Long-term visual outcomes in children with primary congenital glaucoma
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1 EJO ISSN Eur J Ophthalmol 2017; 27 (6): DOI: /ejo ORIGINAL RESEARCH ARTICLE Long-term visual outcomes in children with primary congenital glaucoma Sanaa A. Yassin Department of Ophthalmology, Imam Abdulrahman Bin Faisal University (Formerly University of Dammam), Al-Khobar - Saudi Arabia Abstract Purpose: To determine the long-term visual outcomes and risk factors for visual loss in children with primary congenital glaucoma (PCG) who underwent angle surgery over a 21-year period. Methods: This was a retrospective study of patients who underwent trabeculotomy, trabeculectomy, or combined trabeculotomy-trabeculectomy for PCG. Visual acuity (VA), surgeries, and underlying cause of visual impairment were recorded and compared. Main outcome measures were final best-corrected good VA (20/20 to 20/50), moderate VA (<20/50 to 20/200), or poor VA (<20/200); age at surgery, sex, laterality, type of initial glaucoma surgery, and number of surgeries were recorded. Results: Fifty-three eyes were eligible to be included in the study. The mean logmar VA was 0.61 ± A good VA was attained in 51%, moderate VA in 30%, and poor VA in 19%. The main cause of visual impairment with VA <20/50 was deprivation amblyopia (64%). There was no association between VA level and status of success (controlled with or without medications) (p = 0.202). The mean spherical equivalent of refraction was ± 5.66; myopia was the predominant refractive error (74%) and astigmatism >2 D (40%). A statistically significant high myopic shift was more frequent in the visually impaired group. None of the studied factors was statistically associated with moderate to poor visual outcome (all p>0.05). Conclusions: A favorable VA outcome was achieved. Topical antiglaucoma medication has an adjuvant role in maintaining the success rate of surgery without risking the visual outcome. Corneal opacification and anisometropia were the cause of amblyopia. Keywords: Amblyopia, Anisometropia, Corneal opacification, Outcome, Primary congenital glaucoma, Visual acuity Introduction Children with primary congenital glaucoma (PCG) are challenged with a lifelong burden (1). Even after a timely surgical intervention to control intraocular pressure (IOP), enduring and frequent checkups are still mandatory to prevent further visual impairment (2, 3). The optimal long-term visual outcome is strongly related to early detection of any concomitant amblyopia or refractive errors for proper intervention (4). Early surgical management of PCG can be successful in approximately 70% to 80% (5-7); however, 17.6%-22.5% of these eyes may end up with profound visual loss (8, 9). Vision-threatening difficulties can be due to optic nerve damage, corneal opacities, cataract, and amblyopia (10, 11). Accepted: March 29, 2017 Published online: April 20, 2017 Corresponding author: Sanaa A. Yassin P.O. Box Al-Khobar, Saudi Arabia syassin@uod.edu.sa Several studies have investigated the possible risk factors associated with poor visual outcome in PCG. Factors that have strong evidence to be associated with poor visual outcome were unilateral disease, multiple surgeries, poor vision at diagnosis, and ocular comorbidities (9). Other factors such as age at initial presentation, sex, and IOP at initial presentation were not proven to have influence on the long-term visual outcome (12). Recently, we have reported the demographic criteria of PCG subjects and evaluated the surgical outcomes of children who underwent angle surgery over a 21-year period (13). The study collected and evaluated data for 148 eyes of 85 patients. The majority of the patients were younger than 6 months. Sex distribution was relatively even between female and male patients. Bilateral disease was seen in 74%. The overall success rate was achieved in 80.4%. There was no statistically significant difference in success rate between types of surgery and number of performed procedures. A progressive decline in success rate over time was evident, as success rate dropped from 96.6% at 5 months to less than 50% success after 11 years of follow-up. Adjuvant topical antiglaucoma medications were needed in 75% of eyes. In the present study, the aim was to determine the longterm visual outcomes and risk factors for visual loss in children
2 706 Visual outcomes in children with PCG with PCG who underwent angle surgery over a 21-year period. In addition, the influence of adjuvant postoperative antiglaucoma medications use on final visual acuity (VA) outcome was evaluated. Methods Permission from the university s institutional review board was obtained to review the medical records of sequential pediatric patients who were diagnosed with PCG and underwent trabeculotomy, trabeculectomy, or combined trabeculotomy-trabeculectomy (CTT) between January 1991 and December 2012 at the University Hospital. Exclusion criteria included all those who had follow-up of less than 3 years, all secondary forms of congenital glaucoma (e.g., Sturge-Weber syndrome), and all cases not qualified for surgical success. The implemented protocol for diagnosis and treatment was described in our previous report (13). In summary, the diagnosis was made on the basis of the clinical criteria. The IOP was measured by applanation tonometer (Perkins tonometer). Once the diagnosis of PCG was established, each patient was started on medical therapy consisting of timolol maleate ophthalmic solution 0.25% BID, with acetazolamide 5-10 mg per kg every 6 hours, as indicated while waiting for surgical clearance for general anesthesia. Our preferred surgical intervention for PCG was trabeculotomy, as most cases had marked corneal edema and haziness precluding visualization of the iridocorneal angle structure. Trabeculectomy or CTT was performed in cases of failure to identify Schlemm canal, eyes with corneal diameter exceeding 14 mm, severe cases with scarred cornea, and children older than 3 years. A minimum of 3 years follow-up after surgery was necessary for the patient to be included in this study. Children were examined regularly in the clinic every 3 months or closer as needed. Any development of amblyopia was treated with glasses and patching. Surgical success was defined as 1) stable or improved optic disc appearance, 2) lack of further corneal enlargement disproportionate to normal growth, and 3) average IOP of 21 mm Hg or less with or without topical medication. Data of the following parameters were collected from the patient medical records: sex, age at presentation, number and type of operations, the status of IOP control (controlled with medication or without medication), follow-up period, best-corrected VA (BCVA), cycloplegic refraction, corneal diameter, corneal transparency, IOP at presentation, IOP at latest follow-up, cup-to-disc ratio, and any associated ocular comorbidities at latest follow-up. For those patients with impaired final VA (<20/50), the primary etiology for the poor vision was determined. Although the cause of impaired VA can be attributed to several factors, the most prominent underlying factor was determined in each case depending on history and physical findings. Age-appropriate VA tests were employed, with the simplest being quality of fixation for nonverbal children. For older children, Lea Symbols test and Snellen acuity chart (starting at about 4 years) were used. Final BCVA scores were stratified into 3 visual outcome groups: good VA (20/20 to 20/50), moderate VA (<20/50 to 20/200), and poor VA (<20/200). For statistical analyses, VA was evaluated using the logmar value. Spherical equivalent of refraction (SER) was used to analyze the refractive errors. Spherical equivalent was calculated by adding half the cylindrical value to the spherical value of the refractive error. Subjects were considered hyperopic if SER D and myopic if SER D. Statistical analyses All categorical variables were represented by frequency with percentage and were analyzed using chi-square and Fisher exact test. Continuous data were presented by mean with SD. Independent t test was used to examine the risk factors (sex, age at diagnosis, laterality of glaucoma, SER, type of glaucoma surgery, status of surgical success, number of surgeries, and years of follow-up after diagnosis) for visual impairment (final VA <20/50). All the analyses were performed using SPSS A p value <0.05 was considered significant. Results Fifty-three eyes (34 patients) were eligible to be included in the study. The demographic data (age at diagnosis, sex, bilaterality of the disease, and follow-up duration) are presented in Table I. The median age at diagnosis was 2 months (range 0-36 months). Sex distribution was equal between female and male patients. Bilateral disease was seen in 81%. Mean follow-up period was 8.2 ± 5.48 years (range 3-20 years). Primary surgical intervention was CTT for 26 eyes (49%), trabeculotomy for 19 eyes (36%), and trabeculectomy for 8 eyes (15%). Only 9 eyes needed a second surgery, as shown in Table I. All 53 eyes were qualified for success whether controlled with or without antiglaucoma medications. Table II TABLE I - Patient demographics and types of surgical intervention of 34 patients (53 eyes) with primary congenital glaucoma Demographics Values Age at presentation, mo, median (range) 2 (0-36) Sex, n (%) Male 17 (50) Female 17 (50) Laterality of the disease, n (%) Bilateral 43 (81) Unilateral 10 (19) Follow-up, y, median (range) 6 (3-20) Type of surgical intervention, n (%) Initial surgery Combined trabeculotomy-trabeculectomy 26 (49) Trabeculotomy 19 (36) Trabeculectomy 8 (15) Second surgery None 44 (83) Trabeculectomy 8 (15) Combined trabeculotomy-trabeculectomy 1 (2) Surgeries per eye, mean ± SD; median 1.17 ± 0.38; 1
3 Yassin 707 demonstrates the distribution of eyes controlled with or without medications in relation to number of required surgeries. There were 31 eyes (58%) requiring topical antiglaucoma medication. The mean IOP at presentation was ± 7.99 mm Hg (range mm Hg). At final follow-up visit, the mean IOP was ± 4.28 mm Hg (range 8-21 mm Hg), as shown in Table III. The percentage of IOP reduction was 42.9% (p< , paired t test). The VA outcomes at last examination are shown in Table III. The mean logmar VA was 0.61 ± 0.57 (Snellen equivalent, 20/80). A good VA was achieved in 27 eyes (51%), while 16 eyes (30%) had moderate VA, and 10 eyes (19%) poor VA. Causes of visual impairment with VA <20/50 were deprivation amblyopia due to corneal opacification (64%), anisometropic amblyopia (20%), optic neuropathy (12%), and refractive amblyopia (4%). Table III shows that associated ocular comorbidities were corneal opacification (49%), anisometropia (15%), optic neuropathy (13%), and refractive amblyopia (6%), There was no statistically significant correlation between visual acuity categories and any status of control (with or without medications) (p = 0.202), as shown in Table IV. In univariate analysis, the age at surgery, sex, laterality, type of initial glaucoma surgery, number of surgeries, and type of control were not statistically associated with vision impairment, as exhibited in Table V. Refractive error ranged from to D. The mean SER was ± Myopia was the predominant refractive error, occurring in 39 eyes (74%), and astigmatism >2 D in 21 (40%), as presented in Table III. The mean SER in 22 eyes controlled without medication was ± 5.10; the mean SER in 31 eyes controlled with medication was ± There was no statistically significant correlation between SER and the status of control (with or without medications) (p = 0.212). The distribution of SER at latest visit is presented in an error bar with 95% confidence interval in Figure 1. It shows significant myopic shift among the visual impairment group compared to the good VA group (p = 0.001). Discussion The main goal of this study was to determine the visual outcome of eyes that received successful surgical treatment for PCG. Generally, it is challenging to follow the progression of visual function in infancy. Visual acuity prognosis was not addressed in several studies that evaluated the surgical outcomes of congenital glaucoma (6). However, several other TABLE II - Distribution of eyes controlled with or without medications in relation to number of required surgeries No. of surgeries Controlled, n (%) Without medication With medication 1 21 (40) 23 (43) 2 1 (2) 8 (15) Total 22 (42) 31 (58) TABLE III - Clinical criteria of eyes with primary congenital glaucoma at last clinical evaluation Clinical findings Final clinical assessment Corneal diameter at last visit, mm Mean ± SD 12.9 ± 1.1 Range Intraocular pressure at last visit, mm Hg Mean ± SD ± 4.28 Range 8-21 Cup-to-disc ratio at last visit, mean ± SD 0.5 ± 0.49 BCVA, logmar, mean ± SD (Snellen equivalent) 0.61 ± 0.57(20/80) WHO VA classification, n (%) Good ( ) 27 (51) Moderate (< ) 16 (30) Poor (<0.1) 10 (19) Cause of visual impairment (VA <0.3) (25 eyes), n (%) Deprivation amblyopia 16 (64) (corneal opacification) Anisometropic amblyopia 5 (20) Optic neuropathy 3 (12) Refractive amblyopia 1 (4) Refraction Astigmatism >2 D, n (%) 21 (40) Spherical equivalent, mean ± SD ± 5.66 High myopia ( -6 D), n (%) 19 (36) Mild to moderate myopia 20 (38) (-1.00 to -5.75), n (%) Emmetropia (-0.75 to +0.75), n (%) 6 (11) Mild to moderate hypermetropia 6 (11) (+1.00 to +5.75), n (%) High hypermetropia ( +6 D), n (%) 2 (4) Ocular comorbidity, n (%) Corneal opacification 26 (49) Anisometropia 8 (15) Optic neuropathy 7 (13) Refractive amblyopia 3 (6) BCVA = best-corrected visual acuity; VA = visual acuity. TABLE IV - Correlation of visual acuity category to status of control (with or without medications) Visual acuity Controlled, n (%) p value category Without medication With medication Good ( ) 14 (63.6) 13 (41.9) Moderate 6 (27.3) 10 (32.3) (< ) Poor (<0.1) 2 (9.1) 8 (25.8)
4 708 Visual outcomes in children with PCG TABLE V - Effect of age at surgery, sex, laterality, type of initial glaucoma surgery, number of surgeries, and type of control on moderate to poor visual outcome Factors Total (n = 53) No. (%) of eyes with moderate or poor VA p value Age, mo < (47.5) > (53.8) Sex Male (50) Female (48.3) Laterality Bilateral (48.8) Unilateral 10 5 (50.0) First type of surgery Trabeculectomy 8 5 (62.5) Trabeculotomy (57.8) Combined trabeculotomy (38.5) trabeculectomy No. of surgeries (45.4) (66.7) Control Without medication 22 8 (36.4) With medication (58.1) VA = visual acuity. studies on postoperative PCG outcomes reported variable VA outcome (5, 9, 14-16). A normal to near-normal VA (20/20 to 20/50) was achieved in 41% 79% of eyes, as summarized in Table VI (5, 9, 14, 16-26). Studies that compared the VA prognosis in various subtypes of childhood glaucoma found that PCG carries the best VA prognosis (9, 21). In the current study, VA outcomes were favorable as 51% of eyes achieved a good VA and 30% had moderate VA. The variability in visual outcome among different studies can be attributed to differences in patients demographic criteria (age at onset, numbers, and sex), study designs and selection criteria, and follow-up period. A progressive decline in success rate over time was described in various studies (6, 13, 22, 23). In this study, the comparison between eyes that needed antiglaucoma medications postoperatively and eyes that were controlled without medication revealed no statistically significant difference regarding final visual outcome. These results support the role of topical antiglaucoma medication in the management of postoperative PCG without risking visual outcome. In addition, the postoperative reductions in IOP were comparable to those described in the literature (2, 3, 14, 17). The most common ocular comorbidity was corneal opacification (49%), followed by anisometropia (15%). Similarly, the most common cause of VA impairment was deprivation amblyopia secondary to corneal opacification (64%), while anisometropic amblyopia accounted for 20%. Our results are contrary to the findings by Kargi et al (21) that revealed anisometropic amblyopia to be more frequent than deprivation amblyopia in PCG cases. This dissimilarity between the 2 studies (current and Kargi et al) could be attributed to differences in the age at onset and severity of the disease. Former studies have shown that presence of media opacities during early life (<3 months) leads to profound and longlasting VA impairment (27, 28). In a case series from Saudi Arabia, corneal haze was found to be more pronounced in younger patients with PCG (29). Moreover, in a large Saudi series of PCG cases, corneal opacities were observed in 582 of 820 eyes (71%) (30). The high frequency of corneal scarring in the Saudi population with PCG may indicate a more severe disease than that seen in Western countries (30). The high frequency of anisometropic amblyopia in PCG can be explained by asymmetric disease between the 2 eyes. Thus, amblyopia, irrespective of its subtypes, remains the major cause for VA impairment in well-controlled postoperative PCG cases, as demonstrated in this study and supported by previous studies (9, 10, 17, 21, 24). Another objective of the current study was to identify clinically relevant risk factors that were associated with poor visual outcome. In univariate analysis, none of the studied factors (age at surgery, sex, laterality, type of initial glaucoma surgery, number of surgeries, or type of control) were statistically associated with moderate to poor visual outcome (all p>0.05), as shown in Table V. Khitri et al (9) evaluated risk factors for visual loss in the various subtypes of pediatric glaucoma. They identified unilateral disease, multiple surgeries, poor vision at diagnosis, and other ocular comorbidities to be associated with visual impairment in pediatric glaucoma. Furthermore, the multivariate analysis showed that PCG and Sturge-Weber glaucoma had a less likely risk of visual impairment than those with other glaucoma diagnosis (p = 0.01). However, when looking specifically at PCG alone, only eyes that required more surgeries were more likely to be associated with poor visual outcomes, while sex, age at diagnosis, age at surgery, type of surgery, and years of follow-up did not appear to affect final visual prognosis (9). Myopia and astigmatism are a frequent finding in patients with PCG (5, 6, 8, 16, 22). The prevalence of myopia in this study was 74% and the mean spherical equivalent was D, with the maximum myopic refractive error being D. Early onset of the disease during the first 3 years of life enhances the increase in corneal diameter and the axial elongation of the globe due to the elasticity of the infant eye (16). It has been reported that the enlarged eye causes an anterior displacement of the lens-iris diaphragm, moving the effective focal point forward and inducing both high myopia and high astigmatism (27). Myopia of 3 D or more has been described in almost two-thirds of the eyes of children with PCG (10). Similar results were reported by Mandal et al (22) with a myopic change in (73.8%) of eyes and a mean SER D. Some studies suggested a relation between higher incidence of myopia and the type of surgical intervention (14, 17, 31). Mendicino et al (17) found a higher level of myopia in the goniotomy group compared to the trabeculotomy group. Others have reported myopia to be more frequent after CTT (14, 31). Astigmatism >2 D was seen in 40% of eyes in this series. Corneal irregularities due
5 Yassin 709 TABLE VI - Recent studies with long-term visual outcome of patients with PCG Authors Reference No. of eyes Follow-up, y Surgical intervention BCVA, % Good (20/20-20/50) Fair ( 20/50-20/200) Poor (<20/200) Mendicino et al (2000) (17) trabeculotomy; goniotomy Filous and Brunová (2002) (18) Trabeculotomy 64 a 29.5 b 6.4 b Autrata and Lokaj (2003) (19) Trabeculectomy Trabeculotomy MacKinnon et al (2004) (16) 55 Mixture Ikeda et al (2004) (20) Trabeculotomy Kargi et al (2006) (21) Alsheikheh et al (2007) (5) 68 c Mixture Mandal et al (2007) (22) Mixture Zhang et al (2009) (14) Mixture de Silva et al (2011) (23) Mixture 47.0 d Khitri et al (2012) (9) 49 5 Mixture Saltzmann et al (2012) (24) 19 7 Pseudo trabeculotomy Fung et al (2013) (25) 81 Mixture 41.0% Zagora et al (2015) (26) Mixture a BCVA >20/40. b The percentage included eyes with uncontrolled intraocular pressure. c The study included eyes with secondary congenital glaucoma. d BCVA >20/60. BCVA = best-corrected visual acuity; PCG = primary congenital glaucoma. There are several limitations to the current study, including the retrospective design, the difficulty in measuring VA in very young nonverbal children, the variability in operative and postoperative course, and patient compliance with medication and follow-up. In conclusion, this study highlights long-term visual outcomes of PCG at a university teaching hospital in Saudi Arabia. A favorable VA outcome was achieved. The study also underlines the role of topical antiglaucoma medication in improving the success rate of surgery remarkably without risking visual outcome. Corneal opacification and anisometropia were the main causes of amblyopia, which is a major obstacle in the management of PCG. Successful management of PCG can be achieved by a combination of timely surgical intervention, effective refractive error correction, and amblyopia rehabilitation. Fig. 1 - Distribution of spherical equivalent of refraction at latest visit between good visual acuity and visual impairment groups. to unequal expansion of the anterior segment, corneal scarring, and opacification were considered the main cause of astigmatism (27). Hypermetropia frequency of (15%) as seen in the current study is generally less than the reported occurrence of 22.9%-33.3% (2, 32, 33). Acknowledgments The author thanks the Imam Abdulrahman Bin Faisal University for support, Dr. Elham Al-Tamimi for her valuable contribution, and Dr. Munerah Al-Subaei and Nada Ali for their help with data collection. Disclosures Financial support: No financial support was received for this submission. Conflict of interest: None of the authors has conflict of interest with this submission.
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