The most common surgical techniques for the management of glaucoma are filtering surgery and outflow channel surgery focused on Schlemm’s canal. Trabeculotomy is an outflow channel surgery first reported by Burian1 and Smith2 in 1960. Harms subsequently modified the technique in 1970, employing a scleral flap to more easily identify Schlemm’s canal, which further popularized the surgery.3
The goal of trabeculotomy is to reduce intraocular pressure (IOP) in patients with glaucoma by relieving the resistance of aqueous humor outflow. Numerous studies demonstrated the efficacy of trabeculotomy in reducing the IOP without bleb formation.1–10 As trabeculotomy does not result in bleb formation, postoperative complications, such as bleb leaks, hypotony, flat anterior chambers, and serous choroidal detachment, which are associated with trabeculectomy, develop less frequently than after filtering surgery (trabeculectomy).2,3
Conventional trabeculotomy with metal trabeculotomes applies to a 120-degree incision of Schlemm’s canal,2,4 whereas new techniques performing 360-degree trabeculotomy have been developed to further reduce IOP.5–8 The mechanism of IOP reduction by trabeculotomy is theorized to be through the elimination of the aqueous flow resistance by cleavage of the trabecular meshwork and inner walls of Schlemm’s canal at the point of outflow resistance of aqueous humor. Provided that the inner wall of Schlemm’s canal and the juxtacanalicular tissue are incised circumferentially up to 360 degrees, the resistance between the anterior chamber and Schlemm’s canal becomes negligible. Thus, theoretically, 360-degree trabeculotomy is likely to reduce IOP to a level close to the episcleral venous pressure in healthy human eyes (ie, 6–9 mm Hg).9
It was previously reported that 360-degree suture trabeculotomy (ST) involves making an incision along the entire circumference of the trabecular meshwork and inner wall of Schlemm’s canal using a suture.5,6 We also previously reported the effectiveness of modified 360-degree ST for adult patients with glaucoma,7,8 and revealed that the level of postoperative IOP and number of anti-glaucoma medications after ST were lower than those observed after trabeculotomy with metal trabeculotomes. In addition, the success rate of ST was higher than that of trabeculotomy with metal trabeculotomes.
The aims of this study were (1) to clarify the effects of ST on IOP and aqueous outflow resistance and (2) to delineate the preoperative prognostic predictor of ST using tonographic outflow facility.
MATERIALS AND METHODS
Patients
This study was a retrospective case series of 43 consecutive eyes of 32 patients. Informed consent was received from all patients enrolled in this study. The institutional review board of Hokkaido University Hospital for clinical research approved this study, and it followed the tenets of the Declaration of Helsinki.
In the study group, the patients underwent ST7 at Hokkaido University Hospital, Sapporo, Japan between April 2017 and February 2020. Exclusion criteria were as follows: eyes with a history of previous glaucoma surgery or selective laser trabeculoplasty, eyes that underwent intraocular surgery within 3 months before ST, and secondary glaucoma eyes in the active phase of uveitis.
Measurements
Each patient underwent general health interviews and comprehensive ophthalmologic examinations, including visual acuity, IOP, slit-lamp biomicroscopic, gonioscopic, funduscopic observations, and visual field test.
Aqueous outflow resistance was evaluated by the coefficient of aqueous outflow (C-value), which was measured using tonographic outflow facility; electronic Schiötz tonographer (Auto-Tonograph, Takada Cooper Vision). The C-value was calculated from the rate of decay of IOP in the supine position during the application of a recording probe on the cornea over a period of 4 minutes with a standard weight of 5.5 g.10 After the start of measurement, the point where the waveform stabilized was set as P0 and that 4 minutes later was P4 (Fig. 1). Each 4-minute pressure tracing was recorded and according to Grant’s formula,11 the outflow facility coefficient, C, was calculated using the IOP at P0 and P4.12
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FIGURE 1: The tonographic curve obtained by recording the outflow IOP over time. The C-value was calculated using the IOP at P0 (0 min) and P4 (4 min). IOP indicates intraocular pressure.
Surgical Procedure
Surgery was performed using local peribulbar anesthesia in all cases. ST was performed as described in a previous paper.7 In brief, a fornix-based conjunctival flap was dissected at the inferior-temporal position to create a double scleral flap. After the circumference of Schlemm’s canal was cannulated, a 5–0 nylon suture was inserted from both corners of the scleral flap into the anterior chamber and pulled out with microcapsule forceps from a clear corneal side port incision made at the opposite side, resulting in a 360-degree incision of Schlemm’s canal.
Data Collection and Outcome Measures
The demographic data, including age, sex, type of glaucoma, and glaucoma medications, were reviewed from clinical charts. The preoperative IOP, number of antiglaucoma medications, and C-values were recorded as the baseline. Furthermore, postoperative IOP, the number of antiglaucoma medications, and C-values were evaluated. The surgical success was defined as IOP <21 mm Hg with similar or lower dosage of anti-glaucoma medications and at least 20% reduction from preoperative IOP. IOP <5 mm Hg at any postoperative visit or additional IOP-reducing procedures were considered to be indications of failure. Next, the eyes were divided into a low baseline C-value group (≤0.17) or high baseline C-value group (>0.17), based on the distribution of preoperative C-values (the median baseline C-value was 0.17).
Statistical Analysis
The IOP, antiglaucoma medication scores and C-values at each time point (baseline, 3 and 6 mo) were statistically analyzed using generalized estimation equation models. This modeling allowed for between-eye correlation when both eyes of patients were included for analysis. Rates of change in postoperative IOP and C-values were calculated by dividing the IOP or C-value at 3 or 6 months by the baseline IOP or C-value. Linear regression analysis was used to determine the correlation between rates of change of IOP and C-value. In addition, the correlation between baseline C-values and IOP reduction at 3 and 6 months was statistically analyzed using Pearson correlation coefficient tests.
Kaplan-Meier survival curves were generated to evaluate the success over time and to compare the low baseline C-value group (≤0.17) and the high baseline C-value group (>0.17) by log-rank tests. Multivariate Cox proportional hazards regression model analysis was used to examine the predictive value of the significant factors. The following factors were tested for associations with the qualified failure: age, baseline IOP, and baseline C-value.
All analyses were performed using StatPlus software version v7 (AnalystSoft Inc.) and IBM SPSS Statistics (IBM Corp.). P<0.05 was considered to be significant.
RESULTS
In total, 43 eyes of 32 patients were included. Follow-up for all 43 eyes was performed at 3 months and for 37 eyes at 6 months. The mean age was 58.0±11.6 years (range: 30–80 y); 14 patients (43.8%) were male and 18 (56.2%) were female; 21 cases (65.6%) were unilateral, and 11 cases (34.4%) were bilateral. Glaucoma types are shown in Table 1, which included primary open angle glaucoma (POAG) in 27 eyes (62.8%), uveitic glaucoma (UG) in 7 (16.3%), exfoliation glaucoma (XG) in 6 (13.9%), and steroid glaucoma (SG) in 3 (7.0%). Cataract surgery was performed in 11 of 43 (25.6%) eyes together with ST. The mean number of antiglaucoma medications was 3.8±1.1 at baseline, 0.9±1.3 at 3 months, and 1.0±1.1 at 6 months. Seven eyes were measured under oral carbonic anhydrase inhibitors (acetazolamide: 250–750 mg/day) at baseline, and no eye was measured under oral carbonic anhydrase inhibitors at 3 or 6 months. No eye required additional glaucoma surgery during the follow-up period.
TABLE 1 -
Glaucoma Types by Patient (No. eyes)
| POAG |
27 |
Eyes |
| UG |
7 |
— |
| XG |
6 |
— |
| SG |
3 |
— |
| Total |
43 |
Eyes |
EG indicates exfoliation glaucoma; POAG, primary open angle glaucoma; SG, Steroid glaucoma; UG, uveitic glaucoma
The overall IOP (A) and C-value (B) changes at each postoperative time point compared with the baseline are shown in Figure 2. The mean IOP at baseline was 19.0±7.3 mm Hg and the mean C-value at baseline was 0.19±0.09 µL/min/mm Hg. Although the differences were not significant, IOP decreased to 15.4±3.3 mm Hg at 3 months (P=0.10) and 16.1±3.8 mm Hg at 6 months (P=0.21)(A). In addition, there were significant decreases in anti-glaucoma medication scores at both 3 and 6 months after surgery (P<0.01). There was no significant difference between IOP at 3 months and at 6 months (P=0.67). The C-value increased significantly to 0.24±0.11 µL/min/mm Hg at 3 months (P<0.01) and increased significantly to 0.27±0.14 µL/min/mm Hg at 6 months (P<0.01) (B). There was no significant difference between C-value at 3 months and at 6 months (P=0.47). There was no significant difference in the C-values between the ST alone group and ST with cataract surgery group (ST alone group: 0.19±0.09 at baseline, 0.24±0.09 at 3 months and 0.27±0.15 at 6 months; ST with cataract surgery group: 0.19±0.08 at baseline, 0.27±0.12 at 3 months and 0.28±0.08 at 6 months P=0.73).
FIGURE 2: A, Overall IOP changes at each postoperative time point (3 and 6 mo) compared with baseline IOP. B, Overall C-value changes at each postoperative time point (3 and 6 mo) compared with baseline C-value. *Significant. IOP indicates intraocular pressure.
The correlation between the baseline C-value and baseline IOP is shown in Figure 3. The baseline IOP was negatively correlated with the baseline C-value (r=−0.40 P<0.01).
FIGURE 3: Correlation between baseline intraocular pressure and baseline C-value. *Significant.
Next, the rates of change in IOP and C-value at 3 and 6 months from baseline were calculated to evaluate the relationship between IOP and C-value change. The mean rate of change in IOP was 0.87±0.24 at 3 months and 0.80±0.33 at 6 months. The mean rate of change in the C-value was 1.53±0.79 at 3 months and 1.56±0.68 at 6 months. The correlations between rates of change in C-value and IOP from baseline at 3 months (A) and 6 months (B) postoperatively are shown in Figure 4. The rates of change in C-value were negatively correlated with that in IOP at 3 months (r=−0.49P<0.01) (A) and 6 months (r=−0.46 P<0.01) (B).
FIGURE 4: A, Correlation between rates of change in IOP and C-value from baseline at 3 months. B, Correlation between rates of change in IOP and C-value from baseline at 6 months. *Significant. IOP indicates intraocular pressure.
We next examined the relationship between preoperative C-values and IOP reduction to assess whether baseline C-values can predict the IOP-reducing effects after surgery. The mean IOP reduction was 3.6±6.9 mm Hg at 3 months and 3.8±7.6 mm Hg at 6 months. The correlations between IOP reduction and baseline C-value at 3 months (A) and 6 months (B) are shown in Figure 5. The IOP reductions at 3 months and 6 months were significantly correlated with the baseline C-value (r=−0.39 P<0.05, r=−0.33P<0.05, respectively).
FIGURE 5: A, Correlation between IOP reduction from baseline at 3 months and baseline C-value. B, Correlation between IOP reduction from baseline at 6 months and baseline C-value. *Significant. IOP indicates intraocular pressure.
In addition, Kaplan-Meier survival analysis was performed on each of the 2 groups divided by baseline C-value, applying the definition of success (IOP <21 mm Hg, IOP reduction >20%). The success survival rates at 3 months and 6 months after the surgery were 86.4% and 81.3% in the eyes with low baseline C-value (≤0.17), and 66.7% and 46.7% in the eyes with high baseline C-value (>0.17) (Fig. 6). The survival rate for eyes with low baseline C-value was statistically significantly higher than those with high baseline C-value (P<0.05, Log-rank test). Furthermore, risk factors for surgical failure were identified using cox regression analysis. Table 2 presents the univariable associations with the qualified success. Baseline IOP and C-values were significantly associated with the success (P<0.01, P<0.05), whereas age was not significantly associated with the success (P=0.88).
FIGURE 6: Kaplan-Meier survival curves of success for C-value. The solid line shows a low baseline C-value (≤0.17); high aqueous outflow resistance. The dotted line shows a high baseline C-value (>0.17); low aqueous outflow resistance. Success was greater in the eyes with a low baseline C-value (≤0.17) than those with a high baseline C-value (>0.17) (P<0.05, Log-rank test).
TABLE 2 -
Univariable Associations with Success
|
Univariate |
| Factors |
RR |
HR (95% CI) |
P
|
| Age per year |
1.00 |
0.955–1.040 |
0.88 |
| Baseline IOP per mm Hg |
0.71 |
0.589–0.854 |
<0.01 |
| Baseline C-value per µL/min/mm Hg |
2.7×103
|
4.893–1.5×106
|
<0.05 |
CI indicates confidence interval; HR, hazard ratio; RR, risk ratio.
Finally, we evaluated the effects of ST on IOP (Table 3), a number of anti-glaucoma medications (Table 4), and C-values (Table 5) by subtypes of glaucoma (POAG, UG, XG, and SG).
TABLE 3 -
Mean IOP of each Glaucoma Type
|
Baseline (mm Hg) |
3 M (mm Hg) |
6 M (mm Hg) |
| POAG |
16.7±2.4 |
15.1±3.0*
|
15.8±2.2 |
| Other types of glaucoma |
23.0±10.6 |
15.9±3.9 |
16.5±5.4 |
| UG |
25.1±12.2 |
15.7±4.9 |
17.1±5.3 |
| XG |
19.2±4.2 |
15.7±2.3 |
16.2±6.2 |
| SG |
25.6±11.6 |
17.0±2.8 |
15.3±1.2 |
| Overall |
19.0±7.2 |
15.4±3.3 |
16.1±3.8 |
Generalized estimation equation models were performed at the time points for each glaucoma type, other types of glaucoma, and overall.
*(P<0.01, compared with baseline).
EG indicates exfoliation glaucoma; POAG, primary open angle glaucoma; SG, Steroid glaucoma; UG, uveitic glaucoma
TABLE 4 -
Mean Number of Topical Glaucoma Medications of Each Glaucoma Type
|
Baseline |
3 M |
6 M |
| POAG |
3.7±1.0 |
0.8±1.2*
|
1.0±1.0*
|
| Other types of glaucoma |
3.9±1.4 |
1.0±1.4*
|
1.1±1.3*
|
| UG |
3.9±1.5 |
0.9±1.4 |
1.1±1.4 |
| XG |
4.3±0.7 |
1.7±1.4 |
1.4±1.4 |
| SG |
3.3±1.7 |
0.0±0.0 |
0.3±0.5 |
| Overall |
3.8±1.1 |
0.9±1.3*
|
1.0±1.1*
|
Generalized estimation equation models were performed at the time points for each glaucoma type, other types of glaucoma, and overall.
*P<0.01; compared with baseline.
EG indicates exfoliation glaucoma; POAG, primary open angle glaucoma; SG, Steroid glaucoma; UG, uveitic glaucoma
TABLE 5 -
Mean C-value of Each Glaucoma Type
|
Baseline (µL/min/mm Hg) |
3 M (µL/min/mm Hg) |
6 M (µL/min/mm Hg) |
| POAG |
0.22±0.08 |
0.25±0.10 |
0.32±0.15*
|
| Other types of glaucoma |
0.14±0.08 |
0.25±0.12*
|
0.22±0.11*
|
| UG |
0.16±0.09 |
0.29±0.12 |
0.21±0.09 |
| XG |
0.11±0.03 |
0.16±0.03 |
0.20±0.11 |
| SG |
0.18±0.07 |
0.32±0.11 |
0.25±0.12 |
| Overall |
0.19±0.09 |
0.24±0.11*
|
0.27±0.14*
|
Generalized estimation equation models were performed at the time points for each glaucoma type, other types of glaucoma, and overall.
*(P<0.01; compared with baseline).
EG indicates exfoliation glaucoma; POAG, primary open angle glaucoma; SG, Steroid glaucoma; UG, uveitic glaucoma
The mean IOP at baseline was 16.7±2.4 mm Hg for POAG and 23.0±10.6 mm Hg for the other types of glaucoma (UG, XG, and SG) (Table 3), and the mean C-value at baseline was 0.22±0.08 µl/min/mm Hg for POAG and 0.14±0.08 µl/min/mm Hg for other types of glaucoma (Table 5). Although there were no significant differences, the baseline IOP was lower in POAG than in the other types of glaucoma (POAG: 16.7±2.4 mm Hg; the others: 23.0±10.6 mm Hg P=0.06), and the C-value was higher in POAG than in the other types of glaucoma (POAG: 0.22±0.08 µL/min/mm Hg; and the others: 0.14±0.08 µL/min/mm Hg; P=0.05). On the other hand, there was no significant difference in the antiglaucoma medication scores between the 2 groups (POAG: 3.7±1.0; the others: 3.9±1.4; P=0.55) (Table 4).
In 27 eyes with POAG, excluding other types of glaucoma, IOP significantly decreased in 3 months (P<0.01). However, IOP did not significantly decrease in 6 months (P=0.88). In addition, there was a significant decrease in anti-glaucoma medication scores at both 3 and 6 months after surgery (P<0.05) (Table 4). Regarding C-values, there was a significant increase in POAG eyes at 6 months postoperatively (from 0.22±0.08 µL/min/mm Hg at baseline to 0.32±0.15 µL/min/mm Hg at 6 months, P<0.01) (Table 5).
For other types of glaucoma, although IOP did not decrease significantly, anti-glaucoma medication scores decreased significantly at 3 months (1.0±1.4, P<0.01) and 6 months (1.1±1.3, P<0.01) (Tables 3 and 4). The C-values significantly increased at 3 months and 6 months postoperatively (0.25±0.12 µL/min/mm Hg and 0.22±0.11 µL/min/mm Hg, P<0.01) (Table 5) compared with baseline (23.0±10.6 mm Hg, 3.9±1.4, 0.14±0.08 µL/min/mm Hg, respectively). However, in each subgroup (UG, XG, and SG), there were no significant differences in IOP or C-value due to the small sample size (Tables 3 and 5).
DISCUSSION
After ST, the mean IOP decreased by 3.6 and 2.9 mm Hg, the mean anti-glaucoma medication score decreased by 2.9 and 2.8, and the mean C-value increased by 0.05 and 0.08 µL/min/mm Hg from the baseline at 3 and 6 months. The IOP did not decrease significantly; however, the mean anti-glaucoma medication score significantly decreased in 43 eyes after ST. The C-value increased significantly at 3 months and 6 months.
Aqueous humor flows out of the eye primarily through conventional outflow pathways, including the trabecular meshwork and inner walls of Schlemm’s canal. Trabecular meshwork stiffness is higher in human glaucomatous eyes than in normal eyes.13 Therefore, impairment of aqueous humor outflow, which reduces the C-value and increases IOP, is a central tenet of the pathophysiology and treatment of glaucoma.10,14
Our surgical procedure, ST, can eliminate the most resistant part of the trabecular meshwork and increase aqueous outflow directly to the collector channels by opening the entire circumference of Schlemm’s canal.13,14 To our knowledge, this is the first study to assess the aqueous outflow resistance after ST by measuring the C-value using an electronic Schiötz tonographer.
The C-value reflects the ratio of the outflow rate to relevant pressure. A higher C-value indicates lower outflow resistance. In this study, there was a negative correlation between the preoperative IOP and C-value. The linear regression analysis, which demonstrated that a higher IOP is associated with a lower C-value, was consistent with a previous study.15
Tanito et al reported that the mean C-value of 0.27 µL/min/mm Hg significantly increased to 0.51 µL/min/mm Hg after Microhook ab interno trabeculotomy, although they measured the C-value during the early postoperative period.15 Furthermore, another previous study reported that small-incision cataract surgery increases the C-value.16 Although our present study also included 11 eyes with simultaneous cataract surgery, we considered the effects minimal because our previous study revealed no significant difference in IOP reduction between ST alone and ST combined with cataract surgery.15 In our study, there was no significant difference in the C-values between the ST alone group and ST with the cataract surgery group. We would consider the additive effect of combined cataract surgery to be minimal or negligible on C-values.
The purpose of trabeculotomy is to reduce the resistance of aqueous outflow through mechanical cleavage of the trabecular meshwork and inner layer of Schlemm’s canal. It was reported that 360-degree trabeculotomy eliminated 49% of outflow resistance at 7 mm Hg in enucleated human eyes.17,18 ST removes the resistance of the trabecular meshwork by cutting it circumferentially and may consequently increase aqueous outflow. Indeed, the rates of change in IOP and C-value were negatively correlated in this study. Accordingly, a large part of the IOP reduction after ST can be explained by the increased outflow from Schlemm’s canal.
Alaghband et al reported that the pretreatment C-value is unlikely to be a predictor of the response to selective laser trabeculoplasty, but pretreatment IOP is strongly associated with its success.19 In contrast, there was a negative correlation between the preoperative C-value and IOP reduction after ST in this study. This disparity may be caused by the nearly complete removal of outflow resistance in the trabecular meshwork by ST, whereas SLT has insufficient laser penetration if the trabecular meshwork wall is thick with a low C-value.
Furthermore, this study showed the postoperative qualified success was greater in the eyes with low baseline C-value (≤0.17) than in those with high baseline C-value (>0.17). It was indicated that the outflow resistance after ST may be greatly reduced in the eyes with low baseline C-value. The surgical success was statistically significant in association with baseline IOP and C-value but not with age. These results mean baseline C-value, which shows aqueous outflow resistance, is likely to be a predictor of the ST outcomes along with baseline IOP. If surgical outcomes can be predicted by examining the tonographic outflow facility before surgery, this also makes it possible to create a much more precise informed consent for patients before the surgery.
In addition, this study assessed the effects of the difference in glaucoma types on the aqueous outflow resistance after ST. On the basis of the time course of C-values (Table 5), POAG exhibited a significant increase at 6 months postoperatively, whereas the other types of glaucoma exhibited a significant increase at 3 months postoperatively. When the other types of glaucoma were further divided into UG, XG, and SG, although not significant due to the small sample size, UG and SG had a peak in C-value at 3 months, suggesting a difference in the time course of the C-value between POAG and the others.
This may be explained by the main causes of increased IOP in UG and SG. Typically, increased aqueous outflow resistance in these glaucoma types occurs as a result of mechanical obstruction of the trabecular meshwork, which may be blocked by cells, proteins, debris, or fibrin in UG,20 or extracellular materials in SG.21 Therefore, the C-values at 3 months after ST may be greatly improved, but its decrease at 6 months is due to reblockage in collector channels. The reocclusion also can occur in XG, but outflow obstruction due to deposition of fibrillar extracellular substance in collector channels can occur after more than 6 months. Further studies are required because the sample size was small in this study.
This study has limitations. Its retrospective nature is an issue. The study has limited numbers and follow-ups. In addition, as the number of anti-glaucoma medications decreased after surgery, the influence of antiglaucoma medications cannot be excluded. In particular, the discontinuation of ripasudil, which is thought to affect the conventional outflow pathway, may have affected our data. The effects of discontinuation of other anti-glaucoma medications on the uveoscleral pathway were not evaluated in this study. However, we were able to confirm the mechanism of IOP reduction by ST and to clarify the possibility of identifying patients who may respond better to ST by measuring C-values preoperatively. Based on this study, UG, XG, and SG with low C-values are indicated for ST.
In conclusion, increased conventional outflow by elimination of the aqueous outflow resistance at the trabecular meshwork is the main mechanism of IOP reduction after ST. Preoperative C-value, which shows aqueous outflow resistance, is likely to be useful for predicting the outcomes of ST. Cases with low preoperative C-value, rather than those with high preoperative C-value as seen in POAG, may be suitable for ST.
ACKNOWLEDGMENTS
The authors thank Yuka Ishibashi, Yuna Kaneko, Mai Aritsuka, and Ayako Mizoguchi for supporting this study.
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