Abstract
Purpose/Aim:
Cataract is a known effect of trabeculectomy (TE), but some surgeons are hesitant to perform combined phacoemulsification-TE (PTE) due to a risk of increased TE failure. Herein, we compare intraocular pressure (IOP) lowering between trabeculectomy (TE) and phacoemulsification-TE (PTE) and investigate factors that impact patient outcomes.
Materials and Methods:
We performed a retrospective study of adults undergoing primary TE or PTE at our institution from 2010 to 2017. We used Kaplan-Meier survival analysis to investigate time to TE failure, and Cox proportional hazards modeling to investigate predictors of TE failure, defined as undergoing a second glaucoma surgery or using more IOP-lowering medications than pre-operatively.
Results:
318 surgeries (218 TE; 100 PTE) from 268 patients were included. Median follow-up time was 753 days. Mean baseline IOP was 21.1 mmHg. There were no significant differences in IOP between TE and PTE groups beyond postoperative year 1, with 28.9–46.5% of TE and 35.5–44.4% of PTE groups achieving IOP ≤10. Final IOP was similar in both groups (p=0.22): 12.41 (SD 4.18) mmHg in the TE group and 14.05 (SD 5.45) in the PTE group. 84 (26.4%) surgeries met failure criteria. After adjusting for surgery type, sex, age, race, surgeon, and glaucoma diagnosis there were no significant differences in TE failure.
Conclusion:
This study suggests there is no significant difference in the risk of TE failure in patients receiving TE versus those receiving PTE.
INTRODUCTION
Trabeculectomy (TE) remains a gold-standard surgical treatment for patients with glaucoma and uncontrolled intraocular pressure (IOP) or progressive visual field loss despite maximum medical therapy 1. For many patients, comorbid cataract raises the possibility of performing concurrent cataract extraction at the time of TE surgery. Combined phacoemulsification-trabeculectomy (PTE) is of particular interest given findings of prior studies 2–4 showing progression of cataract in phakic eyes following TE.
The effect of phacoemulsification at the time of TE on TE function is not well characterized. Prior retrospective cohort studies 5–9 comparing filtering bleb performance in eyes undergoing PTE versus TE alone show mixed results, with some reporting similar outcomes, and others 10,11 reporting lower mean IOP in TE compared to PTE eyes. All of these studies are limited by cohort size, the largest including just 42 eyes undergoing PTE, and by median follow-up time, the longest being 17 months. Advances in phacoemulsification technology since the 1990s, when these studies were performed, also limit the generalizability of their findings to current-day practice.
An informatics pipeline developed to automate data extraction from electronic health records (EHR) was used to investigate the IOP outcomes of consecutive cases of TE or PTE in adults diagnosed with glaucoma at a single academic center between 2010 and 2017. We assessed several outcome variables including IOP, number of IOP-lowering glaucoma medications, and need for second glaucoma surgery in the same eye over a 5-year follow-up time period.
MATERIALS AND METHODS
Data Source and Population
We have developed a relational database that captures data from a hospital Electronic Health Record (EHR) system, an EPIC system installed in 2008 (Epic Systems, Verona WI). It contains patient demographics, diagnosis and procedure codes (ICD[1] and CPT[2] codes), medication orders, eye examination findings, and clinical narrative text 12,13.
Using this database, we identified primary trabeculectomies performed at Stanford University Medical Center between August 2009 and January 2018 using Current Procedural Terminology (CPT) codes 66170. Concurrent cataract surgeries were identified by CPT codes 66982 or 66984. Use and duration of mitomycin-C (0.4mg/mL) was collected for all TEs. Surgical technique for TE and clear-cornea cataract extraction were at the discretion of the operating surgeon. Laterality of surgery was determined from the free-text operative notes as previously described by a validated text-processing algorithm 12,14; if laterality was indeterminate, the surgery was excluded. Surgeries without at least one preoperative visit with documented intraocular pressure of the surgical eye were excluded, as well as those with hypotony (IOP<10) documented at the preoperative visit. A total of 10 surgeries were excluded from analysis. This study was approved by the Stanford Institutional Review Board.
Measures
Available measures included demographics such as patient age, sex, and race/ethnicity. Additionally, intraocular pressure obtained by applanation was extracted from the medical record. Patients’ glaucoma-related diagnoses were determined by ICD9 and ICD10 billing codes associated with the surgical encounter or clinical encounters on or before surgery. If there was more than one glaucoma-related diagnosis, each was prioritized in the following order: narrow or closed angle (365.2-, 365.02, 365.06, H402-, H400.3, H400.6), secondary glaucoma (365.03, 365.3–365.6-, 365.81–3, 365.13–365.14, H400.4, H404-H406-, H408.1-H408.3-, H401.3, H401.4, Q150), primary open angle glaucoma (365.10–365.12, 365.15, 365.89, 365.9, H401.0-H401.2-, H401.5-), open angle suspect / ocular hypertension (365.00, 365.01, 365.04–365.05, H400.0-H400.2-, H400.5-).
Main Outcome
The main outcome measure was TE failure, which was defined as undergoing a second glaucoma surgery in the operative eye or using a greater number of IOP-lowering medications, relative to pre-operative baseline, at 6 or more months following initial TE or combined PTE. Composite endpoints have similarly been used in prior studies 15–17 on TE function in patients with glaucoma. IOP was not included among the failure criterion for the primary outcome, as target IOP can vary greatly among glaucoma patients, including some patients with very low target IOPs. However, secondary outcomes used for sensitivity analyses included more IOP criteria for failure of IOP >16 or failure if IOP >21. The results of these analyses are reported in supplementary Tables 1 and 2. Baseline and postoperative IOP were extracted from the EHR. Medications and their laterality were determined from medication orders and text-processing of associated medication signatures available within the EHR 12. The number of topical IOP lowering medications was totaled at baseline and for each postoperative visit date. Combination medications (e.g., dorzolamide-timolol, brimonidine-timolol) were considered as two medications. IOP measurements after any further glaucoma procedures on the operative eye as identified by CPT codes (0191T,0192T,0253T, 0376T, 0449T, 0474T, 65820, 66250, 65850, 65855, 66160,66170, 66172,66174, 66175,66179, 66180, 66183, 66710, 66711) were excluded.
Statistical Analyses
Descriptive statistics were performed using means and standard deviations for continuous measures and counts and percentages for categorical measures. Mean IOP and proportion of patients with an IOP below a particular level were evaluated at baseline and at postoperative visits. As the timing of visits could vary substantially between subjects, visits between a range of post-operative dates were considered for each post-operative time point, as follow: post-operative month (POM) 1: post-operative day (POD) 21 – 56; POM 3: POD 70 – 112; POM 6: POD 150 – 210; post-operative year (POY) 1: POD 300 – 420; POY 2: 700 – 760; POY 3: POD 1050 – 1140; POY 4: POD 1400 – 1520; POY 5: POD 1765 – 1885. We used Kaplan-Meier analysis to investigate time to TE failure, and Cox proportional hazards modeling to investigate predictors of TE failure. Multivariable Cox proportional hazards models included the following covariates: age, sex, race/ethnicity, glaucoma diagnosis type, baseline IOP, and surgery type (TE or PTE). Patients who had a transient increase in the usage of glaucoma medications less than 6 months after surgery were not considered to have failed. Model standard errors accounted for within-patient clustering when patients contributed to the population multiple times due to having undergone TE in both eyes. Similar sensitivity analyses were performed for secondary definitions of failure, which included IOP-based criterion. Analyses were performed and figures were generated with R statistical software version 3.5 and p-value less than 0.05 was considered statistically significant.
RESULTS
Overall, 318 eyes from 268 patients were included in the analysis. Of these surgeries, 218 were TE and 100 were PTE. A total of 116 (43.3%) of patients were female. The racial/ethnic distribution was a majority White (N=104, 38.8%), Asian or Pacific Islander (N=74, 27.6%), or Hispanic/Latino (N=41, 15.3%) (Table 1). Primary open angle glaucoma accounted for 70.5% (N=189) of all glaucoma types undergoing surgery (Table 1).
Table 1:
Population and Clinical Characteristics of Patients Who Underwent Trabeculectomy
| Total Population | |||||
|---|---|---|---|---|---|
| N=268 | |||||
| Mean | Std | ||||
| Age at first surgery (years) | 66.9 | 17.1 | |||
| N | % | ||||
| Female | 116 | 43.28% | |||
| Race/Ethnicity | |||||
| White | 104 | 38.81% | |||
| Black | 19 | 7.10% | |||
| Asian or Pacific Islander | 74 | 27.61% | |||
| Hispanic/Latino | 41 | 15.30% | |||
| Other/Unknown | 30 | 11.19% | |||
| Glaucoma type | POAG | 189 | 70.52% | ||
| Narrow/Closed Angle | 25 | 9.33% | |||
| Secondary Glaucoma | 30 | 11.19% | |||
| Missing/Unknown | 24 | 8.96% | |||
| Total Surgeries | |||||
| N=318 | |||||
| Follow-up Days (Median, IQR) | 753 | 236–1650 | |||
| Baseline IOP (Mean, SD) | 21.1 | 8.27 | |||
| N | % | ||||
| Eye Laterality | Right | 160 | 50.31% | ||
| Left | 158 | 49.69% | |||
| Baseline IOP | ≤15 | 65 | 21.38% | ||
| 16–19 | 86 | 27.04% | |||
| 20–24 | 69 | 21.70% | |||
| 25–29 | 43 | 13.52% | |||
| ≥ 30 | 40 | 12.58% | |||
| Three or More Glaucoma Medications at Baseline | 197 | 61.95% | |||
| Trabeculectomy Alone | 218 | 68.55% | |||
| Combined Phaco-Trabeculectomy | 100 | 31.45% | |||
A summary of clinical characteristics by surgical eye can be found in Table 1. Median follow-up time was approximately 2 years, with interquartile range of 232–1654 days and range of 1 day to 2934 days (Table 1). A majority of patients were on three or more glaucoma medications at baseline (Table 1). TE alone was performed approximately twice as often as PTE during this period (Table 1). All TEs and PTEs with complete operative reports (N = 307) included use of mitomycin-C (0.4mg/mL), for a mean duration of 2.2 minutes patients receiving either PTE or TE (p = 0.72). Of these cases, 80.8% (N = 248) were limbus-based peritomies and 20.2% (N = 59) were fornix-based peritomies.
Pre-operative logMAR visual acuity was 0.528 in the PTE group and 0.375 in the TE group (p<0.001). At post-operative year 1 visit, logMAR visual acuity was 0.388 in the PTE group and 0.473 in the TE group (p=0.351). We observed a modest rise in median IOP between post-operative month one compared to post-operative year one in both groups, however median IOP did not change significantly thereafter (Figure 1). IOP was not significantly different between the two surgical groups at any post-operative time point (Figure 1). The final IOP was similar in both groups (p=0.22): 12.41 (SD 6.70) mmHg in the TE group and 11.05 (SD 5.45) mmHg in the PTE group. Regarding glaucoma medications, we observed a significant reduction in mean IOP-lowering medications following between post-operative day one (mean 3.0 medications) to post-operative month one (mean 1.75 medications) (p < 0.001) (Figure 2). This reduction remained significant at post-operative year 5 (p < 0.001). With the exception of post-operative month 3, the number of glaucoma medications between TE and PTE groups at all time points was not significantly different.
Figure 1:
Violin plot demonstrating the distribution of intraocular pressures in the operative eyes at pre-operative baseline and all post-operative visits following trabeculectomy or phaco-trabeculectomy. POD = post-operative day, POM = post-operative month, POY = post-operative year.
Figure 2:
Bar chart demonstrating the mean number of intraocular pressure-lowering medications used in the operative eye at pre-operative baseline and all post-operative visits following trabeculectomy or phaco-trabeculectomy. Whiskers indicate the standard error. POD = post-operative day, POM = post-operative month, POY = post-operative year.
Finally, Kaplan Meier survival analysis comparing TE failure in eyes that underwent TE with those that underwent PTE did not show a significant difference in survival (p = 0.17, Log-Rank). A total of 84 (25.9%) surgeries met failure criteria over the follow-up period. After adjusting for surgery type, sex, age, race, surgeon, and glaucoma diagnosis in a Cox proportional hazards model with the same failure outcome, there were no significant predictors in TE failure (Table 2). Sensitivity analyses conducted with definitions of TE failure that included IOP criteria (IOP>16 or IOP>21) similarly did not show a significant difference in TE failure between TE and PTE (Supplemental Tables 1 and 2; Supplemental Figures 1 and 2).
Table 2:
Cox proportional hazards model for post-trabeculectomy eyes requiring more IOP-lowering medications than at pre-operative baseline or undergoing second glaucoma surgery
| Hazard Ratio | 95% CI | P-value | |
|---|---|---|---|
| Age (per year increase) | 1.00 | (0.99 – 1.01) | 0.897 |
| Female (reference = male) | 0.89 | (0.68 – 1.18) | 0.425 |
| Race/Ethnicity (reference = White) | |||
| Black | 0.94 | (0.67 – 1.18) | 0.816 |
| Asian or Pacific Islander | 0.83 | (0.59 –1.17) | 0.280 |
| Hispanic/Latino | 0.99 | (0.64 – 1.53) | 0.955 |
| Other/Unknown | 1.02 | (0.69 – 1.51) | 0.905 |
| Glaucoma diagnosis (reference = POAG) | |||
| Narrow/Closed Angle | 0.92 | (0.40 – 2.11) | 0.837 |
| Secondary Glaucomas | 0.89 | (0.37 – 2.18) | 0.802 |
| Other/Unknown | 0.84 | (0.35 – 2.07) | 0.692 |
| Surgeon (reference = Surgeon 4) | |||
| Surgeon 1 | 0.89 | (0.44 – 1.81) | 0.746 |
| Surgeon 2 | 1.29 | (0.90 – 1.84) | 0.160 |
| Surgeon 3 | 0.73 | (0.10 – 5.57) | 0.760 |
| Baseline IOP (per 1-point increase) | 0.99 | (0.97 – 1.00) | 0.090 |
| Phaco-trabeculectomy (reference = TE) | 1.00 | (0.75 – 1.35) | 0.982 |
POAG: primary open-angle glaucoma; TE: trabeculectomy
DISCUSSION
In this hospital-based study, found no difference in mean post-operative IOP or glaucoma medication prescription between TE and PTE groups beyond post-operative month 3, up to and including postoperative year 5. Furthermore, we did not find a significant difference in the TE failure rate between PTE and TE groups. This study highlights that both TE and combined PTE are effective procedures for IOP lowering and performing cataract extraction by phacoemulsification at the time of TE does not appear to have a detrimental effect on the TE.
Several prior studies 5–9 have reported similar TE survival rates comparing patients undergoing TE versus combined cataract surgery and TE. Stewart et al. 6 reviewed 17 consecutive patients undergoing PTE, and patients were found to have no significant difference in IOP control or bleb viability when compared to TE controls over a 1 year follow up. Derick et al. 5 reviewed 42 cases of PTE and found no significant differences in mean IOP or number of glaucoma medications when compared to age-matched TE cases at a mean follow-up time of 21 months. A third study by Tsai et al. 17 reviewing 75 combined cataract and TE surgeries and 24 TE-only surgeries in patients with primary angle closure glaucoma, also found no significant difference in mean IOP, number of glaucoma medications, incidence of postoperative complications, or TE survival at 3 years follow up. However, this study, along with others 7,17,18 that evaluated performance of combined cataract-TE included cases of extracapsular cataract extraction (ECCE) rather than cataract extraction by phacoemulsification, making it difficult to draw conclusions to present day strategies, as ECCE is no longer routinely performed. One prior study by Caprioli et al. 11 that reviewed 40 cases of PTE and 40 TE controls found a significantly greater mean IOP reduction (10.3mmHg versus 6.8mmHg, p<0.05) and lower rate of TE failure (88% versus 62%, p=0.04) among PTE patients over 2-year follow up, using 5-fluorouracil. It is noteworthy, however, that the eyes in this study received 5-fluorouracil but not intra-operative mitomycin C as was the case in our series. A separate prospective study by Ogata-Iwao et al. 19 comparing TE to PTE found that patients who underwent PTE had a significantly lower rate of achieving a 20% or greater IOP reduction at 2 years as compared to pre-operative baseline, however the study group size was relatively low at 26 patients in each group.
An alternative to PTE in patients with comorbid cataract is to perform separate procedures, typically starting with TE followed months later by cataract extraction in eyes with uncontrolled advanced glaucoma or cataract extraction alone followed by TE in eyes with less severe glaucomatous disease. Some in the latter category may be better served with combined cataract and novel minimally invasive glaucoma surgery which can delay and, in some cases, obviate the need for future TE. Outcomes of surgical staging of TE and cataract surgery have been extensively studied. Data from prior studies 8,15,16,20–24, albeit mixed, suggests that clear corneal wound cataract surgery by phacoemulsification in patients with pre-existing TE is associated with an increased risk of IOP elevation or of bleb failure. For example, Husain et al. 24 reported on a large cohort study of patients undergoing cataract surgery, with follow-up of up to a mean of 21 months after TE. They found that patients who had cataract surgery were at a higher risk of IOP increase to above 21 mmHg than those who did not undergo cataract surgery. Although not statistically significant, we observed a trend toward late TE failure in patients who received TE alone (Figure 3). It is unclear if this effect could be attributed to subsequent cataract surgery in post-TE eyes that was not captured by our search parameters. Nevertheless, the observed trend was not statistically significant.
Figure 3:
Kaplan-Meier curves for composite outcome of receiving a greater number of glaucoma medications compared to pre-operative baseline or undergoing a second laser or surgical glaucoma procedure. Log-Rank test to compare eyes that underwent primary trabeculectomy (Trab) compared to those that underwent combined phacoemulsification and trabeculectomy (Phaco-Trab) did not show a significant difference in the chance of survival (p = 0.17).
This study has limitations, including that it is retrospective, observational in nature, and comes from a single institution, limiting the ability to control all potential confounding variables. Information on socioeconomic status was not available. Furthermore, documentation in electronic health records may be incomplete or inaccurate, particularly in regard to medication lists 25. However, generally due to computerized order entry, medication lists are likely to be more inaccurate in capturing discontinuation of medications rather than starting new medications, which typically require entry into the EHR in order to prescribe; a recent manual validation of glaucoma medication usage after cataract surgery showed very high accuracy for determining whether patients were on increased glaucoma medications compared to pre-surgical baseline 26. Therefore, failure due to increasing medication usage would be more likely to be captured. Furthermore, EHR inaccuracies are unlikely to be differential between patients who received PTE vs TE, and therefore unlikely to bias the results towards either group with regard to our study outcome measures. Another limitation of this study design is that it does not address differences in adverse events between the two groups before, during or after surgery. To the extent, however, that some adverse events are related to surgical failure and thus higher IOP, we did not find differences between the two groups. Our study additionally does not include central corneal thickness, which is known to be a risk factor for open angle glaucoma and can impact intraocular pressure measurements, nor do we have data on severity of glaucoma. Finally, comprehensive visual function measured with visual field testing, the ultimate outcome measure, was not compared between the two groups, although visual acuity was found to be not significantly different at postoperative year 1. With these limitations in mind, unique strengths of our study include the significantly larger patient sample size followed over a significantly greater follow-up time period than previous studies comparing TE with or without cataract surgery. Our finding of similar IOP outcomes between TE and PTE eyes suggests that PTE should be considered in the appropriate setting, especially considering findings of prior studies that show a rise in IOP after cataract surgery in eyes with a history of TE.
TE is the gold-standard surgical procedure for patients with progressive glaucomatous vision loss or uncontrolled IOP despite maximum medical therapy. The decision regarding whether to proceed with TE alone, PTE, cataract surgery with a minimally invasive glaucoma surgical procedure or cataract surgery alone as the first procedure in eyes with coexistent cataract and glaucomatous disease is complex and generally based upon multiple factors including disease severity, number of preoperative medications, IOP goals as well as physician and patient preferences. Comparing all cases of TE and combined PTE at our institution between 2009 and 2018, we found no significant difference in the rate of TE failure, suggesting that both TE and PTE result in effective IOP in glaucoma patients. Future controlled studies will be needed to validate the findings of this study.
Supplementary Material
Supplemental Figure 1: Kaplan-Meier curves for outcome of recording an intraocular pressure of greater than 16 mmHg at or greater than 6 months after surgery. Log-Rank test to compare eyes that underwent primary trabeculectomy (Trab) compared to those that underwent combined phacoemulsification and trabeculectomy (Phaco-Trab) did not show a significant difference in the chance of survival (p = 0.31).
Supplemental Figure 2: Kaplan-Meier curves for outcome of recording an intraocular pressure of greater than 16 mmHg at or greater than 6 months after surgery. Log-Rank test to compare eyes that underwent primary trabeculectomy (Trab) compared to those that underwent combined phacoemulsification and trabeculectomy (Phaco-Trab) did not show a significant difference in the chance of survival (p = 0.11).
Acknowledgments
Financial Support: Supported by Research to Prevent Blindness, Inc, New York, New York, and the National Eye Institute, National Institutes of Health (grant no.: P30-026877 [S.Y.W.]); Research to Prevent Blindness Career Development Award [S.Y.W]; the National Library of Medicine, National Institutes of Health (grant no.: T15 LM 007033 [S.Y.W.]). The sponsors or funding organization had no role in the design or conduct of this research.
Footnotes
DECLARATION OF INTEREST
The authors report no conflicts of interest.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author, [S.Y.W.]. The data are not publicly available due to their containing information that could compromise the privacy of research participants.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplemental Figure 1: Kaplan-Meier curves for outcome of recording an intraocular pressure of greater than 16 mmHg at or greater than 6 months after surgery. Log-Rank test to compare eyes that underwent primary trabeculectomy (Trab) compared to those that underwent combined phacoemulsification and trabeculectomy (Phaco-Trab) did not show a significant difference in the chance of survival (p = 0.31).
Supplemental Figure 2: Kaplan-Meier curves for outcome of recording an intraocular pressure of greater than 16 mmHg at or greater than 6 months after surgery. Log-Rank test to compare eyes that underwent primary trabeculectomy (Trab) compared to those that underwent combined phacoemulsification and trabeculectomy (Phaco-Trab) did not show a significant difference in the chance of survival (p = 0.11).
Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author, [S.Y.W.]. The data are not publicly available due to their containing information that could compromise the privacy of research participants.