Darin R. Haivala,
David W. Parke, II
INTRODUCTION
Iwanoff first described the abnormal proliferation of cellular membranes on the inner retinal surface in 1865.[1] Since this initial description, surface proliferation in the macular region has been subsequently described as epimacular membrane, macular pucker, cellophane maculopathy, preretinal macular fibrosis, wrinkling of the internal limiting membrane, among others.[2-8] Although histologically similar to epiretinal proliferation elsewhere associated with proliferative vitreoretinopathy, it is clinically considered a separate entity based on its location, clinical features, and clinical course. Most commonly, macular epiretinal membranes (ERMs) are asymptomatic or cause mild symptoms of metamorphopsia and/or modest decreased central acuity. A minority of these membranes can cause sufficient macular distortion and macular edema to induce clinicians to recommend ERM removal via pars plana vitrectomy (PPV).
EPIDEMIOLOGY
While ERM formation has been associated with and results from a variety of primary intraocular diseases, the vast majority are considered to be idiopathic, unassociated with other systemic or ocular disease. They are found most frequently over the age of 50, and several large clinical studies have noted a clinical prevalence of between 7% and 11.8%.[9,10] Most of these are asymptomatic, with many being extrafoveal in location. There appears to be no significant gender predilection and 20-30% are bilateral. Posterior vitreous detachments are present in up to 90% of clinically significant ERMs. (The absence of a posterior vitreous detachment in the presence of an 'ERM' should alert the clinician to the probability of the vitreomacular traction syndrome). Second eye involvement was reported in the Blue Mountains Eye Study to occur in 13.5% of patients over a 5 year time period.[11]
Nonidiopathic ERMs have been associated with a wide variety of vitreo-retinal diseases including retinal vascular disease, vitreo-retinal inflammatory conditions, postoperative (particularly scleral buckle) and posttraumatic states, inherited and congenital posterior segment anomalies and syndromes, and intraocular tumors. Inflammation and/or vascular leakage appear to be common mediators. Retinal vascular diseases associated with increased vascular permeability and ERMs include diabetic and hypertensive retinopathy, venous occlusive disease, angiomas, telangiectasis, as well as others (Fig. 160.1).[12-23]Intraocular inflammation resulting in an inflammatory cellular infiltrate in the vitreous may also be associated with ERM formation. Any infectious or noninfectious ocular condition resulting in intermediate or posterior uveitis may be causative. Common examples include both toxoplasmosis and pars planitis (Fig. 160.2).[13,24-29] Ocular trauma, including both blunt and penetrating injuries, particularly if there is associated vitreous hemorrhage (as well as nearly all ocular surgery) may lead to ERM formation or to worsening of preexisting ERMs.[30-38] Although cataract surgery has been reported to be associated with new ERMs in 9% of eyes, it is likely that a substantial percentage of these membranes were preexisting and undetected, or were preexisting and worsened during the perioperative period.
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FIGURE 160.1 (a) Acute CRVO. (b) ERM development 1 year later. |
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FIGURE 160.2 ERM after exogenous endophthalmitis. |
Epiretinal membrane formation is not uncommon following successful retinal detachment surgery, occurring in 4-8% of eyes. Retinal breaks both before and after laser or cryoretinopexy are frequently associated with subsequent retinal surface membrane proliferation (Fig. 160.3).[4,30-38] Among the less common associations with ERM are retina tumors (particularly vascular tumors) and retinitis pigmentosa.
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FIGURE 160.3 (a) ERM following cryotherapy of a peripheral retinal break. (b) OCT showing highly reflective ERM, corrugation of retinal surface, loss of foveal depression, and increased central macular thickness. |
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Key Features |
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Causes of Macular ERMs
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PATHOGENESIS AND PATHOLOGY
The cellular origin of epiretinal membranes has long been debated, and almost every possibility has been considered. Iwanoff, in 1865, implicated the endothelial cell in the formation of the membranes.[1]Manschot, in 1958, believed that the membrane was an extension of the Müller cell processes,[39] whereas Wolter considered the cells to originate from fibroblasts in the vascular connective tissue.[40] Smith suggested that the cells in the membrane originated from the pigmented or nonpigmented cells of the pars ciliaris, retinal pigment epithelium (RPE) cells, mesodermal elements of the vascular system, normal vitreous cells, inflammatory cells within the vitreous, or retinal glial cells.[41] In 1962, Kurz and Zimmerman believed that the cells originated from migration of RPE cells.[42] Ashton later suggested that the cells originated from a transformation of vascular mesenchymal cells into fibroblasts,[43] and in 1969, von Gloor proposed that hyalocytes were the cells of origin.[44]
The advent of vitreous surgery has provided an opportunity to advance our understanding of the clinicopathologic relationships of epiretinal membranes. Numerous authors have attempted to characterize the cells of origin and correlate this with the ERM etiology. Many studies have determined that the predominant cells types in idiopathic ERMs removed at surgery include glial cells or fibrous astrocytes and (particularly with clinically severe membranes) elements of retinal pigment epithelial cells, fibrocytes, and macrophages. This is consistent with a theory of idiopathic ERM pathogenesis first advanced by Roth and Foos.
Foos suggested that the glial cells found in the thin, idiopathic membranes were derived from the glial cells of the superficial retina (fibrous astrocytes and Muller cells) that had migrated through breaks in the internal limiting membrane (ILM) to proliferate on the retinal surface.[45] These ILM breaks were hypothesized to be associated with acute separation of the posterior vitreous from the macular region (where it has relatively tight adherence). This hypothesis was subsequently supported by Bellhorn and associates.[46]
ERMs occurring following retinal breaks and detachment are felt to have a different pathogenesis. In these situations, retinal pigment epithelial (RPE) cells gain access to the vitreous cavity through the retinal break and settle on the macular surface, subsequently developing a membrane. These membranes are architecturally enhanced by the presence of fibrocytes and macrophages, stimulated in part by the inflammation associated with vitreous hemorrhage and/or surgical repair.
Most published reports on the ultrastructure of epiretinal macular membranes have been on vitrectomy specimens in elderly patients. Vinores and colleagues studied the ultrastructural and electron immunocytochemical characterization of cells in epiretinal membranes. Their work suggests that both RPE cells and retinal glial cells are most likely to be the major participants in the pathogenesis of epiretinal membranes.[47] Smiddy and co-workers reported on membranes removed in children and young adults. They noted that myofibroblasts, myoblastic differentiation of RPE cells and fibrous astrocytes, and new collagen formation tended to be found more frequently in younger patients.[48] The progressive tangential and anteroposterior traction exerted by ERMs is likely due to the myofibroplast characteristics of the membrane which have been determined on immunohistochemical staining to contain actin, transforming growth factor, and fibronectin.[49]
The dispersion of RPE cells on the retinal surface has been demonstrated clinically and experimentally in cases of retinal breaks and detachment.[50-54] However, the finding of RPE cells in idiopathic membranes is more difficult to explain. Smiddy and colleagues suggested that the RPE cells gain access to the retinal surface by various methods including migration through occult breaks, by inactivation of developmental rests of RPE cells already on the surface of the retina, through transformation from other cell types, or via transretinal migration.[55] The exact mechanism or combination of mechanisms is yet to be elucidated. Stern and co-workers[56] suggested that the contractive forces of the membranes were related to their constituent cell types and not dependent on intercellular collagen, as suggested by previous investigators.[57]
Collagen is a component of all surgically removed epiretinal membranes. The abundance of collagen in some membranes and the presence of fibrocytic and macrophage-like cells suggest that vitreous hyalocytes may be a significant premetaplasia cell of origin in these collagen membranes.[58]
CLINICAL FINDINGS: SYMPTOMATOLOGY
Symptoms associated with epiretinal membrane formation vary greatly depending on the location and characteristics of the membrane as well as the amount of underlying macular architectural disruption. Patients with membranes that are very thin or outside the central macula are oftentimes completely asymptomatic. It is not uncommon for these patients to have normal or near-normal visual acuity. Subtle complaints of blurring of vision or metamorphopsia may develop with increasing traction, membrane opacification, or macular edema, and the onset is often insidious. These patients typically remain very stable with only 10-25% of patients losing one or two lines of vision over a 2 year time period.[11,23,59-62] Of those patients with idiopathic membranes, two-thirds will have 20/30 or better vision and 85% will display a visual acuity of 20/70 or better.[8,63] At the opposite end of the spectrum are those patients with very thick central membranes associated with significant underlying retinal architectural distortion, subtle detachment of the posterior pole, and/or macular edema. Visual acuity at or below the 20/200 level may be seen in a small number of patients (~5%).[64-66] Other complaints may include monocular diplopia and macro or micropsia.
Clinicians will encounter cases of patients with substantially decreased vision but clinically unimpressive ERMs. In such situations, substantial macular edema or (more rarely) a lamellar or full-thickness macular hole may be present. On the other hand, a clinically impressive ERM but with a central pseudohole may result in preservation of good central visual acuity. Optical coherence tomography (OCT) assists substantively in the evaluation of these patients.
CLINICAL ASSESSMENT
Evaluation of an eye with a suspected ERM begins first with testing of central visual acuity and central visual fields (such as via an Amsler grid). Retinal distortion or macular heterotopia may induce metamorphopsia and Amsler grid abnormalities. Indirect ophthalmoscopy and slit-lamp biomicroscopy constitute the next major element in the evaluation process. The clinical findings differ greatly depending on the severity of the membrane and whether it has undergone significant contraction. The membrane may be very fine and translucent without an identifiable edge. These may be identifiable only on careful contact lens biomicroscopy and can be as subtle as a fine 'sheen' in the macular region. There may be blunting or an irregularity of the foveal light reflex. These finding may be best appreciated on red-free or monochromatic green or blue light. Vascular tortuosity may be more evident on fluorescein angiography than on clinical inspection (Fig. 160.4). In such cases, visual acuity may be determined principally by the amount of associated macular edema or macular detachment.
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FIGURE 160.4 (a) Idiopathic ERM. (b) Fluorescein image demonstrating combination of vascular tortuosity and straightening. |
More extensive membranes may take on an opaque appearance and obscure underling retinal vasculature. They may be pigmented, particularly in the case of membrane formation following the treatment of a retinal break or retinal detachment, severe intraocular inflammation, or vitreous hemorrhage.[67-69] More severe membranes may be contractile and result in identifiable striae at the level of the internal limiting membrane and inner retina, or true retinal folds. The contraction of the membrane may also result in traction on surrounding retinal vessels resulting in abnormal distortion and a tethering effect. It is not uncommon for the major vasculature to have a more 'straightened' appearance than that of the fellow eye. Contraction may also result in macular ectopia and traction. The resulting macular heterotopia may cause diplopia. Contraction may also lead to foveolar detachment.
Small intraretinal hemorrhages as well as evidence of presumed axoplasmic stasis or ischemia may be seen as a result of ERM-induced vascular traction. The axoplasmic stasis can manifest itself as cotton-wool spots as well as larger areas of inner retinal whitening.[70] Additional biomicroscopic findings may include macular edema with cystic changes, subfoveal retinal pigment epithelial changes, and macular pseudoholes which have been reported in up to 8-20% of eyes with epiretinal membranes.[71-74] Epiretinal membranes are found in up to 30% of patients with true full-thickness macular holes and these must be differentiated from pseudoholes.[23,75]
A posterior vitreous separation is present in up to 80-90% of patients with epiretinal membrane, but the true vitreoretinal relationships may be difficult to discern clinically.[8,23,59,60,63,66,76] Margherio et al noted that the vitreoretinal interface relationships were more accurately evaluated at the time of vitrectomy surgery by observing the effects of surgical manipulation on the underlying retina.[77] In some cases, large areas of vitreous collapse noted intraoperatively with an adherent posterior hyaloid were misinterpreted as a true vitreous separation preoperatively. In eyes with a partial vitreous separation, spontaneous membrane avulsion with the complete detachment of the posterior vitreous has been reported.[78] The spontaneous 'peeling' of an epiretinal membrane has also been described in patients with a complete vitreous separation. An edge of the ERM may 'scroll' upon itself, contracting to the other edge of the membrane resulting in spontaneous visual improvement.[23,79]
Any eye with an ERM and without evidence of a clear posterior vitreous separation must be carefully inspected clinically and by OCT for evidence of the vitreomacular traction syndrome (VMTS) (Fig. 160.5). In the VMTS, a partially detached posterior hyaloid retains attachments in the posterior pole resulting in traction upon the macular region. VMTS frequently coexists with an epiretinal membrane. Complete surgical management therefore requires not only removal of VMTS-induced traction, but also removal of any associated epiretinal tissue.
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FIGURE 160.5 (a) Fundus photograph demonstrating loss of central foveal depression. (b) OCT demonstrating central vitreomacular traction and traction retinal elevation. |
Attention must always be paid to the peripheral retina as well. The new diagnosis of an ERM, particularly if purely unilateral, pigmented, or associated with pigmented vitreous cells, must stimulate a careful examination for a peripheral retinal break. This is not only an etiologic consideration, but important in ultimate management plans.
OCT can play an important role in the clinical assessment of eyes with ERMs (Fig. 160.6). OCT can not only detect ERMs, but also assist in topographic localization, identification of vitreoretinal relationships (such as in the vitreomacular traction syndrome), detection of macular holes, and quantitation of macular thickness and macular volume. In addition to value in clinical characterization, OCT has therapeutic value in preoperative planning. The co-existence of a macular hole, the presence of a bilaminar ERM, or knowledge of substantive macular edema may lead the surgeon to modify his or her approach. It also has considerable prognostic value in counseling patients as to the eye's likely visual potential. Finally, it can assist in postoperative management by assessing macular thickness and membrane re-growth.
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FIGURE 160.6 OCT showing typical ERM features including highly reflective ERM, multiple points of retinal attachment, loss of foveal depression, and increased retinal thickness. |
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Key Features |
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Value of OCT in Macular ERMs
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Fluorescein angiography, although still useful in evaluating selected ERM cases, has been partially supplanted by OCT. The principal utility of angiography in the setting of an ERM is to rule out the concomitant presence of retinal vascular disease or of underlying pigment epithelial pathology. In some ERM cases with intraretinal hemorrhages, it may be impossible to rule out an associated small branch retinal vein occlusion by ophthalmoscopy alone. Similarly, it may be necessary to perform fluorescein angiography to rule out the presence of a choroidal neovascular membrane in the patient with substantial intraretinal and/or submacular fluid. Finally, stereo fundus photography and angiography may assist in delineation of vitreoretinal relationships, ERM borders, and degree of retinal vascular distortion in the difficult-to-examine patient.
TREATMENT
The vast majority of patients who present with epiretinal membrane will remain stable if observed over a period of time.[11,60,66,80] From the standpoint of the surgeon and the patient, this is characteristically not an inexorably progressive disease. However, visual function may progressively deteriorate in some patients, due to progressive membrane thickening, retinal distortion, macular edema, lamellar hole formation, or retinal pigment epithelial change. Episodes of intraocular inflammation or intraocular surgery may be followed by alterations in ERM architecture or the amount of associated macular edema. Therefore, it is impossible to predict for any patient what will be the course of any specific ERM. This renders decisions difficult regarding surgery and the timing of surgery. In cases with significant or progressive vision loss, debilitating metamorphopsia or diplopia, surgical intervention should be considered. Most surgeons reserve surgery for those patients with vision reduction at least to the 20/50-20/60 level, although earlier surgery may be considered for those with debilitating symptoms or specific visual needs. The goals of surgical intervention include the removal of all epimacular tissue and relief of all macular traction with the subsequent resolution of underlying-traction-induced retinal folds, macular edema, as well as traction-induced axoplasmic stasis.[81]
Once the surgeon and the patient have elected to proceed with surgery, conventional 20-, 23-, or 25-gauge vitrectomy is carried out. A core vitrectomy is completed and the posterior cortical vitreous should be elevated and excised in those cases where a complete vitreous separation is not present. (As noted earlier, posterior vitreous separation is present in the vast majority of ERM cases. Anteroposterior traction indicates that the vitreomacular traction syndrome is present.) Attention is then turned to the macular surface. A prominent edge of the epiretinal tissues can often be identified and this provides a convenient location in which to engage the ERM. Using a barbed micro-vitreoretinal blade, bent 25-gauge needle, or retinal pick, the edge of the membrane can be 'engaged' in a tangential, 'dragging' fashion, elevating the membrane edge. An alternative method involves using an intraocular diamond dusted or end-grasping forceps to 'pinch' the membrane and initiate removal. In cases where a defined edge is not identifiable, the same 'dragging' maneuver can be used to 'snag' the membrane resulting in the elevation of a piece of the membrane that can be further advanced. Additional tools, such as the Tano Diamond Dusted Membrane Scraper,[82,83] can be very helpful in 'snagging' the membrane in cases where an identifiable edge is not present. Recently, the use of surgical adjuncts to help visualize the membrane has gained popularity. Indocyanine green, trypan blue, and triamcinolone acetonide have been used to help visualize epiretinal tissue to facilitate its complete removal.[84-91]
Once an edge has been elevated, the 'peeling' of the tissue can be advanced using intraocular forceps, regrasping the membrane near the retinal surface while advancing across the posterior pole. This should be carried out in a tangential fashion, limiting anterior traction. Care should be taken to minimize traction on a very cystic macula to mitigate the risk of 'unroofing' a large central cyst. It is not uncommon for a seemingly localized ERM to extend well beyond the major vascular arcades. The extent of more peripheral membranectomy should depend on ease of removal and associated pathology. After the membrane has been elevated, it is not uncommon to see superficial retinal whitening in the area where the membrane has been removed. It is important to differentiate this whitening from residual epiretinal tissue in the cases of multilayered membranes. As always, care should be taken to ensure that peripheral or mid-peripheral retinal breaks have not occurred with instrument changes or with traction on the retina by extensive membranes.
RESULTS OF SURGERY
In a majority of patients, the macular surface architecture is greatly improved in the immediate postoperative period, though short-term vision reduction beyond the preoperative level is not uncommon (Figs 160.7 and 160.8). While immediate and significant improvement in acuity may occur, it often takes 4-6 weeks for the patient's vision to return to the preoperative level, with subsequent improvement over the ensuing 3-6 months. This course can be modulated by factors most commonly including cystoid macular edema, cataract formation, and ERM regrowth.
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FIGURE 160.7 (a) ERM following treatment of a retinal detachment. (b) Fluorescein angiography showing ERM and retinal edema. (c) Appearance following vitrectomy with removal of ERM. |
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FIGURE 160.8 (a) Idiopathic ERM before surgery. (b) Idiopathic ERM after vitrectomy showing mild residual retinal fold. |
Numerous authors have attempted to identify prognostic indicators of postoperative vision in vitrectomy for treatment of ERMs. Indicators that have been mentioned are (1) preoperative visual acuity, (2) duration of diminished acuity before surgery, (3) the presence of preoperative cystoid macular edema, (4) the age of the patient, (5) the thickness of the epiretinal membrane, (6) idiopathic versus nonidiopathic epiretinal membranes, and (7) the presence of RPE window defects on fluorescein angiography. Trese and colleagues reported that transparent membranes had a better visual prognosis than opaque ones. They also believed that the presence of cystoid macular edema was a poor prognostic sign.[62] However, Rice and associates found that eyes with thin, transparent membranes had a poorer prognosis than eyes with thicker membranes.[92] Several additional studies found no association between the transparency of the membrane and the final postoperative vision.[69] (Ferencz JR, Mussbaum JJ, Richards SC, et al: Predictive variables in vitrectomy for idiopathic epimacular membranes. Presented at Schepens Alumni Meeting, Boston, MA, 9 Jun 1990.) Other studies have also suggested that the presence of cystoid macular edema is a poor prognostic sign.[62,92,93,94,95,96] However, larger series have shown no relationship between the presence of preoperative cystoid macular edema and the ultimate visual prognosis.[97,98,99,100] Two studies have suggested that even in eyes with severe degrees of macular edema, epiretinal membrane peeling may significantly improve visual acuity.[101,102]
It is worth noting that all of these series were performed before the advent of intravitreal triamcinolone acetonide injection, which is utilized as a surgical adjunct by many surgeons when substantial preoperative cystoid macular edema is identified. It is well recognized that even total removal of ERMs (clinically and by postoperative OCT) may not achieve normal macular thickness in all eyes.
The presence of portions of the internal limiting membrane in surgical specimens has been evaluated as a possible prognostic factor in epiretinal macular membrane surgery. Sivalingam and associates found that surgical specimens from eyes containing long segments of internal limiting membrane had a less favorable visual prognosis.[103] Other series did not find a similar correlation.[104,105] Some surgeons prefer to remove ILM as a routine part of ERM surgery cases, with one preliminary study suggesting a lower incidence of membrane recurrence.[106]
Nonidiopathic ERMs (particularly those following retinal reattachment surgery) have been demonstrated to have an overall worse prognosis than idiopathic ERMs. This is correlated with antecedent macular damage related to underlying pathology such as a prior macula off retinal detachment or macular ischemia or severe cystoid macular edema secondary to retinal vascular disease. A recent paper studying ERM removal in eyes following retinal detachment repair by Council and co-authors noted that 88% of eyes experienced an improvement in acuity postoperatively with 65% of eyes 20/60 or better; 6.7% of eyes had a recurrent retinal detachment.[107]
In those patients undergoing surgery for removal of idiopathic ERMs, 80-90% of patients will gain 2 Snellen lines.[93,108,99] A 2 line gain was seen in 65-80% of patients with membranes associated with previous retinal tear or detachment.[108,99,109] While the Snellen acuity improvement may be limitied in some, the metamorphopsia is improved in most. In a series of 328 eyes, Margherio, Cox, and Trese demonstrated visual acuity improvement of at least 2 lines in 74% of patients. Twenty-four percent were unchanged, and 2% were noted to have a reduction in their preoperative visual acuity level.[99] Twenty-five to fifty percent of eyes will achieve a final acuity of 20/40 or better.[93,99,109,96] Thompson, in a recent review of eyes with 20/50 or better preoperative acuity, reported that mean postoperative pseudophakic acuity improved to 20/32.[110] Some patients will describe a relief of metamorphopsia or diplopia which appears more rewarding to them than their return of Snellen acuity.[111]
SURGICAL COMPLICATIONS
The most common postoperative complication following vitrectomy for epiretinal membrane is progressive nuclear sclerotic cataract in the phakic patient. This has been reported in 12% to nearly 70% of patients.[93,99,109,94,95,100,96,112] It is not uncommon for patients to experience a gradual improvement in vision follow vitrectomy surgery, followed by an insidious decline as the nuclear sclerosis progresses. The final best-corrected visual acuity may very well be following cataract extraction. For this reason, some surgeons routinely recommend combined phacoemulsification, posterior chamber intraocular lens implantation and ERM removal in patients with any preexisting nuclear sclerosis. The cataract surgery is performed first, followed by the vitrectomy surgery. Even patients without preexisting nuclear sclerosis are generally told to expect more rapid progression of lens changes with a likelihood of cataract surgery within several years.
From the opposite perspective, patients with visually significant cataracts and ERMs judged to be clinically insignificant should be informed that cataract surgery may carry with it a higher postoperative incidence of cystoid macular edema and worsening of the ERM.
Peripheral retinal tears are encountered in up to 6% of cases.[38,93,108,99,109,96] Tears are likely related to the insertion of instruments through the vitreous base with resultant peripheral retinal traction. In cases where the posterior cortical vitreous remains attached, inducing a vitreous separation can also lead to peripheral retinal tears. When identified, these tears should be treated with either transcleral cryotherapy or laser photocoagulation, and occasionally fluid-air or gas exchange. Posterior retinal breaks resulting from iatrogenic traction are uncommon. Late retinal detachments have been reported in up to 7% of patients undergoing vitrectomy surgery and are largely related to missed peripheral tears or subsequent contraction of the vitreous base or incarcerated vitreous with resultant tear formation.[93,108,112]
The recurrence of significant epiretinal tissue following vitrecomy is seen in up to 5% of patients, depending on the underlying etiology.[93,108,99,96] Whether the use of dyes and substances to identify the membrane and/or internal limiting membrane peeling will reduce this risk of recurrence is unclear. Only a small percentage of membrane regrowths become visually significant. Other complications including endophthalmitis, retinal phototoxicity, choroidal neovascularization, macular hole, and visual field defects have also been described.[113]
CONCLUSION
Macular epiretinal membranes most commonly represent an idiopathic growth of transparent tissue across the macular region. The majority of these membranes are not visually significant and do not require treatment. A minority of ERMs are associated with a wide variety of ocular conditions generally involving inflammation or retinal vascular leakage or prior retinal detachment. Surgical intervention should be considered when warranted by visual symptomatology. A discussion regarding realistic postsurgical outcomes and well as the potential risk of vitrectomy needs to be carried out prior to proceeding with surgery. Vitrectomy with membrane removal results in symptomatic improvement in a vast majority of patients and plays a very important role in managing patients with this relatively common condition.
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