP ⫽ intraocular pressure. * Additional medications used more than 2 months after cataract extraction.
dural terminology codes was used to identify patients who had undergone CE after trabeculectomy between January 1991 and December 1995 at the Anne Bates Leach Eye Hospital, Miami, Florida. Variables investigated included age at time of CE, gender, race, eye, type of glaucoma, best-corrected Snellen visual acuity, number and type of glaucoma medications, previous incisional ocular surgeries, time elapsed since the most recent trabeculectomy to the cataract surgery, type of antifibrosis agent used with the most recent trabeculectomy, bleb appearance (pre- and postCE), IOP (the average IOP during the 4 months preceding CE, the maximum IOP during the first 2 postoperative weeks, and the IOP at 1, 2, 3, 6, 9, 12, 18, 24, and 36 months and at the last visit after surgery), method of CE (ECCE vs. PE), position of cataract incision relative to the filtering bleb, cataract incision location (clear corneal vs. limbal vs. scleral), length and closure (number and type of sutures), IOL type and placement, intraoperative iris manipulation, intraoperative and postoperative complications, postoperative medications and antifibrosis agents administered, and the dates when new glaucoma medicines were added or further glaucoma surgery was performed. Patients undergoing planned ECCE had a 7.0- to 11.5-mm incision made either in peripheral cornea or through the surgical limbus, either adjacent to or in a separate quadrant from the filtering bleb, followed by can-opener anterior capsulotomy, nuclear mobilization and expression, manual or automated irrigation and aspiration of cortical remnants, placement of a polymethylmethacrylate (PMMA) IOL, and wound closure with 10 – 0 nylon sutures. Patients undergoing PE had a tunnel incision (length, 3.2–7.0 mm) made in peripheral cornea or sclera, followed by continuous-tear capsulorhexis, nuclear hydrodissection and emulsification, automated irrigation and aspiration of cortical remnants, placement of a silicone foldable or PMMA IOL, and wound closure with 10 – 0 nylon sutures in some cases. Iris manipulation (posterior synechiolysis, stretching, sphincterotomies, sector iridectomy, or use of iris retraction hooks [Grieshaber, Kennesaw, Georgia]) was performed as necessary to enable CE. Intraocular lenses were implanted in the posterior capsular bag or the ciliary sulcus; in one patient, an anterior chamber IOL was used. We defined complete success as the absence of additional glaucoma medications, bleb needling, or further glaucoma surgery for long-term IOP control after CE (Table 1); however, additional glaucoma medicines used within the first 2 postoperative months were permitted. Eyes that required additional medications for IOP control after the second postoperative month or that underwent bleb needling at the slit lamp were considered qualified successes. We included bleb needling in the same category as additional medications because some surgeons preferred to needle a previously functioning bleb rather than start new medications (1 surgeon performed 8 of 9 needlings), and the mean IOP at the time bleb needling was performed was not significantly different from
that when additional medication was added (28.6 ⫾ 4.6 vs. 27.1 ⫾ 8.3 mmHg). This indicated that blebs that underwent needling were not failing to a greater degree than blebs that had medications added. Eyes that underwent further glaucoma surgery were considered failures. Based on the above criteria, each variable was evaluated for association with trabeculectomy survival (i.e., time to qualified success or failure) using Kaplan–Meier survival analysis. Although survival analysis predicates inclusion of all patients regardless of length of follow-up, to maintain clinical relevance we excluded patients with less than 6 months of follow-up. Cox multivariate proportional hazards survival regression using forward-stepwise variable selection was used to determine which risk factors were independent predictors of qualified success or failure. All preoperative and intraoperative variables were candidates for entry into the model (not only those identified as significant by univariate analysis). Differences in pre- and post-CE IOP were examined for statistical significance using paired and two-sample, two-tailed Student’s t test. Results are given as the mean ⫾ standard deviation where applicable.
Results The search by CPT codes identified 125 eyes of 125 consecutive patients who had CE after trabeculectomy. Two patients were excluded from analysis because their glaucoma (due to traumatic hyphema) had resolved despite a flat bleb, and the cataract incision was made at the trabeculectomy site without attempt to maintain bleb function. Eight patients were excluded because of follow-up of less than 6 months, resulting in a study population of 115 eyes of 115 patients. The mean age at the time of CE was 68.9 ⫾ 12.0 years (range, 17– 88 years) and differed significantly between patients having ECCE (71.5 ⫾ 8.6 years, N ⫽ 58) and PE (66.2 ⫾ 14.2 years, N ⫽ 57; P ⫽ 0.02). Demographic data and characteristics of the patients in this study are listed in Table 2. No patients had bleb revision in conjunction with CE, but one patient had choroidal effusions drained at the time of ECCE and one patient had pars plana vitrectomy performed on the same date as PE for retained nuclear fragments. The mean follow-up was 21.1 ⫾ 14.3 months (range, 6 – 60 months) and was significantly longer for ECCE (24.5 ⫾ 16.3 months) compared to PE (17.6 ⫾ 10.9 months, P ⬍ 0.001). Nine patients were included in the survival analysis only until the last office visit before the date when nonglaucoma-related intraocular surgery was performed, which included repair of traumatic cataract wound dehiscence on postoperative day 16 (1), pars plana vitrectomy (for vitreous hemorrhage [1, at 3.2 months], bleb-related endophthalmitis [1, at 13 months], and epiretinal membrane [1, at 31.3 months]), bleb revision for hypotony (3, all within 3.5 months), and penetrating keratoplasty for pseudophakic bullous keratopathy (2, at 6 and 6.5 months). Thirty-five eyes (30.4%) required additional medication or filtering bleb needling (i.e., were qualified successes) to maintain IOP control after surgery. Eleven eyes (9.6%) required additional glaucoma surgery (i.e., were failures), including trabeculectomy (6), glaucoma drainage device placement (5), and pars plana vitrectomy for aqueous misdirection (1). All but one patient in the failure group was a qualified success before reoperation. The cumulative proportion of patients who did not need further glaucoma surgery (i.e., were not failures) was 93% at 1 year (N ⫽ 72), 90% at 2 years (N ⫽ 45), and 85% at 3 years (N ⫽ 20) (Fig 1). The cumulative proportion of patients who also did not require additional glaucoma medicines or bleb needling (i.e., were com-
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Ophthalmology Volume 105, Number 10, October 1998 Table 2. Demographic Data and Characteristics of Eyes Having Cataract Extraction (CE) after Trabeculectomy
Gender Male Female Race White Hispanic Black Asian Glaucoma type Primary open-angle Chronic angle closure Pseudoexfoliation Normal tension Mixed mechanism Pigmentary Uveitic Traumatic Neovascular Steroid-induced Trabeculectomy location Superior 180° Inferior 180° Antifibrosis agent with last trabeculectomy None 5-Fluorouracil (10–45 mg) Mitomycin C No. of incisional surgeries before CE 1 trabeculectomy 2 trabeculectomies 3 trabeculectomies No. of glaucoma medications prior to CE 1 2 3 Interval from trabeculectomy to CE (mos) All eyes ECCE (N ⫽ 58) PE (N ⫽ 57) Incision location: ECCE Clear cornea Limbus Incision location: PE Clear cornea Sclera Incision length and type: PE Small (ⱕ4 mm) Unsutured
N
%
57 58
(50) (50)
56 42 17 1
(49) (37) (15) (1)
57 15 11 10 7 5 4 3 2 1
(50) (13) (10) (9) (6) (4) (3) (3) (2) (1)
112 3
(97) (3)
29 36 50
(25) (31) (43)
98 15 2
(85) (13) (2)
11 1 3
(9) (1) (3)
19.9 ⫾ 17.3 18.6 ⫾ 15.5 21.2 ⫾ 19.1 42 16
(72) (28)
12 45
(21) (79)
42 21
(74) (37)
Figure 1. Kaplan–Meier survival curves for intraocular pressure control in eyes undergoing cataract extraction after trabeculectomy.
within the first postoperative week, 5 at 1.0 – 4.3 months), six of whom used additional medications either before or after needling and two of whom eventually had further glaucoma surgery. The median time to qualified success was 1.6 months (range, 0.03–58.0 months) and was before 3 months in 10 (77%) of 13 eyes after PE and in 10 (45%) of 22 eyes after ECCE. The median time from qualified success to failure was 3.6 months (range, 0.3–19.1 months). Six (55%) of 11 failures occurred within 6.5 months after CE.
ECCE ⫽ extracapsular cataract extraction; PE ⫽ phacoemulsification.
plete successes) was 75% at 1 year, 67% at 2 years, and 59% at 3 years (Fig 1). Cumulative survival did not differ significantly by type of CE (ECCE vs. PE) (Fig 2), but Cox multivariate proportional hazards regression, adjusted for other statistically significant variables, estimated a risk ratio of 1.1 for qualified success (95% confidence interval [CI] 0.6, 2.2), and 3.0 for failure (95% CI 0.7, 12.8), for eyes having ECCE compared to PE. Forty-nine patients (43%) required from 1 to 4 medications for IOP control; 32 patients (28%) used medications beyond the second postoperative month, 8 of whom eventually had further glaucoma surgery. Of 15 patients who used glaucoma medications before surgery, 7 used the same number at the last follow-up, 3 required more, and 5 used fewer medications. Nine patients (7.8%) underwent needling revision of the filtering bleb at the slit lamp (4
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Figure 2. Kaplan–Meier survival curves for intraocular pressure control in eyes undergoing extracapsular cataract extraction and phacoemulsification (Phaco) after trabeculectomy.
Chen et al 䡠 Cataract Extraction after Trabeculectomy Table 4. Factors Associated with Failure in Eyes Having Cataract Extraction (CE) after Trabeculectomy Factor Age at time of CE ⱕ50 yrs ⬎50 yrs Glaucoma type POAG Uveitic Time from trabeculectomy to CE ⱕ6 mos ⬎6 mos Early postoperative maximum IOP‡ ⱕ25 mmHg ⬎25 mmHg
Figure 3. Mean intraocular pressure in eyes undergoing cataract extraction after trabeculectomy, for all patients and for those eyes that were complete successes at last follow-up.
The average preoperative IOP was 10.5 ⫾ 3.9 mmHg (range, 3–19). Eyes that became qualified successes or failures had higher mean preoperative IOP compared to those that did not (12.1 ⫾ 3.6 vs. 9.8 ⫾ 3.8 mmHg; P ⫽ 0.005) (Fig 3). Although preoperative IOP as a continuous variable was not associated with trabeculectomy survival, preoperative IOP greater than 10 mmHg was significantly associated with qualified success (P ⫽ 0.036) (Table 3), and this association remained significant (risk ratio, 2.2; 95% CI 1.0, 4.5; P ⫽ 0.030) after multivariate analysis. The mean maximum IOP during the first 2 postoperative weeks was 19.5 ⫾ 10.0 mmHg. However, IOP greater than 25 mmHg during this period was noted in 31 patients (27%) in whom qualified success (P ⬍ 0.001) and failure (P ⫽ 0.008) were subsequently more likely compared to those patients who had IOP less than 25 mmHg (Tables 3 and 4). The mean IOP in all eyes
Table 3. Factors Associated with Qualified Success in Eyes Having Cataract Extraction (CE) after Trabeculectomy Factor Preoperative IOP ⱕ10 mmHg ⬎10 mmHg Intraoperative iris manipulation None Any‡ Early postoperative maximum IOP§ ⱕ25 mmHg ⬎25 mmHg
N
Survival (%)*
P†
58 57
83 ⫾ 5 66 ⫾ 7
0.036㛳
62 53
83 ⫾ 5 64 ⫾ 7
0.027㛳
83
85 ⫾ 4
31
45 ⫾ 9
⬍0.001
IOP ⫽ intraocular pressure. * Kaplan-Meier survival analysis estimate of 12-month survival rate. † Log rank P value. ‡ Includes posterior synechiolysis, pupil stretching, sphincterotomy, iridectomy, iris suturing, and/or use of iris retraction hooks. § Maximum IOP measured within the first 2 postoperative weeks; not included in multivariate survival regression; data missing from one eye. 㛳 Maintained significance after Cox multivariate proportional hazards survival regression analysis of preoperative and intraoperative factors.
N
Survival (%)*
P†
7 108
64 ⫾ 21 95 ⫾ 2
0.062§
57 4
95 ⫾ 3 38 ⫾ 29
18 97
75 ⫾ 11 97 ⫾ 2
83 31
97 ⫾ 2 83 ⫾ 7
0.007 0.038
0.008
IOP ⫽ intraocular pressure; POAG ⫽ primary open-angle glaucoma. * Kaplan-Meier survival analysis estimate of 12-month survival rate. † Log rank P value. ‡ Maximum IOP measured within the first 2 postoperative weeks; not included in multivariate survival regression; data missing from one eye. § Remained significant (P ⫽ 0.033) after Cox multivariate proportional hazards survival regression analysis of preoperative and intraoperative factors.
increased to 12.1 ⫾ 5.1 mmHg at last visit and was increased significantly at each postoperative timepoint through 18 months compared to the pre-CE IOP but did not vary significantly after the first postoperative month. In eyes that were complete successes, the mean IOP increased significantly from 9.8 ⫾ 3.8 to 10.8 ⫾ 4.1 mmHg at last visit. Other preoperative variables associated with further glaucoma surgery by univariate (Kaplan–Meier) analysis included uveitic glaucoma (vs. POAG, P ⫽ 0.007), CE at 6 months or less after trabeculectomy (P ⫽ 0.038), and age of 50 years or younger (P ⫽ 0.062) (Table 4). After multivariate analysis, age of 50 years or younger remained significant (risk ratio, 8.4; 95% CI ⫽ 1.7– 40.9; P ⫽ 0.033), and CE greater than 6 months after trabeculectomy was borderline protective against failure (risk ratio, 0.5; 95% CI 0.2, 1.1; P ⫽ 0.087). No other preoperative variables were shown to be associated with qualified success or failure after CE, including use of antifibrosis agents with the most recent trabeculectomy, number of prior trabeculectomies, or number of glaucoma medications. Preoperative bleb appearance was noted to be “avascular,” “good,” “elevated,” or “large” in 91 eyes (79%); these terms were used for 65 (59%) of 111 eyes in which postoperative bleb appearance was described. The bleb was “small” or “flat” in 8 eyes (7%) before CE; these terms were used for 25 eyes (22%) after surgery. No significant difference in survival was found between the two sets of terms. Intraoperative iris manipulation was associated significantly with the need for additional medications or bleb needling after surgery (P ⫽ 0.027, Table 3), and this association withstood multivariate analysis (risk ratio, 2.3; 95% CI ⫽ 1.1, 4.5; P ⫽ 0.019). Neither the location (clear cornea vs. limbus in ECCE, or vs. sclera in PE), length, nor closure of the incision was associated with different survival. Only 1 (2.4%) of 42 patients who underwent small incision PE (length ⱕ 4 mm) with foldable silicone IOL was a failure because of postoperative aqueous misdirection necessitating pars plana vitrectomy, after which the bleb continued to function. If this case is not considered to be a failure of bleb function, then large incision (length ⬎ 4 mm) CE is associated significantly with bleb failure (10 [13.7%] of 73 eyes; P ⫽ 0.035).
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Ophthalmology Volume 105, Number 10, October 1998 Table 5. Studies on Intraocular Pressure (IOP) Control in Eyes Having Extracapsular Cataract Extraction (ECCE) or Phacoemulsification (PE) with Intraocular Lens (IOL) after Glaucoma Filtering Surgery* N (ECCE/PE)
Follow-up (months)
3/7
⬎12
Binkhorst (1981)
26/0
Mean “almost 36”
Obstbaum6 (1986)
15/0
ⱖ9
Antonios28 (1988)
29/0
Median 13
Murchison7 (1989)
22/0
Mean 22.3
Brooks30 (1992)
43/0
12
36/9 (before exclusion)
24
Study Alpar
15
(1979) 5
Yamagami8 (1994)
Dickens9 (1996)
23/0
Median 70
Seah14 (1996)
16/6
Mean 13.6
Present study
58/57
24.5/17.6 Mean 21.1
Definition of Success Not defined
% Success (ECCE/PE) 66/86
“Normal” IOP and no See comment glaucoma medications
Comments Excluded if ⬍1 year follow-up or complication during CE 3 of 33 eyes required additional medications or reoperation, not noted whether these were after ICCE or ECCE Excluded if ⬍9 mos follow-up
IOP unchanged and 80/NA no increase in glaucoma medications Same as current study CS-69/NA QS-31/NA Excluded if ⬍8 mos follow-up; 7 eyes F-0/NA had IOLs; all had ECCE ⬎1 yr after filtering surgery Same as current study CS-68/NA QS-23/NA Excluded if ⬍6 mos follow-up F-9/NA No further glaucoma 98/NA 43 eyes of 33 patients; pre- and postsurgery cataract extraction medications not provided No increase in 67 (see comment) Excluded 6 patients with post-CE iritis; glaucoma included 13 patients without medications functioning filtering bleb pre-CE; separate analysis of ECCE and PE not provided Same as current study CS-65/NA QS-26/NA Excluded if ⬍4 yrs follow-up F-9/NA See comment CS-38/67 QS-31/0 Excluded if ⬍6 mos follow-up; CS ⫽ F-31/33 IOP ⱕ 19 without intervention; QS ⫽ IOP ⱕ 19 with medication; F ⫽ IOP ⬎ 19 or further surgery See text/Table 1 CS-64/74 QS-22/19 Excluded if ⬍ 6 mos follow-up F-14/5
NA ⫽ not applicable; CS ⫽ complete success; QS ⫽ qualified success; F ⫽ failure. * With minimum follow-up of (mean) 6 months.
Intraoperative complications occurred in 7 eyes (6%) and postoperative complications developed in 31 eyes (27%), including posterior capsular tear with (3) and without (1) vitreous loss, retained nuclear fragments (2), retained cortical remnants (3), hyphema (5), transient bleb leak (3) or cataract wound leak (6), traumatic wound dehiscence (1), aqueous misdirection (1), persistent corneal edema (5), persistent inflammation (3), IOL capture (2), vitreous hemorrhage (1), cystoid macular edema (4), epiretinal membrane formation (1), late bleb-related endophthalmitis (1), and ptosis (2). Of two eyes noted to have bleb leaks before surgery, one leaked intermittently after CE. No intraoperative or postoperative complication was associated significantly with different trabeculectomy survival, nor was use of postoperative subconjunctival 5-fluorouracil (5-FU) injections (9 patients; total dose, 5–25 mg). Nineteen eyes (17% of all eyes) had hypotony (IOP ⱕ 6 mmHg) before CE (mean IOP, 4.6 ⫾ 1.1 mmHg). Trabeculectomy had been performed with mitomycin C in 13 eyes and with 5-FU in 3 eyes. Phacoemulsification was performed in 13 eyes and ECCE in 6 eyes. Eleven eyes (58%) continued to have hypotony after CE, including 3 eyes that required revision of trabeculectomy for hypotony-related corneal folds, after mean follow-up of 14.6 ⫾ 11 months (17 ⫾ 10.5 months if eyes censored for trabeculectomy revision are excluded). The mean peak IOP in the first 2 postoperative weeks was 15.8 ⫾ 11.5 mmHg and did not differ significantly for those eyes in which hypotony resolved after CE. Although the mean IOP at last follow-up increased significantly to
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7.5 ⫾ 3.6 mmHg (P ⫽ 0.002), no factor was associated significantly with resolution of hypotony. After CE, two eyes required glaucoma medications for less than 1 month and two eyes underwent bleb needling (at 0.3 and 1 month). One eye had pre-CE hypotony maculopathy, which had not resolved after 7.4 months’ follow-up. Of 115 eyes, 110 (96%) had corrected preoperative Snellen visual acuity of 20/50 or worse. Postoperative visual acuity was 20/40 or better in 82 eyes (71%) and 20/100 or worse in 16 eyes (14%). Only two eyes (1.7%) had worse postoperative visual acuity during follow-up. The method of CE was not associated significantly with different postoperative visual acuity.
Discussion Several reports have described the effect of CE on IOP control after trabeculectomy.5–9,14,15 Table 5 summarizes studies with follow-up of at least 6 months and sufficient information to allow comparison with our patients. The few that have investigated outcomes after PE are limited by small sample size (6 –9 eyes).8,14,15 Variations in exclusion and success criteria, follow-up time, and methods of statis-
Chen et al 䡠 Cataract Extraction after Trabeculectomy tical analysis make comparisons with previous studies difficult. In addition, practice patterns may vary by physician, and the pre-existing severity of glaucomatous damage undoubtedly influences the threshold for adding medications or performing further glaucoma surgery, so the use of medical or surgical intervention as an indicator for trabeculectomy failure may not provide the most accurate benchmarks for comparison. Nonetheless, the proportion of patients who were in each outcome category in our study was similar to that in several previous studies that included primarily ECCE with IOL after glaucoma-filtering surgery.7–9,14 We found 22% of patients required only medical intervention or bleb needling, and 9.6% required further glaucoma surgery. We found an encouraging cumulative failure-avoidance rate of 93% and 90% at 1 and 2 years, respectively, but the cumulative complete success rate was lower at 75% and 67% at 1 and 2 years, respectively (Fig 1). Yamagami et al8 also used Kaplan–Meier survival analysis and found IOP control was maintained in 22 (56%) of 39 eyes 2 years after ECCE or PE; however, 6 eyes with postoperative iritis were excluded from analysis. We identified several preoperative variables that were associated significantly (by univariate Kaplan–Meier survival analysis) with loss of IOP control, including uveitic glaucoma, period less than 6 months between trabeculectomy and CE, pre-CE IOP greater than 10 mmHg, and age of 50 years or younger. Patients with uveitis have been reported to have an exaggerated postoperative inflammatory response after CE with IOL implantation.18 Although the diagnosis of uveitic glaucoma includes numerous openangle and angle-closure etiologies of elevated IOP, chronic intraocular inflammation is the underlying factor that may contribute to bleb failure after CE. An interval between trabeculectomy and CE of 6 months or less was associated significantly with reoperation for glaucoma. Other authors have reached similar conclusions and believe the filtering bleb needs sufficient time to develop properly19,20; the inflammation associated with cataract surgery presumably curtails this process. In our study, patients who maintained IOP control without additional intervention had a significantly lower mean pre-CE IOP than did those who were qualified successes or failures (9.8 vs. 12.1 mmHg). Patients with higher IOP before CE may have filtering blebs with borderline function, which are likely more susceptible to fibrosis after CE. Relative youth is a well-recognized risk factor for filtering surgery failure10 and is likely related to loss of IOP control after CE for similar reasons. After multivariate analysis, only IOP greater than 10 mmHg and age of 50 years or younger remained significantly associated with further glaucoma surgery. An interval greater than 6 months between trabeculectomy and CE was of borderline significance as protective from failure. Of 57 patients who had PE, 3 (5.3%) required further glaucoma surgery after mean follow-up of 18 months. Two patients had uveitic glaucoma and had their cataract incisions enlarged to 6 and 7 mm for PMMA lens placement. In the third patient, small-incision PE precipitated aqueous misdirection that required pars plana vitrectomy for resolution, but bleb function was not lost. In comparison, 8 (13.7%) of 58 patients who had ECCE were failures after
mean follow-up of 24.5 months (Fig 2). However, Kaplan– Meier survival analysis and Cox multivariate proportional hazards regression showed no statistically significant difference between ECCE and PE in progression to qualified success (risk ratio, 1.1 for ECCE) or failure (risk ratio, 3.0 for ECCE) (the risk ratio is larger for failure, although the difference between ECCE and PE in Fig 2 appears larger for qualified success, because the standard errors are smaller when survival is close to 1). The lack of significance may be because of the small number of failures in our study population, the significant difference in follow-up time between the two methods of CE, and the total sample size. A clinically important difference in failure between small (ⱕ4 mm) and large incision size (2.4% vs. 13.7% failure, respectively) may not have been statistically significant because the one failure after small-incision PE occurred 2 weeks after surgery. Some authors have noted mitomycin C to be associated with long-term protection from subsequent failure despite severe inflammation.21 Use of antifibrosis agents with the most recent trabeculectomy did not influence survival after CE in our study. Both 5-FU and mitomycin C affect local fibroblast proliferation rather than migration,22,23 and although mitomycin C may have considerably prolonged effects compared to those of 5-FU,23 its half-life after topical administration is limited,24 and inflammation occurring after CE may result in further recruitment and migration of cicatrix-forming cells. In this study, use of 5-FU injections after CE did not influence bleb survival and IOP control, but the number of patients was small and patient selection was likely biased toward those with more intraocular inflammation or external vascularization. A randomized, prospective study would be needed to properly investigate the role of 5-FU injections after CE in patients with functioning filtering blebs. Intraoperative iris manipulation was associated significantly with the need for additional medications or bleb needling, probably through long-term postoperative inflammation due to blood–aqueous barrier breakdown25 and the underlying cause of the posterior synechiae (miotic use, diabetes mellitus, previous uveitis, previous surgery, or pseudoexfoliation syndrome). In the current study, 46% of patients required iris manipulation. The surgical challenge these patients may pose is reflected in the relatively high complication rate seen in this and previous studies.7,8,14 One study found intraoperative complications frequently led to bleb failure,14 but this association was not seen in our study. The mechanism for loss of IOP control in most patients with previously functioning filtering blebs is external scarring at the level of Tenon capsule and episclera.26,27 Other authors have observed bleb scarring and shrinkage after CE,5,8,9 sometimes with worsened IOP control.8 Reduced bleb size was noted in approximately 18% of eyes in our study, but change in bleb appearance was not associated with different survival, although this is difficult to assess accurately in a retrospective study. Different authors have noted changes in mean IOP after CE ranging from a decrease of 0.8 mmHg to an increase of 6.6 mmHg, after mean or median follow-up ranging from 8 to 70 months.5–9,14,28 –31 We found an increase in mean IOP
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Ophthalmology Volume 105, Number 10, October 1998 of 1.6 mmHg overall, 1.0 mmHg for patients who were complete successes. Of note, the mean IOP stabilized quickly and did not vary significantly after the first postoperative month. A marked postoperative IOP rise is not uncommon after uncomplicated ECCE in patients with glaucoma.32 In our study, eyes with a postoperative IOP spike greater than 25 mmHg subsequently had significantly worse IOP control. These patients should be monitored carefully as their bleb function may be tenuous. Some IOP spikes may be related to retained viscoelastic material after CE. Mechanical causes of decreased filtration after CE, such as iris, vitreous, or IOL haptic incarceration into the internal sclerostomy, were not noted in our study. Cataract surgery has been advocated to treat postfiltering surgery hypotony maculopathy16,17 and chronic choroidal detachment33 in those patients with coexisting cataract. In our series, 19 patients had hypotony (IOP ⱕ 6 mmHg) after trabeculectomy, 11 (58%) of whom continued to have hypotony or needed bleb revision for hypotony at last followup. Although the mean IOP increased significantly from 4.6 to 7.5 mmHg, none of the factors investigated was associated significantly with resolution of hypotony. Cataract surgery did not reliably resolve hypotony after filtration surgery in our study. A decrease in IOP control over time after successful trabeculectomy, even without intervening nonglaucoma-related surgical intervention, has been reported.2,3,11,34 –37 Loss of bleb function related to such attrition was not distinguished from that due to CE in the current study. Nonetheless, our findings suggest that CE in the presence of a functioning filtering bleb results in a low cumulative rate of severe loss of IOP control, and few patients (9.6%) require reoperation for glaucoma. Patients 50 years of age or younger, with IOP of 11 mmHg or greater, or who need intraoperative iris manipulation for CE, are at significantly higher risk for loss of IOP control, as are those with early postoperative IOP greater than 25 mmHg. The mean postoperative IOP did not vary significantly after the first postoperative month, and most eyes that needed additional medications or needling, or further glaucoma surgery, required intervention before the 3rd and 7th postoperative months, respectively. For most patients with glaucoma with functioning filtering blebs, CE may be recommended with the anticipation of both restoration of visual acuity and continued IOP control.
References 1. Sugar HS. Postoperative cataract in successfully filtering glaucomatous eyes. Am J Ophthalmol 1970;69:740 – 6. 2. D’Ermo F, Bonomi L, Doro D. A critical analysis of the long-term results of trabeculectomy. Am J Ophthalmol 1979; 88:829 –35. 3. Mills KB. Trabeculectomy: a retrospective long-term follow-up of 444 cases. Br J Ophthalmol 1981;65:790 –5. 4. Vesti E. Development of cataract after trabeculectomy. Acta Ophthalmol (Copenh) 1993;71:777– 81.
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5. Binkhorst CD, Huber C. Cataract extraction and intraocular lens implantation after fistulizing glaucoma surgery. J Am Intraocular Implant Soc 1981;7:133–7. 6. Obstbaum SA. Glaucoma and intraocular lens implantation. J Cataract Refract Surg 1986;12:257– 61. 7. Murchison JF Jr, Shields MB. An evaluation of three surgical approaches for coexisting cataract and glaucoma. Ophthalmic Surg 1989;20:393– 8. 8. Yamagami S, Araie M, Mori M, Mishima K. Posterior chamber intraocular lens implantation in filtered or nonfiltered glaucoma eyes. Jpn J Ophthalmol 1994;38:71–9. 9. Dickens MA, Cashwell LF. Long-term effect of cataract extraction on the function of an established filtering bleb. Ophthalmic Surg Lasers 1996;27:9 –14. 10. Skuta GL, Parrish RK II. Wound healing in glaucoma filtering surgery. Surv Ophthalmol 1987;32:149 –70. 11. Araujo SV, Spaeth GL, Roth SM, Starita RJ. A ten-year follow-up on a prospective, randomized trial of postoperative corticosteroids after trabeculectomy. Ophthalmology 1995; 102:1753–9. 12. Oshika T, Yoshimura K, Miyata N. Postsurgical inflammation after phacoemulsification and extracapsular extraction with soft or conventional intraocular lens implantation. J Cataract Refract Surg 1992;18:356 – 61. 13. Pande MV, Spalton DJ, Kerr–Muir MG, Marshall J. Postoperative inflammatory response to phacoemulsification and extracapsular cataract surgery: aqueous flare and cells. J Cataract Refract Surg 1996;22(Suppl 1):770 – 4. 14. Seah SKL, Jap A, Prata JA Jr, et al. Cataract surgery after trabeculectomy. Ophthalmic Surg Lasers 1996;27:587–94. 15. Alpar JJ. Cataract extraction and lens implantation in eyes with pre-existing filtering blebs. J Am Intraocular Implant Soc 1979;5:33–5. 16. Sibayan SAB, Igarashi S, Kasahara N, et al. Cataract extraction as a means of treating postfiltration hypotony maculopathy [case reports]. Ophthalmic Surg Lasers 1997;28:241–3. 17. Allingham RR. Treatment of hypotonous maculopathy. In: Epstein DL, Allingham RR, Schuman JS, eds. Chandler and Grant’s Glaucoma, 4th ed. Baltimore: Williams & Wilkins, 1997;549. 18. Foster RE, Lowder CY, Meisler DM, Zakov ZN. Extracapsular cataract extraction and posterior chamber intraocular lens implantation in uveitis patients. Ophthalmology 1992;99: 1234 – 41. 19. Shields MB. Combined cataract extraction and guarded sclerectomy. Reevaluation in the extracapsular era. Ophthalmology 1986;93:366 –70. 20. Shields MB. Textbook of glaucoma, 4th ed. Baltimore: Williams & Wilkins, 1998;566. 21. Yaldo MK, Stamper RL. Long-term effects of mitomycin on filtering blebs. Lack of fibrovascular proliferative response following severe inflammation. Arch Ophthalmol 1993;111: 824 – 6. 22. Yamamoto T, Varani J, Soong HK, Lichter PR. Effects of 5-fluorouracil and mitomycin C on cultured rabbit subconjunctival fibroblasts. Ophthalmology 1990;97:1204 –10. 23. Khaw PT, Doyle JW, Sherwood MB, et al. Prolonged localized tissue effects from 5-minute exposures to fluorouracil and mitomycin C. Arch Ophthalmol 1993;111:263–7. 24. Kawase K, Matsushita H, Yamamoto T, Kitazawa Y. Mitomycin concentration in rabbit and human ocular tissues after topical administration. Ophthalmology 1992;99:203–7. 25. Ferguson VMG, Spalton DJ. Continued breakdown of the blood aqueous barrier following cataract surgery. Br J Ophthalmol 1992;76:453– 6.
Chen et al 䡠 Cataract Extraction after Trabeculectomy 26. Addicks EM, Quigley HA, Green WR, Robin AL. Histologic characteristics of filtering blebs in glaucomatous eyes. Arch Ophthalmol 1983;101:795– 8. 27. Maumenee AE. External filtering operations for glaucoma: the mechanism of function and failure. Trans Am Ophthalmol Soc 1960;58:319 –28. 28. Antonios SR, Traverso CE, Tomey KF. Extracapsular cataract extraction using a temporal limbal approach after filtering operations. Arch Ophthalmol 1988;106:608 –10. 29. Burratto L, Ferrari M. Extracapsular cataract surgery and intraocular lens implantation in glaucomatous eyes that had a filtering bleb operation. J Cataract Refract Surg 1990;16:315–9. 30. Brooks AMV, Gillies WE. The effect of cataract extraction with implant in glaucomatous eyes. Aust N Z J Ophthalmol 1992;20:235– 8. 31. Drolsum L, Haaskjold E. Extracapsular cataract extraction in eyes previously operated for glaucoma. Acta Ophthalmol (Copenh) 1994;72:273– 8.
32. Krupin T, Feitl ME, Bishop KI. Postoperative intraocular pressure rise in open-angle glaucoma patients after cataract or combined cataract-filtration surgery. Ophthalmology 1989;96: 579 – 84. 33. Berke SJ, Bellows AR, Shingleton BJ, et al. Chronic and recurrent choroidal detachment after glaucoma filtering surgery. Ophthalmology 1987;94:154 – 62. 34. Watson PG, Barnett F. Effectiveness of trabeculectomy in glaucoma. Am J Ophthalmol 1975;79:831– 45. 35. Costa VP, Katz LJ, Spaeth GL, et al. Primary trabeculectomy in young adults. Ophthalmology 1993;100:1071– 6. 36. Robinson DIM, Lertsumitkul S, Billson FA, Robinson LP. Long-term intraocular pressure control by trabeculectomy: a ten-year life table. Aust N Z J Ophthalmol 1993;21: 79 – 85. 37. Chen TC, Wilensky JT, Viani MAG. Long-term follow-up of initially successful trabeculectomy. Ophthalmology 1997;104: 1120 –5.
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Originally received: November 24, 1997. Revision accepted: April 10, 1998. Manuscript no. 97810. 1 Department of Ophthalmology, University of Washington, Seattle, Washington. 2 Department of Ophthalmology, University of Miami School of Medicine, Bascom Palmer Eye Institute, Miami, Florida. Supported in part by an unrestricted grant from Research to Prevent Blindness, Inc, New York, New York; and Public Health Service Research Grant EY10410, Department of Health and Human Services, National Institutes of Health, National Eye Institute, Bethesda, Maryland. None of the authors have any proprietary interest in any of the products mentioned in this article. Reprint requests to Philip P. Chen, MD, Department of Ophthalmology, University of Washington, Box 356485, Seattle, WA 98195.
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to maintain IOP control after extracapsular cataract extraction (ECCE) with intraocular lens (IOL) placement.5–9 Minimizing intraoperative tissue trauma and postoperative inflammation may play a role in maintaining bleb function after CE.10,11 Uncomplicated phacoemulsification (PE) has been shown to result in significantly lower aqueous flare and cells after surgery than ECCE12,13 and fewer filtering bleb failures.14,15 Other authors have noted resolution of posttrabeculectomy hypotony after CE.16,17 We retrospectively examined preoperative, intraoperative, and postoperative factors to identify risk factors associated with loss of IOP control after ECCE or PE with IOL placement. We also investigated the resolution of post-trabeculectomy hypotony after CE.
Methods Before medical records were reviewed, approval for this study was given by the Medical Sciences Subcommittee for the Protection of Human Subjects in Research at the University of Miami School of Medicine. A computerized search using surgical current proce-
Chen et al 䡠 Cataract Extraction after Trabeculectomy Table 1. Outcomes of Trabeculectomy Function after Cataract Extraction Outcome
Definition
Complete success Qualified success Failure
No additional medications,* bleb needling, or further glaucoma surgery Additional medication* or bleb needling needed for IOP control Further glaucoma surgery needed for IOP control
IOP ⫽ intraocular pressure. * Additional medications used more than 2 months after cataract extraction.
dural terminology codes was used to identify patients who had undergone CE after trabeculectomy between January 1991 and December 1995 at the Anne Bates Leach Eye Hospital, Miami, Florida. Variables investigated included age at time of CE, gender, race, eye, type of glaucoma, best-corrected Snellen visual acuity, number and type of glaucoma medications, previous incisional ocular surgeries, time elapsed since the most recent trabeculectomy to the cataract surgery, type of antifibrosis agent used with the most recent trabeculectomy, bleb appearance (pre- and postCE), IOP (the average IOP during the 4 months preceding CE, the maximum IOP during the first 2 postoperative weeks, and the IOP at 1, 2, 3, 6, 9, 12, 18, 24, and 36 months and at the last visit after surgery), method of CE (ECCE vs. PE), position of cataract incision relative to the filtering bleb, cataract incision location (clear corneal vs. limbal vs. scleral), length and closure (number and type of sutures), IOL type and placement, intraoperative iris manipulation, intraoperative and postoperative complications, postoperative medications and antifibrosis agents administered, and the dates when new glaucoma medicines were added or further glaucoma surgery was performed. Patients undergoing planned ECCE had a 7.0- to 11.5-mm incision made either in peripheral cornea or through the surgical limbus, either adjacent to or in a separate quadrant from the filtering bleb, followed by can-opener anterior capsulotomy, nuclear mobilization and expression, manual or automated irrigation and aspiration of cortical remnants, placement of a polymethylmethacrylate (PMMA) IOL, and wound closure with 10 – 0 nylon sutures. Patients undergoing PE had a tunnel incision (length, 3.2–7.0 mm) made in peripheral cornea or sclera, followed by continuous-tear capsulorhexis, nuclear hydrodissection and emulsification, automated irrigation and aspiration of cortical remnants, placement of a silicone foldable or PMMA IOL, and wound closure with 10 – 0 nylon sutures in some cases. Iris manipulation (posterior synechiolysis, stretching, sphincterotomies, sector iridectomy, or use of iris retraction hooks [Grieshaber, Kennesaw, Georgia]) was performed as necessary to enable CE. Intraocular lenses were implanted in the posterior capsular bag or the ciliary sulcus; in one patient, an anterior chamber IOL was used. We defined complete success as the absence of additional glaucoma medications, bleb needling, or further glaucoma surgery for long-term IOP control after CE (Table 1); however, additional glaucoma medicines used within the first 2 postoperative months were permitted. Eyes that required additional medications for IOP control after the second postoperative month or that underwent bleb needling at the slit lamp were considered qualified successes. We included bleb needling in the same category as additional medications because some surgeons preferred to needle a previously functioning bleb rather than start new medications (1 surgeon performed 8 of 9 needlings), and the mean IOP at the time bleb needling was performed was not significantly different from
that when additional medication was added (28.6 ⫾ 4.6 vs. 27.1 ⫾ 8.3 mmHg). This indicated that blebs that underwent needling were not failing to a greater degree than blebs that had medications added. Eyes that underwent further glaucoma surgery were considered failures. Based on the above criteria, each variable was evaluated for association with trabeculectomy survival (i.e., time to qualified success or failure) using Kaplan–Meier survival analysis. Although survival analysis predicates inclusion of all patients regardless of length of follow-up, to maintain clinical relevance we excluded patients with less than 6 months of follow-up. Cox multivariate proportional hazards survival regression using forward-stepwise variable selection was used to determine which risk factors were independent predictors of qualified success or failure. All preoperative and intraoperative variables were candidates for entry into the model (not only those identified as significant by univariate analysis). Differences in pre- and post-CE IOP were examined for statistical significance using paired and two-sample, two-tailed Student’s t test. Results are given as the mean ⫾ standard deviation where applicable.
Results The search by CPT codes identified 125 eyes of 125 consecutive patients who had CE after trabeculectomy. Two patients were excluded from analysis because their glaucoma (due to traumatic hyphema) had resolved despite a flat bleb, and the cataract incision was made at the trabeculectomy site without attempt to maintain bleb function. Eight patients were excluded because of follow-up of less than 6 months, resulting in a study population of 115 eyes of 115 patients. The mean age at the time of CE was 68.9 ⫾ 12.0 years (range, 17– 88 years) and differed significantly between patients having ECCE (71.5 ⫾ 8.6 years, N ⫽ 58) and PE (66.2 ⫾ 14.2 years, N ⫽ 57; P ⫽ 0.02). Demographic data and characteristics of the patients in this study are listed in Table 2. No patients had bleb revision in conjunction with CE, but one patient had choroidal effusions drained at the time of ECCE and one patient had pars plana vitrectomy performed on the same date as PE for retained nuclear fragments. The mean follow-up was 21.1 ⫾ 14.3 months (range, 6 – 60 months) and was significantly longer for ECCE (24.5 ⫾ 16.3 months) compared to PE (17.6 ⫾ 10.9 months, P ⬍ 0.001). Nine patients were included in the survival analysis only until the last office visit before the date when nonglaucoma-related intraocular surgery was performed, which included repair of traumatic cataract wound dehiscence on postoperative day 16 (1), pars plana vitrectomy (for vitreous hemorrhage [1, at 3.2 months], bleb-related endophthalmitis [1, at 13 months], and epiretinal membrane [1, at 31.3 months]), bleb revision for hypotony (3, all within 3.5 months), and penetrating keratoplasty for pseudophakic bullous keratopathy (2, at 6 and 6.5 months). Thirty-five eyes (30.4%) required additional medication or filtering bleb needling (i.e., were qualified successes) to maintain IOP control after surgery. Eleven eyes (9.6%) required additional glaucoma surgery (i.e., were failures), including trabeculectomy (6), glaucoma drainage device placement (5), and pars plana vitrectomy for aqueous misdirection (1). All but one patient in the failure group was a qualified success before reoperation. The cumulative proportion of patients who did not need further glaucoma surgery (i.e., were not failures) was 93% at 1 year (N ⫽ 72), 90% at 2 years (N ⫽ 45), and 85% at 3 years (N ⫽ 20) (Fig 1). The cumulative proportion of patients who also did not require additional glaucoma medicines or bleb needling (i.e., were com-
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Ophthalmology Volume 105, Number 10, October 1998 Table 2. Demographic Data and Characteristics of Eyes Having Cataract Extraction (CE) after Trabeculectomy
Gender Male Female Race White Hispanic Black Asian Glaucoma type Primary open-angle Chronic angle closure Pseudoexfoliation Normal tension Mixed mechanism Pigmentary Uveitic Traumatic Neovascular Steroid-induced Trabeculectomy location Superior 180° Inferior 180° Antifibrosis agent with last trabeculectomy None 5-Fluorouracil (10–45 mg) Mitomycin C No. of incisional surgeries before CE 1 trabeculectomy 2 trabeculectomies 3 trabeculectomies No. of glaucoma medications prior to CE 1 2 3 Interval from trabeculectomy to CE (mos) All eyes ECCE (N ⫽ 58) PE (N ⫽ 57) Incision location: ECCE Clear cornea Limbus Incision location: PE Clear cornea Sclera Incision length and type: PE Small (ⱕ4 mm) Unsutured
N
%
57 58
(50) (50)
56 42 17 1
(49) (37) (15) (1)
57 15 11 10 7 5 4 3 2 1
(50) (13) (10) (9) (6) (4) (3) (3) (2) (1)
112 3
(97) (3)
29 36 50
(25) (31) (43)
98 15 2
(85) (13) (2)
11 1 3
(9) (1) (3)
19.9 ⫾ 17.3 18.6 ⫾ 15.5 21.2 ⫾ 19.1 42 16
(72) (28)
12 45
(21) (79)
42 21
(74) (37)
Figure 1. Kaplan–Meier survival curves for intraocular pressure control in eyes undergoing cataract extraction after trabeculectomy.
within the first postoperative week, 5 at 1.0 – 4.3 months), six of whom used additional medications either before or after needling and two of whom eventually had further glaucoma surgery. The median time to qualified success was 1.6 months (range, 0.03–58.0 months) and was before 3 months in 10 (77%) of 13 eyes after PE and in 10 (45%) of 22 eyes after ECCE. The median time from qualified success to failure was 3.6 months (range, 0.3–19.1 months). Six (55%) of 11 failures occurred within 6.5 months after CE.
ECCE ⫽ extracapsular cataract extraction; PE ⫽ phacoemulsification.
plete successes) was 75% at 1 year, 67% at 2 years, and 59% at 3 years (Fig 1). Cumulative survival did not differ significantly by type of CE (ECCE vs. PE) (Fig 2), but Cox multivariate proportional hazards regression, adjusted for other statistically significant variables, estimated a risk ratio of 1.1 for qualified success (95% confidence interval [CI] 0.6, 2.2), and 3.0 for failure (95% CI 0.7, 12.8), for eyes having ECCE compared to PE. Forty-nine patients (43%) required from 1 to 4 medications for IOP control; 32 patients (28%) used medications beyond the second postoperative month, 8 of whom eventually had further glaucoma surgery. Of 15 patients who used glaucoma medications before surgery, 7 used the same number at the last follow-up, 3 required more, and 5 used fewer medications. Nine patients (7.8%) underwent needling revision of the filtering bleb at the slit lamp (4
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Figure 2. Kaplan–Meier survival curves for intraocular pressure control in eyes undergoing extracapsular cataract extraction and phacoemulsification (Phaco) after trabeculectomy.
Chen et al 䡠 Cataract Extraction after Trabeculectomy Table 4. Factors Associated with Failure in Eyes Having Cataract Extraction (CE) after Trabeculectomy Factor Age at time of CE ⱕ50 yrs ⬎50 yrs Glaucoma type POAG Uveitic Time from trabeculectomy to CE ⱕ6 mos ⬎6 mos Early postoperative maximum IOP‡ ⱕ25 mmHg ⬎25 mmHg
Figure 3. Mean intraocular pressure in eyes undergoing cataract extraction after trabeculectomy, for all patients and for those eyes that were complete successes at last follow-up.
The average preoperative IOP was 10.5 ⫾ 3.9 mmHg (range, 3–19). Eyes that became qualified successes or failures had higher mean preoperative IOP compared to those that did not (12.1 ⫾ 3.6 vs. 9.8 ⫾ 3.8 mmHg; P ⫽ 0.005) (Fig 3). Although preoperative IOP as a continuous variable was not associated with trabeculectomy survival, preoperative IOP greater than 10 mmHg was significantly associated with qualified success (P ⫽ 0.036) (Table 3), and this association remained significant (risk ratio, 2.2; 95% CI 1.0, 4.5; P ⫽ 0.030) after multivariate analysis. The mean maximum IOP during the first 2 postoperative weeks was 19.5 ⫾ 10.0 mmHg. However, IOP greater than 25 mmHg during this period was noted in 31 patients (27%) in whom qualified success (P ⬍ 0.001) and failure (P ⫽ 0.008) were subsequently more likely compared to those patients who had IOP less than 25 mmHg (Tables 3 and 4). The mean IOP in all eyes
Table 3. Factors Associated with Qualified Success in Eyes Having Cataract Extraction (CE) after Trabeculectomy Factor Preoperative IOP ⱕ10 mmHg ⬎10 mmHg Intraoperative iris manipulation None Any‡ Early postoperative maximum IOP§ ⱕ25 mmHg ⬎25 mmHg
N
Survival (%)*
P†
58 57
83 ⫾ 5 66 ⫾ 7
0.036㛳
62 53
83 ⫾ 5 64 ⫾ 7
0.027㛳
83
85 ⫾ 4
31
45 ⫾ 9
⬍0.001
IOP ⫽ intraocular pressure. * Kaplan-Meier survival analysis estimate of 12-month survival rate. † Log rank P value. ‡ Includes posterior synechiolysis, pupil stretching, sphincterotomy, iridectomy, iris suturing, and/or use of iris retraction hooks. § Maximum IOP measured within the first 2 postoperative weeks; not included in multivariate survival regression; data missing from one eye. 㛳 Maintained significance after Cox multivariate proportional hazards survival regression analysis of preoperative and intraoperative factors.
N
Survival (%)*
P†
7 108
64 ⫾ 21 95 ⫾ 2
0.062§
57 4
95 ⫾ 3 38 ⫾ 29
18 97
75 ⫾ 11 97 ⫾ 2
83 31
97 ⫾ 2 83 ⫾ 7
0.007 0.038
0.008
IOP ⫽ intraocular pressure; POAG ⫽ primary open-angle glaucoma. * Kaplan-Meier survival analysis estimate of 12-month survival rate. † Log rank P value. ‡ Maximum IOP measured within the first 2 postoperative weeks; not included in multivariate survival regression; data missing from one eye. § Remained significant (P ⫽ 0.033) after Cox multivariate proportional hazards survival regression analysis of preoperative and intraoperative factors.
increased to 12.1 ⫾ 5.1 mmHg at last visit and was increased significantly at each postoperative timepoint through 18 months compared to the pre-CE IOP but did not vary significantly after the first postoperative month. In eyes that were complete successes, the mean IOP increased significantly from 9.8 ⫾ 3.8 to 10.8 ⫾ 4.1 mmHg at last visit. Other preoperative variables associated with further glaucoma surgery by univariate (Kaplan–Meier) analysis included uveitic glaucoma (vs. POAG, P ⫽ 0.007), CE at 6 months or less after trabeculectomy (P ⫽ 0.038), and age of 50 years or younger (P ⫽ 0.062) (Table 4). After multivariate analysis, age of 50 years or younger remained significant (risk ratio, 8.4; 95% CI ⫽ 1.7– 40.9; P ⫽ 0.033), and CE greater than 6 months after trabeculectomy was borderline protective against failure (risk ratio, 0.5; 95% CI 0.2, 1.1; P ⫽ 0.087). No other preoperative variables were shown to be associated with qualified success or failure after CE, including use of antifibrosis agents with the most recent trabeculectomy, number of prior trabeculectomies, or number of glaucoma medications. Preoperative bleb appearance was noted to be “avascular,” “good,” “elevated,” or “large” in 91 eyes (79%); these terms were used for 65 (59%) of 111 eyes in which postoperative bleb appearance was described. The bleb was “small” or “flat” in 8 eyes (7%) before CE; these terms were used for 25 eyes (22%) after surgery. No significant difference in survival was found between the two sets of terms. Intraoperative iris manipulation was associated significantly with the need for additional medications or bleb needling after surgery (P ⫽ 0.027, Table 3), and this association withstood multivariate analysis (risk ratio, 2.3; 95% CI ⫽ 1.1, 4.5; P ⫽ 0.019). Neither the location (clear cornea vs. limbus in ECCE, or vs. sclera in PE), length, nor closure of the incision was associated with different survival. Only 1 (2.4%) of 42 patients who underwent small incision PE (length ⱕ 4 mm) with foldable silicone IOL was a failure because of postoperative aqueous misdirection necessitating pars plana vitrectomy, after which the bleb continued to function. If this case is not considered to be a failure of bleb function, then large incision (length ⬎ 4 mm) CE is associated significantly with bleb failure (10 [13.7%] of 73 eyes; P ⫽ 0.035).
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Ophthalmology Volume 105, Number 10, October 1998 Table 5. Studies on Intraocular Pressure (IOP) Control in Eyes Having Extracapsular Cataract Extraction (ECCE) or Phacoemulsification (PE) with Intraocular Lens (IOL) after Glaucoma Filtering Surgery* N (ECCE/PE)
Follow-up (months)
3/7
⬎12
Binkhorst (1981)
26/0
Mean “almost 36”
Obstbaum6 (1986)
15/0
ⱖ9
Antonios28 (1988)
29/0
Median 13
Murchison7 (1989)
22/0
Mean 22.3
Brooks30 (1992)
43/0
12
36/9 (before exclusion)
24
Study Alpar
15
(1979) 5
Yamagami8 (1994)
Dickens9 (1996)
23/0
Median 70
Seah14 (1996)
16/6
Mean 13.6
Present study
58/57
24.5/17.6 Mean 21.1
Definition of Success Not defined
% Success (ECCE/PE) 66/86
“Normal” IOP and no See comment glaucoma medications
Comments Excluded if ⬍1 year follow-up or complication during CE 3 of 33 eyes required additional medications or reoperation, not noted whether these were after ICCE or ECCE Excluded if ⬍9 mos follow-up
IOP unchanged and 80/NA no increase in glaucoma medications Same as current study CS-69/NA QS-31/NA Excluded if ⬍8 mos follow-up; 7 eyes F-0/NA had IOLs; all had ECCE ⬎1 yr after filtering surgery Same as current study CS-68/NA QS-23/NA Excluded if ⬍6 mos follow-up F-9/NA No further glaucoma 98/NA 43 eyes of 33 patients; pre- and postsurgery cataract extraction medications not provided No increase in 67 (see comment) Excluded 6 patients with post-CE iritis; glaucoma included 13 patients without medications functioning filtering bleb pre-CE; separate analysis of ECCE and PE not provided Same as current study CS-65/NA QS-26/NA Excluded if ⬍4 yrs follow-up F-9/NA See comment CS-38/67 QS-31/0 Excluded if ⬍6 mos follow-up; CS ⫽ F-31/33 IOP ⱕ 19 without intervention; QS ⫽ IOP ⱕ 19 with medication; F ⫽ IOP ⬎ 19 or further surgery See text/Table 1 CS-64/74 QS-22/19 Excluded if ⬍ 6 mos follow-up F-14/5
NA ⫽ not applicable; CS ⫽ complete success; QS ⫽ qualified success; F ⫽ failure. * With minimum follow-up of (mean) 6 months.
Intraoperative complications occurred in 7 eyes (6%) and postoperative complications developed in 31 eyes (27%), including posterior capsular tear with (3) and without (1) vitreous loss, retained nuclear fragments (2), retained cortical remnants (3), hyphema (5), transient bleb leak (3) or cataract wound leak (6), traumatic wound dehiscence (1), aqueous misdirection (1), persistent corneal edema (5), persistent inflammation (3), IOL capture (2), vitreous hemorrhage (1), cystoid macular edema (4), epiretinal membrane formation (1), late bleb-related endophthalmitis (1), and ptosis (2). Of two eyes noted to have bleb leaks before surgery, one leaked intermittently after CE. No intraoperative or postoperative complication was associated significantly with different trabeculectomy survival, nor was use of postoperative subconjunctival 5-fluorouracil (5-FU) injections (9 patients; total dose, 5–25 mg). Nineteen eyes (17% of all eyes) had hypotony (IOP ⱕ 6 mmHg) before CE (mean IOP, 4.6 ⫾ 1.1 mmHg). Trabeculectomy had been performed with mitomycin C in 13 eyes and with 5-FU in 3 eyes. Phacoemulsification was performed in 13 eyes and ECCE in 6 eyes. Eleven eyes (58%) continued to have hypotony after CE, including 3 eyes that required revision of trabeculectomy for hypotony-related corneal folds, after mean follow-up of 14.6 ⫾ 11 months (17 ⫾ 10.5 months if eyes censored for trabeculectomy revision are excluded). The mean peak IOP in the first 2 postoperative weeks was 15.8 ⫾ 11.5 mmHg and did not differ significantly for those eyes in which hypotony resolved after CE. Although the mean IOP at last follow-up increased significantly to
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7.5 ⫾ 3.6 mmHg (P ⫽ 0.002), no factor was associated significantly with resolution of hypotony. After CE, two eyes required glaucoma medications for less than 1 month and two eyes underwent bleb needling (at 0.3 and 1 month). One eye had pre-CE hypotony maculopathy, which had not resolved after 7.4 months’ follow-up. Of 115 eyes, 110 (96%) had corrected preoperative Snellen visual acuity of 20/50 or worse. Postoperative visual acuity was 20/40 or better in 82 eyes (71%) and 20/100 or worse in 16 eyes (14%). Only two eyes (1.7%) had worse postoperative visual acuity during follow-up. The method of CE was not associated significantly with different postoperative visual acuity.
Discussion Several reports have described the effect of CE on IOP control after trabeculectomy.5–9,14,15 Table 5 summarizes studies with follow-up of at least 6 months and sufficient information to allow comparison with our patients. The few that have investigated outcomes after PE are limited by small sample size (6 –9 eyes).8,14,15 Variations in exclusion and success criteria, follow-up time, and methods of statis-
Chen et al 䡠 Cataract Extraction after Trabeculectomy tical analysis make comparisons with previous studies difficult. In addition, practice patterns may vary by physician, and the pre-existing severity of glaucomatous damage undoubtedly influences the threshold for adding medications or performing further glaucoma surgery, so the use of medical or surgical intervention as an indicator for trabeculectomy failure may not provide the most accurate benchmarks for comparison. Nonetheless, the proportion of patients who were in each outcome category in our study was similar to that in several previous studies that included primarily ECCE with IOL after glaucoma-filtering surgery.7–9,14 We found 22% of patients required only medical intervention or bleb needling, and 9.6% required further glaucoma surgery. We found an encouraging cumulative failure-avoidance rate of 93% and 90% at 1 and 2 years, respectively, but the cumulative complete success rate was lower at 75% and 67% at 1 and 2 years, respectively (Fig 1). Yamagami et al8 also used Kaplan–Meier survival analysis and found IOP control was maintained in 22 (56%) of 39 eyes 2 years after ECCE or PE; however, 6 eyes with postoperative iritis were excluded from analysis. We identified several preoperative variables that were associated significantly (by univariate Kaplan–Meier survival analysis) with loss of IOP control, including uveitic glaucoma, period less than 6 months between trabeculectomy and CE, pre-CE IOP greater than 10 mmHg, and age of 50 years or younger. Patients with uveitis have been reported to have an exaggerated postoperative inflammatory response after CE with IOL implantation.18 Although the diagnosis of uveitic glaucoma includes numerous openangle and angle-closure etiologies of elevated IOP, chronic intraocular inflammation is the underlying factor that may contribute to bleb failure after CE. An interval between trabeculectomy and CE of 6 months or less was associated significantly with reoperation for glaucoma. Other authors have reached similar conclusions and believe the filtering bleb needs sufficient time to develop properly19,20; the inflammation associated with cataract surgery presumably curtails this process. In our study, patients who maintained IOP control without additional intervention had a significantly lower mean pre-CE IOP than did those who were qualified successes or failures (9.8 vs. 12.1 mmHg). Patients with higher IOP before CE may have filtering blebs with borderline function, which are likely more susceptible to fibrosis after CE. Relative youth is a well-recognized risk factor for filtering surgery failure10 and is likely related to loss of IOP control after CE for similar reasons. After multivariate analysis, only IOP greater than 10 mmHg and age of 50 years or younger remained significantly associated with further glaucoma surgery. An interval greater than 6 months between trabeculectomy and CE was of borderline significance as protective from failure. Of 57 patients who had PE, 3 (5.3%) required further glaucoma surgery after mean follow-up of 18 months. Two patients had uveitic glaucoma and had their cataract incisions enlarged to 6 and 7 mm for PMMA lens placement. In the third patient, small-incision PE precipitated aqueous misdirection that required pars plana vitrectomy for resolution, but bleb function was not lost. In comparison, 8 (13.7%) of 58 patients who had ECCE were failures after
mean follow-up of 24.5 months (Fig 2). However, Kaplan– Meier survival analysis and Cox multivariate proportional hazards regression showed no statistically significant difference between ECCE and PE in progression to qualified success (risk ratio, 1.1 for ECCE) or failure (risk ratio, 3.0 for ECCE) (the risk ratio is larger for failure, although the difference between ECCE and PE in Fig 2 appears larger for qualified success, because the standard errors are smaller when survival is close to 1). The lack of significance may be because of the small number of failures in our study population, the significant difference in follow-up time between the two methods of CE, and the total sample size. A clinically important difference in failure between small (ⱕ4 mm) and large incision size (2.4% vs. 13.7% failure, respectively) may not have been statistically significant because the one failure after small-incision PE occurred 2 weeks after surgery. Some authors have noted mitomycin C to be associated with long-term protection from subsequent failure despite severe inflammation.21 Use of antifibrosis agents with the most recent trabeculectomy did not influence survival after CE in our study. Both 5-FU and mitomycin C affect local fibroblast proliferation rather than migration,22,23 and although mitomycin C may have considerably prolonged effects compared to those of 5-FU,23 its half-life after topical administration is limited,24 and inflammation occurring after CE may result in further recruitment and migration of cicatrix-forming cells. In this study, use of 5-FU injections after CE did not influence bleb survival and IOP control, but the number of patients was small and patient selection was likely biased toward those with more intraocular inflammation or external vascularization. A randomized, prospective study would be needed to properly investigate the role of 5-FU injections after CE in patients with functioning filtering blebs. Intraoperative iris manipulation was associated significantly with the need for additional medications or bleb needling, probably through long-term postoperative inflammation due to blood–aqueous barrier breakdown25 and the underlying cause of the posterior synechiae (miotic use, diabetes mellitus, previous uveitis, previous surgery, or pseudoexfoliation syndrome). In the current study, 46% of patients required iris manipulation. The surgical challenge these patients may pose is reflected in the relatively high complication rate seen in this and previous studies.7,8,14 One study found intraoperative complications frequently led to bleb failure,14 but this association was not seen in our study. The mechanism for loss of IOP control in most patients with previously functioning filtering blebs is external scarring at the level of Tenon capsule and episclera.26,27 Other authors have observed bleb scarring and shrinkage after CE,5,8,9 sometimes with worsened IOP control.8 Reduced bleb size was noted in approximately 18% of eyes in our study, but change in bleb appearance was not associated with different survival, although this is difficult to assess accurately in a retrospective study. Different authors have noted changes in mean IOP after CE ranging from a decrease of 0.8 mmHg to an increase of 6.6 mmHg, after mean or median follow-up ranging from 8 to 70 months.5–9,14,28 –31 We found an increase in mean IOP
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Ophthalmology Volume 105, Number 10, October 1998 of 1.6 mmHg overall, 1.0 mmHg for patients who were complete successes. Of note, the mean IOP stabilized quickly and did not vary significantly after the first postoperative month. A marked postoperative IOP rise is not uncommon after uncomplicated ECCE in patients with glaucoma.32 In our study, eyes with a postoperative IOP spike greater than 25 mmHg subsequently had significantly worse IOP control. These patients should be monitored carefully as their bleb function may be tenuous. Some IOP spikes may be related to retained viscoelastic material after CE. Mechanical causes of decreased filtration after CE, such as iris, vitreous, or IOL haptic incarceration into the internal sclerostomy, were not noted in our study. Cataract surgery has been advocated to treat postfiltering surgery hypotony maculopathy16,17 and chronic choroidal detachment33 in those patients with coexisting cataract. In our series, 19 patients had hypotony (IOP ⱕ 6 mmHg) after trabeculectomy, 11 (58%) of whom continued to have hypotony or needed bleb revision for hypotony at last followup. Although the mean IOP increased significantly from 4.6 to 7.5 mmHg, none of the factors investigated was associated significantly with resolution of hypotony. Cataract surgery did not reliably resolve hypotony after filtration surgery in our study. A decrease in IOP control over time after successful trabeculectomy, even without intervening nonglaucoma-related surgical intervention, has been reported.2,3,11,34 –37 Loss of bleb function related to such attrition was not distinguished from that due to CE in the current study. Nonetheless, our findings suggest that CE in the presence of a functioning filtering bleb results in a low cumulative rate of severe loss of IOP control, and few patients (9.6%) require reoperation for glaucoma. Patients 50 years of age or younger, with IOP of 11 mmHg or greater, or who need intraoperative iris manipulation for CE, are at significantly higher risk for loss of IOP control, as are those with early postoperative IOP greater than 25 mmHg. The mean postoperative IOP did not vary significantly after the first postoperative month, and most eyes that needed additional medications or needling, or further glaucoma surgery, required intervention before the 3rd and 7th postoperative months, respectively. For most patients with glaucoma with functioning filtering blebs, CE may be recommended with the anticipation of both restoration of visual acuity and continued IOP control.
References 1. Sugar HS. Postoperative cataract in successfully filtering glaucomatous eyes. Am J Ophthalmol 1970;69:740 – 6. 2. D’Ermo F, Bonomi L, Doro D. A critical analysis of the long-term results of trabeculectomy. Am J Ophthalmol 1979; 88:829 –35. 3. Mills KB. Trabeculectomy: a retrospective long-term follow-up of 444 cases. Br J Ophthalmol 1981;65:790 –5. 4. Vesti E. Development of cataract after trabeculectomy. Acta Ophthalmol (Copenh) 1993;71:777– 81.
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5. Binkhorst CD, Huber C. Cataract extraction and intraocular lens implantation after fistulizing glaucoma surgery. J Am Intraocular Implant Soc 1981;7:133–7. 6. Obstbaum SA. Glaucoma and intraocular lens implantation. J Cataract Refract Surg 1986;12:257– 61. 7. Murchison JF Jr, Shields MB. An evaluation of three surgical approaches for coexisting cataract and glaucoma. Ophthalmic Surg 1989;20:393– 8. 8. Yamagami S, Araie M, Mori M, Mishima K. Posterior chamber intraocular lens implantation in filtered or nonfiltered glaucoma eyes. Jpn J Ophthalmol 1994;38:71–9. 9. Dickens MA, Cashwell LF. Long-term effect of cataract extraction on the function of an established filtering bleb. Ophthalmic Surg Lasers 1996;27:9 –14. 10. Skuta GL, Parrish RK II. Wound healing in glaucoma filtering surgery. Surv Ophthalmol 1987;32:149 –70. 11. Araujo SV, Spaeth GL, Roth SM, Starita RJ. A ten-year follow-up on a prospective, randomized trial of postoperative corticosteroids after trabeculectomy. Ophthalmology 1995; 102:1753–9. 12. Oshika T, Yoshimura K, Miyata N. Postsurgical inflammation after phacoemulsification and extracapsular extraction with soft or conventional intraocular lens implantation. J Cataract Refract Surg 1992;18:356 – 61. 13. Pande MV, Spalton DJ, Kerr–Muir MG, Marshall J. Postoperative inflammatory response to phacoemulsification and extracapsular cataract surgery: aqueous flare and cells. J Cataract Refract Surg 1996;22(Suppl 1):770 – 4. 14. Seah SKL, Jap A, Prata JA Jr, et al. Cataract surgery after trabeculectomy. Ophthalmic Surg Lasers 1996;27:587–94. 15. Alpar JJ. Cataract extraction and lens implantation in eyes with pre-existing filtering blebs. J Am Intraocular Implant Soc 1979;5:33–5. 16. Sibayan SAB, Igarashi S, Kasahara N, et al. Cataract extraction as a means of treating postfiltration hypotony maculopathy [case reports]. Ophthalmic Surg Lasers 1997;28:241–3. 17. Allingham RR. Treatment of hypotonous maculopathy. In: Epstein DL, Allingham RR, Schuman JS, eds. Chandler and Grant’s Glaucoma, 4th ed. Baltimore: Williams & Wilkins, 1997;549. 18. Foster RE, Lowder CY, Meisler DM, Zakov ZN. Extracapsular cataract extraction and posterior chamber intraocular lens implantation in uveitis patients. Ophthalmology 1992;99: 1234 – 41. 19. Shields MB. Combined cataract extraction and guarded sclerectomy. Reevaluation in the extracapsular era. Ophthalmology 1986;93:366 –70. 20. Shields MB. Textbook of glaucoma, 4th ed. Baltimore: Williams & Wilkins, 1998;566. 21. Yaldo MK, Stamper RL. Long-term effects of mitomycin on filtering blebs. Lack of fibrovascular proliferative response following severe inflammation. Arch Ophthalmol 1993;111: 824 – 6. 22. Yamamoto T, Varani J, Soong HK, Lichter PR. Effects of 5-fluorouracil and mitomycin C on cultured rabbit subconjunctival fibroblasts. Ophthalmology 1990;97:1204 –10. 23. Khaw PT, Doyle JW, Sherwood MB, et al. Prolonged localized tissue effects from 5-minute exposures to fluorouracil and mitomycin C. Arch Ophthalmol 1993;111:263–7. 24. Kawase K, Matsushita H, Yamamoto T, Kitazawa Y. Mitomycin concentration in rabbit and human ocular tissues after topical administration. Ophthalmology 1992;99:203–7. 25. Ferguson VMG, Spalton DJ. Continued breakdown of the blood aqueous barrier following cataract surgery. Br J Ophthalmol 1992;76:453– 6.
Chen et al 䡠 Cataract Extraction after Trabeculectomy 26. Addicks EM, Quigley HA, Green WR, Robin AL. Histologic characteristics of filtering blebs in glaucomatous eyes. Arch Ophthalmol 1983;101:795– 8. 27. Maumenee AE. External filtering operations for glaucoma: the mechanism of function and failure. Trans Am Ophthalmol Soc 1960;58:319 –28. 28. Antonios SR, Traverso CE, Tomey KF. Extracapsular cataract extraction using a temporal limbal approach after filtering operations. Arch Ophthalmol 1988;106:608 –10. 29. Burratto L, Ferrari M. Extracapsular cataract surgery and intraocular lens implantation in glaucomatous eyes that had a filtering bleb operation. J Cataract Refract Surg 1990;16:315–9. 30. Brooks AMV, Gillies WE. The effect of cataract extraction with implant in glaucomatous eyes. Aust N Z J Ophthalmol 1992;20:235– 8. 31. Drolsum L, Haaskjold E. Extracapsular cataract extraction in eyes previously operated for glaucoma. Acta Ophthalmol (Copenh) 1994;72:273– 8.
32. Krupin T, Feitl ME, Bishop KI. Postoperative intraocular pressure rise in open-angle glaucoma patients after cataract or combined cataract-filtration surgery. Ophthalmology 1989;96: 579 – 84. 33. Berke SJ, Bellows AR, Shingleton BJ, et al. Chronic and recurrent choroidal detachment after glaucoma filtering surgery. Ophthalmology 1987;94:154 – 62. 34. Watson PG, Barnett F. Effectiveness of trabeculectomy in glaucoma. Am J Ophthalmol 1975;79:831– 45. 35. Costa VP, Katz LJ, Spaeth GL, et al. Primary trabeculectomy in young adults. Ophthalmology 1993;100:1071– 6. 36. Robinson DIM, Lertsumitkul S, Billson FA, Robinson LP. Long-term intraocular pressure control by trabeculectomy: a ten-year life table. Aust N Z J Ophthalmol 1993;21: 79 – 85. 37. Chen TC, Wilensky JT, Viani MAG. Long-term follow-up of initially successful trabeculectomy. Ophthalmology 1997;104: 1120 –5.
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