Vitreomacular traction and Epiretinal membrane

Author: Ameen Marashi, MD

History

Documentation of age, duration of visual loss is essential, which includes reduced vision, difficulty in seeing in both eyes, central photopsia, micropsia, metamorphopsia, diplopia; however, it can be asymptomatic in some patients especially for those presented with noncentral ERM.

It is essential to document familial and ocular history such as ocular inflammation, peripheral retinal break, retinal detachment [1] previous ocular or head trauma, vitrectomy, or cataract extraction surgery to this eye and if there is a history of treatment with laser photocoagulation or cryopexy, this will help to differentiate the idiopathic ERM from secondary ERM.

Systemic history of retinal vascular diseases such as diabetic retinopathy and retinal vein occlusion that may induce cystoid macular edema; older females are more prone to develop epiretinal membrane than men [2].

Ocular Examination

A list of ocular examination should set

1) Best-corrected visual acuity (BCVA) for near and far is an essential step that can be performed by a trained optometrist or certified ophthalmologist to document the visual impairment. As a better visual acuity at baseline, the better visual outcome post-surgery, the same applies for contrast sensitivity.

2) A slit-lamp examination done with a thorough exam of clarity and regularity of the cornea and conjunctival abnormality such injection of conjunctival vessels should be documented. Any other inflammations of the conjunctiva or eyelids documented, along with iris exam to rule out posterior synechia or other findings, suggest anterior uveitis.

Crystalline lens exam to rule out cataract or intraocular lens (IOL) to document the position and clarity of the posterior capsule, its integrity whether it ruptured during cataract extraction or YAG laser capsulotomy was done.

3) Anterior hyaloid examination with retro illumination using slit-lamp microscopy to rule out tobacco dust (pigmented cells) and differentiate it from blood and inflammatory cells.

4) Intra Ocular Pressure (IOP) documentation is essential as high IOP may be associated with patients with glaucoma history; Note when high IOP spotted a corrected IOP documented after central corneal thickness measurement

5) Bilateral dilated fundus exam is an essential and detailed examination of the optic disc, macula, posterior pole, a mid-peripheral and peripheral retinal exam with specialized indirect wide-field lenses using slit-lamp biomicroscopy using wide-field lenses and indirect ophthalmoscopy with scleral indentation [3] to document the following:

  1. Core and posterior cortical of the vitreous searching for pigmented, blood, and inflammatory cells along with the presence of the Weiss ring.

  2. Documenting the extent of posterior vitreous detachment and syneresis if possible as VMT with ERM has a detached vitreous in the mid periphery where ERM without VMT the vitreous would be attached in the mid periphery [4].

  3. Posterior pole examination to rule out the presence of a full-thickness macular hole

  4. Peripheral and mid-peripheral retinal exam to rule out lattice degeneration, tufts, degenerative schisis, retinal breaks, retinal dialysis, and vascular avulsion.

  5. The Watzke-Allen sign evaluated by shining the slit-lamp on the full-thickness macular hole and make sure the patient sees a break in the slit lamp light confirming a positive test

  6. Retinal exam in case of ocular trauma history should rule out the presence of choroidal rupture, commotio retinae, and retinal hemorrhages.

  7. Vitreomacular traction appears as taut glistering faintly translucent membrane presenting the residual vitreomacular adhesion; it can vary in size and shape.

  8. Epiretinal membrane appears in early stages as cellophane maculopathy, which presented as semi translucent membrane avascular fibro cellular membranes (grade 0) may cause wrinkling (grade 1) without causing distortion of underlying retinal tissues.

  9. ERM can be presented as macular pucker, which appears as an opaque membrane (grade 2) that causes pulling on retinal vessels causing vascular tortuosity, laying on the inner surface of the retina at the fovea and parafoveal area. ERM best visualized using a red-free filter.

  10. A gap in ERM may cause a macular pseudohole, which features a rounded or oval reddish central area surrounded by the epiretinal membrane.

  11. VMT and ERM can cause macular edema with or without cystic changes and sometimes intraretinal hemorrhage and cotton wool spots (in cases of full-thickness retinal distortion) and should be differentiated from other pathologies causing these intraretinal abnormalities. However, the lamellar hole is less likely to form due to ERM ruptures the inner retinal tissues.


Diagnostic tests


Fundus images

Fundus images may help to differentiate the secondary from idiopathic ERM as it reveals any associated pathology along with monitoring progression and grading of ERM/VMT.

Any ERM or VMT associated retinal vascular changes, including microaneurysms, neovascularization, intraretinal microvascular abnormalities, or/and intraretinal hard exudates, cotton-wool spots, intraretinal dot-blot hemorrhages, pre retinal or vitreous hemorrhage may indicate that the vitreomacular abnormalities secondary to diabetic retinopathy. The same principle applies for retinal vein occlusion, especially when there is retinal vein dilated and tortuous along with intraretinal or/and flamed shape hemorrhages the vitreomacular abnormalities are secondary to retinal vein occlusion.

In cases that there are vitreomacular abnormalities such as ERM or/and VMT, but there are vitritis, signs of retinitis, choroiditis, or chorioretinitis with or without vasculitis, the vitreomacular abnormalities are secondary to uveitis. However, in cases of retinitis pigmentosa, there are bone spicule peripheral retinal pigmentations with retinal vascular attenuation and pale optic disc; any associated vitreomacular abnormalities are secondary.

Idiopathic ERM or VMT not associated with other retinal vascular or inflammatory pathology and fundus image can show retinal changes associated with vitreomacular abnormalities such as dragging retinal vessels, macular edema and in cases of full-thickness retinal distortion, retinal hemorrhages and cotton wool spots can be changed in advance stages there would be a lamellar or pseudo macular hole formation.

Fundus images can help to grade and monitor the progression of ERM, which appears in grade 0 as a semi translucent membrane. In grade 1, it will show wrinklings without any distortion of underlying retinal tissues where grade 2 will show opaque membrane pulling on retinal vessels, causing tortuosity and sometimes foveal ectopia. However, VMT presented as taut glistering faintly translucent membrane.

Optical coherence tomography (OCT)

The OCT is essential to diagnose and monitor vitreomacular abnormalities as ERM may appear as a hyperreflective band over the inner surface of the retina forming pegs from the inner retinal tissues forming hyporeflective pockets and corrugated inner retinal surface. The attachment can be broad in idiopathic ERM, while in secondary ERM, there would be multiple inner retinal attachments [5] .

The hyperreflective band can be thin in cellophane maculopathy and thick in a macular pucker.

The ERM looks like a scroll of tissue adjacent to the inner retinal surface, in cases of spontaneous release of ERM [6]

Usually, there would be an elevation of foveal depression, and inner retinal tissues will have folds along with retinal tissue thickening with or without the intraretinal cystic formation and subretinal fluids along with disruption of the ellipsoid zone. In advanced cases, a pseudo hole or lamellar hole may develop.

VMT features non-complete detachment of the posterior cortical hyaloid in the perifoveal area with a plate-like attachment on the center of the fovea and oblique anterior-posterior traction of the posterior cortical vitreous and may induce oval or tubular intraretinal cystic spaces [7].

The posterior cortical hyaloid may feature proliferative contractive characteristics that appear non-mobile, taut and thick, leading to ERM. On the other hand, the posterior cortical hyaloid may be presented as non-proliferative, which appears to be mobile, and thin leading to form anterior-posterior traction and even, in some cases, macular hole [35].

The vitreomacular attachment can be measured with OCT as small attachments are about 500 μm, which is usually combined with intraretinal cystic formation. In comparison, broad attachments that are about 1500 μm may induce macular detachment but are less prone to spontaneous release and less like to form intraretinal cystic spaces [8]. However, in some cases of VMT, an avulsion of inner retinal tissue occurs in process VMT release, causing a lamellar hole.

In cases of VMT with diabetic macular edema, it can be associated with diffuse thickening of the macula with or without cystic changes and subretinal fluids.

Some cases may be presented as vitreopapillary traction and may appear clinically as swollen optic disc, which may confuse with other optic disc diseases.

In cases combined with VMT and ERM, both up mentioned features could be found, along with splitting in posterior cortical hyaloid sometimes are witnessed.

When ERM and VMT are together, the chances of spontaneous release of ERM are higher.

One of the most important biomarkers of OCT in ERM and VMT the integrity of the ellipsoid zone and interdigitation pre-operatively as disruption of these layers along with severe disorganization of inner retinal layers have poor post-surgical prognosis and vice versa. [9]

OCT is essential to assess the natural course while observation or surgical success to release vitreomacular adhesion and normalizing retinal anatomy [10].

Pseudo hole presents with verticalization and thickening of the macula and reshaping the fovea in U or V shape without any focal tissue loss; the Enface OCT would show the hole surrounded with the smooth area and then retinal folds corresponding the distribution of the epiretinal membrane [33].

OCT angiography (OCTa)

OCTa may show vascular traction and help to differentiate the idiopathic ERM from secondary by revealing underlying retinal vascular pathologies such as aneurysmal changes, neovascularization, collateral vessels, or ischemic changes along with choroidal neovascularization.

Fluorescein Fundus Angiography (FFA)

ERM may not show any vascular leakage at the early stages, but it will show wrinklings of retinal tissues along with epicentral retinal vascular traction and straightening and sometimes foveal ectopia, but in late stages, it might show non uniformly circular leak and staining [11]

When fundus image can’t diagnose the underlying pathology associated with secondary vitreomacular abnormalities.

FFA is useful in these cases as it shows hyperfluorescence from microaneurysms and may show leak in late stages along with showing any associated subtle NVE, NVD, or intraretinal microvascular abnormalities which indicates that vitreomacular abnormality is due to diabetic retinopathy. In these cases, when are combined with leaking microaneurysms and cystoid changes on OCT with a vitreomacular abnormality, not causing significant inner retinal distortion may indicate that vitreomacular abnormality not the primary cause of the edema and help the physician to tailor a treatment plan. Nevertheless, when planning to do PPV to release vitreomacular traction, FFA may reveal macular perfusion status, for that in cases of ischemic maculopathy may hold bad visual prognosis.

In cases of vitreomacular abnormality and FFA shows delayed retinal vein filling and collateral vessels with or without retinal hypoperfusion or block fluorescence due to retinal hemorrhages may indicate the vitreomacular abnormality is secondary to retinal vein occlusion.

In some cases, vitreomacular abnormality secondary to choroidal neovascularization, which FFA can show leakage or/and pooling from choroidal neovascularization along.

FFA can be useful as well in diagnosing vasculitis and chorioretinitis along with hereditary retinal diseases, FFA may show as well capillary dilatation with telangiectasia and central macular petaloid leak with staining of the optic disc in pseudophakic cystoid macular edema.

Managing patients with VMT and ERM


Treatment options


Pars Plana Vitrectomy (PPV)

PPV with ILM peeling using a wide-field viewing system and transition to sutureless PPV has shortened the operation time and improved postoperative recovery and results.

PPV offers a high success rate of vitreomacular traction, combined surgery with cataract removal and intraocular lens (IOL) implantation considered in patients above 60 years old.

The principle of PPV is to induce complete posterior vitreous detachment (PVD) with complete vitreous removal and to stain the ILM and to peel it along with epiretinal membrane (ERM) removal (if presented) then to put air or gas tamponade.

Preoperatively consideration includes the ban of air traveling and to examine the retinal periphery to rule out any retinal breaks and to manage it with laser retinopexy preoperatively.

Surgical techniques:

The type of anesthesia depends on surgeon preference as young patients require general anesthesia while other simpler cases may be done with local anesthesia and sedation.

When using the trocar system, the available sizes are 23, 25, and 27 gauge the conjunctiva displaced using cotton applicator or conjunctival forceps. The trocar knife is inserted 30 degrees into the sclera then perpendicular to create a self-sealed scleral incision 4.00 mm from the limbus in phakic eyes and 3.5 mm in pseudophakic or aphakic eyes.

The trocar is inserted in the inferior temporal just below the horizontal meridian, and this site is used for infusion cannula. The infusion is turned on before inserting it to release air bubbles, then inserted.

Insertion of infusion in the intravitreal cavity should be inspected under the microscope with an external light source. Care is taken, not to insert the infusion cannula in the suprachoroidal space.

While the other trocars one trocar is inserted in the superior nasal. The trocar is inserted from the lowest point of the nose bridge, and the additional trocar is interested in the superior temporal.

Areas of conjunctival scar or abnormalities should not be used as trocar insertion sites. If a 20 gauge system is used then, conjunctival peritomy is needed and sclerotomies made with MVR blade and the inferior temporal sclerotomy made after placing fixation suture which will fixate the infusion cannula.

The core vitrectomy is initiated, and the core vitreous removed posterior vitreous detachment (PVD) is provoked if it is not already presented using triamcinolone [12] which stains the vitreous and helps to complete removal of posterior vitreous, care must be taken not to induce iatrogenic retinal break while inducing PVD [13], it is advisable to complete removal of vitreous up to Ora with vitreous base shaving as this will reduce the risk of iatrogenic retinal break formation.

In the case of the epiretinal membrane presented, it can be stained with trypan blue or negatively stained with Brilliant Blue and removed with forceps after elevating its edge with a diamond-dusted scraper. However, when there is a very adherent area, the membrane is peeled in multiple locations leaving only the adherent area to the last so it is peeled gently and won’t exert traction on the surrounding retinal tissue. In contrast, when the membrane, not adherent firmly on the inner retinal surface, it can be removed with end gripping forceps opened and gently pressed into the inner retinal surface, and the membrane is gripped after closing the forceps and removed with applying tangential traction. However, to avoid damaging inner retinal tissue, a grasping of ERM by slightly reopening the forceps after applying the first traction to release any gripped retinal tissue initially and then regripping of the ERM and removed by applying tangential traction.

ILM is stained with Brilliant Blue 0.025% (0.25mg/ml) for several seconds [14], but ILM can be stained with trypan blue as well but after fluid-air exchange [15] or ICG 0.05 % for less than 30 seconds to avoid RPE toxicity [16].

The ILM is pinched by ILM end grasping forceps from the temporal of the macula to avoid harming the RNFL in the nasal to the fovea. After flap creation, the ILM is peeled in a circular motion [16] (macular rhexis), peeling all the ILM up to the arcades.

A peripheral retinal examination with scleral indication searching for any iatrogenic retinal breaks, which are managed with endo laser photocoagulation with three confluent rows of laser burns where cryopexy can be used in anterior breaks.

During the last ten minutes during fluid air exchange, the nitrous oxides are turned off in general anesthesia to avoid unpredictable post-operative gas expansion.

Fluid-air exchange continues to remove any water from the eye, then the air is used as a tamponade, but when there is a suspicion of the presence of a macular hole, then air gas exchange either by 20% SF6, 16% C2F6, or 14% C3F8.

All sclerotomies are closes with 8.0 vicryl suture, especially when silicone oil used as tamponade and subconjunctival steroids and antibiotic injection administered.

The down head position should be maintained for 10-14 days for cases suspected to have a macular hole.

Postoperative complications:

Cataract one of the most common postoperative complications up to 65% [17] especially for patients above 60 and can reduce the visual significantly and manages with cataract removal by phacoemulsification and IOL implantation combined with vitrectomy or post vitrectomy

Retinal detachment or/and retinal breaks usually an iatrogenic retinal break that occurs in the inferior retina and may lead to retinal detachment (up to 14% of cases). [18] This can be avoided easily by managing any existing retinal breaks preoperatively or/and complete vitreous removal and vitreous base shaving and using smaller gauge sclerotomies along with inspecting retinal periphery for retinal breaks and managing them as mentioned above.

Other complications such as low rate of endophthalmitis up to 0.05% and macular hole formation, recurrence of the ERM in less than 20% [19] of cases, and visual field defect.


Pneumatic vitreolysis

This procedure aims to minimize the costs of surgical intervention to release a vitreomacular traction adhesion.

The principle of pneumatic vitreolysis is in office injecting of pure gas to induce posterior vitreous detachment to facilitate vitreomacular traction release then the postoperative head posture.

Presurgical consideration before pneumatic vitreolysis includes:

•Patients cannot maintain head position due to neck or back problems, or patients are not mentally competent, are not candidates for this procedure as it requires drinking bird head position (face down position with bobbing the head up every 10 min) for ten days.

• Any preexisting retinal breaks and lattice degeneration requires prophylactic laser retinopexy.

• Cases presented with certain vitreofoveal traction (e.g., less than 1500 μm ) without epiretinal membranes and phakic patients are the best candidates.

• In contrast, large vitreofoveal traction with or without epiretinal membranes is not the best candidate for this procedure.

• All mentioned above should be explained to the patient with details, and the patient should understand that this procedure requires postoperative head posture and that this procedure is prone to failure and may need further surgical intervention or even may induce postoperative retinal detachment.

Surgical technique:

Usually 0.3 ml of pure C3F8 or 0.3 ml of pure SF6 used in pneumatic vitreolysis, the syringes are filled using a 20 mm filter after evacuating all air from the syringe.

The injection should be carried out in sterile conditions where the injection site is prepared by disinfecting the skin using povidone-iodine 10%.

After installing topical anesthesia, and the conjunctiva disinfected using povidone-iodine 4%. Then placing sterile drape and lid speculum isolating eyelashes, a paracentesis performed first. Injection site measured with calipers 4 mm from the limbus in phakic patients and 3.5 mm in pseudophakic or aphakic patients. A 30 gauge half-inch needle is used to inject gas perpendicularly in the uppermost site needle should penetrate only one-third of the needle and inject moderately and briskly. The head is rotated before withdrawing the needle.

The IOP is assessed along with patency of central retinal artery, which should be checked using ophthalmoscopy; if this failed to achieve, then secondary paracentesis is required.

In case that fish eggs occurred the gas bubbles will coalesce spontaneously within 24 hours.

Postoperative complications:

New or missed retinal breaks may be treated with laser photocoagulation if not associated with retinal detachment, as the gas itself may be the cause of new retinal tears. However, cases with new retinal breaks associated with retinal detachment managed with pars plana vitrectomy.


Pharmacological vitreolysis

The principle of pharmacological vitreolysis is in office injecting of ocriplasmin to induce posterior vitreous detachment to facilitate macular hole closure to release vitreomacular traction.

Presurgical consideration before pharmacological vitreolysis includes:

• Any preexisting retinal breaks and lattice degeneration requires prophylactic laser retinopexy.

• Cases presented with certain vitreofoveal traction (e.g., less than 1500 μm) without epiretinal membranes are the best candidates.

•In contrast, large vitreofoveal traction with or without epiretinal membranes is not a good candidate for this procedure.

•All mentioned above should be explained to the patient with details, and the patient should understand that this procedure is prone to failure and may need further surgical intervention or even may induce postoperative retinal detachment.

Injection technique:

Ocriplasmin should be diluted first as it comes in vial 0.5 mg in 0.2 ml and kept freeze then it thawed after that a sterile 0.2 ml of sodium chloride solution 0.9 % is injected in the vial after swapping it with alcohol and then swirled until the solution is clear without any participates then 0.1 ml is withdraw using the 19 gauge needle and then the needle changed to 30 gauge needle for injection of 0.125 mg of ocriplasmin.

The injection should be carried out in sterile conditions where the injection site is prepared by disinfecting the skin using povidone-iodine 10%.

After installing topical anesthesia, and the conjunctiva disinfected using povidone-iodine 4%. Then placing sterile drape and lid speculum isolating eyelashes

Injection site measured with calipers 4 mm from the limbus in phakic patients and 3.5 mm in pseudophakic patients. A 30 gauge half-inch needle is used to inject ocriplasmin 0.125 mg in 0.1ml diluted solution.

Postoperative complications:

New or missed retinal breaks may be treated with laser photocoagulation if not associated with retinal detachment, as ocriplasmin itself may be the cause of new retinal tears. However, cases with new retinal breaks associated with retinal detachment managed with pars plana vitrectomy.

Other complications may occur, such as visual field defect, blue color dyschromatopsia, macular hole, floaters, photopsia, and weakening of lens zonules and subluxation[20].


Treatment plan

In the case of VMT/ERM with good vision more than 20/60

-When VMT presented with stable visual acuity and vitreomacular adhesion, less than 1500 μm are observed as a spontaneous release of vitreomacular adhesion that may occur by 47% within two years [21]. Especially is those small VMT with no ERM.

-ERM tends to be stable by 39% of cases, and vision might not change in 38 months follow up therefor, if the patient presented with good visual acuity without metamorphopsia or diplopia, then only follow up recommended [22]; however, in cases of ERM not associated with PVD, ERM separation by 13.6% and those cases associated with PVD, separation of ERM may occur in 1.3%.

-The patient instructed to do self-monitoring using the Amsler grid and schedule for an eye exam whenever worsening of symptoms occurs; otherwise, OCT should be repeated every three months to monitor the progression of VMT/ERM.

In the case of VMT with vision less than 20/60 or/and metamorphopsia or diplopia

- In cases VMT is less than 1500 μm without ERM pneumatic vitreolysis may release the vitreomacular traction up to 60% [23] or pharmacological vitreolysis may release the vitreomacular traction up to 35% [19] therefor pneumatic vitreolysis may be a more cost-effective treatment. Especially in patients with VMT around 600 μm with central macular thickness is less than 360 μm, non-highly myopic, with no AMD, ERM, or macular hole.

- In cases VMT is more than 1500 μm with or without ERM, especially for cases that VMT is causing macular detachment, PPV is indicated with ILM peeling. [8] This applies for secondary VMT associated with diabetic retinopathy, retinal vein occlusion, or uveitis; however, ILM peeling has a favorable outcome [24], the visual outcome is debatable.


In the case of ERM with or without VMT with vision less than 20/60 or/and metamorphopsia or diplopia

-PPV with ILM peeling [25] which offer improved visual acuity to more than 20/50 up to 55% of cases in the first six to twelve months [26] this applies for idiopathic and secondary ERM.

- The pseudo hole usually requires only observation; however, if the progressive contraction of ERM caused a drop of vision to 20/80, then PPV with ILM peeling and ERM removing is indicated.

Flow chart summarizes the approach and management of vitreomacular traction and epiretinal membrane

Follow up and prognosis


- Patients followed the first day then every week then monthly postoperatively to check IOP. The peripheral retinal exam is done to rule out retinal breaks or retinal detachment, macula best assessed with OCT post-surgery, vision may not be improved in the first weeks of follow up[30]. However, the macular thickness may take time to improve, and the foveal pit may not always be restored.

- Long-term anatomical and functional improvement can be expected in ERM cases post-operatively presented with outer retinal layer disruption within follow-up after one year. Nevertheless, full functional recovery is unlikely in patients with persistent visual loss [34].

- Although vision improves two Snellen lines up to 64% in VMT cases, patients presented with intraretinal cystic changes tend to have guarded prognosis [27], and 20% of VMT cases treated with ocriplasmin may need PPV within six months [28].

- In cases of VMT associated with diabetic macular edema, PPV may offer success rate up to 80% with an improvement of vision up-to ten letters in 38% of patients, while 22% of patients may get worse with a significant reduction in central macular thickness[32].

- ERM may progress in 29% of cases and may be combined with a reduction of visual acuity in 37.4%.This is especially true in cases of vitreoretinal detachment, absence of PVD global ERM attachment, and early stages of PVD. Only 20% of cellophane maculopathy may progress [22] when the idiopathic ERM is unilateral, and the other eye may get involved in 13.5%. Recurrence of ERM may occur within 20 months within 25% of patients post-surgically[31].

- On average, the improvement in vision is about two lines, and most patients got their metamorphopsia improved or normalized, 10%-20% of patients may have a worse vision [28].

-The majority of ERMs do not require surgery, as progression is generally slow, mainly occurring in the early stages.

-Patients under 75 years of age, with symptoms less than 12 months and better preoperative vision, with preserved outer retinal anatomy, preserved inner retinal anatomy, thinner central foveal thickness, and no epiretinal proliferation are most likely to achieve successful results.

-Visual acuity may correlate poorly with other intolerable functional symptoms, whereas metamorphopsia is the key symptom that responds well to surgery.

-It might be that a higher VMT grade on OCT is correlated with a lower baseline BCVA and a poorer outcome, especially if the fovea has outer retinal dehiscence and if there are intraretinal cysts.

References

  1. Xin Rong Duan, Yuan Bo Liang, David S. Friedman, Lan Ping Sun, Wen Bin Wei, Jie Jin Wang, Guang Lu Wang, Wu Liu, Qiu Shan Tao, Ning Li Wang, Tien Yin Wong; Prevalence and Associations of Epiretinal Membranes in a Rural Chinese Adult Population: The Handan Eye Study. Invest. Ophthalmol. Vis. Sci. 2009;50(5):2018-2023. doi: https://doi.org/10.1167/iovs.08-2624.

  2. Steel DH, Lotery AJ. Idiopathic vitreomacular traction and macular hole: a comprehensive review of pathophysiology, diagnosis, and treatment. Eye (Lond). 2013;27 Suppl 1(Suppl 1):S1–S21. doi:10.1038/eye.2013.21

  3. Natkunarajah M, Goldsmith C, Goble R. Diagnostic effectiveness of noncontact slitlampexamination in the identification of retinal tears. Eye. 2003;17(5):607-609.

  4. Heilskov TW, Massicotte SJ, Folk JC. Epiretinal macular mem- branes in eyes with attached posterior cortical vitreous. Retina 1996;16(4):279–84.

  5. Watanabe K, Tsunoda K, Mizuno Y, Akiyama K, Noda T.Outer retinal morphology and visual function in patients with idiopathic epiretinal membrane.JAMA Ophthalmol. 2013 Feb;131(2):172-7. doi: 10.1001/jamaophthalmol.2013.686.

  6. Yang HS, Hong JW, Kim YJ, Kim JG, Joe SG. Characteristics of spontaneous idiopathic epiretinal membrane separation in spectral domain optical coherence tomography. Retina 2014; 34(10):2079–87.

  7. Bottos J, Elizalde J, Rodrigues EB, Farah M, Maia M. Vitreomacular traction syndrome: postoperative functional and anatomic outcomes. Ophthalmic Surgery, Lasers & Imaging Retina. 2015 Feb;46(2):235-242. DOI: 10.3928/23258160-20150213-14.

  8. Spaide RF Vitreomacular traction syndrome. Retina. 2012 Sep;32 Suppl 2:S187-90; discussion S190-3. doi: 10.1097/IAE.0b013e31825befb6.

  9. Kim HJ1, Kang JW, Chung H, Kim HC. Correlation of foveal photoreceptor integrity with visual outcome in idiopathic epiretinal membrane.Curr Eye Res. 2014 Jun;39(6):626-33. doi: 10.3109/02713683.2013.860990. Epub 2014 Jan 8.

  10. Falkner-Radler CI, Glittenberg C, Hagen S, Benesch T, Binder S. Spectral-domain optical coherence tomography for monitoring epiretinal membrane surgery. Ophthalmology 2010;117(4): 798–805.

  11. Wise G. Clinical features of idiopathic preretinal macular fibrosis. Am J Ophthalmol 1975;79(3):349–57.

  12. Shah GK, Rosenblatt BJ, Blinder KJ, Grand MG, Smith M. Triamcinolone-assisted internal limitingmembrane peeling. Retina. 2005;25(8):972-975.

  13. Enaida H, Hisatomi T, Hata Y, et al. Brilliant blue G selectively stains the internal limiting membrane/brilliant blue G-assisted membrane peeling. Retina 2006;26(6):631–6

  14. Grisanti S, Szurman P, Tatar O, et al. Histopathological analysis in experimental macular surgery with trypan blue. Br J Ophthal- mol 2004;88(9):1206–8.

  15. Stalmans P, Van Aken EH, Veckeneer M, et al. Toxic effect of indocyanine green on retinal pigment epithelium related to osmotic effects of the solvent. Am J Ophthalmol 2002;134(2): 282–5.

  16. Williamson T Macular disorders. Vitreoretinal surgery: Springer- Verlag Berlin Heidelberg; 2008. p. 120.

  17. Wong JG, Sachdev N, Beaumont PE, Chang AA. Visual outcomes following vitrectomy and peeling of epiretinal membrane. Clin Exp Ophthalmol 2005;33(4):373–8.

  18. Sandali O, El Sanharawi M, Basli E, et al. Epiretinal membrane recurrence: incidence, characteristics, evolution, and preventive and risk factors. Retina 2013;33(10):2032–8.

  19. Stalmans P, Benz MS, Gandorfer A, et al. Enzymatic vitreolysis with ocriplasmin for vitreomacular traction and macular holes. N Engl J Med 2012;367(7):606–15.

  20. Johnson MW. How should we release vitreomacular traction: surgically, pharmacologically, or pneumatically? Am J Ophthalmol. 2013;155(2):203–205. e1.

  21. Theodossiadis GP, Grigoropoulos VG, Theodoropoulou S, Datseris I, Theodossiadis PG Spontaneous resolution of vitreomacular traction demonstrated by spectral-domain optical coherence tomography. Am J Ophthalmol. 2014 Apr;157(4):842-851.e1. doi: 10.1016/j.ajo.2014.01.011. Epub 2014 Jan 18.

  22. Wiznia RA.Natural history of idiopathic preretinal macular fibrosis. Ann Ophthalmol. 1982 Sep;14(9):876-8.

  23. Rodrigues IA, Stangos AN, McHugh DA, Jackson TL. Intravitreal injection of expansile perfluoropropane (c(3)f(8)) for the treat- ment of vitreomacular traction. Am J Ophthalmol 2013; 155(2):270–6.e2.

  24. Bahadir M, Ertan A, Mertoglu O. Visual acuity comparison of vitrectomy with and without internal limiting membrane removal in the treatment of diabetic macular edema. Int Oph- thalmol 2005;26(1–2):3–8.

  25. Rahman, R., Stephenson, J. Early surgery for epiretinal membrane preserves more vision for patients. Eye 28, 410–414 (2014). https://doi.org/10.1038/eye.2013.305

  26. Scheerlinck LM, van der Valk R, van Leeuwen R. Predictive factors for postoperative visual acuity in idiopathic epiretinal mem- brane: a systematic review. Acta Ophthalmol 2015;93(3): 203–12.

  27. Hikichi T, Yoshida A, Trempe CL Course of vitreomacular traction syndrome Am J Ophthalmol. 1995 Jan;119(1):55-61.

  28. Neffendorf JE, Kirthi V, Pringle E, Jackson TL. Ocriplasmin for symptomatic vitreomacular adhesion. Cochrane Database Syst Rev. 2017;10(10):CD011874. Published 2017 Oct 17. doi:10.1002/14651858.CD011874.pub2

  29. Ghazi-Nouri SM, Tranos PG, Rubin GS, Adams ZC, Charteris DG. Visual function and quality of life following vitrectomy and epiretinal membrane peel surgery. Br J Ophthalmol. 2006;90(5):559–562. doi:10.1136/bjo.2005.085142

  30. Klein R, Klein BE, Wang Q, Moss SE. The epidemiology of epiretinal membranes. Trans Am Ophthalmol Soc 1994;92: 403–30.

  31. McLeod D, Hiscott PS, Grierson I. Age-related cellular prolifera- tion at the vitreoretinal juncture. Eye 1987;1:263–81.

  32. Noma H, Funatsu H, Mimura T, Shimada K. Visual acuity and foveal thickness after vitrectomy for macular edema. Ophthal- mologica 2010;224(6):367–73.

  33. Haouchine B, Massin P, Tadayoni R, et al. Diagnosis of macular pseudoholes and lamellar macular holes by optical coherence tomography. Am J Ophthalmol 2004;138(5):732–9.

  34. Ozdek, S., Ozdemir Zeydanli, E., Karabas, L. et al. Relation of anatomy with function following the surgical treatment of idiopathic epiretinal membrane: a multicenter retrospective study. Graefes Arch Clin Exp Ophthalmol (2020). https://doi.org/10.1007/s00417-020-05002-1

  35. Yoko Ito, Yuki Takatsudo, Peter L. Gehlbach, Keisuke Mori, Mechanistic Insights into the Pathogenesis of Proliferative and Non-proliferative Vitreomacular Traction, American Journal of Ophthalmology, 2021, ISSN 0002 9394, https://doi.org/10.1016/j.ajo.2021.11.026.

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These guidelines were reviewed and updated in December 2022