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 Table of Contents  
REVIEW ARTICLE
Year : 2014  |  Volume : 4  |  Issue : 2  |  Page : 63-68

Vitreomacular interface diseases: Diagnosis and management


Cole Eye Institute, Cleveland Clinic Foundation, Cleveland, OH, USA

Date of Web Publication6-Jun-2014

Correspondence Address:
Peter K Kaiser
Cole Eye Institute, Cleveland Clinic Foundation, 9500 Euclid Avenue i-13, Cleveland, OH 44195
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.1016/j.tjo.2013.12.001

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  Abstract 


This article discusses the diagnosis and management of abnormal vitreomacular interfaces disorders including vitreomacular adhesion, vitreomacular traction, epiretinal membrane, full thickness macular holes, lamellar holes and pseudoholes. Optical coherence tomography has better enabled our ability to diagnose abnormalities of the vitreoretinal interface by providing clinical information that cannot be obtained by other ophthalmic diagnostic techniques. While vitrectomy remains the most commonly performed treatment for these disorders, the recent introduction of pharmacologic vitreolysis represents the development of non-surgical treatment options of certain diseases of the vitreoretinal interface.

Keywords: epiretinal membrane, lamellar hole, macular hole, pseudohole, vitreomacular adhesion, vitreomacular interface disorders, vitreomacular traction


How to cite this article:
Levison AL, Kaiser PK. Vitreomacular interface diseases: Diagnosis and management. Taiwan J Ophthalmol 2014;4:63-8

How to cite this URL:
Levison AL, Kaiser PK. Vitreomacular interface diseases: Diagnosis and management. Taiwan J Ophthalmol [serial online] 2014 [cited 2020 Sep 21];4:63-8. Available from: http://www.e-tjo.org/text.asp?2014/4/2/63/204027




  1. Introduction Top


The vitreous fills the space between the lens and the ciliary body anteriorly and the lens and the retina posteriorly. The vitreous comprises approximately 80% of the volume of the eye. It is composed of approximately 98% water and 2% proteins and an extracellular matrix. Collagen is the major structural protein; type II collagen and type IX collagen are the most common proteins, and make up 75% and 15%, respectively, of the collagen in the vitreous.[1],[2] The vitreous also contains hyaluronan, chondroitin sulfate, fibrillins, and opticin.

The strongest points of attachment of the vitreous to the retina are at the optic nerve, macula, ora serrata, and around the blood vessels.[3] The equatorial and posterior vitreoretinal interfaces consist of the posterior vitreous cortex, the internal limiting membrane (ILM), and the intervening extracellular matrix.[1] The ILM is primarily composed of type IV collagen. The posterior vitreous cortex and retinal ILM are bound at their interface by this macromolecular attachment complex, which is composed of fibronectin, laminin, and other extracellular components that form a glue-like matrix. Chondroitin sulfate is present at this interface and has an important role in the strong vitreoretinal interface.[1]

The normal aging process of the vitreous gel causes the development of posterior vitreous detachment (PVD). Liquefaction of the vitreous occurs over time, thereby creating lacunae or pockets in the vitreous.[1] Synchysis (i.e., the process of vitreous gel liquefaction) first begins at approximately the age of 4 years.[2] Vitreoretinal separation normally occurs at many sites throughout the peripheral fundus. This process occurs for years prior to a final separation of the vitreous from the macula and optic nerve occurs and leads to PVD. The early stages are typically asymptomatic.[4] Posterior vitreous detachment normally results in a complete and clean separation between the ILM of the retina and the cortical vitreous.[5]

An anomalous separation of the vitreous cortex from the ILM can lead to an abnormal vitreoretinal interface. This separation can happen when liquefaction occurs faster than the detachment of the vitreous cortex or when an abnormal adhesion of the vitreous cortex to the ILM occurs.[6] Various pathologic vitreomacular interface diseases can develop when there is an anomalous PVD.[7]

Most abnormal vitreomacular interface diseases were historically diagnosed by slit lamp biomicroscopy with or without the addition of fluorescein angiography. Thus, many subtle alterations to the vitreomacular interface were often missed clinically. The introduction of optical coherence tomography (OCT) approximately two decades ago has dramatically altered the ability to diagnose abnormalities of the vitreoretinal interface by providing clinical information that cannot be obtained by other ophthalmic diagnostic techniques. In 2004, the development of spectral domain OCT, which has increased resolution and more rapid scanning capabilities, has permitted physicians to visualize and monitor the vitreomacular interface with better consistency and accuracy.[8]

In this manuscript, we will explore the diagnosis and management of abnormal vitreomacular interfaces diseases such as vitreomacular adhesion (VMA), vitreomacular traction (VMT), epiretinal membrane (ERM), full-thickness macular holes (FTMH), and lamellar holes and pseudoholes [Figure 1].
Figure 1: Disorders of the vitreoretinal interface. (A) Vitreomacular adhesion, which is adhesion of the vitreous at the fovea without distortion of the retinal contour. (B) Vitreomacular traction, which is abnormal vitreous adhesion with excessive traction of the fovea that causes pseudocyst formation. (C) Full-thickness macular hole, which is a full-thickness retinal defect with posterior vitreous detachment. (D) Epiretinal membrane, which has cellular proliferation on the surface of the inner retina that creates traction and loss of the foveal contour. (E) Lamellar hole, which is a partial-thickness foveal defect with an irregular foveal contour and a splitting of the inner and outer retina. (F) Pseudohole, which is an epiretinal membrane with a central opening that causes a steep macular contour at the central fovea.

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  2. Vitreomacular adhesion Top


The diagnosis of VMA is applied to patients who have incomplete separation of the posterior vitreous with persistent attachment to the macula. This term has been broadly used to include patients with and without distortion of the retinal architecture; however, the term should only be used for patients who have an intact retinal architecture. In the past, VMA has been classified by symptomatic patients versus asymptomatic patients (i.e., based on a patient’s visual complaints). With the introduction of OCT, physicians have become aware that VMA is a more common entity than was previously clinically known and may be part of the normal formation of PVD.[9]

A group of retina specialists, the International Vitreomacular Traction Study (IVTS) Group, recently defined the OCT characteristics of VMA.[5] The IVTS new definition of VMA is more restrictive than the definition previously used. On OCT, VMA is a specific stage of vitreous separation when partial detachment of the vitreous in the perifoveal area has occurred without any abnormalities to the retinal contour. The slit lamp examination is clinically normal. Eyes with VMA are subclassified by the size of the adhesion. An adhesion is either focal (i.e., less than 1500 μm) or broad (i.e., greater than 1500 μm). Focal points of dehiscence between the vitreous and retina can be present within areas of broad VMA.[5] Vitreomacular adhesion is typically asymptomatic and non-pathologic, and does not cause any apparent retinal changes.[10] It is a natural component of the development of a PVD and can therefore be considered an incomplete PVD.[9],[11] Vitreomacular adhesion, although asymptomatic, has been hypothesized as playing a role in the pathogenesis of many macular conditions such as neovascular age-related macular degeneration, macular hole, and diabetic macular edema.[9]

Based on the new characterization of VMA defined by the International Vitreomacular Traction Study Group, VMA is a normal stage in the process of PVD, is not associated with symptoms, and causes no change in the retinal architecture. Treatment is not required. These patients should be observed for resolution or for the progression to vitreomacular traction or, possibly, a macular hole.[5]


  3. Vitreomacular traction Top


In certain patients with abnormal vitreous adhesion, there can be excessive traction on the macula from the vitreous that changes the contour of the foveal surface. Findings on slit lamp biomicroscopy may be subtle, but there may be a distortion of the fovea, a blunted foveal reflex, cystic changes, or (in severe cases) subretinal fluid. Optical coherence tomography allows the direct visualization of the vitreoretinal interface; therefore, very subtle distortion of the foveal contour on OCT may be the only feature that distinguishes VMT from focal VMA when the retinal anatomy is otherwise normal.[10] In addition, there may be elevation of the retina at the fovea at the level of the retinal pigment epithelium (RPE). The combination of anatomical changes on OCT with signs of perifoveolar PVD constitutes a diagnosis of VMT.[5] In accordance with the International Vitreomacular Traction Study Group definition, VMT (like VMA) can be classified as “focal” or “broad”, based on the horizontal width of the adhesion. These broad areas of attachment with traction can be associated with thickening of the macula, vascular leakage on fluorescein angiography, macular schisis, and cystoid macular edema.[5] The anatomical changes to the fovea induced by VMT can lead to reduced visual acuity,[9] metamorphopsia, and micropsia.[8]

The natural history of patients with VMT is not well established. John et al[9] performed a consecutive case series evaluating the clinical course of what they referred to as “vitreomacular adhesion”. Based on the new definitions by the IVTS, the eyes included in their study would have various levels of severity of vitreomacular traction. The IVTS defined Grade 1 as incomplete separation of the cortical vitreous with persistent vitreous attachment at the fovea and ILM. In the study by John et al,[9] eyes at Grade 1 did show evidence of abnormal foveal contour. They defined Grade 2 as eyes with the features of Grade 1 and either a intraretinal cyst, cleft, or schisis; and they defined Grade 3 as eyes with the features of Grade 2 and subretinal fluid resulting from neurosensory elevation of the retina from the retinal pigment epithelium.[9] At the end of their study, overall 32% of eyes had spontaneously resolved, including eyes from all grades. The difference in the resolution rates between the various grades was not statistically significant. The rate of a clinically worsening anatomy was also the same among the three grades. John et al[9] concluded that an initial observation period is a reasonable option for patients with at least milder forms of vitreomacular traction.

The standard treatment for severe vitreomacular traction is pars plana vitrectomy. The goal of vitreous surgery is to eliminate anteroposterior and tangential traction, thereby relieving the attachment of the vitreous to the macula. The visual acuity outcomes are mixed for pars plana vitrectomy for vitreomacular traction. Various studies have reported visual acuity improvement in approximately 44–78% of patients; vision improvement was limited by cystoid macular edema, fibrosis, chronic retinal detachment, and macular schisis.[12],[13] A recently published systematic review found that only approximately one-third of eyes gained two lines on the Snellen chart.[14] Visual acuity may not improve, although metamorphopsia often does improve.

Vitreoretinal surgery has risks such as bleeding, infection, retinal detachment, cataract development, and anesthesia risks. A meta-analysis of pars plana vitrectomy for vitreomacular traction reported that intraoperative retinal tears occur in 1.6% of eyes and postoperative retinal detachment occurs in 4.6% of eyes.[14] Therefore, nonsurgical treatment of VMT with pharmacological vitreolysis has important implications for the treatment of vitreomacular traction.[3] In October 2012, the medication ocriplasmin (Jetrea; ThromboGenics, Leuven, Belgium and Alcon, Basel, Switzerland) received FDA approval for the treatment of symptomatic VMA. Ocriplasmin is a recombinant human serine protease plasmin with proteolytic activity against several target proteins (e.g., laminin, fibronectin, and collagen) in the vitreous and vitreoretinal interface. The protease activity induces vitreous liquefaction and the separation of the vitreous from the retina, thereby creating PVD and releasing the vitreous traction.[15],[16]

The Microplasmin Intravitreal Injection—Traction Release without Surgical Treatment (MIVI-TRUST) Study Group conducted two multicenter, randomized, double-blinded Phase 3 clinical trials to compare an intravitreal injection of ocriplasmin with a placebo injection in patients with symptomatic VMA, which included VMA associated with a full-thickness macular hole.[17] The MIVI-TRUST group found that ocriplasmin can resolve VMT, induce PVD, and cause the anatomic closure of nearly 40% of macular holes. The study included 652 eyes, 464 of which received ocriplasmin and 188 of which received placebo. The VMA resolved in 26.5% of eyes treated with ocriplasmin, compared to 10.1% of the placebo-treated eyes. Total PVD occurred in 13.4% of ocriplasmin eyes, compared to 3.7% of eyes treated with a placebo. Women, phakic patients, and patients without an ERM more often met the endpoint at 28 days, compared to their counterparts.[17]

Two interventions are now available for vitreomacular traction: pars plana vitrectomy and pharmacologic vitreolysis. The risks and benefits, appropriate fit for treatment, and rate of treatment success should be considered when determining the best treatment for individual patients.


  4. Full-thickness macular hole Top


A full-thickness macular hole (FTMH) is a full thickness defect in the fovea, and includes the complete interruption of all neural retinal layers from the ILM to the retinal pigment epithelium. Anteroposterior traction, secondary to abnormal vitreoretinal attachment at the fovea, and tangential contraction of the perifoveal vitreous cortex may be responsible for the development of macular holes.[18]

Vitreoretinal specialists have classically diagnosed idiopathic FTMHs by using slit lamp biomicroscopy. It clinically appears as an eccentric oval, crescent, or central round retinal defect at the fovea. Gass’ clinical classification scheme has long been the standard for classifying macular holes. A stage 1 hole represents a partial thickness macular hole, whereas a stage 2 macular hole is a FTMH that is less than 400 microns; a stage 3 macular hole corresponds to a central round defect exceeding 400 microns but without complete PVD. A FTMH in the setting of a complete PVD is a stage 4 macular hole, regardless of the diameter of the retinal defect.[19],[20]

The Gass classification is commonly used in clinical practice; however, OCT images now further add to our understanding of macular holes. The International Vitreomacular Traction Study Group has developed an OCT-based anatomic classification system for FTMHs. The criteria are based on the size of the hole, the status of the vitreous, and on whether the etiology of the macular hole is primary or secondary. The minimum hole width is measured at the narrowest point in the mid-retina. This can be measured by using the caliper function of the OCT machine. Macular holes less than 250 microns are classified as small; holes 250–400 microns are classified as medium; and holes greater than 400 microns are classified as large.[5] The second and third components of the new IVTS classification system are the presence or absence of vitreous attachment on OCT and the etiology of the macular hole (i.e., primary or secondary). A primary macular hole is commonly referred to as an idiopathic macular hole. These are caused by vitreous traction on the fovea from an abnormal vitreous separation. A secondary macular hole is caused by other pathologies not associated with previous VMT. Examples include blunt trauma, high myopia, macular telangiectasia type 2, surgical trauma, and other causes of macular edema.

Prior to the introduction of ocriplasmin in 2012, there were only two options available for the management of macular holes: observation and surgical intervention with vitrectomy. In 1991, surgery was introduced for FTMHs.[21] Pars plana vitrectomy is performed with or without ILM peeling. In 2013, a Cochrane review was published that examined the literature regarding the effectiveness of ILM peeling.[22] The analysis indicated that more patients in the ILM peeling group had primary macular hole closure with an odds ratio of 9.27 and a 95% confidence interval (CI) of 4.98–17.24. However, there was no difference in the primary outcome of distance visual acuity at 6 months or 12 months after surgery. The final conclusion of the meta-analysis was that ILM peeling was possibly more cost effective because of the higher likelihood of primary closure and decreased likelihood of having to return to the operating room for further surgery.[22]

If the decision is made to peel the ILM, dyes that stain the ILM are commonly used to differentiate the ILM from underlying retinal layers. The most commonly used vital dye in the United States is indocyanine green (ICG).[23] On light exposure, ICG increases the stiffness of the ILM, thereby easing the peeling of the ILM. However, the use of ICG is not without risk and has been associated with toxicity, which causes RPE damage, visual field defects, and possible optic nerve atrophy.[24] Surgeons must avoid excessive light exposure because it is potentially toxic; in addition, surgeons should not hold the illumination instruments close to the retina.[23] Brilliant

Blue has also been used to stain the ILM; however, ICG remains the most consistently used agent by vitreoretinal surgeons.[25],[26]

Gas tamponade is typically used after vitrectomy for macular hole closure. Options include air, sulfur hexafluoride (SF6), and perfluoropropane (C3F8). Thompson et al[27] reported a 97% closure rate with C3F8 and a 53% closure rate with air. In their study there was no statistically significant difference between 20% SF6 gas and 16% C3F8 gas in the closure rate, regardless of the stage or duration of symptoms.[27] In general, physicians recommend using short-acting gases such as SF6 for small and medium holes (i.e., <400 microns) and long-lasting gases such as C3F8 for large holes (i.e., >400 microns).

Face-down positioning is a key component of postoperative care after macular hole surgery. In 2011, a Cochrane review was published that evaluated the role of positioning in macular hole repair. Only three randomized control trials were identified. A meta-analysis was not possible because of the heterogeneity of the duration of face-down positioning. However, each of the studies showed no benefit to face-down positioning for holes less than 400 microns. For holes larger than 400 microns, face-down positioning effectively aided hole closure after vitrectomy.[28] Most surgeons continue to use face-down positioning, regardless of the hole size.

Pharmacologic vitreolysis is a new nonsurgical option that can aid closure of macular holes that are associated with vitreomacular traction. The treatment degrades the macromolecular vitreous attachment complex and relieves the tractional forces that caused the foveal lesion. In the MIVI-TRUST study patients with FTMHs less than 400 microns in width, the closure of the holes occurred in 40.6% of ocriplasmin-treated eyes and 10.6% of placebo-treated eyes.[15],[17] In patients with small holes, the success rate was even higher. This occurred without face-down positioning, surgery, or a gas bubble. This makes it an appealing option for the appropriate patients.[17]


  5. Epiretinal membrane Top


The epiretinal membrane (ERM) is a cellular proliferation that creates a semitranslucent, fibrocellular proliferation on the surface of the inner retina. Because ERMs contain contractile cellular elements, they can be associated with retinal folding and macular thickening, thereby leading to decreased visual acuity, metamorphopsia, micropsia, and monocular diplopia. Most epiretinal membranes can be detected clinically on slit lamp examination. They appear as a reflective sheen over the retina and cause wrinkling of the retinal surface. An ERM can progressively become more opaque, thereby obscuring retinal details and leading to intraretinal fluid accumulation.[1]

Epiretinal membranes affect approximately seven percent of the population and are bilateral in 10–20% of patients.[29] In the Blue Mountain Eye Study, the 5-year incidence of ERMs was 5.3%.[29] Epiretinal membranes are idiopathic if they occur in otherwise healthy eyes. In idiopathic cases of ERM, cellular proliferation may be associated with an incomplete PVD.[30] Epiretinal membranes can also arise secondary to retinal vascular disease, diabetes, trauma, inflammatory conditions, tumors, and retinal dystrophies.

Slit lamp biomicroscopy and fluorescein angiography historically have been used to evaluate epiretinal membranes. Because of the introduction of OCT, fluorescein angiography is no longer performed, unless evaluating the etiology of the ERM such as branch retinal vein occlusion. On OCT, ERMs appear as a hyper-reflective layer on the surface of the inner retina. Epiretinal membranes may cause distortion of the retinal surface, blunting of the foveal contour, and pseudocyst formation.[1]

Time-domain OCT was an important tool for the diagnosis of epiretinal membranes; however, with the development of spectral domain OCT, physicians are better able to evaluate the predictors of outcomes after surgery. Cobos et al[31] showed the integrity of the inner segment/outer segment junction is essential for improving visual acuity after surgically removing the ERM. Several factors (e.g., preoperative visual acuity, duration of the symptoms prior to surgery, and the presence or absence of cystoid macular edema) have been suggested as prognostic factors that influence postoperative visual acuity.[32]

If visual acuity is only mildly reduced, ERMs are typically observed. In patients with ERM, vision is less than 20/70 in only15% of patients. Wiznia et al[33] showed no further decrease in visual acuity in 87% of 47 eyes during 2–4 years of follow-up. If there is a severe reduction in visual acuity, the standard surgical approach includes a pars plana vitrectomy and peeling of the epiretinal membrane. Some surgeons also peel the ILM in an attempt to prevent reproliferation of the membrane.[30] The overall rate of recurrence of idiopathic ERM is reportedly up to 21%. Peeling the ILM is the only reported factor in preventing recurrence.[34] Sandali et al[35] reported a lower rate of recurrence at 5%, but consistently found that ILM peeling was the only factor that prevented ERM recurrence.


  6. Lamellar holes Top


In 1975, Gass described a lamellar hole as a macular lesion resulting from cystoid macular edema.[36] A lamellar macular hole (LMH) is now known as a partial thickness foveal defect; however, there is no universally accepted definition of lamellar macular holes. On slit lamp biomicroscopy, lamellar holes typically appear as a round or oval, reddish lesion. The introduction of OCT has greatly improved the ability to diagnose a LMH.[37] In studies by Haouchine et al[38] and Witkin et al,[39] only 28% and 37%, respectively, of LMH cases diagnosed by OCT examination were clinically detected on fundus examination. Witkin et al[39] used OCT findings to create a formal definition of a lamellar macular hole. These include an irregular foveal contour, a defect or break in the inner fovea, a splitting of the inner and outer retina, lack of a full-thickness foveal defect, and intact photoreceptors.[39] The International Vitreomacular Traction Study Group included this definition in their recent categorization of lamellar macular holes.[5]

Lamellar macular holes are typically accompanied by complaints of mild central vision loss and metamorphopsia.[5] Many believe they arise from incomplete full-thickness macular hole formation.[5] Epiretinal membranes are commonly associated with eyes that have lamellar macular holes. The pathogenesis, configuration, and progression of lamellar macular holes are therefore believed to be affected by tangential retinal traction due to ERM contraction.[37]

Lamellar macular holes are most often present because most patients with a lamellar macular hole only have a mild reduction in visual acuity and mild metamorphopsia; rarely do these symptoms progress to significant vision loss.[40] Theodossiadis et al[41] found that visual acuity was stable in approximately 80% of patients during a follow-up period of 37.1 months. Bottoni et al[42] had similar findings in that patients had stable visual acuity for more than 18 months.

Lamellar macular holes that present with progressive thinning of foveal thickness and decreased visual acuity may benefit from vitrectomy.[42] Duker et al[5] reviewed the literature and found that, after surgery for lamellar macular holes, the rate of visual acuity improvement ranged 25–75% and was typically because of epiretinal membrane peeling. There are no prospective studies examining pars plana vitrectomy for lamellar macular holes. Reibaldi et al[36] found that preservation of the External limiting membrane (ELM) on OCT appears to be important in the potential preservation of visual acuity. Most clinicians believe that surgical treatment of lamellar macular holes is unproven.[43]


  7. Macular pseudohole Top


On slit lamp biomicroscopy, a macular pseudohole clinically appears as a discrete, reddish, round or oval lesion in the fovea that is typically 200–400 microns in diameter and similar in appearance to a small or medium-sized FTMH. Pseudoholes are caused by contraction of the ERM and have been reported in 8–20% of eyes with ERM.[44]

Optical coherence tomography better detects the anatomic changes at the vitreomacular interface that leads to a macular pseudohole. Of most importance is that pseudoholes have no loss of retinal tissue. They have an invaginated or heaped foveal edge, an ERM with a central opening, and a steep macular contour to the central fovea. The steep foveal contour creates the appearance of a hole, even though there is no true loss of retinal tissue. It may be that the absence or loss of foveal tissue is responsible for the better visual acuity in eyes with pseudoholes, compared to eyes with lamellar holes.[45]

The natural history of pseudoholes suggests that good visual acuity can be maintained for a long period.[45] If the ERM is the cause of the decreased vision, then pars plana vitrectomy with membrane peel is an option. Restoration of a normal foveal contour can lead to some improvement in vision.[5] Massin et al[44] examined 50 eyes that underwent vitrectomy for ERM with pseudoholes and compared them to eyes with ERM without pseudoholes. Massin[44] found that the preoperative and the postoperative visual acuity differed significantly between the group with pseudoholes and the group without pseudoholes.[44] In addition, the presence of a pseudohole did not suggest a poor prognosis. Pseudoholes are typically observed, unless there is a significant reduction in vision.


  8. Conclusion Top


In summary, a variety of diseases of the vitreoretinal interface exists. Optical coherence tomography has allowed physicians to describe, classify, and understand better the vitreoretinal interface and the abnormalities that can develop. Vitrectomy remains the most commonly performed treatment for the various interface disorders, but the recent introduction of pharmacologic vitreolysis represents a movement towards developing nonsurgical treatment options for certain diseases of the vitreoretinal interface.

Conflicts of interest: Peter K. Kaiser is a consultant for Alcon, Novartis, Thrombogenics, and Allegro.



 
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Abstract
1. Introduction
2. Vitreomacular...
3. Vitreomacular...
4. Full-thicknes...
5. Epiretinal me...
6. Lamellar holes
7. Macular pseud...
8. Conclusion
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