- Email: [email protected]
Factors Affecting Visual Acuity after Cataract Surgery in Patients with Retinitis Pigmentosa
Factors Affecting Visual Acuity after Cataract Surgery in Patients with Retinitis Pigmentosa Noriko Yoshida, MD, PhD,1 Yasuhiro Ikeda, MD, PhD,1 Yusuke Murakami, MD, PhD,1 Shunji Nakatake, MD,1 Kota Fujiwara, MD,2 Shoji Notomi, MD, PhD,1 Toshio Hisatomi, MD, PhD,1 Tatsuro Ishibashi, MD, PhD1 Purpose: To investigate the factors affecting visual acuity after cataract surgery in patients with retinitis pigmentosa (RP). Design: Retrospective, observational study. Participants: We retrospectively reviewed the charts of a consecutive series of 40 patients with RP who underwent cataract surgery. Methods: The changes in preoperative and postoperative best-corrected visual acuity (BCVA) were measured. We investigated the relation between preoperative mean deviation (MD) value on the Humphrey Field Analyzer (HFA: the central 10-2 program; Humphrey Instruments, Inc, San Leandro, CA) and final BCVA. We also investigated the relationship between preoperative ellipsoid zone (EZ; also called the inner/outer segment junction) conditions and final BCVA. In addition, we showed the prevalence of macular complications and capsule complications. Main Outcome Measures: The BCVA, slit-lamp biomicroscopic analysis, visual field, and optical coherence tomography (OCT) were obtained. Results: The mean of the BCVA significantly improved after cataract surgery from 0.76 (range, 0.08 to 2.30) to 0.45 (range, 0.18 to 2.00) (P < 0.005). However, final BCVA did not improve in 30 eyes (53.6%). The preoperative MD value and the final BCVA were significantly correlated, and the final BCVA significantly improved in the less advanced RP group (MD was 15 decibels [dB]). The final BCVA was significantly better in the group in which preoperative OCT showed a normal EZ than in the groups in which the EZ was abnormal or not visible. Posterior capsular opacification was observed in 47 eyes (83.9%), and 23 eyes (41.1%) underwent YAG laser capsulotomy within a mean follow-up time of 3 years. Conclusions: Final BCVA in approximately half of the eyes improved after cataract surgery in patients with RP. The preoperative ophthalmic examinations that may reflect macular (or foveal) function, such as HFA 10-2 program and OCT, are important parameters to assess postoperative visual outcome. Ophthalmology 2015;:1e6 ª 2015 by the American Academy of Ophthalmology.
Retinitis pigmentosa (RP) is an inherited retinal degenerative disease that affects photoreceptor and retinal pigment epithelial function and is a major cause of blindness in adults.1,2 In addition to retinal manifestations, such as equatorial bone spicule pigment figures and attenuated retinal vessels along with rod-cone degeneration, cataracts are among the most common eye complications of all hereditary forms of RP.3 As a specific clinical feature of cataract in patients with RP, previous studies have reported that lens opacities develop at a relatively young age.4e6 It has been reported that the mean age at surgery in patients with RP is 47 to 58 years and that in those with age-related cataracts is 72 to 74 years.5e7 It has also been reported that posterior subcapsular cataract (PSC) is the most common morphologic category in patients with RP.5,6,8,9 Fishman et al7 demonstrated a 41% (with autosomal dominant form) to 90% (with X linked recessive disease) probability of PSC by age 40 years, whereas the probabilities reach more than 80% by age 60 years for many genetic types of RP. This PSC may
2015 by the American Academy of Ophthalmology Published by Elsevier Inc.
not only cause severe visual dysfunction but also exacerbate glare symptoms, especially among workingage people. It is suggested that cataract surgery may help this patient group gain visual acuity.10 However, several factors that may result in a poor visual outcome after cataract surgery in patients with RP have been reported.5,6 These factors include posterior capsular opacification (PCO), anterior capsular contraction, zonular weakness, outer retinal atrophy, macular edema, and phototoxic retinal damage. Despite the potentially poor result in visual acuity, cataract surgery is necessary for patients with RP. To provide better data on these eye complications and their effect on outcome, and the potential risks and benefits of surgery, we need further knowledge about the outcome of surgery.5 In this study, we performed a retrospective observational clinical study with patients with RP who underwent cataract surgery. We investigated the clinical course of cataract surgery and evaluated the factors affecting postoperative visual acuity in patients with RP.
http://dx.doi.org/10.1016/j.ophtha.2014.12.003 ISSN 0161-6420/15
1
Ophthalmology Volume -, Number -, Month 2015
Methods This retrospective study included 56 eyes of 40 patients with RP (14 male and 26 female), 41 to 82 years of age (mean, 62.610.4 years), who underwent cataract surgery between May 2007 and October 2012. All patients had phacoemulsification and intraocular lens (IOL) implantation. We usually used blue light filtering hydrophobic IOLs in our cataract surgeries for patients with RP both to prevent the phototoxicity of blue light and to reduce the possibility of PCO formation. In this study, each patient received an AF1 YA65BB IOL (HOYA Corporation, Tokyo, Japan) (n ¼ 27), an AcrySof SN60AT IOL (Alcon Japan, Tokyo, Japan) (n ¼ 25), or an AN6K IOL (Kowa, Tokyo, Japan) (n ¼ 4). The mean follow-up period was 37.522.6 months (range, 6e73 months). All patients in this study were seen at Kyushu University Hospital (Fukuoka, Japan). The investigation was carried out under approval from the Institutional Review Board and was conducted in accordance with the tenets of the Declaration of Helsinki on biomedical research involving human subjects. The diagnosis of RP was based on the patients’ history of night blindness, side vision restriction, and markedly reduced or nonrecordable a- and b-wave amplitudes on electroretinogram testing, in addition to ophthalmoscopic findings (i.e., characteristic fundus changes in the attenuated retinal vessels and bone spiculeelike pigment clumping). We excluded any patient with uveitis or any disease that could cause RP-like fundus changes. Baseline acuity for subsequent best-corrected visual acuity (BCVA) was measured for all patients with full subjective refraction using a Landolt ring chart at 5 m in decimal units. The decimal acuities were converted into a logarithm of the minimum angle of resolution (logMAR) for statistical evaluation. We performed automated static perimetry testing (Humphrey Field Analyzer [HFA]; Humphrey Instruments, Inc, San Leandro, CA) using the central 10-2 SITA Standard Program. An appropriate lens correction was made for the test distance. The HFA 10-2 program was repeated if the test reliability was not satisfactory (fixation loss >20%, false positive >15%, or false-negative >33%). We obtained data on 35 eyes from the HFA 10-2 program. The data were not obtained for all eyes because of patient unavailability for measurement. The eyes included 22 (62.9%) with advanced RP, with a mean deviation (MD) less than 15 decibels (dB), and 13 (37.1%) with less advanced RP, with an MD of 15 dB or greater.11 We investigated the relation between preoperative MD and final BCVA. Slit-lamp biomicroscopy of the anterior segment and funduscopic examination by both direct and indirect ophthalmoscopy were also carried out on all patients. We observed the details of lens, vitreous, and fundus findings. Detailed macular information was confirmed by optical coherence tomography (OCT), which is a well-recognized method of analyzing the retinal architecture and has been used for the diagnosis and monitoring of RP.12 Optical coherence tomography (Carl Zeiss Cirrus HD-OCT MODEL 4000, Dublin, CA) demonstrated macular complications, such as cystoid macular edema (CME) and epiretinal membrane. The parameters used to monitor CME have been limited to the retinal thickness or the size of the cystoid space. All OCT images were also used for the ellipsoid zone (EZ; also called the inner/outer segment junction), with a distinct and continuous line indicating normal alignment of the membranous discs in the photoreceptor outer segments.13,14 We graded the appearance of the EZ at the fovea from 1 to 3: grade 1, EZ was not visible; grade 2, abnormal EZ; and grade 3, normal EZ.15 In addition, we investigated the relationship between preoperative EZ conditions and final BCVA. We divided PCO into 3 groups: mild, the outlines of the optic nerve head and main retinal vessels were clearly distinguishable;
2
moderate, the outlines of the optic nerve head or of the main retinal blood vessels were blurred; and severe, the optic nerve head and blood vessels were barely visible.16 Data are presented as arithmetic mean values standard deviations. Statistical analysis was performed using the Wilcoxon test or Wilcoxon/KruskaleWallis test. P values < 0.05 were considered statistically significant.
Results Visual Acuity Changes in preoperative and postoperative BCVA are shown in Figure 1. The mean preoperative BCVA was 0.760.65 (range, 0.08 to 2.30). The mean BCVA at 6 months after surgery was 0.420.55 (range, 0.18 to 2.00), and the mean final BCVA was 0.450.53 (range, 0.18 to 2.00). Postoperative BCVA was significantly improved compared with preoperative BCVA, both at 6 months after surgery and at the final examination (P < 0.0005 and P < 0.005, Wilcoxon test). Final BCVA improved (>0.3 logMAR) in 26 eyes (46.4%) and was unchanged in 30 eyes (53.6%). Furthermore, there was no eye in which final BCVA worsened more than 0.3 logMAR from baseline.
Visual Field We investigated the relationship between preoperative MD value on the HFA10-2 program and final BCVA (Table 1). In the group with less advanced RP (MD was 15 dB), the final BCVA improved significantly (P < 0.01, Wilcoxon/KruskaleWallis test); however, the final BCVA did not improve significantly in the group with advanced RP (MD <15 dB). Moreover, the final BCVA was significantly worse in the group with advanced RP than in the group with less advanced RP (P < 0.01, Wilcoxon/KruskaleWallis test); in contrast, preoperative BCVA was not significantly different between the 2 groups. We also investigated the correlation between preoperative MD and final BCVA (Fig 2). The correlation coefficient was 0.51, and they were significantly correlated (P < 0.005).
Figure 1. Changes in preoperative best-corrected visual acuity (BCVA) and postoperative BCVA. Postoperative BCVA was significantly improved compared with preoperative BCVA, both at 6 months after surgery and at the final examination. **P < 0.0005 and *P < 0.005. logMAR ¼ logarithm of the minimum angle of resolution.
Yoshida et al
Cataract Surgery in Patients with RP
Table 1. Visual Field Preoperative MD
Preoperative BCVA
Final BCVA
P Values
15 dB (n ¼ 13) <15 dB (n ¼ 22) P values
0.500.38 0.740.55 0.20
0.110.34 0.310.34 <0.01
<0.01 0.06
BCVA ¼ best-corrected visual acuity; dB ¼ decibels; MD ¼ mean deviation.
follow-up time of 3 years. Mild PCO was detected in 21 eyes, and moderate PCO was detected in 3 eyes. No eyes showed severe PCO. In addition, PCO occurred within 6 months after surgery in 38 eyes (67.9%). Neodymium:YAG laser capsulotomy was performed in 23 eyes (41.1%) within the mean follow-up time of 3 years. In 5 of these 23 eyes (21.7%), YAG treatment was performed within 6 months after surgery. Anterior capsular contraction was detected in 13 eyes (23.2%). Intraocular lens dislocation was not detected.
Discussion Ellipsoid Zone A representative image of each of the 3 EZ groups obtained by OCT images is shown in Figure 3A. The EZ was not visible (grade 1) in 16 eyes (28.6%), an abnormal EZ (grade 2) was identified in 12 eyes (21.4%), and EZ was normal (grade 3) in 28 eyes (50.0%). The final BCVA of each EZ grade is shown in Figure 3B. The mean final BCVA was 0.830.41 in grade 1, 0.820.59 in grade 2, and 0.070.15 in grade 3. Final BCVA was significantly better in grade 3 than in grades 1 and 2 (P < 0.0001, Wilcoxon test). However, the difference in final BCVA between patients with grade 1 and patients with grade 2 was not significant.
Cystoid Macular Edema On preoperative OCT examination, CME was identified in 3 eyes (5.4%) of 2 patients. After cataract surgery, none of these 3 CME cases worsened on postoperative OCT examination. Moreover, no new CME cases were identified in patients with RP postoperatively.
Capsule Opacification Posterior subcapsular cataract was detected in 37 eyes (66.1%). We investigated the relationship between PSC cataract and final BCVA. However, we did not find a significant relation between final BCVA and presence or absence of PSC preoperatively. The postoperative capsule complications are shown in Table 2. The incidence of PCO was 83.9% (47 eyes) within the mean
Figure 2. The correlation between preoperative mean deviation (MD) value on the Humphrey Field Analyzer 10-2 program (Humphrey Instruments, Inc, San Leandro, CA) and final best-corrected visual acuity (BCVA). The correlation coefficient was 0.51, and they were significantly correlated (P<0.005). dB ¼ decibels; logMAR ¼ logarithm of the minimum angle of resolution.
Cataracts are among the most common eye complications in patients with RP. Apart from the general risk of cataract surgery, several specific factors that may result in a poor visual outcome have been reported in patients with RP. In the present retrospective study, we investigated the factors affecting postoperative visual acuity in patients with RP. We demonstrated the following: (1) The mean BCVA significantly improved after surgery, and there was no eye in which final BCVA worsened; (2) the preoperative MD value on the HFA 10-2 program and final BCVA were significantly correlated, and the final BCVA significantly improved in the less advanced RP group; (3) final BCVA was significantly better in the group whose preoperative OCT examination showed a normal EZ; and (4) PCO occurred in 47 eyes (83.9%) and was subjected to YAG laser capsulotomy in 23 eyes (41.1%) within the mean follow-up time of 3 years. Cataracts have been reported to develop at a relatively young age in patients with RP, with a mean age at surgery of 47 to 58 years.4e6 In our study, the mean age of patients undergoing cataract surgery was 62.6 years. This was greater than that in previous reports because our surgical indications might be slightly more strict. Previous studies have reported that the mean of BCVA was significantly improved after cataract surgery in patients with RP.5,6 However, it has also been reported that postoperative BCVA did not improve in 12.5% to 23% eyes. As in these previous studies, the mean final BCVA showed significant improvement, whereas the final BCVA did not improve in 53.6% of eyes in our study. In a study by Jackson et al,5 more than 96% of patients reported a functional improvement in visual symptoms despite the acuity being unchanged or worse; therefore, other measures of visual function may be needed when assessing patients with RP for cataract surgery and evaluating its benefit. The MD value on the HFA 10-2 program, which assesses the sensitivity distribution in the macular area, has been used for monitoring the progression of RP.11,17 In previous studies of patients with general RP, most eyes with an MD value of 15 dB or greater had better acuity, whereas eyes with an MD value less than 15 dB had various degrees of acuity loss. In our study, final BCVA significantly improved in the less advanced RP group, and the preoperative MD value significantly correlated with the final BCVA. Therefore, it was suggested that examination of the preoperative HFA 10-2 program may be important for prognosis of visual outcome. In the general population, the existence of a correlation between preoperative photoreceptor EZ disruption and
3
Ophthalmology Volume -, Number -, Month 2015
Figure 3. Typical horizontal optical coherence tomography (OCT) macular scan of the ellipsoid zone (EZ) of each grade and final best-corrected visual acuity (BCVA) of each EZ grade. (A) The EZ was not visible (grade 1) in 16 eyes (28.6%), abnormal (grade 2) in 12 eyes (21.4%), and normal (grade 3) in 28 eyes (50.0%). (B) Final BCVA was significantly better in grade 3 than in grades 1 and 2. *P < 0.0001. logMAR ¼ logarithm of the minimum angle of resolution.
decreased postoperative visual acuity has been reported.18,19 In patients with RP, it has been reported that the presence of a normal EZ may be associated with better visual acuity and that the absence of EZ may reflect a foveal dysfunction.15 In our study, the group with preoperatively normal EZ had significantly better final BCVA than the group with not visible or abnormal EZ. Thus, the presence of preoperatively normal EZ may be another important prognostic factor for better postoperative visual outcome in patients with RP. Table 2. Times of Postoperative Capsule Opacification and Contraction or Capsulotomy Eyes (%) PCO Mild Moderate Nd:YAG laser capsulotomy Anterior capsular contraction
Within 6 Months Final Evaluation Date 38 (67.9) 32 1 5 9 (16.1)
47 (83.9) 21 3 23 13 (23.2)
Nd:YAG ¼ neodymium:YAG; PCO ¼ posterior capsular opacification.
4
Macular complications, such as epiretinal membrane and CME, are important because of their effect on central visual function.20e23 Recently, the prevalence of these complications has been reported as being higher than before. This can be explained as a result of the higher sensitivity of OCT than fluorescein angiography.24 Thus, the reported prevalence of CME in patients with RP has varied widely, from 10% to 40%.21,25,26 In previous studies, the prevalence of macular edema after cataract surgery detected by fluorescein angiography or OCT was reported in 10% to 14% of eyes in patients with RP.5,6 In our study, the prevalence of CME by preoperative OCT was 3 eyes (5.4%); no new CME or CME advancement was detected postoperatively by OCT examination. The reason for the low incidence of postoperative CME is not clear. However, to reduce phototoxic retinal damage, we decreased illumination by 15% compared with the case of normal cataract surgery. Posterior capsular opacification is one of the most common complications of cataract surgery. Posterior capsular opacification develops as a result of proliferation and migration of residual lens epithelial cells from the lens equator lesion, causing development of an opaque membrane across the posterior capsule.27,28 There are several
Yoshida et al
Cataract Surgery in Patients with RP
new methods of objective PCO evaluation, such as the Automated Quantification of After Cataract (AQUA) and the manual posterior capsule opacification software system (POCOman) using the digital examination technique.29,30 In our retrospective study, we assessed subjective PCO evaluation using slit-lamp observation; however, we need to perform the objective evaluation on PCO severity in our next prospective study. The prevalence of PCO after cataract surgery has been reported as 14.5% to 18.4% in the general population.31e33 In patients with RP, previous reports demonstrated that PCO occurred in 63% to 82.5%, and that 43.2% to 52.5% required capsulotomy after cataract surgery.5,6 In our study, the prevalence of PCO was 83.9%, and 41.1% of patients underwent neodymium:YAG laser capsulotomy. This result was comparable to those of previous reports. Previous studies have reported that one reason for the high incidence of PCO after cataract surgery is disruption of the bloodeocular barrier in RP, allowing for high aqueous levels of inflammatory cytokines, such as interleukin-1 and -6.6,34 Interleukin-1 and -6 are released by macrophages and may play an important role in increasing lens epithelial cell activation. In our previous study, we also reported that levels of several proinflammatory mediators increased in eyes of patients with RP.35 Sustained chronic inflammation in affected eyes of patients with RP also may result in the high prevalence of PCO. Similar factors may cause the anterior capsular contraction. Hayashi et al36 reported that the percent of decrease in the anterior capsule opening at 6 months after was 45.2% in the RP group, whereas it was only 4.6% in the control group.36 In our study, the prevalence of anterior capsular contraction was 23.2%. In conclusion, the mean BCVA showed significant improvement after cataract surgery in patients with RP. Moreover, there was no case in which the final BCVA worsened during a 3-year postoperative period. The preoperative MD value on the HFA 10-2 program and the presence of a normal inner/outer segment on OCT significantly influenced the final BCVA. Posterior capsular opacification occurred with high frequency a short time after surgery. Our findings show that preoperative ophthalmic examinations that may reflect macular (or foveal) function are important parameters to predict visual outcome. However, our study was limited by being of short duration. Further extensive clinical observations will be needed for long-term outcome of cataract surgery in patients with RP.
References 1. Wong P. Apoptosis, retinitis pigmentosa, and degeneration. Biochem Cell Biol 1994;72:489–98. 2. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet 2006;368:1795–809. 3. Pruett RC. Retinitis pigmentosa: clinical observations and correlations. Trans Am Ophthalmol Soc 1983;81:693–735. 4. Bastek JV, Heckenlively JR, Straatsma BR. Cataract surgery in retinitis pigmentosa patients. Ophthalmology 1982;89: 880–4.
5. Jackson H, Garway-Heath D, Rosen P, et al. Outcome of cataract surgery in patients with retinitis pigmentosa. Br J Ophthalmol 2001;85:936–8. 6. Dikopf MS, Chow CC, Mieler WF, Tu EY. Cataract extraction outcomes and the prevalence of zonular insufficiency in retinitis pigmentosa. Am J Ophthalmol 2013;156:82–88 e2. 7. Fishman GA, Anderson RJ, Lourenco P. Prevalence of posterior subcapsular lens opacities in patients with retinitis pigmentosa. Br J Ophthalmol 1985;69:263–6. 8. Auffarth GU, Nimsgern C, Tetz MR, et al. [Increased cataract rate and characteristics of Nd:YAG laser capsulotomy in retinitis pigmentosa]. Ophthalmologe 1997;94:791–5. 9. Heckenlively J. The frequency of posterior subcapsular cataract in the hereditary retinal degenerations. Am J Ophthalmol 1982;93:733–8. 10. Bayyoud T, Bartz-Schmidt KU, Yoeruek E. Long-term clinical results after cataract surgery with and without capsular tension ring in patients with retinitis pigmentosa: a retrospective study. BMJ Open 2013;3:e002616. 11. Abe K, Iijima H, Hirakawa H, et al. Visual acuity and 10 degrees automated static perimetry in eyes with retinitis pigmentosa. Jpn J Ophthalmol 2002;46:581–5. 12. Oishi A, Otani A, Sasahara M, et al. Photoreceptor integrity and visual acuity in cystoid macular oedema associated with retinitis pigmentosa. Eye (Lond) 2009;23:1411–6. 13. Ko TH, Fujimoto JG, Duker JS, et al. Comparison of ultrahigh- and standard-resolution optical coherence tomography for imaging macular hole pathology and repair. Ophthalmology 2004;111:2033–43. 14. Spaide RF, Curcio CA. Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina 2011;31:1609–19. 15. Aizawa S, Mitamura Y, Baba T, et al. Correlation between visual function and photoreceptor inner/outer segment junction in patients with retinitis pigmentosa. Eye (Lond) 2009;23: 304–8. 16. Elgohary MA, Beckingsale AB. Effect of posterior capsular opacification on visual function in patients with monofocal and multifocal intraocular lenses. Eye (Lond) 2008;22:613–9. 17. Iijima H. Correlation between visual sensitivity loss and years affected for eyes with retinitis pigmentosa. Jpn J Ophthalmol 2012;56:224–9. 18. Inoue M, Morita S, Watanabe Y, et al. Inner segment/outer segment junction assessed by spectral-domain optical coherence tomography in patients with idiopathic epiretinal membrane. Am J Ophthalmol 2010;150:834–9. 19. Itoh Y, Inoue M, Rii T, et al. Correlation between length of foveal cone outer segment tips line defect and visual acuity after macular hole closure. Ophthalmology 2012;119:1438–46. 20. Grigoropoulos VG, Emfietzoglou J, Nikolaidis P, et al. Optical coherence tomography findings in patients with retinitis pigmentosa and low visual acuity. Ophthalmic Surg Lasers Imaging 2010;41:35–9. 21. Hagiwara A, Yamamoto S, Ogata K, et al. Macular abnormalities in patients with retinitis pigmentosa: prevalence on OCT examination and outcomes of vitreoretinal surgery. Acta Ophthalmol 2011;89:e122–5. 22. Ikeda Y, Yoshida N, Notomi S, et al. Therapeutic effect of prolonged treatment with topical dorzolamide for cystoid macular oedema in patients with retinitis pigmentosa. Br J Ophthalmol 2013;97:1187–91. 23. Ikeda Y, Hisatomi T, Yoshida N, et al. The clinical efficacy of a topical dorzolamide in the management of cystoid macular edema in patients with retinitis pigmentosa. Graefes Arch Clin Exp Ophthalmol 2012;250:809–14.
5
Ophthalmology Volume -, Number -, Month 2015 24. Apushkin MA, Fishman GA, Janowicz MJ. Monitoring cystoid macular edema by optical coherence tomography in patients with retinitis pigmentosa. Ophthalmology 2004;111:1899–904. 25. Hirakawa H, Iijima H, Gohdo T, Tsukahara S. Optical coherence tomography of cystoid macular edema associated with retinitis pigmentosa. Am J Ophthalmol 1999;128:185–91. 26. Hajali M, Fishman GA, Anderson RJ. The prevalence of cystoid macular oedema in retinitis pigmentosa patients determined by optical coherence tomography. Br J Ophthalmol 2008;92:1065–8. 27. Hollick EJ, Spalton DJ, Ursell PG, Pande MV. Lens epithelial cell regression on the posterior capsule with different intraocular lens materials. Br J Ophthalmol 1998;82:1182–8. 28. Trivedi RH, Werner L, Apple DJ, et al. Post cataractintraocular lens (IOL) surgery opacification. Eye (Lond) 2002;16:217–41. 29. Findl O, Buehl W, Menapace R, et al. Comparison of 4 methods for quantifying posterior capsule opacification. J Cataract Refract Surg 2003;29:106–11. 30. Bender L, Spalton DJ, Uyanonvara B, et al. POCOman: new system for quantifying posterior capsule opacification. J Cataract Refract Surg 2004;30:2058–63.
31. Gupta P, Zheng Y, Ting TW, et al. Prevalence of cataract surgery and visual outcomes in Indian immigrants in Singapore: the Singapore Indian eye study. PLoS One 2013;8: e75584. 32. Huang W, Huang G, Wang D, et al. Outcomes of cataract surgery in urban southern China: the Liwan Eye Study. Invest Ophthalmol Vis Sci 2011;52:16–20. 33. Lavanya R, Wong TY, Aung T, et al. Prevalence of cataract surgery and post-surgical visual outcomes in an urban Asian population: the Singapore Malay Eye Study. Br J Ophthalmol 2009;93:299–304. 34. Nishi O, Nishi K, Fujiwara T, et al. Effects of the cytokines on the proliferation of and collagen synthesis by human cataract lens epithelial cells. Br J Ophthalmol 1996;80:63–8. 35. Yoshida N, Ikeda Y, Notomi S, et al. Clinical evidence of sustained chronic inflammatory reaction in retinitis pigmentosa. Ophthalmology 2013;120:100–5. 36. Hayashi K, Hayashi H, Matsuo K, et al. Anterior capsule contraction and intraocular lens dislocation after implant surgery in eyes with retinitis pigmentosa. Ophthalmology 1998;105:1239–43.
Footnotes and Financial Disclosures Originally received: July 24, 2014. Final revision: December 3, 2014. Accepted: December 4, 2014. Available online: ---.
Manuscript no. 2014-1170.
1
Department of Ophthalmology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
2
Department of Ophthalmology, Akita University Graduate School of Medicine, Akita, Japan. Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article. Supported in part by a Grant-in-Aid (to Y.I.) from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (grant no. 24659763).
6
Abbreviations and Acronyms: BCVA ¼ best-corrected visual acuity; CME ¼ cystoid macular edema; dB ¼ decibels; EZ ¼ ellipsoid zone; HFA ¼ Humphrey Field Analyzer; IOL ¼ intraocular lens; logMAR ¼ logarithm of the minimum angle of resolution; MD ¼ mean deviation; OCT ¼ optical coherence tomography; PCO ¼ posterior capsular opacification; PSC ¼ posterior subcapsular cataract; RP ¼ retinitis pigmentosa. Correspondence: Yasuhiro Ikeda, MD, PhD, Department of Ophthalmology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan. E-mail: [email protected].
Retinitis pigmentosa (RP) is an inherited retinal degenerative disease that affects photoreceptor and retinal pigment epithelial function and is a major cause of blindness in adults.1,2 In addition to retinal manifestations, such as equatorial bone spicule pigment figures and attenuated retinal vessels along with rod-cone degeneration, cataracts are among the most common eye complications of all hereditary forms of RP.3 As a specific clinical feature of cataract in patients with RP, previous studies have reported that lens opacities develop at a relatively young age.4e6 It has been reported that the mean age at surgery in patients with RP is 47 to 58 years and that in those with age-related cataracts is 72 to 74 years.5e7 It has also been reported that posterior subcapsular cataract (PSC) is the most common morphologic category in patients with RP.5,6,8,9 Fishman et al7 demonstrated a 41% (with autosomal dominant form) to 90% (with X linked recessive disease) probability of PSC by age 40 years, whereas the probabilities reach more than 80% by age 60 years for many genetic types of RP. This PSC may
2015 by the American Academy of Ophthalmology Published by Elsevier Inc.
not only cause severe visual dysfunction but also exacerbate glare symptoms, especially among workingage people. It is suggested that cataract surgery may help this patient group gain visual acuity.10 However, several factors that may result in a poor visual outcome after cataract surgery in patients with RP have been reported.5,6 These factors include posterior capsular opacification (PCO), anterior capsular contraction, zonular weakness, outer retinal atrophy, macular edema, and phototoxic retinal damage. Despite the potentially poor result in visual acuity, cataract surgery is necessary for patients with RP. To provide better data on these eye complications and their effect on outcome, and the potential risks and benefits of surgery, we need further knowledge about the outcome of surgery.5 In this study, we performed a retrospective observational clinical study with patients with RP who underwent cataract surgery. We investigated the clinical course of cataract surgery and evaluated the factors affecting postoperative visual acuity in patients with RP.
http://dx.doi.org/10.1016/j.ophtha.2014.12.003 ISSN 0161-6420/15
1
Ophthalmology Volume -, Number -, Month 2015
Methods This retrospective study included 56 eyes of 40 patients with RP (14 male and 26 female), 41 to 82 years of age (mean, 62.610.4 years), who underwent cataract surgery between May 2007 and October 2012. All patients had phacoemulsification and intraocular lens (IOL) implantation. We usually used blue light filtering hydrophobic IOLs in our cataract surgeries for patients with RP both to prevent the phototoxicity of blue light and to reduce the possibility of PCO formation. In this study, each patient received an AF1 YA65BB IOL (HOYA Corporation, Tokyo, Japan) (n ¼ 27), an AcrySof SN60AT IOL (Alcon Japan, Tokyo, Japan) (n ¼ 25), or an AN6K IOL (Kowa, Tokyo, Japan) (n ¼ 4). The mean follow-up period was 37.522.6 months (range, 6e73 months). All patients in this study were seen at Kyushu University Hospital (Fukuoka, Japan). The investigation was carried out under approval from the Institutional Review Board and was conducted in accordance with the tenets of the Declaration of Helsinki on biomedical research involving human subjects. The diagnosis of RP was based on the patients’ history of night blindness, side vision restriction, and markedly reduced or nonrecordable a- and b-wave amplitudes on electroretinogram testing, in addition to ophthalmoscopic findings (i.e., characteristic fundus changes in the attenuated retinal vessels and bone spiculeelike pigment clumping). We excluded any patient with uveitis or any disease that could cause RP-like fundus changes. Baseline acuity for subsequent best-corrected visual acuity (BCVA) was measured for all patients with full subjective refraction using a Landolt ring chart at 5 m in decimal units. The decimal acuities were converted into a logarithm of the minimum angle of resolution (logMAR) for statistical evaluation. We performed automated static perimetry testing (Humphrey Field Analyzer [HFA]; Humphrey Instruments, Inc, San Leandro, CA) using the central 10-2 SITA Standard Program. An appropriate lens correction was made for the test distance. The HFA 10-2 program was repeated if the test reliability was not satisfactory (fixation loss >20%, false positive >15%, or false-negative >33%). We obtained data on 35 eyes from the HFA 10-2 program. The data were not obtained for all eyes because of patient unavailability for measurement. The eyes included 22 (62.9%) with advanced RP, with a mean deviation (MD) less than 15 decibels (dB), and 13 (37.1%) with less advanced RP, with an MD of 15 dB or greater.11 We investigated the relation between preoperative MD and final BCVA. Slit-lamp biomicroscopy of the anterior segment and funduscopic examination by both direct and indirect ophthalmoscopy were also carried out on all patients. We observed the details of lens, vitreous, and fundus findings. Detailed macular information was confirmed by optical coherence tomography (OCT), which is a well-recognized method of analyzing the retinal architecture and has been used for the diagnosis and monitoring of RP.12 Optical coherence tomography (Carl Zeiss Cirrus HD-OCT MODEL 4000, Dublin, CA) demonstrated macular complications, such as cystoid macular edema (CME) and epiretinal membrane. The parameters used to monitor CME have been limited to the retinal thickness or the size of the cystoid space. All OCT images were also used for the ellipsoid zone (EZ; also called the inner/outer segment junction), with a distinct and continuous line indicating normal alignment of the membranous discs in the photoreceptor outer segments.13,14 We graded the appearance of the EZ at the fovea from 1 to 3: grade 1, EZ was not visible; grade 2, abnormal EZ; and grade 3, normal EZ.15 In addition, we investigated the relationship between preoperative EZ conditions and final BCVA. We divided PCO into 3 groups: mild, the outlines of the optic nerve head and main retinal vessels were clearly distinguishable;
2
moderate, the outlines of the optic nerve head or of the main retinal blood vessels were blurred; and severe, the optic nerve head and blood vessels were barely visible.16 Data are presented as arithmetic mean values standard deviations. Statistical analysis was performed using the Wilcoxon test or Wilcoxon/KruskaleWallis test. P values < 0.05 were considered statistically significant.
Results Visual Acuity Changes in preoperative and postoperative BCVA are shown in Figure 1. The mean preoperative BCVA was 0.760.65 (range, 0.08 to 2.30). The mean BCVA at 6 months after surgery was 0.420.55 (range, 0.18 to 2.00), and the mean final BCVA was 0.450.53 (range, 0.18 to 2.00). Postoperative BCVA was significantly improved compared with preoperative BCVA, both at 6 months after surgery and at the final examination (P < 0.0005 and P < 0.005, Wilcoxon test). Final BCVA improved (>0.3 logMAR) in 26 eyes (46.4%) and was unchanged in 30 eyes (53.6%). Furthermore, there was no eye in which final BCVA worsened more than 0.3 logMAR from baseline.
Visual Field We investigated the relationship between preoperative MD value on the HFA10-2 program and final BCVA (Table 1). In the group with less advanced RP (MD was 15 dB), the final BCVA improved significantly (P < 0.01, Wilcoxon/KruskaleWallis test); however, the final BCVA did not improve significantly in the group with advanced RP (MD <15 dB). Moreover, the final BCVA was significantly worse in the group with advanced RP than in the group with less advanced RP (P < 0.01, Wilcoxon/KruskaleWallis test); in contrast, preoperative BCVA was not significantly different between the 2 groups. We also investigated the correlation between preoperative MD and final BCVA (Fig 2). The correlation coefficient was 0.51, and they were significantly correlated (P < 0.005).
Figure 1. Changes in preoperative best-corrected visual acuity (BCVA) and postoperative BCVA. Postoperative BCVA was significantly improved compared with preoperative BCVA, both at 6 months after surgery and at the final examination. **P < 0.0005 and *P < 0.005. logMAR ¼ logarithm of the minimum angle of resolution.
Yoshida et al
Cataract Surgery in Patients with RP
Table 1. Visual Field Preoperative MD
Preoperative BCVA
Final BCVA
P Values
15 dB (n ¼ 13) <15 dB (n ¼ 22) P values
0.500.38 0.740.55 0.20
0.110.34 0.310.34 <0.01
<0.01 0.06
BCVA ¼ best-corrected visual acuity; dB ¼ decibels; MD ¼ mean deviation.
follow-up time of 3 years. Mild PCO was detected in 21 eyes, and moderate PCO was detected in 3 eyes. No eyes showed severe PCO. In addition, PCO occurred within 6 months after surgery in 38 eyes (67.9%). Neodymium:YAG laser capsulotomy was performed in 23 eyes (41.1%) within the mean follow-up time of 3 years. In 5 of these 23 eyes (21.7%), YAG treatment was performed within 6 months after surgery. Anterior capsular contraction was detected in 13 eyes (23.2%). Intraocular lens dislocation was not detected.
Discussion Ellipsoid Zone A representative image of each of the 3 EZ groups obtained by OCT images is shown in Figure 3A. The EZ was not visible (grade 1) in 16 eyes (28.6%), an abnormal EZ (grade 2) was identified in 12 eyes (21.4%), and EZ was normal (grade 3) in 28 eyes (50.0%). The final BCVA of each EZ grade is shown in Figure 3B. The mean final BCVA was 0.830.41 in grade 1, 0.820.59 in grade 2, and 0.070.15 in grade 3. Final BCVA was significantly better in grade 3 than in grades 1 and 2 (P < 0.0001, Wilcoxon test). However, the difference in final BCVA between patients with grade 1 and patients with grade 2 was not significant.
Cystoid Macular Edema On preoperative OCT examination, CME was identified in 3 eyes (5.4%) of 2 patients. After cataract surgery, none of these 3 CME cases worsened on postoperative OCT examination. Moreover, no new CME cases were identified in patients with RP postoperatively.
Capsule Opacification Posterior subcapsular cataract was detected in 37 eyes (66.1%). We investigated the relationship between PSC cataract and final BCVA. However, we did not find a significant relation between final BCVA and presence or absence of PSC preoperatively. The postoperative capsule complications are shown in Table 2. The incidence of PCO was 83.9% (47 eyes) within the mean
Figure 2. The correlation between preoperative mean deviation (MD) value on the Humphrey Field Analyzer 10-2 program (Humphrey Instruments, Inc, San Leandro, CA) and final best-corrected visual acuity (BCVA). The correlation coefficient was 0.51, and they were significantly correlated (P<0.005). dB ¼ decibels; logMAR ¼ logarithm of the minimum angle of resolution.
Cataracts are among the most common eye complications in patients with RP. Apart from the general risk of cataract surgery, several specific factors that may result in a poor visual outcome have been reported in patients with RP. In the present retrospective study, we investigated the factors affecting postoperative visual acuity in patients with RP. We demonstrated the following: (1) The mean BCVA significantly improved after surgery, and there was no eye in which final BCVA worsened; (2) the preoperative MD value on the HFA 10-2 program and final BCVA were significantly correlated, and the final BCVA significantly improved in the less advanced RP group; (3) final BCVA was significantly better in the group whose preoperative OCT examination showed a normal EZ; and (4) PCO occurred in 47 eyes (83.9%) and was subjected to YAG laser capsulotomy in 23 eyes (41.1%) within the mean follow-up time of 3 years. Cataracts have been reported to develop at a relatively young age in patients with RP, with a mean age at surgery of 47 to 58 years.4e6 In our study, the mean age of patients undergoing cataract surgery was 62.6 years. This was greater than that in previous reports because our surgical indications might be slightly more strict. Previous studies have reported that the mean of BCVA was significantly improved after cataract surgery in patients with RP.5,6 However, it has also been reported that postoperative BCVA did not improve in 12.5% to 23% eyes. As in these previous studies, the mean final BCVA showed significant improvement, whereas the final BCVA did not improve in 53.6% of eyes in our study. In a study by Jackson et al,5 more than 96% of patients reported a functional improvement in visual symptoms despite the acuity being unchanged or worse; therefore, other measures of visual function may be needed when assessing patients with RP for cataract surgery and evaluating its benefit. The MD value on the HFA 10-2 program, which assesses the sensitivity distribution in the macular area, has been used for monitoring the progression of RP.11,17 In previous studies of patients with general RP, most eyes with an MD value of 15 dB or greater had better acuity, whereas eyes with an MD value less than 15 dB had various degrees of acuity loss. In our study, final BCVA significantly improved in the less advanced RP group, and the preoperative MD value significantly correlated with the final BCVA. Therefore, it was suggested that examination of the preoperative HFA 10-2 program may be important for prognosis of visual outcome. In the general population, the existence of a correlation between preoperative photoreceptor EZ disruption and
3
Ophthalmology Volume -, Number -, Month 2015
Figure 3. Typical horizontal optical coherence tomography (OCT) macular scan of the ellipsoid zone (EZ) of each grade and final best-corrected visual acuity (BCVA) of each EZ grade. (A) The EZ was not visible (grade 1) in 16 eyes (28.6%), abnormal (grade 2) in 12 eyes (21.4%), and normal (grade 3) in 28 eyes (50.0%). (B) Final BCVA was significantly better in grade 3 than in grades 1 and 2. *P < 0.0001. logMAR ¼ logarithm of the minimum angle of resolution.
decreased postoperative visual acuity has been reported.18,19 In patients with RP, it has been reported that the presence of a normal EZ may be associated with better visual acuity and that the absence of EZ may reflect a foveal dysfunction.15 In our study, the group with preoperatively normal EZ had significantly better final BCVA than the group with not visible or abnormal EZ. Thus, the presence of preoperatively normal EZ may be another important prognostic factor for better postoperative visual outcome in patients with RP. Table 2. Times of Postoperative Capsule Opacification and Contraction or Capsulotomy Eyes (%) PCO Mild Moderate Nd:YAG laser capsulotomy Anterior capsular contraction
Within 6 Months Final Evaluation Date 38 (67.9) 32 1 5 9 (16.1)
47 (83.9) 21 3 23 13 (23.2)
Nd:YAG ¼ neodymium:YAG; PCO ¼ posterior capsular opacification.
4
Macular complications, such as epiretinal membrane and CME, are important because of their effect on central visual function.20e23 Recently, the prevalence of these complications has been reported as being higher than before. This can be explained as a result of the higher sensitivity of OCT than fluorescein angiography.24 Thus, the reported prevalence of CME in patients with RP has varied widely, from 10% to 40%.21,25,26 In previous studies, the prevalence of macular edema after cataract surgery detected by fluorescein angiography or OCT was reported in 10% to 14% of eyes in patients with RP.5,6 In our study, the prevalence of CME by preoperative OCT was 3 eyes (5.4%); no new CME or CME advancement was detected postoperatively by OCT examination. The reason for the low incidence of postoperative CME is not clear. However, to reduce phototoxic retinal damage, we decreased illumination by 15% compared with the case of normal cataract surgery. Posterior capsular opacification is one of the most common complications of cataract surgery. Posterior capsular opacification develops as a result of proliferation and migration of residual lens epithelial cells from the lens equator lesion, causing development of an opaque membrane across the posterior capsule.27,28 There are several
Yoshida et al
Cataract Surgery in Patients with RP
new methods of objective PCO evaluation, such as the Automated Quantification of After Cataract (AQUA) and the manual posterior capsule opacification software system (POCOman) using the digital examination technique.29,30 In our retrospective study, we assessed subjective PCO evaluation using slit-lamp observation; however, we need to perform the objective evaluation on PCO severity in our next prospective study. The prevalence of PCO after cataract surgery has been reported as 14.5% to 18.4% in the general population.31e33 In patients with RP, previous reports demonstrated that PCO occurred in 63% to 82.5%, and that 43.2% to 52.5% required capsulotomy after cataract surgery.5,6 In our study, the prevalence of PCO was 83.9%, and 41.1% of patients underwent neodymium:YAG laser capsulotomy. This result was comparable to those of previous reports. Previous studies have reported that one reason for the high incidence of PCO after cataract surgery is disruption of the bloodeocular barrier in RP, allowing for high aqueous levels of inflammatory cytokines, such as interleukin-1 and -6.6,34 Interleukin-1 and -6 are released by macrophages and may play an important role in increasing lens epithelial cell activation. In our previous study, we also reported that levels of several proinflammatory mediators increased in eyes of patients with RP.35 Sustained chronic inflammation in affected eyes of patients with RP also may result in the high prevalence of PCO. Similar factors may cause the anterior capsular contraction. Hayashi et al36 reported that the percent of decrease in the anterior capsule opening at 6 months after was 45.2% in the RP group, whereas it was only 4.6% in the control group.36 In our study, the prevalence of anterior capsular contraction was 23.2%. In conclusion, the mean BCVA showed significant improvement after cataract surgery in patients with RP. Moreover, there was no case in which the final BCVA worsened during a 3-year postoperative period. The preoperative MD value on the HFA 10-2 program and the presence of a normal inner/outer segment on OCT significantly influenced the final BCVA. Posterior capsular opacification occurred with high frequency a short time after surgery. Our findings show that preoperative ophthalmic examinations that may reflect macular (or foveal) function are important parameters to predict visual outcome. However, our study was limited by being of short duration. Further extensive clinical observations will be needed for long-term outcome of cataract surgery in patients with RP.
References 1. Wong P. Apoptosis, retinitis pigmentosa, and degeneration. Biochem Cell Biol 1994;72:489–98. 2. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet 2006;368:1795–809. 3. Pruett RC. Retinitis pigmentosa: clinical observations and correlations. Trans Am Ophthalmol Soc 1983;81:693–735. 4. Bastek JV, Heckenlively JR, Straatsma BR. Cataract surgery in retinitis pigmentosa patients. Ophthalmology 1982;89: 880–4.
5. Jackson H, Garway-Heath D, Rosen P, et al. Outcome of cataract surgery in patients with retinitis pigmentosa. Br J Ophthalmol 2001;85:936–8. 6. Dikopf MS, Chow CC, Mieler WF, Tu EY. Cataract extraction outcomes and the prevalence of zonular insufficiency in retinitis pigmentosa. Am J Ophthalmol 2013;156:82–88 e2. 7. Fishman GA, Anderson RJ, Lourenco P. Prevalence of posterior subcapsular lens opacities in patients with retinitis pigmentosa. Br J Ophthalmol 1985;69:263–6. 8. Auffarth GU, Nimsgern C, Tetz MR, et al. [Increased cataract rate and characteristics of Nd:YAG laser capsulotomy in retinitis pigmentosa]. Ophthalmologe 1997;94:791–5. 9. Heckenlively J. The frequency of posterior subcapsular cataract in the hereditary retinal degenerations. Am J Ophthalmol 1982;93:733–8. 10. Bayyoud T, Bartz-Schmidt KU, Yoeruek E. Long-term clinical results after cataract surgery with and without capsular tension ring in patients with retinitis pigmentosa: a retrospective study. BMJ Open 2013;3:e002616. 11. Abe K, Iijima H, Hirakawa H, et al. Visual acuity and 10 degrees automated static perimetry in eyes with retinitis pigmentosa. Jpn J Ophthalmol 2002;46:581–5. 12. Oishi A, Otani A, Sasahara M, et al. Photoreceptor integrity and visual acuity in cystoid macular oedema associated with retinitis pigmentosa. Eye (Lond) 2009;23:1411–6. 13. Ko TH, Fujimoto JG, Duker JS, et al. Comparison of ultrahigh- and standard-resolution optical coherence tomography for imaging macular hole pathology and repair. Ophthalmology 2004;111:2033–43. 14. Spaide RF, Curcio CA. Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina 2011;31:1609–19. 15. Aizawa S, Mitamura Y, Baba T, et al. Correlation between visual function and photoreceptor inner/outer segment junction in patients with retinitis pigmentosa. Eye (Lond) 2009;23: 304–8. 16. Elgohary MA, Beckingsale AB. Effect of posterior capsular opacification on visual function in patients with monofocal and multifocal intraocular lenses. Eye (Lond) 2008;22:613–9. 17. Iijima H. Correlation between visual sensitivity loss and years affected for eyes with retinitis pigmentosa. Jpn J Ophthalmol 2012;56:224–9. 18. Inoue M, Morita S, Watanabe Y, et al. Inner segment/outer segment junction assessed by spectral-domain optical coherence tomography in patients with idiopathic epiretinal membrane. Am J Ophthalmol 2010;150:834–9. 19. Itoh Y, Inoue M, Rii T, et al. Correlation between length of foveal cone outer segment tips line defect and visual acuity after macular hole closure. Ophthalmology 2012;119:1438–46. 20. Grigoropoulos VG, Emfietzoglou J, Nikolaidis P, et al. Optical coherence tomography findings in patients with retinitis pigmentosa and low visual acuity. Ophthalmic Surg Lasers Imaging 2010;41:35–9. 21. Hagiwara A, Yamamoto S, Ogata K, et al. Macular abnormalities in patients with retinitis pigmentosa: prevalence on OCT examination and outcomes of vitreoretinal surgery. Acta Ophthalmol 2011;89:e122–5. 22. Ikeda Y, Yoshida N, Notomi S, et al. Therapeutic effect of prolonged treatment with topical dorzolamide for cystoid macular oedema in patients with retinitis pigmentosa. Br J Ophthalmol 2013;97:1187–91. 23. Ikeda Y, Hisatomi T, Yoshida N, et al. The clinical efficacy of a topical dorzolamide in the management of cystoid macular edema in patients with retinitis pigmentosa. Graefes Arch Clin Exp Ophthalmol 2012;250:809–14.
5
Ophthalmology Volume -, Number -, Month 2015 24. Apushkin MA, Fishman GA, Janowicz MJ. Monitoring cystoid macular edema by optical coherence tomography in patients with retinitis pigmentosa. Ophthalmology 2004;111:1899–904. 25. Hirakawa H, Iijima H, Gohdo T, Tsukahara S. Optical coherence tomography of cystoid macular edema associated with retinitis pigmentosa. Am J Ophthalmol 1999;128:185–91. 26. Hajali M, Fishman GA, Anderson RJ. The prevalence of cystoid macular oedema in retinitis pigmentosa patients determined by optical coherence tomography. Br J Ophthalmol 2008;92:1065–8. 27. Hollick EJ, Spalton DJ, Ursell PG, Pande MV. Lens epithelial cell regression on the posterior capsule with different intraocular lens materials. Br J Ophthalmol 1998;82:1182–8. 28. Trivedi RH, Werner L, Apple DJ, et al. Post cataractintraocular lens (IOL) surgery opacification. Eye (Lond) 2002;16:217–41. 29. Findl O, Buehl W, Menapace R, et al. Comparison of 4 methods for quantifying posterior capsule opacification. J Cataract Refract Surg 2003;29:106–11. 30. Bender L, Spalton DJ, Uyanonvara B, et al. POCOman: new system for quantifying posterior capsule opacification. J Cataract Refract Surg 2004;30:2058–63.
31. Gupta P, Zheng Y, Ting TW, et al. Prevalence of cataract surgery and visual outcomes in Indian immigrants in Singapore: the Singapore Indian eye study. PLoS One 2013;8: e75584. 32. Huang W, Huang G, Wang D, et al. Outcomes of cataract surgery in urban southern China: the Liwan Eye Study. Invest Ophthalmol Vis Sci 2011;52:16–20. 33. Lavanya R, Wong TY, Aung T, et al. Prevalence of cataract surgery and post-surgical visual outcomes in an urban Asian population: the Singapore Malay Eye Study. Br J Ophthalmol 2009;93:299–304. 34. Nishi O, Nishi K, Fujiwara T, et al. Effects of the cytokines on the proliferation of and collagen synthesis by human cataract lens epithelial cells. Br J Ophthalmol 1996;80:63–8. 35. Yoshida N, Ikeda Y, Notomi S, et al. Clinical evidence of sustained chronic inflammatory reaction in retinitis pigmentosa. Ophthalmology 2013;120:100–5. 36. Hayashi K, Hayashi H, Matsuo K, et al. Anterior capsule contraction and intraocular lens dislocation after implant surgery in eyes with retinitis pigmentosa. Ophthalmology 1998;105:1239–43.
Footnotes and Financial Disclosures Originally received: July 24, 2014. Final revision: December 3, 2014. Accepted: December 4, 2014. Available online: ---.
Manuscript no. 2014-1170.
1
Department of Ophthalmology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
2
Department of Ophthalmology, Akita University Graduate School of Medicine, Akita, Japan. Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article. Supported in part by a Grant-in-Aid (to Y.I.) from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (grant no. 24659763).
6
Abbreviations and Acronyms: BCVA ¼ best-corrected visual acuity; CME ¼ cystoid macular edema; dB ¼ decibels; EZ ¼ ellipsoid zone; HFA ¼ Humphrey Field Analyzer; IOL ¼ intraocular lens; logMAR ¼ logarithm of the minimum angle of resolution; MD ¼ mean deviation; OCT ¼ optical coherence tomography; PCO ¼ posterior capsular opacification; PSC ¼ posterior subcapsular cataract; RP ¼ retinitis pigmentosa. Correspondence: Yasuhiro Ikeda, MD, PhD, Department of Ophthalmology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan. E-mail: [email protected].