Comparison of phaco time parameters in eyes with and without glaucoma filtration surgery due to pseudoexfoliation glaucoma

Abstract

Purpose:

To compare the phaco time parameters including ultrasound time (UST), effective phaco time (EPT), and average phaco power (APP) in eyes with pseudoexfoliation glaucoma (PEG) and had or had not glaucoma filtration surgery.

Methods:

In this retrospective comparative study, Group 1 was constructed with 84 PEG patients who had not operated previously, and Group 2 was constructed with 49 PEG patients who had glaucoma filtration surgery. The mean values of UST, EPT, and APP were compared. The preoperative clinical characteristics and surgical manipulations were also compared.

Results:

The mean ages and male-to-female ratios of the groups were similar (p > 0.05, for both). There was no difference in the preoperative clinical characteristics, including biometric values between the groups (p > 0.05, for all). Some surgical manipulations, including pupillary stretching (p = 0.004), pupillary membrane peeling (p = 0.021), iris hook using (p = 0.041), and capsular tension ring implantation (p = 0.041), were significantly performed more commonly in Group 2. Although the mean UST and EPT values were similar (p > 0.05, for both), the mean APP value was significantly lower in Group 2 (p = 0.011).

Conclusion:

The lower APP parameter was observed in PEG patients having had glaucoma filtration surgery. Needing more surgical manipulation to overcome poor pupillary dilation and weak zonular instability can be a reason for this result.

Keywords

Cataract filtration surgery glaucoma phacoemulsification pseudoexfoliation

Pseudoexfoliation syndrome (PES) is a chronic age-related ocular disease that has been proposed as a kind of elastosis. It is characterized by the accumulation of pseudoexfoliation material which is composed of the amyloid-beta peptide, laminin, collagen, fibrillin, elastin, and other elastic fibers at the various part of the eye, such as pupillary margin, anterior lens capsule, along with the insertions of the zonules in the ciliary body, anterior chamber angle due to degeneration and localized autolysis of the epithelium on the various tissues of the anterior segment.^1–4 Beside excessive production of elastic microfibril components, enzymatic cross-linking, transforming growth factor-1 (TGF-1) overexpression, a proteolytic imbalance between matrix metalloproteinases (MMPs) and tissue inhibitor of metalloproteinases (TIMPs), low-grade inflammatory processes, increased cellular and oxidative stress, and defective cellular stress response associated with the downregulation of antioxidative enzymes, ubiquitin-conjugating enzymes, clustering, and DNA repair proteins, are play role in PES pathogenesis.⁵

The most important cause of elevated intraocular pressure (IOP) in PES is aqueous outflow blockage due to PES material accumulation in the intertrabecular spaces, juxtacanalicular meshwork, and beneath the endothelium of Schlemm’s canal.⁵ Decreased phospholipid metabolism, disrupted membrane homeostasis, cellular dysfunction, and increased aqueous protein concentrations also contribute to the pathological process.^5,6 Defected structural stability and flexibility, and reduced oxidative stress protection in trabecular meshwork cells lead to progress pseudoexfoliation glaucoma (PEG).

In the anterior chamber of eyes with PES, levels of antioxidants including glutathione and ascorbic acid decrease, and oxidative stress markers including malondialdehyde and 8-isoprostaglandin-F2a increase.^7,8 Oxidative stress is also a prominent risk factor for the development and the progression of cataract which is another common finding associated with PES.^7,8 Structural abnormalities associated with PES increase the intraoperative or postoperative complications of cataract surgery, such as difficulty in capsulorhexis due to poor pupillary dilation, lens dislocation caused by the preexisting zonular weakness, and vitreous loss due to posterior capsular rupture.^1–3 Cataract surgery in eyes having had glaucoma filtration surgery previously associated with PEG is considered even more challenging than eyes with PES not having undergone any surgery previously. Because additional special attention should be paid during surgical manipulations to minimizing intraoperative trauma on the filtration bleb side to prevent bleb-related complications. Besides, fine-tuning can be necessary for the phacoemulsification parameters for each surgery to prevent cataract surgery-related intraoperative and postoperative complications.

WhiteStar Signature Pro surgical system (Abbott Medical Optics Inc., Santa Ana, CA) on longitudinal mode gives some details about phaco time parameters. Ultrasound time (UST) is the total length of time given ultrasonic power during the phacoemulsification surgery, effective phaco time (EPT) indicates the amount of phaco energy delivered into the eye at 100% power, and average phaco power (APP) that is another parameter calculated by the [(EPT/UST) × 100] formula. This study aimed to compare the phaco time parameters during cataract surgery in eyes with PEG which had or had not glaucoma filtration surgery operation previously. For this purpose, the difference in phacoemulsification parameters, including UST, EPT, and APP, were evaluated. Also, the possible reasons for the difference in the results were simultaneously investigated.

Methods

This retrospective comparative study was conducted in a single tertiary referral center. All procedures were performed under the tenets of the Declaration of Helsinki for human subjects. The study protocol was reviewed and approved by the Local Medical Research Ethics Committee (E-18-2055). Written informed consent was obtained from each patient before the invasive procedures.

The medical records of the patients diagnosed with PEG who underwent phacoemulsification and intraocular lens implantation surgery were investigated. Patients ⩾18 years old who had grade 3 or grade 4 nuclear sclerotic cataract according to the lens opacities classification system III⁹ and PEG were included in the study. Patients were excluded who had a history or clinical signs for cataract-related ocular diseases except for PES (e.g. uveitis), angle-closure glaucoma, secondary reasons for glaucoma except for PES (e.g. pigment dispersion syndrome, uveitis), congenital lens abnormalities, ocular media opacity (e.g. hyphema, vitreous hemorrhage), ocular trauma, intraocular surgery except for glaucoma filtration surgery (e.g. laser treatments, pars plana vitrectomy, intravitreal pharmacotherapy), topical or systemic corticosteroid use, or cataract-related systemic diseases (e.g. atopic dermatitis, neurofibromatosis, Down syndrome, myotonic dystrophy). Group 1 was constructed with 84 eyes of 84 patients with PEG and cataract. Group 2 was constructed with 49 eyes of 49 patients with PEG, cataract, and a history of glaucoma filtration surgery.

After obtaining medical history, all patients underwent a complete ophthalmological examination, including corrected visual acuity with a Snellen chart, IOP with Goldmann applanation tonometry, slit-lamp biomicroscopy for the anterior and posterior segment. Macular thickness and configuration were evaluated using spectral-domain optical coherence tomography (Spectralis; Heidelberg, Germany). Intraocular lens power, anterior chamber depth, axial length, and central corneal thickness were measured using optical biometry (LenStar LS 900; Haag Streit Diagnostics, Köniz, Switzerland) preoperatively.

The PEG patients were diagnosed according to the presence of PES and glaucomatous defects according to the European Glaucoma Society Guidelines.¹⁰ BesidesIOP and central corneal thickness measurement, anterior chamber angle was examined using a Goldmannthree-mirror lens. Optic disc assessment was done with slit-lamp examination and a +90-diopter lens, and glaucomatous optic disc damages were noted. Automated visual field analysis (Humphrey Field Analyzer; Carl Zeiss Meditech, Inc., Dublin, CA, USA) was performed using the Swedish standard interactive threshold algorithm 24-2and glaucomatous visual field defects were recorded with high reliability indexed results (⩽15% false positive and false negative responses and ⩽3 fixation losses). Peripapillary nerve fiber layer thickness evaluations (Spectralis; Heidelberg, Germany) had been performed and progressive thinning in the nerve fiber layer was investigated using only ⩾20 quality scored images.

For phacoemulsification and intraocular lens implantation surgeries, superotemporal or superonasal main incisions were preferred on the right and left eye, respectively, for Group 1. Temporal or superotemporal clear corneal main incisions were preferred for Group 2 because all glaucoma filtration surgery blebs were located superiorly and with limbus-based conjunctival flap. Pupillary stretching and/or iris retractor hook using were performed to achieve a minimum of 5.5 mm pupillary dilation in patients with poor pupillary dilatation. Synechiotomy or pupillary membrane peeling was performed for some eyes in Group 2 due to previous glaucoma filtration surgery-related fibrosis or adhesion. The anterior capsule was stained with trypan blue for some eyes with mature cataract. Same WhiteStar Signature Pro surgical system on longitudinal mode and the same divide and conqueror nucleo-fractis technique were used. A capsular tension ring was implanted for some eyes having serious zonular instability. A foldable hydrophilic acrylic intraocular lens (IOL) (Acrysof IQ monofocalIOL; Alcon Laboratories Inc., Forth Worth, TX) was inserted into the capsular bag. In the case of posterior capsular rupture, IOL was implanted into the ciliary sulcus (Tecnisthree-piece aspheric monofocal IOL; Abbott Medical Optics Inc., Santa Ana, CA) or anterior chamber (PMS 603; Freedom Medicare, Le Relecq-Kerhuon, France) after anterior vitrectomy. Corneal incisions were sutured in some eyes to prevent postoperative leaking. All surgeries were performed by the same experienced surgeon (AKA). The phacoemulsification parameters, including UST, EPT, and APP, were taken from the phacoemulsification system at the end of the surgery and recorded for each patient as a routine procedure. The postoperative treatment regimen was the same for all cataract surgeries which includes topical moxifloxacin (Vigamox; Alcon, Fort Worth, TX) 4 × 1 for two weeks and topical 0.1% dexamethasone (Maxidex; Alcon, Fort Worth, TX) 5 × 1 for four weeks.

The study data were analyzed using the Statistical Package for the Social Sciences (SPSS) 23.0 software (IBM Corp., NY, USA). Descriptive statistics were presented as mean ± standard deviations (minimum-maximum values). The Kolmogorov–Smirnov test was used to test the normal distribution of the variables. The Mann–Whitney U test was used in comparisons of the groups as the numerical data did not fit to a normal distribution; p < 0.05 was determined as statistical significance level for all two-tailed tests.

Results

The mean age of the subjects was 71.2±8.4 years (51–89) in Group 1 and 70.0 ± 11.3 years (34–85) in Group 2. There was no significant difference in demographic characteristics including the mean age and male-to-female ratio of the groups (p > 0.05, for both). There was also no significant difference in the mean values of preoperative IOP[16.1 ± 4.2 mmHg (8–25)in Group 1 and 13.9 ± 5.1 mmHg (8–24) in Group 2], central corneal thickness [546.2 ± 38.1 µm (462–632) in Group 1 and 536.8 ± 41.3 µm (455–629) in Group 2], and anterior chamber depth [3.0 ± 0.5 mm (2.0–4.2) in Group 1 and 2.9 ± 0.5 mm (1.6–3.6) in Group 2] of the groups (p > 0.05, for all). The rates for the number of the patients using topical anti-glaucomatous medication were 80/84 in Group 1 and 22/49 in Group 2 (p < 0.001).

Some surgical manipulations, including pupillary stretching [eight patients in Group 1 (9.5%) and 14 patients in Group 2 (28.5%)] (p = 0.004), pupillary membrane peeling [no patient in Group 1 (0%) and one patient in Group 2 (2.0%)] (p = 0.021), iris hook using [one patient in Group 1 (1.1%) and four patients in Group 2 (8.1%)] (p = 0.041), and capsular tension ring implantation [one patient in Group 1 (1.1%) and four patients in Group 2 (8.1%)] (p = 0.041), were significantly performed more commonly in Group 2. There was no significant difference in terms of other surgical manipulations, including sinechiotomy, capsular staining, and corneal suturing (p > 0.05, for all). Three patients in Group 1 (2.3%) and two patients in Group 2 (4.0%) had posterior capsule rupture and a limited amount of vitreous loss without nucleus or lens fragment dropped into the vitreous (p > 0.05). The rates of the sulcus or anterior chamber IOL implantation were similar (p > 0.05, for both). Any other intraoperative complications, including bleb perforation, bleb leakage, corneal burn, Descemet’s membrane rupture, or choroidal detachment, did not occur in any patient.

The mean UST was 116.1 ± 71.1 s (4.1–356.6) in Group 1 and 132.2 ± 76.7s (15.4–357.5) in Group 2. The mean EPT was 16.5 ± 11.1 s (1.4–49.9) in Group 1 and 17.9 ± 13.4 s (2.3–49.0) in Group 2. The mean APP was 15.8 ± 5.3% (8–34) in Group 1 and 12.6 ± 4.2% (7–22) in Group 2. Although both mean UST and EPT were higher in Group 2, the differences were not statistically significant (p > 0.05, for both). On the other hand, the APP was significantly lower in Group 2 (p = 0.011). The demonstration of the phacoemulsification parameters is given in Figure 1.

Discussion

Increased IOP has been observed in 28.8% of patients with PES as opposed to5.4% of patients without PES.¹¹ Ringvold¹² reported that glaucoma is occurred in 30% of eyes with PES, in contrast to 4% of those without PES. Andrikopoulos et al.¹³ found that glaucoma prevalence could be increased up to 8.5-fold in patients with PES. Many eyes with PEG need glaucoma filtration surgery to decrease IOP and risk of peripapillary retinal nerve fiber layer defect. Other than glaucoma, Kanthan et al.³ found a significant association between the increased incidence of cataract and the presence of PES. Phacoemulsification surgery is a more challenging situation for those eyes due to probable higher intraoperative complications. Poor pupillary dilatation, weak zonules, and harder nucleus make this surgery riskier.^2,3,13,14 Eyes with PEG having had glaucoma filtration surgery are even more disadvantageous because of preexisting filtration bleb localization and functioning, degenerated pupillary margin-anterior lens capsule relationship, and additional zonular instability. Special attention is needed during surgical manipulation for these patients. Some surgical manipulations, including stretching, pupillary membrane peeling, and iris hook using, which are related to poor pupillary dilation, and capsular tension ring using, which is related to weak zonulas, were significantly performed more commonly in this study for PEG patients having had glaucoma filtration surgery. Otherwise, there was no difference in complication rate and this result is consistent with the literature knowledge.

WhiteStar Signature Pro phacoemulsification system gives some opportunity to measure the duration of given ultrasonic power. Higher EPT values are generally considered as related to lower corneal endothelial cell loss, lesser corneal decompensation, and higher patient satisfaction.¹⁵ According to the results of this study, UST and EPT values were higher in PEG patients having had glaucoma filtration surgery; however, the differences were not statistically significant. On the other hand, APP was significantly lower in PEG patients having had glaucoma filtration surgery. The conditions that increase EPT or decrease UST or absolute phaco time decrease APP value. So, this result can be considered to be consistent with higher EPT results found for these patients. Several surgical manipulations and phacoemulsification techniques have been developed to increase the success rate, especially for complicated cases. Surgical parameters can be changed by the phaco machine, phaco mode, nucloefracture techniques, nuclear hardness, anatomic factors, and other comorbidities such as PES and preexisting surgeries.^14,16–19 To the best of our knowledge, no report in the literature compares the phacoemulsification parameters in eyes with PEG, having had glaucoma filtration surgery or not. Therefore, comparing the results of this study with previous studies is not possible.

According to the outcomes of this study, lower APP values and higher, both UST and EPT values (despite some variables not being statistically significant) in phacoemulsification surgery of PEG patients having had glaucoma filtration surgery can be considered as in favor of lesser phaco power, lesser absolute phaco time, longer total phaco time, combined with more surgical manipulation, longer surgical time, and greater surgical safety. Some of these considerations were evaluated in this study, such as surgical manipulations, and it was shown that PEG patients having had glaucoma filtration surgery needed more surgical manipulations. These results can be interpreted in two ways: (1) Even though APP, UST, and EPT results seem to be worse in PEG patients having had glaucoma filtration surgery, these alterations are understandable and acceptable for these challenging cases because this study shows that PEG patients having had glaucoma filtration surgery needed more surgical manipulations. Thus, these slightly altered results are considered to be normal by the nature of these challenging cases. Additionally, many studies reported that the EPT is related to the surgical properties of the cases, especially the nuclear hardness of cataract, and longer EPT results were recorded for harder cataracts.^19,20 (2) To make up for the different results in APP, UST, and EPT in PEG patients having had glaucoma filtration surgery novel techniques, methods, equipment, and more experience are needed. This interpretation is supported by the previous studies which reported different results in the surgical parameters using different techniques. Wong et al.²¹ found that EPT was 50.4 s with the divide and conquer technique compared to 17.4 s with the phaco chop technique. Similarly, Pierazzoli et al.²² reported 87.26 s for EPT with the divide and conquer technique compared to 25.53 s with the phaco chop technique. In the light of these studies, surgical parameters can be changed using different techniques. On the other hand, Elnaby et al.²³ reported the mean EPT was 24.44 s by divide and conquer technique and this value was much closer to the values given in this study for the same technique.

Küchle et al.²⁴ evaluated the ocular anatomic parameters and surgical complications during phacoemulsification surgery in eyes with PES. They found that the anterior chamber depth was 2.36 versus 2.74 mm in eyes had or had no intraoperative complication, and reported that an anterior chamber depth of less than 2.5 mm increased the risk of surgical complications.²⁴ On the other hand, they did not evaluate the eyes having trabeculectomy in their series.²⁴ In the present study, the mean anterior chamber depth value was 2.9 versus 3.0 mm in the PEG patients with and without glaucoma filtration surgery, respectively. Both of these mean values were higher than 2.5 mm and no intraoperative nucleus-, cornea-, or bleb-related complications were observed. The deeper anterior chamber values of the eyes in this series may be advantageous to the high surgical success rate of the present study. Besides, the relationship between the surgical parameters and the anatomic structure could not be evaluated.

Shingleton et al.²⁵ reported that vitreous loss was observed in 4% in the eyes with PES while 0% in patients without PES. Drolsum et al.²⁶ reported that capsular rupture, vitreous loss, and zonular dehiscence were observed in 9.6% of eyes with PES. On the other hand, different series reported that no significant difference was observed regarding complication rate between eyes with and without PES.^27,28 In this study, all procedures were performed by the same experienced surgeon. Special attention was paid to every step and some auxiliary techniques, such as pupillary stretching, sinechiotomy, pupillary membrane peeling, capsular staining, anterior vitrectomy, and corneal suturing, and equipment such as iris hook and capsular tension ring, were used. Thanks to these auxiliary techniques and equipment, the intraoperative complication rates were very low for the presenting study.

The main limitations of this study are being a retrospective and single-center study. The lack of vacuum and balanced salt solution consumption standardization, and no investigation of the hardness of cataracts, anterior chamber depth fluctuation, and phaco power are other important limitations. Additionally, for the same patient groups, further studies with long follow-up time investigating the relationship between phaco time parameters and clinical findings including anterior chamber inflammation or changes in corneal endothelial parameters will provide important information.

As far as we know, the present study is the first that evaluates some phacoemulsification parameters, including UST, EPT, and APP, in PEG patients having had glaucoma filtration surgery. The lower APP parameter observed in PEG patients having had glaucoma filtration surgery is found to be consistent with needing more surgical manipulation to overcome poor pupillary dilation and weak zonular instability.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

ORCID iD

Cagri Ilhan

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