Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science Long-term functional results following vitrectomy for advanced retinopathy of prematurity Murat Karacorlu, Mumin Hocaoglu, Isil Sayman Muslubas, Serra Arf

Istanbul Retina Institute, ABSTRACT treated in a consistent manner, and were Istanbul, Turkey Purpose To assess long-term functional results after followed-up closely postoperatively to enable early vitrectomy for stages 4 and 5 retinopathy of prematurity intervention. We aimed to perform a meticulous Correspondence to (ROP). assessment of visual function by using a standard Professor Murat Karacorlu, İstanbul RETINA Enstitüsü, Methods Retrospective analysis of data from eyes that protocol and to investigate whether such an orga- Hakkı Yeten Cad. Unimed underwent lens-sparing vitrectomy (LSV) or combined nised attempt at appropriate diagnosis, a current Center No: 19/7, Fulya—Şişli, lensectomy and vitrectomy (LV) and had a follow-up of surgical approach, and postoperative management Istanbul 34349, Turkey; at least 5 years. could yield visual results in the long-term. [email protected] Results Eighty-eight eyes of 65 infants who underwent Received 16 June 2016 LSV or LV for stage 4 or 5 ROP were included in the METHODS Revised 13 July 2016 study. The mean follow-up was 6.9 years. The anatomic We retrospectively reviewed the records of infants Accepted 24 August 2016 success rate was 89% (17/19) for stage 4A, 63% (24/38) with stage 4 and 5 ROP who underwent vitrectomy Published Online First for stage 4B, and 42% (13/31) for stage 5. Forty-five eyes 15 September 2016 between January 1996 and December 2010 per- (51%) had measurable visual acuity (VA). The formed by a single surgeon (MK) at a tertiary refer- approximate Snellen VA equivalent was 20/550 for stage ral centre. Detailed informed consent was taken 4A, 20/1600 for stage 4B, and 20/4000 for stage 5. The from the parents before each surgical procedure. The remaining 39% (34/88) had light perception or no light study protocol was approved by the Institutional perception. Owing to neurological conditions, VA in nine Review Board of Sisli Memorial Hospital, Istanbul. eyes (10%) could not be measured. Anatomic and visual The study was in accordance with the principles of outcomes were not associated with surgical technique. the Declaration of Helsinki. Conclusions Surgery for stage 4A ROP has better visual The clinical charts were retrospectively reviewed success. Acceptable vision for stage 4B and poor for to collect the following data: birth weight, gesta- stage 5 ROP, despite retinal reattachment, is thought to tional age, sex, clinical characteristics of the ROP, be secondary to irreversible injury to either the retina or timing of surgery, intraoperative procedures, post- visual nervous pathways, or both. operative complications, follow-up duration, ana- tomic status, and visual acuity (VA) at the final visit. Patients who had been lost to follow-up and those INTRODUCTION with insufficient medical records were excluded. Retinopathy of prematurity (ROP) is a complex All the infants were examined preoperatively condition characterised by onset of vascular abnor- with indirect ophthalmoscopy, and B-mode orbital malities in the developing retina, a major cause of ultrasonography was performed by an experienced visual impairment and blindness in premature radiologist if indicated. neonates. Screening and treatment guidelines established Surgical procedures by the Cryotherapy for ROP and Early Treatment All patients underwent 3-port vitrectomy through a for Retinopathy (ETROP) studies have reduced the pars plicata approach, with or without lensect- rates of stage 4 and 5 ROP and its resultant visual omy.815After lateral canthotomy and a standard loss.12Despite early treatment of high-risk cases, conjunctival opening, a 2.5 mm, 20-gauge infusion unfortunately 12% of the eyes progress to stage 4 cannula was placed 1 mm posterior to the limbus or 5 ROP and need surgical repair.2 Open-sky (ie, through the pars plicata) in the inferotemporal vitrectomy,3 scleral buckling,45lensectomy and quadrant. Additional sclerotomies were made at the vitrectomy (LV) with or without scleral buckling,67 10 and 2 o’clock positions, either limbal or 1 mm and lens-sparing vitrectomy (LSV)8 are the surgical posterior to the limbus. A lensectomy was per- techniques that have been used for the management formed if the lens was found to impede adequate of retinal detachments associated with ROP. management of anterior-posterior traction, or if Some studies have reported anatomic outcomes there was limiting intraoperative visualisation. after vitreoretinal surgery for stage 4 and stage 5 Vitreous and membranes were removed, and – ROP.3 8 However, anatomic success may not equate anterior-posterior and circumferential tractions to functional success, and few studies have focused were released using the Associate 2500 vitrectomy – on assessing functional outcomes.9 17 Most of system (DORC, Zuidland, Netherlands). For visual- these publications are limited by small sample size, isation of the residual vitreous and posterior surgery performed by multiple surgeons, a short hyaloid membrane, after removal of the anterior To cite: Karacorlu M, – Hocaoglu M, Sayman follow-up period, and reporting bias. and core vitreous, 0.2 0.3 mL (40 mg/mL) triamci- Muslubas I, et al. This study describes a retrospectively analysed nolone acetonide aqueous suspension was injected Br J Ophthalmol series of patients with stages 4 and 5 ROP treated into the mid-vitreous cavity, followed by partial or 2017;101:730–734. by single surgeon in Turkey. All the children were complete removal of the posterior hyaloid. Other

730 Karacorlu M, et al. Br J Ophthalmol 2017;101:730–734. doi:10.1136/bjophthalmol-2016-309198 Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com Clinical science

surgical procedures included retrolental membrane dissection, between initial laser and surgery was 6.5±4.8 weeks. The mean epiretinal membrane delamination, forceps membrane peeling, follow-up period was 6.9±1.9 years. Of the 88 eyes, 51 (58%) fluid-air exchange, and fluid-gas exchange. No intravitreal anti- had received prior retinal ablative treatment. vascular endothelial growth factor (anti-VEGF) was given pre- LSV was performed on 39 eyes (44%) and combined LV was operatively or intraoperatively. The parents were advised to use performed on 49 eyes (56%) (table 2). Six eyes after LSV (4 a topical antibiotic and corticosteroid drops four times a day for stage 4A and 2 stage 4B) and one after LV (stage 5) required 1 month during the postoperative period. reoperation (mean 9 weeks later) due to vitreous haemorrhage or reproliferation. Favourable anatomic and visual outcomes Follow-up examination were achieved in only two (stage 4A) of these seven eyes despite All the infants were routinely examined on day 1 after surgery, the second surgical procedure. There were no significant differ- then 1 week, 1 month, and every 3 months for a year, and then ences in anatomic success between LSV and LV for stage 4A yearly. All the patients were closely followed up in our institu- (93% vs 75%, p=0.39) or for stage 4B (67% vs 57%, p=0.35). tion and were referred to a paediatric ophthalmologist for com- Forty-five eyes (51%) had measurable VA at the final visit and prehensive postoperative visual rehabilitation. Ametropic and 34 (39%) had vision of LP or no LP (NLP). Owing to various anisometropic amblyopia were managed by correction with neurological conditions, VA could not be measured in nine eyes contact lenses or spectacles and subsequent eye patching. (10%) that had the ability to fix and follow. Table 3 summarises VA measurements were performed using the Tumbling E or the long-term visual results after vitrectomy for stages 4 and 5 Early Treatment Diabetic Retinopathy Study (ETDRS) charts. ROP. Following a standardised protocol, the ETDRS charts were used Of the 11 eyes (58% of all stage 4A eyes) for which a VA with a maximum distance of 4 m, but the distance was reduced could be measured, 42% (8/19) had VA of 20/200 or better, and to 1 m or to 0.5 m if needed to permit letter identification in an 16% (3/19) had ambulatory VA of 20/2000 or better. Of the 22 eye with poor vision.18 In some patients, VA testing was not per- eyes (58% of all stage 4B eyes) for which a VA could be mea- formed because of developmental limitations (the chart-measured sured, seven (32%) had VA of 20/400 or better. The mean vision as ‘fixes and follows’ or ‘central-steady-maintained’)orif approximate Snellen VA equivalent of the 11 eyes that under- both eyes had vision of light perception (LP) or worse. went surgery for stage 5 ROP and had measurable VA (35% of Anatomic success was defined as complete retinal attachment all stage 5 eyes) was 20/4000 (range 20/2000–20/20 000). for stage 4A ROP,partial retinal detachment for stage 4B, and at The visual outcomes of stage 4A were better than those of least posterior pole attachment for stage 5. stage 5 ROP (p=0.001). Earlier retinal ablation was associated Data were analysed using the Kruskal-Wallis test, Pearson with better visual results for stage 4B ROP (p=0.04). There was χ2 test, Fisher’s exact test, Mann-Whitney test, and Spearman’s no statistically significant difference in the visual results between rank correlation depending on the variables. A value of p<0.05 LSV and LV for stage 4B (p=0.39), but numbers were too small was considered statistically significant. Statistical analyses used to allow statistical comparison for stage 4A. SPSS V.20.0(SPSS, Inc, Chicago, Illinois, USA). Glaucoma occurred most often in aphakic eyes (92%, 11/12), and was controlled with topical ocular hypotensive agents. One RESULTS patient underwent glaucoma surgery. Table 4 summarises the Of the 136 patients who underwent vitrectomy for stage 4A, 4B long-term postoperative complications after vitrectomy for or 5 ROP whose charts were reviewed, 88 eyes of 65 patients stages 4 and 5 ROP. who had been followed up for at least 5 years were included (table 1). DISCUSSION None of these patients had previously undergone intravitreal While 51% of eyes with stage 4A (63%), stage 4B (58%), and anti-VEGF injection or a scleral buckle procedure. Of the 65 stage 5 (35%) had measurable VA, the remaining 49% had no infants included, 34 were male (52%). Overall, the mean±SD functional vision or exhibited behaviour consistent with form gestational age at birth was 28.4±2.3 weeks, mean±SD birth vision, but had developmental comorbidity precluding measure- weight was 1212±355 g, mean±SD postconceptional age at the ment of VA. Of the eyes with measurable VA following LSV or time of surgery was 43.1±6.2 weeks, and mean±SD interval LV for stage 4A ROP, 42% (8/19) had VA of 20/200 or better

Table 1 Baseline characteristics of the infants who underwent vitrectomy for stage 4 or 5 retinopathy of prematurity Stage 4A Stage 4B Stage 5 Characteristics n=19 n=38 n=31

Sex male/female, % 63/37 55/45 36/64 Mean±SD gestational age, weeks 28.0±1.7 28.5±2.5 28.7±2.3 Mean±SD birth weight, g 1202±331 1180±412 1257±293 History of cryotherapy, n (%) 1 (5) 1 (2) 1 (3) History of laser photocoagulation, n (%) 14 (74) 27 (71) 17 (55) Mean±SD time of retinal ablation, weeks 35.5±1.8 35.4±2.8 35.1±1.8 Plus disease at the time of surgery, n (%) 17 (89) 31 (82) 5 (16) Mean±SD postconceptional age at surgery, weeks 41.6±6.3 43.1±5.6 44.0±6.8 Median (range) 44 (34–58) 43 (32–57) 43 (34–60) Mean±SD interval between initial retinal ablation and surgery, weeks 5.0±4.7 6.8±4.1 7.1±5.9 Median (range) 4 (1–20) 6.5 (1–19) 5 (2–16) n, number.

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Table 2 Surgical procedures and long-term anatomic outcomes of infants who underwent vitreoretinal surgery for stage 4 and 5 retinopathy of prematurity Stage 4A Stage 4B Stage 5 Characteristics n=19 n=38 n=31

Lens-sparing vitrectomy, n (%) 15 (79) 24 (63) 0 Lensectomy and vitrectomy, n (%) 4 (21) 14 (37) 31 (100) Mean±SD duration of surgery, min 28.4±5.4 30.3±3.9 44.8±11.0 Resurgery, n (%) 4 (21) 2 (5) 1 (3) Anatomic success Total, n (%) 17 (89) 24 (63) 13 (42) Lens-sparing vitrectomy, n (%) 14 (93) 16 (67) 0 Lensectomy and vitrectomy, n (%) 3 (75) 8 (57) 13 (42) Additional procedures during surgery Laser photocoagulation, n (%) 8 (42) 8 (21) 6 (31) Cryotherapy, n (%) 0 2 (5) 0 Posterior hyaloid dissection, n (%) 7 (34) 14 (37) 3 (10) Epiretinal membrane dissection, n (%) 9 (47) 15 (39) 15 (48) Fluid-air exchange, n (%) 0 2 (5) 0 Fluid-gas exchange, n (%) 0 4 (11) 2 (6) Mean±SD follow-up duration, years 6.0±1.0 7.1±2.0 7.1±2.1 Median (range) 6.0 (5–9) 6.0 (5–14) 6.0 (5–13) n, number.

and 16% (3/19) had ambulatory VA of 20/2000 or better. The Table 3 Long-term visual results after vitrectomy for stages 4 and 5 anatomic success rate for stage 4A ROP was 89%. retinopathy of prematurity Stage 4A ROP without surgical intervention leads to poor Approximate visual outcomes, and only 20% of eyes develop VA of 20/200 19 12 Snellen or better. Singh et al focused on long-term visual outcomes visual acuity LP or FF or (mean age at last follow-up, 7.4 years) and reported slightly equivalent NLP CSM better results for LSV with or without scleral buckle for stage Stage 4A 4A ROP. Of the 23 eyes that underwent surgery for stage 4A Overall (n=19) 20/550* (n=12) 5/19 2/19 ROP, 21 (91%) were successfully attached. The mean VA of the Lens-sparing vitrectomy (n=15) 20/500 (n=10) 3/15 2/15 16 eyes (70%) for which a Snellen VA could be measured was Lensectomy and vitrectomy (n=4) 20/650 (n=2) 2/4 0/4 20/189, and 12 eyes (75%) had VA of 20/400 or better. The fi Stage 4B remaining seven eyes (30%) had LP or NLP,or xing and fol- Overall (n=38) 20/1600 (n=22) 11/38 5/38 lowing. It was concluded that the placement of a scleral buckle Lens-sparing vitrectomy (n=23) 20/1300 (n=16) 7/23 0/23 in conjunction with LSV did not adversely affect VA. Prenner et al9 et al10 Lensectomy and vitrectomy (n=15) 20/2000 (n=6) 4/15 5/15 and Lakhanpal reported VA outcomes better than Stage 5 most reported results. Although the average age was only et al Lensectomy and vitrectomy (n=31) 20/4000* 18/31 2/31 3.5 years, Prenner reported that 11 (48%) of the 23 eyes (n=11) achieved VA of 20/40 or better after undergoing LSV for stage *p=0.001 Kruskal-Wallis test with post-hoc Dunn’s test. 4A ROP. The overall mean VA was 20/58 and no child had a VA 10 CSM, central-steady-maintained; FF, fixes and follows; LP, light perception only; n, worse than 20/200. Lakhanpal et al achieved reattachment in number; NLP, no light perception. all eyes and reported mean visual VA of 20/62 (range 20/50–20/ 100) for stage 4A ROP (14 eyes) treated with LSV. The mean age at VA testing was only 3.7 years. These results suggest that eyes with stage 4A ROP have the potential for good visual results after LSV. By contrast, in the only prospectively followed cohort of patients with stage 4A ROP from the ETROP study at Table 4 Long-term postoperative complications for infants who 6 years, vitrectomy was associated with macular attachment in underwent vitrectomy for stage 4 or 5 retinopathy of prematurity only five of 16 eyes (31%).11 Only one of 16 (6%) eyes had VA Stage 4A Stage 4B Stage 5 of 20/200 or better, six had VA worse than 20/200, and eight Complications n=19 n=38 n=31 had LP or NLP.The authors considered that the worse outcomes Cataract, n (%) 1 (5) 2 (5) 0 might be related to the indications for surgery, timing of Corneal opacity, n (%) 2 (11) 5 (13) 6 (19) surgery, use of lensectomy/vitrectomy as well as LSV, and the Glaucoma, n (%) 0 3 (8) 9 (29) experience of the vitreoretinal surgeons. fi Strabismus, n (%) 4 (21) 9 (29) 7 (23) The staging of ROP is based on the clinical ndings deter- High myopia, n (%) 10 (53) 9 (24) 0 mined by ophthalmoscopic examination. Although LSV in stage Phthisis, n (%) 2 (11) 3 (8) 3 (10) 4A was associated with better functional and anatomical out- comes, it is possible that some of the stage 4A cases in our study n, number. population might actually be stage 4B. In addition, 21% of stage

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4A eyes were managed with LV as well, suggesting a very pro- who were lost to follow-up may have had poor functional and gressive stage 4A with dragging at least of the photoreceptors. anatomic outcomes. We also had several patients with additional This could explain why these eyes achieved VA outcomes worse neurological abnormalities that prevented reporting of VA. than previously reported. Snellen letters have been regarded as the gold standard for The anatomic and visual outcomes following surgery for stage determining resolvable VA.20 VA has been determined in previ- 4B ROP have generally been poorer. We found that 22 of the ous studies by a variety of means, Teller or Allen optotypes 38 eyes (58%) had measurable VA, with seven of these (32%) being preferred.91013However, it has been suggested that having VA of 20/400 or better. The anatomic success rate for Allen optotypes overestimate VA in children.20 The lack of stage 4B ROP in our study population was 63%. El Rayes standardisation in evaluation makes it difficult to compare the et al13 reported results similar to ours in 24 eyes having LSV outcomes of different studies. and 32 eyes having LV for stage 4B ROP. The structural out- In conclusion, LSV and LV for stage 4A may have favourable comes after LSV and LV were 75% and 72%, respectively. VA anatomic results leading to functional vision in the long-term. following surgery ranged between 20/300 and hand motions Anatomic and visual outcomes are acceptable for stage 4B and (median follow-up period, 3.3 years). VA of 20/800 or better poor for stage 5 ROP. The treatment of ROP should be was noted in 24 eyes (43%). Lakhanpal et al10 reported VA out- weighted toward avoiding advanced ROP. Appropriate screen- comes for stage 4B substantially better than most published ing, timely peripheral ablation and vitreoretinal surgery remain results: mean VA 20/200 (range 20/126–20/502) for 16 eyes the best alternatives for the management of ROP. Large pro- treated with LSV. VA was tested at an early age (only 3.7 years). spective randomised trials and standardisation of VA testing Again, by contrast, in the ETROP study, of 10 eyes undergoing would be helpful to investigate the indications for each surgical vitrectomy with or without scleral buckling for stage 4B ROP, technique, optimal timing of surgery, and postoperative manage- only two (20%) achieved measurable VA, which was worse than ment at each stage of ROP. 20/200 at 6 years.11 In another study, Singh et al12 reported a mean VA of 20/846 for four of the nine eyes that underwent Acknowledgements We thank O Uysal for assistance with statistical analysis. surgery for stage 4B ROP (all of the four eyes had an LSV with Contributors MK, MH, ISM and AS were involved in the conception and design of scleral buckling) at an average age of 8.6 years. Three of these the study. MK, MH and AS were involved in the analysis, interpretation and critical revision of the article. MK, MH, and ISM were involved in the drafting of the four eyes had VA of 20/800 or better. manuscript. MK, MH, ISM and SA were involved in the final approval of the article. Anatomic and functional outcomes following vitreoretinal MH and ISM were involved in the data collection and literature research. surgery for stage 5 ROP are worse than those for stage 4A or Competing interests None declared. 4B. In our study, only 11 (35%) of 31 eyes had measurable Parental consent Obtained. vision, an approximate Snellen VA equivalent of 20/4000 (range 20/20 000–20/2000). The remaining 20 (65%) had VA of LP or Ethics approval Institutional Review Board of Sisli Memorial Hospital, Istanbul. NLP,orfixing and following only. The anatomic success rate for Provenance and peer review Not commissioned; externally peer reviewed. stage 5 ROP was 42%. Cusick et al15 has reported the largest series for infants with stage 5 ROP having vitreoretinal surgery. 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734 Karacorlu M, et al. Br J Ophthalmol 2017;101:730–734. doi:10.1136/bjophthalmol-2016-309198 Downloaded from http://bjo.bmj.com/ on August 21, 2017 - Published by group.bmj.com

Long-term functional results following vitrectomy for advanced retinopathy of prematurity Murat Karacorlu, Mumin Hocaoglu, Isil Sayman Muslubas and Serra Arf

Br J Ophthalmol 2017 101: 730-734 originally published online September 15, 2016 doi: 10.1136/bjophthalmol-2016-309198

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