Incidence and risk factors of early transient intraocular pressure elevation after canaloplasty for primary open-angle glaucoma

Incidence and risk factors of early transient intraocular pressure elevation after canaloplasty for primary open-angle glaucoma 原发性开角型青光眼黏小管成形术后早期短暂性高眼压的发生率及危险因素分析 1 2 3 first-author 1 2 3 1 2 3 1 2 3 4 1 2 3 1 2 3 1 2 3 1 2 3 corresp corresp Yuanbo LIANG, yuanboliang@wmu.edu.cn Yuanbo LIANG, yuanboliang@wmu.edu.cn Ruiyi REN, renruiyi@bu.edu Ruiyi REN, renruiyi@bu.edu renruiyi@bu.edu https://orcid.org/0000-0001-5785-2165 1 2 3 corresp Yuanbo LIANG, yuanboliang@wmu.edu.cn Yuanbo LIANG, yuanboliang@wmu.edu.cn yuanboliang@wmu.edu.cn https://orcid.org/0000-0001-9685-7356 温州医科大学附属眼视光医院，国家眼耳鼻喉疾病临床医学研究中心（眼部疾病），中国温州市，325027 温州医科大学附属眼视光医院，国家眼耳鼻喉疾病临床医学研究中心（眼部疾病），中国温州市，325027 National Clinical Research Center for Ocular Diseases, Eye Hospital, Wenzhou Medical University, Wenzhou 325027, China National Clinical Research Center for Ocular Diseases, Eye Hospital, Wenzhou Medical University, Wenzhou 325027, China 温州医科大学附属眼视光医院，省部共建国家眼视光学和视觉科学重点实验室，中国温州市，325027 温州医科大学附属眼视光医院，省部共建国家眼视光学和视觉科学重点实验室，中国温州市，325027 State Key Laboratory of Ophthalmology, Optometry and Visual Science, Eye Hospital, Wenzhou Medical University, Wenzhou 325027, China State Key Laboratory of Ophthalmology, Optometry and Visual Science, Eye Hospital, Wenzhou Medical University, Wenzhou 325027, China 温州医科大学青光眼研究所，中国温州市，325027 温州医科大学青光眼研究所，中国温州市，325027 Institute of Glaucoma, Wenzhou Medical University, Wenzhou 325027, China Institute of Glaucoma, Wenzhou Medical University, Wenzhou 325027, China 成都大学附属医院，中国成都市，610086 成都大学附属医院，中国成都市，610086 Clinical Medical College & Affiliated Hospital of Chengdu University, Chengdu 610086, China Clinical Medical College & Affiliated Hospital of Chengdu University, Chengdu 610086, China 为分析原发性开角型青光眼（primary open-angle glaucoma，POAG）黏小管成形术后早期短暂性高眼压的发生率及危险因素，本研究纳入了本院顺利完成360°黏小管成形术的POAG患者。我们收集了以下数据：术后各随访时间点眼压（intraocular pressure，IOP），术后早期是否发生短暂性高眼压（定义：术后1周至3月内IOP > 21 mmHg但能回落至≤21 mmHg）及术后一周最低IOP（IOP min-1w ）。根据是否发生术后早期短暂性高眼压，将其分为正常眼压组（normal IOP，NIOP）和短暂性高眼压组（high IOP，HIOP）。此外，我们也对术后早期短暂性高眼压的相关危险因素进行了分析。最终来自57位患者的57只眼纳入分析。他们的平均视野缺损值(mean defect, MD)为(-15.57±10.13) dB，IOP由术前 (29.43±10.27) mmHg显著降低至术后1年的(14.73±3.60) mmHg（ P < 0.01）。其中，20只眼发生HIOP（35.1%）。HIOP组的IOP min-1w 显著高于NIOP组（ P < 0.01），并与较低的1年完全成功率相关。本研究结果提示POAG中黏小管成形术后HIOP组患者可能IOP min-1w 较高，1年手术效果较差，且IOP min-1w ≥12 mmHg可能是HIOP发生的独立危险因素。 早期短暂性高眼压 黏小管成形术 原发性开角型青光眼（POAG） 危险因素 Glaucoma is one of the most common optic neuropathies, featuring progressive retinal ganglion cell damage and visual field loss ( Tham et al., 2014 Tham et al., 2014 ; Xu et al., 2020 Xu et al., 2020 ). Currently, the only effective treatment for this condition is the reduction of intraocular pressure (IOP) ( Palmberg, 2001 Palmberg, 2001 ; Heijl et al., 2002 Heijl et al., 2002 ). Canaloplasty is a proven bleb-independent surgery with good efficacy and safety profiles in primary open-angle glaucoma (POAG) ( Gołaszewska et al., 2021 Gołaszewska et al., 2021 ). However, early transient postoperative IOP elevation has been reported in up to 30% of cases ( Riva et al., 2019 Riva et al., 2019 ), similar to that commonly observed in other internal drainage glaucoma surgeries such as implantation using iStent (0%–21.0%), CyPass (10.8%), and Hydrus (4.8%–6.5%) ( Lavia et al., 2017 Lavia et al., 2017 ). This complication may be a predictor of poor reserve in the outflow system and is potentially associated with surgical failure. Nonetheless, the exact pathophysiology of glaucoma remains unknown, and studies clarifying the risk factors for postoperative IOP elevation have been scarce. In light of previous work, we speculated that both pre- and postocular factors are responsible for the postoperative dysfunction of the outflow system, which results in early transient postsurgical IOP elevation. Moreover, we analyzed the incidence and risk factors of IOP elevation within the first three postoperative months following canaloplasty, with the goal of optimizing the postoperative care of patients and clarifying the underlying mechanisms. Among the 77 eyes of 73 consecutive Chinese POAG patients who underwent canaloplasty with records for 12 months of follow-up, 16 eyes were excluded for the following reasons: trabeculectomy was performed in four eyes (5.2%) due to the failure of 360° catheterization during the operation; nine eyes (11.7%) required additional trabeculectomy within three months postoperatively due to persistent IOP elevation, despite that medical treatments were considered early failures; and three eyes (3.9%) were excluded because of incomplete or unreliable data during the one-year follow-up. Both eyes met the inclusion criteria in four patients, where only one eye was randomly selected. Finally, 57 eyes of 57 patients were included in the analysis. Patients were divided into subgroups with normal IOP (NIOP) and high IOP (HIOP) based on the presence of early transient IOP elevation, defined as IOP > 21 mmHg (1 mmHg=0.133 kPa), which reduced to ≤21 mmHg within one week to three months postoperatively. The baseline demographics are summarized in Table 1 Table 1 . The participants were predominantly male (73.7%), and the majority presented advanced POAG (59.5% and 55.0% in the NIOP and HIOP groups, respectively) according to the Hodapp-Anderson-Parrish criteria ( Wang et al., 2020 Wang et al., 2020 ). The mean ages of patients with NIOP and HIOP were (47.27±12.72) and (47.25±17.24) years, respectively. Patients with HIOP had longer glaucoma duration than those with NIOP ((4.39±6.87) vs. (2.57±2.33) years), although the difference was not statistically significant. * Previous intraocular surgery included anti-glaucoma, cataract, and vitreoretinal surgeries. Data are expressed as mean±standard deviation (SD), number (percentage), or percentage, except for gender. Significantly different P values were written in bold. OD, right eye; OS, left eye; IOP, intraocular pressure; BCVA, best-corrected visual acuity; RNFL, retinal nerve fiber layer; AL, axial length; min, minimum; IOP min-1w , lowest recorded IOP during the first postoperative week; Postoperative IOP min-1w ≥12 mmHg, the number of eyes with postoperative IOP min-1w above 12 mmHg; NIOP, normal IOP; HIOP, high IOP. Characteristics NIOP ( n =37) HIOP ( n =20) P value Age (years) 47.27±12.72 47.25±17.24 0.99 Gender (female/male) 10/27 5/15 0.87 OD/OS 19/18 10/10 0.92 Previous intraocular surgery * 0.31±0.63 0.11±0.32 0.11 Glaucoma duration (years) 2.57±2.33 4.39±6.87 0.28 Glaucoma stage 0.77 Early 8 (21.6%) 6 (30.0%) Moderate 7 (18.9%) 3 (15.0%) Late 22 (59.5%) 11 (55.0%) Preoperative IOP (mmHg) 30.08±10.62 28.26±9.79 0.53 Maximum recorded preoperative IOP (mmHg) 35.10±11.22 30.28±10.53 0.12 Preoperative medications 2.58±1.05 2.55±1.19 0.91 BCVA 0.78±0.29 0.78±0.27 0.96 Cup-to-disc ratio 0.82±0.15 0.79±0.15 0.35 Mean deviation (dB) -15.64±9.98 -15.45±10.64 0.95 RNFL thickness (μm) 68.82±17.73 71.78±18.87 0.58 AL (mm) 25.07±2.25 25.30±3.53 0.77 Postoperative IOP min-1w (mmHg) 9.16±2.76 12.76±3.70 <0.01 Postoperative IOP min-1w ≥12 mmHg 5 (13.5%) 12 (60.0%) <0.01 Follow-up period (months) 22.70±14.43 24.60±16.85 0.66 Qualified success rate for IOP≤21 mmHg 91.9% 85.0% 0.72 Complete success rate for IOP≤21 mmHg 78.4% 45.0% 0.01 Qualified success rate for IOP≤18 mmHg 86.5% 75.0% 0.28 Complete success rate for IOP≤18 mmHg 73.0% 35.0% <0.01 Qualified success rate for IOP≤15 mmHg 59.5% 30.0% 0.03 Complete success rate for IOP≤15 mmHg 54.1% 15.0% <0.01 HIOP occurred in 20 eyes (35.1%) with an average initial onset time of postoperative (2.45±1.40) weeks and a duration of (1.66±1.79) weeks. In all patients with HIOP, the IOP reduced to ≤21 mmHg during the first three postoperative months, with a mean follow-up time of (24.60±16.85) months. Surgical success was defined as postoperative 5 mmHg<IOP≤21 mmHg at each postoperative visit with (qualified success) or without (complete success) the use of anti-glaucoma medication and without additional surgical therapy. At 12 months, the cumulative complete and qualified success rates for all participants were 66.7% and 89.5% at IOP≤21 mmHg, respectively. Previous studies have shown that IOP in severe glaucoma eyes needs to be better controlled to achieve a better surgery outcome and the average value was 12 mmHg in those stable eyes ( Chandler, 1970 Chandler, 1970 ; Warjri et al., 2021 Warjri et al., 2021 ). Accordingly, the number of eyes with postoperative IOP min-1w (lowest recorded IOP during the first postoperative week) above 12 mmHg was compared between the two groups. Compared to the NIOP group, patients in the HIOP group had significantly higher postoperative IOP min-1w ((12.76±3.70) vs. (9.17±2.76) mmHg), and more cases were observed with IOP min-1w ≥12 mmHg (60.0% vs. 13.5%), and lower complete success rates (45.0% vs. 78.4%) (all P < 0.01). In the entire cohort, IOP significantly reduced from (29.43±10.27) mmHg to (12.98±5.80) mmHg at Day 1, (14.85±3.05) mmHg at three months, and (14.73±3.60) mmHg at one year (all P < 0.01). Compared to IOP at baseline, the mean IOP reduction in all participants was (37.81±26.31)% at the last follow-up, with a mean reduction of (2.05±1.33) medications. Fig. 1 Fig. 1 shows the longitudinal pre- and postoperative outcomes in terms of mean IOP, number of medications, and best-corrected visual acuity (BCVA) in the HIOP and NIOP groups. From Day 1 to 6 months postoperatively, patients in the HIOP group had a significantly higher IOP than those in the NIOP group (all P < 0.01). The mean BCVA remained stable during the one-year follow-up period. HIOP and complete success were significantly negatively correlated at one year postoperatively ( r =-‍0.34, P= 0.01). The variables compared between NIOP and HIOP with P < 0.15, including recorded IOP max-pre (the highest preoperative IOP value), IOP min-1w , IOP min-1w ≥12 mmHg, and number of previous intraocular surgery, were selected for further linear logistic regression analysis to evaluate the risk factors for HIOP. Among them, the only unique risk factor was IOP min-1w ≥12 mmHg (hazard ratio: 10.29, 95% confidence interval (CI): 2.72‍–38.84, P < 0.01) after adjusting for age, gender, and the eye laterally. Canaloplasty, a bleb-independent surgery that focuses on the dilation of Schlemm’s canal to facilitate the drainage of aqueous humor through the physiological route, is an increasingly popular procedure for POAG. In this study, the one-year qualified and complete success rates were 89.5% and 66.7%, respectively. These results were similar to those of previous studies that demonstrated the remarkable safety and efficacy of canaloplasty with qualified success rates between 86.2% and 95.5% (for IOP≤21 mmHg) and failure rates between 5% and 14% ( Lewis et al., 2011 Lewis et al., 2011 ; Brusini, 2014 Brusini, 2014 ; Seuthe et al., 2016 Seuthe et al., 2016 ). However, our success rates might have been overestimated due to the exclusion of early failures. Significant reductions in IOP and the number of medications were observed; however, little is known about early transient postoperative IOP elevation. While direct comparison is unfeasible, the incidence of HIOP in the present study (35.1%) was higher than that previously reported for Schlemm’s canal-based drainage surgeries, such as Ab interno viscocanaloplasty (22.2%) ( Gillmann et al., 2021 Gillmann et al., 2021 ) and Hydrus implantation (4.8%–6.5%) ( Lavia et al., 2017 Lavia et al., 2017 ). In our study, the most likely cause was the high prevalence of advanced glaucoma (57.9%), which might have severely disturbed aqueous humor outflow (AHO). This hypothesis is supported by the findings of prior studies that collector channels and intrascleral plexus sclerosis are destroyed in advanced glaucoma ( Fellman and Grover, 2014 Fellman and Grover, 2014 ). Early transient IOP elevation indicates the transient dysfunction of the AHO system, either due to the excessive production of obstructive materials or due to pathological changes in the outflow system. Brusini (2014) Brusini (2014) has suggested that viscoelastic substances and inflammatory cytokines can decrease outflow through the trabecular meshwork (TM) and collector channels. However, surgery-related viscoelastic substances or inflammation-induced IOP elevation usually diminish within one week; therefore, they cannot explain the longer duration of HIOP. Another presumed cause is corticosteroid-induced IOP elevation. While our patients received steroids for 2‍–‍4 weeks, HIOP was usually elevated at one week and reduced later, even with the continued use of steroids. Moreover, according to another study conducted by our group ( Hu et al., 2022 Hu et al., 2022 ), the HIOP developed in two out of ten corticosteroid-induced glaucoma eyes after penetrating canaloplasty with the continued use of steroid, implying that HIOP may go beyond steroid usage. Preoperative anatomical differences in AHO may be correlated with postoperative IOP elevation. Qi et al. (2020) Qi et al. (2020) found that in myopic eyes undergoing cataract surgery, eyes with early elevated IOP had smaller vertical diameter and area of Schlemm’s canal, as well as lesser TM thickness and width compared to those in the non-elevation group. Nonetheless, owing to the retrospective nature of this study, information on the structural characteristics of AHO was not available, and thus we could not evaluate these anatomical differences. Compared to the NIOP group, patients in the HIOP group had a higher average postoperative IOP min-1w , and IOP min-1w ≥12 mmHg was the only unique risk factor for HIOP. Moreover, HIOP was significantly negatively correlated with one-year complete success, implying that eyes with HIOP may have poorer AHO pump function and increased risk of surgical failure. Healthy TM cells can phagocytose debris and particulate material in the aqueous humor to maintain an unobstructed AHO ( Buller et al., 1990 Buller et al., 1990 ), and Schlemm’s canal plays an important role in regulating IOP ( Johnstone et al., 2021 Johnstone et al., 2021 ). This indicates that the postoperative AHO anatomy might be reshaped during disease or surgery, which could account for alterations in the microenvironment of the related cells (including TM cells and endothelial cells of Schlemm’s canal and its downstream pathways). These factors may impact IOP regulation. This hypothesis is supported by the findings of Yoshikawa et al. (2018) Yoshikawa et al. (2018) , who evaluated the morphological changes in AHO canals by optical coherence tomography (OCT) in glaucoma patients before and after trabecular-targeted minimally invasive glaucoma surgery. Alterations in the pre- and post-trabecular outflow system may be reversible in eyes with mild pathological AHO and rescue high IOP, whereas the circumferential opening of Schlemm’s canal after surgery may not have a significant effect on IOP in eyes with high distal post-trabecular outflow system resistance. We speculate that in the early postoperative (≤3 months) stage, the main reason for HIOP may be the reversible distal outflow resistance, while surgical failure may be due to TM dysfunction; therefore, identifying the precise mechanism requires further research. This study has several limitations. First, it had a single-center design, and only Chinese patients were included. Second, a selection bias could have resulted from the retrospective design, and the exclusion of patients with persistent IOP elevations and generally advanced glaucoma. These must have had a negative impact on the evidence intensity of these results. Third, the postoperative follow-up duration was only one year, and it is possible that further changes in the AHO patterns, collector channel entrances, and deep scleral plexus after canaloplasty may affect long-term prognosis. Conclusively, HIOP, which was more likely to develop in eyes with higher postoperative IOP min-1w , was associated with significantly lower one-year complete success rates than NIOP. Approximately 40% of the patients who underwent canaloplasty experienced early postoperative IOP elevation. Among these, 70% had transiently elevated IOP and 30% showed persistently high IOP, who were deemed to be subjects of surgical failure. These patients are difficult to distinguish at the early stage. Thus, regular follow-ups within three months postoperatively and timely IOP lowering are recommended for cases with early elevated IOP. 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Pilot study assessing the structural changes in posttrabecular aqueous humor outflow pathway after trabecular meshwork surgery using swept-source optical coherence tomography . PLoS ONE , 13 ( 6 ): e0199739 . https://doi.org/10.1371/journal.pone.0199739 https://doi.org/10.1371/journal.pone.0199739 Pilot study assessing the structural changes in posttrabecular aqueous humor outflow pathway after trabecular meshwork surgery using swept-source optical coherence tomography Lijuan XU: methodology, software, data acquisition and analysis, writing‒original draft, revision, and funding acquisition; Xinyao ZHANG and Yang CAO: data acquisition and analysis; Yin ZHAO, Juan GU, Wenqing YE, and Jinxin LI: data acquisition; Xiaojie WANG: data analysis; Ruiyi REN: methodology, writing‒reviewing and editing, revision, and supervision; Yuanbo LIANG: conceptualization, methodology, writing‍‒‍reviewing and editing, funding acquisition, and supervision. All authors have read and approved the final manuscript, and therefore, have full access to all the data in the study and take responsibility for the integrity and security of the data. This work was supported by the National Natural Science Foundation of China (No. 82201177), the Health Commission of Zhejiang Province (No. 2023KY914), the Key R&D Program of Zhejiang (No. 2022C03112), the National Key R&D Program of China (No. 2020YFC2008200), the Zhejiang Provincial National Science Foundation of China (No. LQ18H120010), the Zhejiang Health Innovation Talents Program (No. 2016025), the Key Innovation and Guidance Program of the Eye Hospital, School of Ophthalmology & Optometry, Wenzhou Medical University (No. YNZD2201903), and the Wenzhou Municipal Technological Innovation Program of High-level Talents (No. 604090352/577). 10.1631/jzus.B2200485 1673-1581（2023）04-0366-05 徐丽娟,张欣瑶,曹阳等.原发性开角型青光眼黏小管成形术后早期短暂性高眼压的发生率及危险因素分析[J].浙江大学学报（英文版）（B辑：生物医学和生物技术）,2023,24(04):366-370. 徐丽娟,张欣瑶,曹阳等.原发性开角型青光眼黏小管成形术后早期短暂性高眼压的发生率及危险因素分析[J].浙江大学学报（英文版）（B辑：生物医学和生物技术）,2023,24(04):366-370. This work was supported by the National Natural Science Foundation of China (No. 82201177), the Health Commission of Zhejiang Province (No. 2023KY914), the Key R&D Program of Zhejiang (No. 2022C03112), the National Key R&D Program of China (No. 2020YFC2008200), the Zhejiang Provincial National Science Foundation of China (No. LQ18H120010), the Zhejiang Health Innovation Talents Program (No. 2016025), the Key Innovation and Guidance Program of the Eye Hospital, School of Ophthalmology & Optometry, Wenzhou Medical University (No. YNZD2201903), and the Wenzhou Municipal Technological Innovation Program of High-level Talents (No. 604090352/577). 2022-10-06 2022-12-13 2023-04-15 2023-04-14 2023-03-23 Copyright © Zhejiang University and Springer-Verlag GmbH Germany, part of Springer Nature 2022 2023 浙江大学出版社 Lijuan XU, Xinyao ZHANG, Yang CAO, Yin ZHAO, Juan GU, Wenqing YE, Xiaojie WANG, Jinxin LI, Ruiyi REN, and Yuanbo LIANG declare that they have no conflict of interest. This cross-sectional study adhered to the tenets of the Declaration of Helsinki and was approved by the Institutional Review Board of the Eye Hospital of Wenzhou Medical University (KYK[2014] No. 47). Written informed consent was exempted due to the nature of retrospective study. Compliance with ethics guidelines Supplementary information 1 Materials and methods 浙江大学学报（英文版）（B辑：生物医学和生物技术） 4 24