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Macular pucker removal with and without internal limiting membrane peeling: pilot study
Macular Pucker Removal with and without Internal Limiting Membrane Peeling: Pilot Study Donald W. Park, MD, Pravin U. Dugel, MD, Jennifer Garda, BS, Jack O. Sipperley, MD, Allen Thach, MD, Scott R. Sneed, MD, Jennifer Blaisdell, BS Objective: To investigate results of macular pucker surgery with and without internal limiting membrane (ILM) peeling. Design: Retrospective noncomparative interventional case series. Participants: Forty-four consecutive patients underwent pars plana vitrectomy to remove an idiopathic macular pucker by two surgeons from June 1999 to July 2000. Intervention: During the vitrectomy, one surgeon removed only the macular epiretinal membrane (24 patients), whereas the other surgeon removed the macular epiretinal membrane and then performed an additional ILM peeling (20 patients). Main Outcome Measures: Visual acuity and recurrence of macular pucker. Results: Twenty-four (55%) patients underwent pars plana vitrectomy without ILM peeling, and 20 patients (45%) underwent pars plana vitrectomy with ILM peeling. Visual acuity improved or was unchanged in 79% of operated eyes without ILM peeling and 100% of operated eyes with ILM peeling (P ⫽ 0.01). Visual acuity improved 5 or more lines in 25% of operated eyes without ILM peeling and 30% of operated eyes with ILM peeling. At the final visit, 21% of eyes without ILM peeling at the initial surgery showed postoperative recurrent macular pucker or persistent contraction to the ILM, whereas none of the eyes with ILM peeling had evidence of this. Conclusions: This pilot study provides evidence that peeling of the ILM during macular pucker surgery may not have deleterious effects. Ophthalmology 2003;110:62– 64 © 2003 by the American Academy of Ophthalmology.
Macular puckers are composed of cellular membranes that proliferate over the central macular region. These epiretinal membranes have been found to be composed of fibroblasts, glial cells, macrophages, myofibroblasts, and retinal pigment epithelium.1,2 Epiretinal membranes may result from a variety of causes, including retinal tears, retinal vascular occlusions, and trauma. Idiopathic epiretinal membranes have no obvious cause, although most are associated with a posterior vitreous detachment.2 The internal limiting membrane (ILM) is adherent to epiretinal membranes; surgically removed specimens of epiretinal membranes often demonstrate varying degrees of attached ILM.1,3–5 There is some debate as to whether removing the ILM during macular pucker surgery leads to a poorer visual outcome.2,4 To help explain the effects of ILM removal in macular pucker surgery, we examined the anatomic and visual acuity
Originally received: September 4, 2001. Accepted: August 13, 2002. Manuscript no. 210593. From Retina Consultants of Arizona, Mesa, Arizona. Presented in part at the annual meeting of the American Academy of Ophthalmology, New Orleans, Louisiana, November 2001. Reprint requests to Donald W. Park, MD, Retinal Consultants of Arizona, 560 West Brown Road, #2004, Mesa, AZ 85201.
62
© 2003 by the American Academy of Ophthalmology Published by Elsevier Science Inc.
results of 44 consecutive patients who underwent pars plana vitrectomy with and without removal of the ILM.
Patients and Methods We performed a retrospective chart review (from two surgeons) of all patients who underwent pars plana vitrectomy for idiopathic macular puckers from June 1999 to July 2000. Institutional review board approval was not required for this retrospective series. Only eyes with idiopathic macular puckers were reviewed. Eyes with a history of retinal detachment, retinal vascular occlusion, uveitis, vitreous hemorrhage, trauma, and ocular tumors were excluded. Forty-four consecutive cases from these two surgeons were identified for that time period. All 44 patients had a postsurgical follow-up of at least 3 months’ duration. We report the results and findings of these 44 consecutive patients. All patients had a detailed medical and ocular history with a complete eye examination, including biomicroscopy. Best-corrected visual acuity was taken preoperatively and at the final visit. The operated eyes underwent a pars plana vitrectomy to remove the central and peripheral vitreous. In all cases, an epiretinal membrane was removed from the macula using a 20-gauge microvitreoretinal blade, Sinskey hook, and intraocular forceps. One surgeon made no further attempts to peel the ILM on all of his consecutive patients, whereas the other surgeon always performed a second peeling procedure to remove the ILM on all of his ISSN 0161-6420/03/$–see front matter PII S0161-6420(02)01440-9
Park et al 䡠 Macular Pucker Removal with and without ILM Peeling consecutive patients. When the ILM was removed by the second surgeon, it was removed to at least a disc diameter from the central fovea. In general, the removed ILM had a more smooth, translucent appearance than the epiretinal membrane. Indocyanine green dye was not used to stain the ILM, and the extent of the ILM removal beyond a disc diameter from the central fovea was not assessed. The retina was then inspected with indirect ophthalmoscopy and scleral depression, and any iatrogenic retinal holes or tears were treated with argon laser photocoagulation. Statistical significance was determined by using a two-tailed t test for two samples, assuming equal variances. The significance level used was alpha ⫽ 0.05. If the results were statistically significant, a two-tailed t test for two samples assuming unequal variances was also performed. Microsoft Excel software was used to perform the statistical testing.
Results All 44 consecutive patients undergoing pars plana vitrectomy to remove idiopathic macular pucker had a postsurgical follow-up of 3 months’ or longer duration. The mean postsurgical follow-up for operated eyes without ILM peeling was 392 days, and the mean follow-up for eyes with ILM peeling was 384 days. The mean age for both groups was 69 years old. Twenty-four (55%) patients underwent pars plana vitrectomy surgery without ILM peeling, and 20 patients (45%) underwent pars plana vitrectomy with ILM peeling. The visual acuities were converted to logarithm of the minimum angle of resolution scores and compared. Visual acuity improved or was unchanged in 79% (19 of 24 eyes) of operated eyes without ILM peeling and in 100% (20 of 20 eyes) of operated eyes with ILM peeling (P ⫽ 0.01). The average increase in logarithm of the minimum angle of resolution vision scores was 0.33 for operated eyes without ILM peeling and 0.41 for operated eyes with ILM peeling. The visual acuity improved 2 or more lines in 50% (12 of 24 eyes) of operated eyes without ILM peeling and in 50% (10 of 20 eyes) of operated eyes with ILM peeling. Visual acuity improved 5 or more lines in 25% (6 of 24 eyes) of operated eyes without ILM peeling and in 30% (6 of 20 eyes) of operated eyes with ILM peeling. These differences were not statistically different. At the final visit, 21% of eyes without ILM peeling at the initial surgery showed biomicroscopic evidence of a recurrent macular pucker or persistent contraction to the ILM and retinal vessels, whereas none of the eyes with ILM peeling at the initial surgery had evidence of a recurrent macular pucker or persistent contraction to the ILM and retinal vessels. None of the operated eyes in either group had evidence of postsurgical cystoid macular edema, macular retinal hemorrhage, macular hole, or retinal detachment at their final visit.
Discussion Forty-four consecutive eyes with idiopathic macular pucker underwent pars plana vitrectomy. Twenty-four had removal of the macular pucker only, and 20 had removal of the macular pucker with an additional macular ILM. One surgeon did not intentionally remove the ILM for his 24 consecutive cases, and the other surgeon always removed the ILM for his 20 consecutive cases. In this study, none of the eyes that had the additional ILM peeling developed recurrent macular puckers at the final visit, whereas 21% of the eyes without the ILM peeling
had either a recurrent macular pucker or persistent contraction to the ILM and macular retinal vessels. Although the 21% recurrence rate seems high compared with other studies in the literature,6 a recurrence in this study was judged as any biomicroscopic evidence of a recurrent epiretinal membrane or continued contraction to the ILM and macular retinal vessels. Many of these recurrent macular puckers, though, were visually insignificant, because the final visual acuity results were essentially the same between the two groups. Mittleman et al3 have reported that the ILM has a limited capacity for regeneration when removed during macular pucker surgery. Maguire et al5 reported that myofibroblasts are present with increasing frequency in recurrent epiretinal membranes compared with primary idiopathic epiretinal membranes. Removal of the ILM during macular pucker surgery may remove a scaffold for proliferative cells, as well as remove myofibroblasts and other proliferative cells that may cause recurrent macular pucker or persistent contraction to the macula. Sivalingam et al4 have reported that eyes with long segments of ILM removed during macular pucker surgery were less likely to achieve a final visual acuity of 20/60 or better. Moreover, because the ILM is composed of the footplates of the Muller cells, it is possible that shearing of cells may injure the retina.7 However, this study did not show visual acuity loss when ILM peeling was performed during macular pucker surgery. Visual acuity improved or was unchanged in 100% of operated eyes with ILM peeling and 79% of operated eyes without ILM peeling (P ⫽ 0.01). However, no statistically significant visual acuity benefit was found when visual acuity improved by 2 or more lines or 5 or more lines was examined. This lack of statistical significance may reflect the relatively small sample size or no true visual acuity benefit to ILM peeling in macular pucker surgery. Further studies are needed to evaluate the effects of ILM peeling on visual acuity in macular pucker surgery, although studies using ILM peeling during macular hole surgery have not shown a deleterious effect on final visual acuity.7–9 This study has limitations because of its retrospective data analysis. The surgical cases were, however, consecutive, and each group’s surgeries were performed by a single surgeon. The two surgeons used almost identical techniques, except one surgeon only removed the macular pucker in his consecutive surgeries, whereas the other surgeon always performed an additional ILM peeling. This pilot study provides evidence that peeling of the ILM during macular pucker surgery may not have deleterious effects. A prospective, randomized study is needed to more definitively address this hypothesis. The authors are currently engaged in such a study of macular pucker surgery with and without ILM peeling to better understand the implications of this initial study.
References 1. Green WR, Kenyon KR, Michels RG, et al. Ultrastructure of epiretinal membranes causing macular pucker after retinal
63
Ophthalmology Volume 110, Number 1, January 2003
2.
3. 4.
5.
64
re-attachment surgery. Trans Ophthalmol Soc UK 1979;99: 65–77. Smiddy WE, Maguire AM, Green WR, et al. Idiopathic epiretinal membranes. Ultrastructural characteristics and clinicopathologic correlation. Ophthalmology 1989;96:811–20; discussion 821. Mittleman D, Green WR, Michels RG, de la Cruz Z. Clinicopathologic correlation of an eye after surgical removal of an epiretinal membrane. Retina 1989;9:143–7. Sivalingam A, Eagle RC Jr, Duker JS, et al. Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery. Ophthalmology 1990;97:1549 –52. Maguire AM, Smiddy WE, Nanda SK, et al. Clinicopathologic
6. 7. 8. 9.
correlation of recurrent epiretinal membranes after previous surgical removal. Retina 1990;10:213–22. Margherio RR, Cox MS Jr, Trese MT, et al. Removal of epimacular membranes. Ophthalmology 1985;92:1075–83. Smiddy WE, Feuer W, Cordahi G. Internal limiting membrane peeling in macular hole surgery. Ophthalmology 2001;108: 1471– 6; discussion 1477– 8. Park DW, Sipperley JO, Sneed SR, et al. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology 1999;106:1392–7; discussion 1397– 8. Olsen TW, Sternberg P Jr, Capone A Jr, et al. Macular hole surgery using thrombin-activated fibrinogen and selective removal of the internal limiting membrane. Retina 1998;18: 322–9.
Macular puckers are composed of cellular membranes that proliferate over the central macular region. These epiretinal membranes have been found to be composed of fibroblasts, glial cells, macrophages, myofibroblasts, and retinal pigment epithelium.1,2 Epiretinal membranes may result from a variety of causes, including retinal tears, retinal vascular occlusions, and trauma. Idiopathic epiretinal membranes have no obvious cause, although most are associated with a posterior vitreous detachment.2 The internal limiting membrane (ILM) is adherent to epiretinal membranes; surgically removed specimens of epiretinal membranes often demonstrate varying degrees of attached ILM.1,3–5 There is some debate as to whether removing the ILM during macular pucker surgery leads to a poorer visual outcome.2,4 To help explain the effects of ILM removal in macular pucker surgery, we examined the anatomic and visual acuity
Originally received: September 4, 2001. Accepted: August 13, 2002. Manuscript no. 210593. From Retina Consultants of Arizona, Mesa, Arizona. Presented in part at the annual meeting of the American Academy of Ophthalmology, New Orleans, Louisiana, November 2001. Reprint requests to Donald W. Park, MD, Retinal Consultants of Arizona, 560 West Brown Road, #2004, Mesa, AZ 85201.
62
© 2003 by the American Academy of Ophthalmology Published by Elsevier Science Inc.
results of 44 consecutive patients who underwent pars plana vitrectomy with and without removal of the ILM.
Patients and Methods We performed a retrospective chart review (from two surgeons) of all patients who underwent pars plana vitrectomy for idiopathic macular puckers from June 1999 to July 2000. Institutional review board approval was not required for this retrospective series. Only eyes with idiopathic macular puckers were reviewed. Eyes with a history of retinal detachment, retinal vascular occlusion, uveitis, vitreous hemorrhage, trauma, and ocular tumors were excluded. Forty-four consecutive cases from these two surgeons were identified for that time period. All 44 patients had a postsurgical follow-up of at least 3 months’ duration. We report the results and findings of these 44 consecutive patients. All patients had a detailed medical and ocular history with a complete eye examination, including biomicroscopy. Best-corrected visual acuity was taken preoperatively and at the final visit. The operated eyes underwent a pars plana vitrectomy to remove the central and peripheral vitreous. In all cases, an epiretinal membrane was removed from the macula using a 20-gauge microvitreoretinal blade, Sinskey hook, and intraocular forceps. One surgeon made no further attempts to peel the ILM on all of his consecutive patients, whereas the other surgeon always performed a second peeling procedure to remove the ILM on all of his ISSN 0161-6420/03/$–see front matter PII S0161-6420(02)01440-9
Park et al 䡠 Macular Pucker Removal with and without ILM Peeling consecutive patients. When the ILM was removed by the second surgeon, it was removed to at least a disc diameter from the central fovea. In general, the removed ILM had a more smooth, translucent appearance than the epiretinal membrane. Indocyanine green dye was not used to stain the ILM, and the extent of the ILM removal beyond a disc diameter from the central fovea was not assessed. The retina was then inspected with indirect ophthalmoscopy and scleral depression, and any iatrogenic retinal holes or tears were treated with argon laser photocoagulation. Statistical significance was determined by using a two-tailed t test for two samples, assuming equal variances. The significance level used was alpha ⫽ 0.05. If the results were statistically significant, a two-tailed t test for two samples assuming unequal variances was also performed. Microsoft Excel software was used to perform the statistical testing.
Results All 44 consecutive patients undergoing pars plana vitrectomy to remove idiopathic macular pucker had a postsurgical follow-up of 3 months’ or longer duration. The mean postsurgical follow-up for operated eyes without ILM peeling was 392 days, and the mean follow-up for eyes with ILM peeling was 384 days. The mean age for both groups was 69 years old. Twenty-four (55%) patients underwent pars plana vitrectomy surgery without ILM peeling, and 20 patients (45%) underwent pars plana vitrectomy with ILM peeling. The visual acuities were converted to logarithm of the minimum angle of resolution scores and compared. Visual acuity improved or was unchanged in 79% (19 of 24 eyes) of operated eyes without ILM peeling and in 100% (20 of 20 eyes) of operated eyes with ILM peeling (P ⫽ 0.01). The average increase in logarithm of the minimum angle of resolution vision scores was 0.33 for operated eyes without ILM peeling and 0.41 for operated eyes with ILM peeling. The visual acuity improved 2 or more lines in 50% (12 of 24 eyes) of operated eyes without ILM peeling and in 50% (10 of 20 eyes) of operated eyes with ILM peeling. Visual acuity improved 5 or more lines in 25% (6 of 24 eyes) of operated eyes without ILM peeling and in 30% (6 of 20 eyes) of operated eyes with ILM peeling. These differences were not statistically different. At the final visit, 21% of eyes without ILM peeling at the initial surgery showed biomicroscopic evidence of a recurrent macular pucker or persistent contraction to the ILM and retinal vessels, whereas none of the eyes with ILM peeling at the initial surgery had evidence of a recurrent macular pucker or persistent contraction to the ILM and retinal vessels. None of the operated eyes in either group had evidence of postsurgical cystoid macular edema, macular retinal hemorrhage, macular hole, or retinal detachment at their final visit.
Discussion Forty-four consecutive eyes with idiopathic macular pucker underwent pars plana vitrectomy. Twenty-four had removal of the macular pucker only, and 20 had removal of the macular pucker with an additional macular ILM. One surgeon did not intentionally remove the ILM for his 24 consecutive cases, and the other surgeon always removed the ILM for his 20 consecutive cases. In this study, none of the eyes that had the additional ILM peeling developed recurrent macular puckers at the final visit, whereas 21% of the eyes without the ILM peeling
had either a recurrent macular pucker or persistent contraction to the ILM and macular retinal vessels. Although the 21% recurrence rate seems high compared with other studies in the literature,6 a recurrence in this study was judged as any biomicroscopic evidence of a recurrent epiretinal membrane or continued contraction to the ILM and macular retinal vessels. Many of these recurrent macular puckers, though, were visually insignificant, because the final visual acuity results were essentially the same between the two groups. Mittleman et al3 have reported that the ILM has a limited capacity for regeneration when removed during macular pucker surgery. Maguire et al5 reported that myofibroblasts are present with increasing frequency in recurrent epiretinal membranes compared with primary idiopathic epiretinal membranes. Removal of the ILM during macular pucker surgery may remove a scaffold for proliferative cells, as well as remove myofibroblasts and other proliferative cells that may cause recurrent macular pucker or persistent contraction to the macula. Sivalingam et al4 have reported that eyes with long segments of ILM removed during macular pucker surgery were less likely to achieve a final visual acuity of 20/60 or better. Moreover, because the ILM is composed of the footplates of the Muller cells, it is possible that shearing of cells may injure the retina.7 However, this study did not show visual acuity loss when ILM peeling was performed during macular pucker surgery. Visual acuity improved or was unchanged in 100% of operated eyes with ILM peeling and 79% of operated eyes without ILM peeling (P ⫽ 0.01). However, no statistically significant visual acuity benefit was found when visual acuity improved by 2 or more lines or 5 or more lines was examined. This lack of statistical significance may reflect the relatively small sample size or no true visual acuity benefit to ILM peeling in macular pucker surgery. Further studies are needed to evaluate the effects of ILM peeling on visual acuity in macular pucker surgery, although studies using ILM peeling during macular hole surgery have not shown a deleterious effect on final visual acuity.7–9 This study has limitations because of its retrospective data analysis. The surgical cases were, however, consecutive, and each group’s surgeries were performed by a single surgeon. The two surgeons used almost identical techniques, except one surgeon only removed the macular pucker in his consecutive surgeries, whereas the other surgeon always performed an additional ILM peeling. This pilot study provides evidence that peeling of the ILM during macular pucker surgery may not have deleterious effects. A prospective, randomized study is needed to more definitively address this hypothesis. The authors are currently engaged in such a study of macular pucker surgery with and without ILM peeling to better understand the implications of this initial study.
References 1. Green WR, Kenyon KR, Michels RG, et al. Ultrastructure of epiretinal membranes causing macular pucker after retinal
63
Ophthalmology Volume 110, Number 1, January 2003
2.
3. 4.
5.
64
re-attachment surgery. Trans Ophthalmol Soc UK 1979;99: 65–77. Smiddy WE, Maguire AM, Green WR, et al. Idiopathic epiretinal membranes. Ultrastructural characteristics and clinicopathologic correlation. Ophthalmology 1989;96:811–20; discussion 821. Mittleman D, Green WR, Michels RG, de la Cruz Z. Clinicopathologic correlation of an eye after surgical removal of an epiretinal membrane. Retina 1989;9:143–7. Sivalingam A, Eagle RC Jr, Duker JS, et al. Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery. Ophthalmology 1990;97:1549 –52. Maguire AM, Smiddy WE, Nanda SK, et al. Clinicopathologic
6. 7. 8. 9.
correlation of recurrent epiretinal membranes after previous surgical removal. Retina 1990;10:213–22. Margherio RR, Cox MS Jr, Trese MT, et al. Removal of epimacular membranes. Ophthalmology 1985;92:1075–83. Smiddy WE, Feuer W, Cordahi G. Internal limiting membrane peeling in macular hole surgery. Ophthalmology 2001;108: 1471– 6; discussion 1477– 8. Park DW, Sipperley JO, Sneed SR, et al. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology 1999;106:1392–7; discussion 1397– 8. Olsen TW, Sternberg P Jr, Capone A Jr, et al. Macular hole surgery using thrombin-activated fibrinogen and selective removal of the internal limiting membrane. Retina 1998;18: 322–9.