Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science Prevalence and predictors of metamorphopsia after successful rhegmatogenous retinal detachment surgery: a cross-sectional, comparative study Chuandi Zhou,1 Qiurong Lin,2 Fenge Chen2

1Department of Ophthalmology, ABSTRACT metamorphopsia. In another study, which consisted Ninth People’s Hospital of Aims To evaluate the prevalence of metamorphopsia of 129 RRD patients, 50 (38.76%) cases had meta- Shanghai, Shanghai Jiaotong after successful rhegmatogenous retinal detachment morphopsia after a 6–12-month follow-up.3 For University, Shanghai, China 2Department of Ophthalmology, (RRD) surgery and determine the independent predictors studies that only included macula-off cases, the inci- First People’s Hospital of of metamorphopsia. dence of metamorphopsia was much higher, varying – Shanghai, Shanghai Jiaotong Methods A cross-sectional, comparative study. The from 66.7% to 88.6%.4 7 However, these studies University, Shanghai, China study included 380 eyes of 357 patients who underwent had relatively small sample sizes and short follow-up a successful RRD surgery between 2009 and 2015. The periods. Therefore, they might not capture the true Correspondence to presence of metamorphopsia was tested with an Amsler characteristics of the entire RRD population. Dr Fenge Chen, Department of Ophthalmology, First People’s grid and the foveal microstructure was scanned with The pathophysiology of metamorphopsia is not Hospital of Shanghai, Shanghai high-resolution spectral-domain optical coherence completely understood.38It was generally believed Jiaotong University, 100 tomography (OCT) at a follow-up visit. Medical records to be a symptom of retinal distortion from intrinsic Haining Road, Hongkou District, were reviewed for preoperative and intraoperative factors retinal disease because of poor orientation of photo- Shanghai 200080, China; 9 [email protected] associated with postoperative visual recovery. receptors. Optical coherence tomography (OCT) Results The mean follow-up period was 35.1 has been widely used to detect the abnormal micro- Received 25 May 2016 ±19.6 months. The prevalence of metamorphopsia in structures in relation to metamorphopsia after Revised 22 August 2016 our study was 46.58% (177/380), whereas in macula- RRD surgeries. Dell’Omo et al8 demonstrated that Accepted 28 August 2016 the presence of outer retinal folds was an inde- Published Online First off cases this number increased to 56.69% (144/254). 15 September 2016 Stepwise logistic regression analysis indicated that pendent predictor for metamorphopsia. However, younger age at the diagnosis (OR=0.97, p<0.01), the pathophysiology of metamorphopsia is multifac- preoperative macula-off status (OR=3.34, p<0.01), torial, and their study only included the independ- postoperative presence of subretinal fluid (SRF) ent variables of OCT findings, which had limited (OR=3.58, p=0.01) and disrupted external limiting explanatory effects. Other factors not included in membrane (ELM) junction (OR=1.79, p=0.02) were the that study should also be considered, such as demo- independent predictors for metamorphopsia after graphic and baseline clinical characteristics. surgery. The abnormal foveal microstructures after The purpose of this cross-sectional, comparative successful surgeries mainly included six types: disrupted study was to determine the prevalence of metamor- inner segment/outer segment (133 eyes, 35.00%), phopsia after RRD surgery, and its possible disrupted ELM (131 eyes, 34.47%), predictors. (44 eyes, 11.58%), SRF (26 eyes, 6.84%), macular hole (9 eyes, 2.37%) and cystoid macular oedema (6 eyes, METHODS 1.58%). Patients Conclusions Considering metamorphopsia, special The medical records of patients operated for RRDs attention should be paid to young patients and/or the by one surgeon (FC) were reviewed (1006 pat- cases with involvement of macula. High-resolution OCT ients). These patients were admitted to the First is informative in detecting anatomic abnormalities after People’s Hospital of Shanghai from January 2009 RRD surgery. The postoperative presence of SRF and to April 2015. Chart review yielded 678 consecu- disrupted ELM line are independent predictors of tive eyes that had RRDs, which either underwent metamorphopsia. vitrectomy or scleral buckling or a combination of both. The exclusion criteria were (1) prolifera- tive vitreoretinopathy (PVR) worse than grade INTRODUCTION C. Because, first, very few patients had funnel- The success rate of the surgical repair of rhegmato- shaped RRD, and second, the extremely poor post- genous retinal detachment (RRD) is now up to operative limited the use of an Amsler 90%.1 However, anatomic reattachment of the grid to test of the presence of metamorphopsia; does not always mean recovery of visual (2) other severe vision-impaired eye diseases (eg, function. Metamorphopsia is one of the most uveitis, glaucoma or trauma), especially involving common postoperative complaints. the macula (eg, macula hole, epiretinal membrane Reports are emerging in the literature about meta- (ERM), cystoid macula oedema (CMO), age-related morphopsia after successful RRD surgery. The con- or any signs of discontinuity clusions, however, are varied. Amemiya et al2 in photoreceptor inner and outer segment junction To cite: Zhou C, Lin Q, conducted a study among 299 patients with RRD, (IS/OS) or external limiting membrane (ELM) in Chen F. Br J Ophthalmol and all of them underwent scleral buckling and 93 the initial OCT test); and (3) the follow-up period 2017;101:725–729. (31.10%) patients experienced persistent <6 months. We contacted all patients who met the

Zhou C, et al. Br J Ophthalmol 2017;101:725–729. doi:10.1136/bjophthalmol-2016-309097 725 Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science

inclusion criteria and explained the purpose of the study, and each eye using analysis software V.5.1.3. In selected cases, verti- they participated in this study voluntarily without any additional cal or oblique scans were obtained to better evaluate the compensation. Of the 588 patients who met the inclusion cri- observed abnormalities. Two doctors (CZ, QL) assessed the teria, 88 patients were not reached, and 71 declined to partici- integrity of IS/OS and ELM. Diagnosis of a disrupted line was pate in this study for other reasons, such as geographic or time made based on loss and irregularity of the hyper-reflective line limitations. Of the 429 subjects who agreed to return for the of the IS/OS or ELM junction. The consistency between the follow-up visit, 26 patients were excluded for the re-detachment results from the two graders was 98.42%. A third grader, who of the retina, and 46 patients were excluded from the analysis was not involved in the above assessment, was asked to deliber- because of incomplete data collection (eg, the unsatisfied quality ate discrepancies. All of the graders were masked to the clinical of OCT caused by media opacity), leaving a final sample of 380 outcomes of the patients. Abnormal macula structures, for eyes of 357 patients. example, ERM, subretinal fluid (SRF), macula hole and CMO, were also documented. Data collection Informed consent was obtained from all patients at the Statistical analysis follow-up visit. This study adhered to the tenets of the BCVA was converted to the logarithm of the minimum angle of Declaration of Helsinki and was approved by the Shanghai resolution (logMAR). Counting fingers, hand motion and light Jiaotong University research ethics committee. perception were assigned the logMAR units of 2.1, 2.4 and 2.7, Age, gender, refractive status, number of quadrants involved respectively. The data were analysed using SAS software (V.9.2, in retinal detachment (RD), grade of PVR, preoperative and SAS Institute, Cary, North Carolina, USA) and were reported as postoperative best-corrected visual acuity (BCVA), surgical the mean±SD or n (%). Univariate analyses, either Student’s 2 approaches, baseline macula status tested by OCT, refractive t-test (continuous factors) or a χ test (categorical factors), were error and tamponade types were collected by chart review. At used to identify the possible correlates of metamorphopsia. the follow-up, the of all patients were examined by the When evaluating the impact of different surgical approaches on same surgeon (FC) with slit-lamp biomicroscopy through metamorphopsia, 32 eyes were excluded because they received dilated pupil. BCVA was tested using the Snellen visual acuity multiple types of surgery. Then, the significant factors were chart. In addition, each patient was questioned about the pres- entered into a stepwise logistic regression model as independent ence of metamorphopsia with an . If present, the variables to explore the independent predictors for metamor- patients were asked to show the examiner the location of phopsia. All tests were two sided, and a p value <0.05 was con- the distorted lines on the grid. No quantitative assessment of sidered statistically significant. the metamorphopsia was performed. Images were acquired with Spectralis OCT (Heidelberg RESULTS Engineering, Heidelberg, Germany) at the same follow-up visit. A total of 380 eyes of 357 patients were included in this study, We performed five horizontal and five vertical raster scans for among whom 222 patients (62.18%) were male and 135

Table 1 Demographic and baseline clinical characteristics Total Metamorphopsia (+) Metamorphopsia (−) p Value

Gender 0.71 Male 241 114 127 Female 139 63 76 Age 46.4 43.9 48.5 <0. 01* Duration of symptoms (days) 52.1 73.8 33.3 0.02* Number of quadrants involved 2.1 2.3 1.9 <0. 01* Proliferative vitreoretinopathy 0.03* A 35 13 22 B 309 140 169 C 36 24 12 Macular status <0. 01* On 126 33 93 Off 254 144 110 Preoperative spheroequivalent refraction (dioptre) −4.8 −4.9 −4.6 0.53 Baseline logarithm of the minimum angle of resolution best-corrected visual acuity 1.4 1.6 1.3 <0. 01* Surgical approach 0.27 Vitrectomy 241 104 137 Scleral buckling 107 53 54 Tamponade type 0.45 Gas 163 71 92 Silicone oil 110 53 57 Primary/recurrent retinal detachment 0.33 Primary retinal detachment 351 161 190 Recurrent retinal detachment 29 16 13 *Statistically significant.

726 Zhou C, et al. Br J Ophthalmol 2017;101:725–729. doi:10.1136/bjophthalmol-2016-309097 Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science

Table 2 Univariate analyses of anatomic and visual outcomes at the follow-up visit for patients with and without metamorphopsia Total Metamorphopsia (+) Metamorphopsia (−) p Value

Follow-up period (months) 35.1 34.7 35.4 0.72 Final logMAR BCVA 0.5 0.6 0.5 <0.01* Changes in logMAR BCVA 0.9 1.0 0.8 <0.01* With disrupted inner segment/outer segment junction 133 77 56 <0.01* With disrupted external limiting membrane 131 79 52 <0.01* With epiretinal membrane 44 25 19 0.15 With subretinal fluid 26 20 6 <0.01* With macular hole 9 9 0 <0.01* With cystoid macular oedema 6 3 3 1.00 *Statistically significant. BCVA, best-corrected visual acuity; logMAR, logarithm of the minimum angle of resolution.

(37.82%) were female. The age of our patients ranged from trend of worsening visual acuity with increasing prevalence of 9 years to 79 years, with an average age of 46.4±16.4 years. metamorphopsia after RRD surgery except for the patients The age distribution had two peaks, one at 20–22 years and with BCVA <0.1. The OCT findings also indicated that the eyes another at 53–61 years. The follow-up period ranged from 6 with metamorphopsia were more likely to have disrupted IS/OS to 81 months, with a mean time of 35.1±19.6 months. A total (p<0.01) and ELM (p<0.01) than those without this symptom of 177 eyes (46.58%) presented with metamorphopsia. (figure 2). Apart from this, the abnormal foveal microstructures Demographic and baseline clinical characteristics were com- after successful surgeries mainly included four types: ERM (44 pared between the eyes with and without metamorphopsia, and eyes, 11.58%), SRF (26 eyes, 6.84%), macula hole (9 eyes, the results are summarised in table 1. The two groups had sig- 2.37%) and CMO (6 eyes, 1.58%). Notably, patients with meta- nificant differences in age (p<0.01), duration of symptoms morphopsia had more cases of SRF (p<0.01) and macula hole (p=0.02), number of quadrants involved (p<0.01), grade of (p<0.01) than those without this symptom. PVR (p=0.03), macula status (p<0.01) and baseline logMAR To determine the independent risk factors of metamorphopsia BCVA (p<0.01). However, no statistical significance was found after successful RRD surgery, stepwise multivariate logistic regres- with regard to gender, preoperative spheroequivalent refraction, sion was used. The independent variables included all significant surgical approach, tamponade type and distribution of primary baseline demographic and clinical indices, and OCT findings at or recurrent RD. the follow-up visit. The results indicated that younger age at the The anatomic and visual outcomes at the follow-up for both diagnosis (OR=0.97, p<0.01), preoperative macula-off status groups are summarised in table 2. Eyes without metamorphop- (OR=3.34, p<0.01), disrupted ELM junction (OR=1.79, sia had significantly better final BCVA than those with com- p=0.02) and presence of SRF (OR=3.58, p=0.01) were the inde- plaints of metamorphopsia (p<0.01). Figure 1 shows the pendent predictors for metamorphopsia after surgery (table 3). association between postoperative BCVA and the prevalence of metamorphopsia after RRD surgery. It revealed a clear DISCUSSION The results of this cross-sectional, comparative study indicated that the prevalence of metamorphopsia in our study was 46.58%. Younger age at the diagnoses, preoperative macula-off status, disrupted ELM junction and the presence of SRF were the independent predictors of metamorphopsia after surgery. Early in the 1980s, Amemiya et al2 administered a question- naire about postoperative visual disturbances to 299 RRD patients who underwent scleral buckling. Metamorphopsia was present in 31.10% of them. Okamoto et al3 conducted a pro- spective study among 129 patients who had repaired RRD by either vitrectomy or scleral buckling. Fifty patients (38.76%) had metamorphopsia, which was quantified by M-CHARTS. In another prospective study of 33 patients who had RRDs after vitrectomy, 22 patients (66.67%) presented with metamorphop- sia.8 The prevalence of metamorphopsia in our study was 46.58%, which is at a moderate level when compared with the results from other countries. Many studies have specifically ana- lysed metamorphopsia among RRD patients with involvement of the macula. van de Put et al4 prospectively followed up 45 patients with macula-off RRDs, and metamorphopsia was present in 39 patients (86.67%). In another study, a total of 46 eyes with macula-off RRDs were prospectively studied. Figure 1 The association between postoperative best-corrected visual Thirty-one patients (66.67%) had metamorphopsia 2 months acuity and the prevalence of metamorphopsia after rhegmatogenous after successful scleral buckling surgery.5 In another series con- retinal detachment surgery. sisting of six eyes with macula-off RRDs, all patients presented

Zhou C, et al. Br J Ophthalmol 2017;101:725–729. doi:10.1136/bjophthalmol-2016-309097 727 Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science

Table 3 Multivariate logistic regressions of predictors for metamorphopsia after a successful rhegmatogenous retinal detachment surgery B OR 95% CI for OR p Value

Age (years) −0.03 0.97 0.96 to 0.99 <0.01* Macular status (off vs on) 1.21 3.34 1.98 to 5.64 <0.01* Disrupted external limiting 0.58 1.79 1.10 to 2.92 0.02* membrane (yes vs no) Subretinal fluid (yes vs no) 1.28 3.58 1.33 to 9.69 0.01* *Statistically significant.

van de Put’s study, the patients either underwent vitrectomy or scleral buckling. Moreover, the age distributions of the patients differed greatly among the studies. Notably, our research covered a broader age span (9–79 years). Additionally, other var- iances may relate to the different measures to test metamor- phopsia, multiple surgeons with diverse experiences, dissimilar patient selection criteria and varied follow-up periods. Macula involvement is a strong established risk factor for poorer anatomic and visual success in RRD.10 11 Our findings also validated this point. However, in our series, 33 eyes with macula-sparing RRDs also had metamorphopsia after surgery. Clinically detectable pathologic changes indicated by post- operative OCT among these 33 eyes included ERM in three eyes, macula hole in two eyes and persistent SRF in one eye. Assuming that the above-abnormal foveal structures contributed to metamorphopsia, however, in the remaining 27 eyes with Figure 2 Three representative patterns of the photoreceptor inner and normal-appearing OCT examinations, metamorphopsia still per- outer segment junction (IS/OS) or external limiting membrane (ELM) indicated by optical coherence tomography (OCT) after macula-off sisted over time. This fact suggested that there might be other rhegmatogenous retinal detachment (RRD) surgery. (A) The OCT image factors involved in the origin of metamorphopsia in RD than of a 31-year-old man 12 months after vitrectomy. The IS/OS and ELM those detected by OCT. In these 27 eyes, 16 underwent scleral are intact in the macula. He does not experience metamorphopsia after buckling, 10 had vitrectomy (eight eyes were with gas tampon- surgery. The baseline and final best-corrected visual acuity (BCVA) are ade and two eyes were with silicone oil tamponade) and one finger counting (FC) and 12/20, respectively. (B) The OCT image of a received scleral buckling combined with vitrectomy and gas 58-year-old woman of RRD 13 months after vitrectomy. The ELM line is injection. Nevertheless, during the scleral buckling surgery for preserved, but the IS/OS is disrupted. She does not suffer from macula-sparing RRD, if SRF was dense or in a non-drainage fi metamorphopsia. The baseline and nal BCVA are light perception and procedure,12 then the above conditions can promote a tempor- 2/20, respectively. (C) The OCT image of a 27-year-old woman of RRD ary macula-off detachment as a result of displacement of fluid 7 months after scleral buckling. The IS/OS and ELM are all discontinued 13 in the macula. She reported the symptom of metamorphopsia. The from the periphery towards the centre. In vitrectomy, it is baseline and final BCVA are FC and 2/20, respectively. often the case that there is a certain amount of SRF remaining between the break and the posterior pole at the end of the air– fluid exchange. The residual SRF could also shift to the macula with metamorphopsia, which faded with time but persisted in and lead to macula detachment. Moreover, the intraocular four eyes (66.67%) at 5 years to 6 years after scleral buckling.6 tamponade, especially gas, could cause retinal slippage after Similarly, in a study7 that included seven eyes with macula-off surgery.14 However, further researches facilitated by surgical RRDs, during the postoperative period all seven patients video and fundus autofluorescence14 are still needed to fully vali- showed metamorphopsia of varying degrees. And this symptom date our assumptions. remained in five eyes (71.43%) at 18–27 months after scleral In our study, OCT detected SRF in 26 eyes (6.84%), and buckling surgery. From our observations, in the 254 eyes with among them, 20 eyes had persistent metamorphopsia. Likewise, macula-off RRDs, 144 eyes (56.69%) had metamorphopsia after previous studies demonstrated that SRF in the macula persist- a mean follow-up period of 33.94 months. The prevalence of ence up to 6 months was significantly associated with poor func- metamorphopsia in macula-off cases in our study compared tional recovery after macula-off RD surgery.615Persistent SRF favourably with the results from other studies. Potential expla- could cause long-standing separation of the macula photorecep- nations for this discrepancy may lie in the following aspects. tors and retinal pigment epithelium (RPE), and subsequently First, the sample sizes differed greatly (our study included 254 impair metabolic function of the photoreceptor–RPE eyes and the other studies included 6–46 eyes). However, small complex.16 Therefore, the persistent SRF could compromise sample sizes might be unable to capture the true characteristics visual recovery after RRD surgery. of an RRD population. Second, the surgical approaches were On the basis of our findings, the disrupted ELM could dissimilar. In our study, patients either underwent vitrectomy or increase the chances of metamorphopsia after successful RRD scleral buckling or a combination of both. Most of the other surgery. In parallel with our findings, Wakabayashi et al17 studies had only scleral buckling to repair the RRD. Only in the observed that the IS/OS junction was restored in 7 (63.64%) of

728 Zhou C, et al. Br J Ophthalmol 2017;101:725–729. doi:10.1136/bjophthalmol-2016-309097 Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science the 11 eyes with a disrupted IS/OS junction and an intact ELM metamorphopsia. Nevertheless, a large, prospective, randomised at the initial examination. However, none of the five eyes with trial is needed to fully validate our findings. both a disrupted IS/OS junction and ELM had complete restor- ation of the photoreceptor microstructure. Therefore, they con- Contributors CZ, FC and QL designed the study. CZ, FC and QL undertook the sample and data collection. CZ was responsible for the data analysis and drafting of cluded that preservation of the ELM postoperatively might the manuscript. All authors helped interpret data and critically revise drafts of the predict subsequent restoration of the photoreceptor layer. The manuscript. They have had full access to the data on which the study was based. All reflection of the IS/OS junction represents the boundary authors believe that the manuscript represents valid work. They have reviewed the fi between the IS structures and the highly organised OS, and the nal version of the submitted manuscript and have approved it for publication. reflection of ELM signifies the border between the outermost Competing interests None declared. limit of the outer nuclear layer consisting of photoreceptor cell Patient consent Obtained. bodies and the photoreceptor IS myoid portion. At the fovea, Ethics approval Shanghai Jiaotong University Institutional Review Board. histopathologic research showed that the IS consists of an Provenance and peer review Not commissioned; externally peer reviewed. inverted Müller cell cone, the truncated apex of which was at the ELM.18 Therefore, a disrupted IS/OS junction with an intact ELM presumably indicated that the morphologic changes in the REFERENCES photoreceptor layer were limited to the photoreceptor IS/OS 1 Kobashi H, Takano M, Yanagita T, et al. Scleral buckling and pars plana vitrectomy level and did not extend to the cell bodies. This led us to specu- for rhegmatogenous retinal detachment: an analysis of 542 eyes. Curr Eye Res 2014;39:204–11. late that restoration of the photoreceptor layer can occur in 2 Amemiya T, Iida Y, Yoshida H. 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Prevalence and predictors of metamorphopsia after successful rhegmatogenous retinal detachment surgery: a cross-sectional, comparative study Chuandi Zhou, Qiurong Lin and Fenge Chen

Br J Ophthalmol 2017 101: 725-729 originally published online September 15, 2016 doi: 10.1136/bjophthalmol-2016-309097

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