Uploaded byNarciso Atienza Jr, MD, MBA, FPCS, FPAO
ILM Friend or Foe
The document discusses the management of the internal limiting membrane (ILM) in macular surgery. It finds that ILM peeling improves outcomes for various vitreo-retinal conditions by removing traction on the macula and preventing recurrent epiretinal membranes. Specifically, ILM peeling improves closure and vision for macular holes compared to no peeling. For large holes, an inverted ILM flap technique provides even higher closure rates. ILM peeling also benefits diabetic vitrectomy and retinal detachment surgery but may not improve outcomes for uncomplicated retinal detachments. Thus, the ILM can act as both a "friend and foe" in macular surgery.
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ILM Friend or Foe
- 1. Management of theInternal Limiting Membrane in Macular Surgery. “Friend or Foe” Narciso F. Atienza, Jr. MD, MBA, FPCS, FPAO Cardinal Santos Medical Center St. Lukes Medical Center, QC Legazpi Eye Center/Bicol Access Health Centrum Tzu Chi Charity Eye Clinic
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- 3. Indications for ILM removal •Vitreo-Macular Surface Disorders o Macular hole o Epiretinal membranes o Vitreo-macular Traction Syndrome o Myopic foveo-schisis • Retinal detachment • Diabetic vitrectomy surgery (traction detachment/unresponsive diabetic macular edema)
- 4. Questions • Is ILMremoval needed in macular surgery? o Does ILM removal improve the post-operative anatomy of the macula o Does ILM removal improve the functional visual acuity of patients • Does removal of the ILM have any other effect on retinal function?
- 5. • Fragments ofILM together with myoblastic elements, collagen were seen on ERM specimens from vitrectomized eyes Maguire AM, Smiddy WE, Nanda SK, Michels RG. Clinicopathologic correlation of recurrent epiretinal membranes after previous surgical removal. Retina. 1989;9(2) • 11 out of 41 specimens of ERM contained long strands of ILM. Sivallingam A, Eagle RC Jr. Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery. Ophthalmology. 1990 Nov;97(11)
- 6. Rationale for ILMpeeling during macular surgery • Internal limiting membrane has been implicated in the different vitreo-macular surface disorders. • Internal limiting membrane removal has been shown to o Remove residual traction on the macular area. o Removes of potential scaffold for recurrent ERM after vitrectomy surgery. o Can act as a scaffold for the closure of macular holes (inverted flap)
- 7. What was published beforehand •Led to very good anatomic and functional results • Complete closure of the hole in 92-100% Eckardt C, Eckardt U. Removal of the internal limiting membrane in macular holes. Clinical and morphological findings. Ophthalmologe 1997 Aug;94(8). Park DW, Lee JH. The use of internal limiting membrane maculorrhexis in treatment of idiopathic macular holes. Korean J Ophthalmol. 1998 Dec ;12(2)
- 8. • Macular holesurgery with ILM Peeling and air tamponade results showed: (58 eyes) o 91% closure rate in one surgery o 95% with subsequent surgery o 53% of eyes have VA of 20/50 or better o Macular holes of less than 6 months duration vs greater than 6 months – 98% closure vs 69%. Park DW, Sipperley JO, Sneed SR, Dugel PU, Jacobsen J. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology. 1999 Jul;106(7):
- 9. Peeling the ILMvs non peeling • ILM peeling has proven effective in closing macular holes compared to non performance of peeling. o 93% (ILM peel) vs 79.3% (non-peel eyes) Al-Abdulla NA, Thompson JT, Sjaarda RN. Results of macular hole surgery with and without epiretinal dissection or internal limiting membrane removal. Ophthalmology 2004;111(1) • ILM peeling significantly improves visual and anatomic success in all stages of recent and chronic macular holes and reopened and failed holes, while eliminating reopening for holes greater than 300 microns. • 100% (ILM Peel) vs 82% (Non-ILM Peel) Brooks HL. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology. 2000 Oct; 107 (10)
- 11. “Problems” encountered during ILMpeeling • Potential toxicity (ICG, Typhan Blue, Brilliant Blue) • Mechanical Neurosensory retinal damage from surgical trauma. • Scotoma formation after macular surgery • May not be enough for large macular holes
- 12. Macular holes failingto close despite ILM peeling • ILM peeling alone may not be enough for large macular holes • Also seen in patients with chronic macular holes o Failure to closure – 20%
- 13. Inverted flap technique •Macular holes greater than 400 um • Closure rate – 98% (inverted flap) vs 88% (non-inverted flap) • Vision – 0.17 (non-inverted) vs 0.28 (inverted flap) Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology. 2010;117.
- 14. Rationale for theinverted flap technique • Induces glial cell proliferation where the macular hole is filled with proliferating cells
- 15. Theory behind theILM (inverted flap) • the ILM functioned as a scaffold for the proliferation and migration of Muller cells, and may promote Muller cell activation. • Neurotrophic factors and bFGF produced by activated Muller cells and present on the surface of the ILM may contribute to MH closure. Yusuke Shiode, Yuki Morizane, Ryo Matoba, The Role of Inverted Internal Limiting Membrane Flap in Macular Hole Closure IOVS j September 2017 j Vol. 58 j No. 11.
- 17. Macular holes • ILMpeeling in macular hole is supported by literature. • ILM peeling alone is suited for small holes • Large holes (>400 um) may benefit from ILM inverted flap techniques
- 18. ILM peeling indiabetic vitrectomies • Fewer incidence of formation of epiretinal membranes • Can be used in non-responsive diabetic macular edema. • Visual results for surgery may not be significantly different Michalewska Z, Bednarski M, Jerzy N. The role of ILM peeling in vitreous surgery for proliferative diabetic retinopathy. Ophthalmic Sur Lasers Imaging Retina. 2013 May-Jun; 44(3) Rinaldi M, del Omo R. ILM peeling in non tractional diabetic macular edema: review and meta analysis. Int Ophthal. 2017 Oct 31.
- 21. ILM Peeling inretinal detachment • Prevents post-operative macular pucker formation • Improvement in visual results of surgery • Can be helpful in patients with PVR with macula on/off cases Aras C, Arici C, Akar S et al (2009) Peeling of internal limiting membrane during vitrectomy for complicated retinal detachment prevents epimacular membrane formation. Graefes Arch Clin Exp Ophthalmol 247(5): Akiyama K, Fujinami K, Watanabe K3, Tsunoda K Noda T. Internal Limiting Membrane Peeling to Prevent Post- vitrectomy Epiretinal Membrane Development in Retinal Detachment. Am J Ophthal. 2016 Nov;171
- 22. • Although ILMpeeling prevented ERM, it resulted in poorer visual outcomes in uncomplicated retinal detachment surgery. o MRS, FRS (mean and foveal sensitivity test) where higher in non ILM peelied patients o Retinal dimpling is seen more in ILM peeled eyes Eissa MGAM, Abdelhakim, MASE. Functional and structural outcomes of ILM peeling in uncomplicated macula-off RRD using microperimetry and en-face OCT. Graefes Arch Clin Exp Ophthalmol. 2018 Feb; 256 (2)
- 24. Myopic foveoschisis • Mayplay a role in resolution if done during surgery Ikuno Y, Sayanagi K, Ohji M, Kamei M, Gomi F, Harino S, Fujikado T, Tano Y. Vitrectomy and Internal Limiting Membrane Peeling in Myopic Foveoschisis Am J Ophthalmol. 2004 Apr;137(4) • Fovea sparring ILM peel done on myopic foveoschisis reduces risk of opening or unroofing to full thickness macular hole. Rate of hole formation (16.7%) Shimada N, Sugamoto Y, Ogawa M, Takase H, Ohno-Matsui K. Fovea-Sparring internal limiting membrane peeling for myopic traction maculopathy. Am J Ophthalmol 2012 Oct; 154(4)
- 25. Conclusions • ILM peelinghas become an integral part in vitrectomy surgery. • Removing the ILM far out-weigh the risks on non- removal of the ILM in current available literature. • For large macular holes, retinal detachment with concurrent macular holes, the fibroblastic activity in the inner ILM surface can act as a scaffold when it is positions on top of the hole. • For uncomplicated RD, or very thin myopic foveoschisis, sparring the ILM may result in better visual outcomes • The ILM can be both. “Friend and a Foe”
Editor's Notes
- #2 Good morning. It is a privilege and honor for me to speak in front of our colleagues from around the Asia Pacific Region and the world who have a common interest in Vitreo-Retinal surgery. I would also like to thank the organizers to for the kind invite. The topic I have been asked to lecture is on the Management of the ILM in macular surgery. Whether it is a “friend or foe” in our surgical armamentareum. As we all have experience in macular surgery, it is but fitting to review some of the points in we have used to in deciding whether ILM peeling is warranted in the cases we have to deal with. Majority of decisions that we do are based on the experiences of our predecessors when the OCT was still non-existent or its in infancy. We are now blessed with the technology to help us decide nowadays.
- #3 I have no relevant financial disclosures related to this lecture
- #4 First of all, I would like a show of hands, how many of us here are VR surgery specialists? G.O.? And those who are in training? Well, to begin with, current literature from journal reports and case series have stated that ILM removal is useful in the following indications. Majority of cases that deal with the involvement of the internal limiting membrane are with Vitreo-macular surface disorders, with a clear majority dealing with macular holes. It was only in 5 - 10 years that we have expanded our indications for surgery to include other Vitreo-macular surface disorders such as epiretinal membranes, VMTs and myopic foveo-schisis, thanks in part to non-invasive tests, such as the improvement in OCT technology, in terms of anatomic determination, and micro-perimetric and multi-focal neuro ophthalmologic modalities which test macular function. Other diseases that does not necessarily primarily involve the vitreo-macular surface has been explored if they will also benefit from ILM peeling, such as in retinal detachment surgery with pars plana vitrectomy, and diabetic vitrectomy for proliferative disease or for macular edema unresponsive to current treatment options of anti-VEGF, steroids, laser.
- #5 So, the question we have to ask now is 1) Is the removal of ILM needed in macular surgery. , does it improve the post-operative anatomy of the macula, and does this improve the functional visual acuity of the patients. Another question we have asked is that if the removal of the ILM has any other effect on retinal function
- #6 The presence of the ILM was found in histopathologic examinations of epiretinal membranes removed during pars plana vitrectomy. Fragments of ILM with myoblastic elements, collagen are seen. However, not all ERM removed will have ILM present. ILM present accounts to 25% ERM removed in other studies. However, reports vary with the presence of ILM on the ERM removed in terms of visual acuity after surgical removal.
- #7 The ILM has been implicated in as a major contributor to the pathology and symptomatology of the different vitreo-macular disorders. And removal of the ILM has been shown to remove residual traction on the macular area. It also removes the scaffold with recurrent ERM. In macular holes however, the ILM can be used to stimulate closure of the holes. Among the vitreo-macular surface disorders, macular holes have been seen to have benefitted from ILM peeling, vs that of all other diseases.
- #8 The first reports of ILM peeling dealt with case series of macular holes, and did not explore comparison of ILM peeling vs non-ILM peeling. Though this studies may have at first known to have bias, however from clinical experience and other reports, it was reproducible. It was the initial reports of Claus Eckardt in 1997, and Park in 1998 which showed that ILM removal in macular hole surgery can increase the closure rate, and improve visual outcomes.
- #9 Park and his co-authors subsequently reported that in vitrectomy cases, ILM peeling, is associated with increased single surgery closure rate, better final visual acuity , and better closure rates for chronic macular holes.
- #10 Soon after, the first reports of comparing ILM peeling and non-ILM peeling with ILM peeling showing higher closure rates compared to non-ILM peeling cases. Brooks showed that 100% of patients who had ILM peel closed, while only 82% on the non peel population had the same results. The same results were also reproduced on subsequent reports, such as that of Al-Abdula with 93% closure rates on the ILM peeled population compared to 79% of the non ILM peeled cases.
- #11 This is a short video of a small macular hole, approximately 234 um measured with the OCT. As you can see here, there was minimal staining of the ILM with Tryphan blue, and the peel as completed with a ILM peel with an area approximated 3000 um in diameter. The patient did well after the surgery with her vision improving to 20/40
- #12 Despite the increasing closure rates, and better visual acuity results in the subsequent reports and clinical experience, ILM peeling also has problems. Visualizing the ILM has been difficult without dyes, and the available dyes have the potential to cause toxicity. Among the dyes, ICG has been seen in several case reports to cause RPE toxicity. Mechanical trauma has been seen in most if not al VR surgeons basing on our experience. Scotoma formation has also been seen in patients who underwent macular hole surgery, with the culprit being theorized as removing the ILM to dehydration of the NFL during an air-fluid exchange. Also, despite removing the ILM, large macular holes may fail to close.
- #13 Failure of closure of macular holes has been seen in large macular holes (Stage III-iV) compared to smaller macular holes, with 25% in some series. This has been problematic in VR surgery, as re-operationsmay have poorer results
- #14 Nawrocki reported that inverting the ILM after macular surgery peeling may close macular holes with closure rates of 98% vs that of ILM peeling alone cases at 88%. He also reported that logMar vision was better in the ILM inverted population. This case series was done using air as tamponade.
- #15 The rationale for using the inverted flap technique came about as the ILM may induce glial cell proliferation, plugging the hole with the proliferating cells.
- #16 In a paper by Yusuke, et al, they noted the ILM function acted as a scaffold for the Muller cells as what was theorized. Also, neurotrophic factors and other growth factors from the activated Mueller cells may also contribute to macular hole closure.
- #17 This a short video of how I do an inverted flap for a stage 4 macular hole. The diameter was approximated 683 um. Brilliant Blue dye was used to stain the internal limiting membrane after instilling the dye and letting it stand for 2 minutes after an air fluid exchange. I usually start at the temporal side with and grip then release manuever to create the intial ILM flap. I carry out the flap to both superior and inferior portions thru the temporal side, and leave part of the ILM to be inverted after completing the maculorrhexis. Another air fluid exchange is done without touching the flap because of the risk of removing the flap, and SF6 gas is instilled at 20%. I usually ask the patient to maintain a face down position for 24 hours graduating to a head erect position, and sleeping on the contralateral side of the operated eye.
- #18 So for macular holes, ILM peeling has been extensively reported to be beneficial, and I do as what I also believe as most of us, do ILM peeling alone on small holes, and usually reserve the inverted flap technique to larger holes of greater than 400 um, using a non expansile volume of SF6 in a majority of cases.
- #19 Now, how about in diabetics. I do not usually do ILM peeling in most diabetics. However in cases with severe fibrovascular proliferation, ILM peeling maybe needed as there is a chance of surface wrinking. Diabetic CME treated with laser, anti-VEGF, or intravitreal steroids may be good candidates to a vitrectomy with ILM peel if there is a concomitant ERM or macular hole, however, visual results may not translate to anatomic changes are these retinas are diseased.
- #20 This is a case of a previously vitrectomized eye for vitreous hemorrhage who developed a macular hole 2 months post-operatively. He also had recurrent vitreous hemorrhage which probably cause a CME and unroofing of the macular edema or an ERM formation from the vitreous hemorrhage which settled on the macular area. The patient had very adherent ILM upon surgery, which was poorly stained. However, the ILM was successfully done with the pre and post-op OCT showing flatenning of the hole edges
- #21 This is he pre-operative and post-operative OCT which showed flattening of the edges of the macular hole. Pre-op vision was a CF 2 feet, improving to 20/400 after the surgery
- #22 Aras and Akayama found value in ILM peeling for PVR complicated retinal detachments, as ILM peeling can prevent post-operative macular pucker formation and at the same time, relieve other tractional components pulling on the retinal surface. This also helps in improving post-operative visual acuity in most patients, and can be done on both macula on/off retinal detacments complicated by PVR
- #23 However, this may not be the case for uncomplicated retinal detachments as ILM peeled retinal detachments on uncomplicated RD repaired with vitrectomy surgery tend to have poorer mean retinal and foveal sensitivity tests, and visual outcomes, and changes in en-face OCT as described by Eissa and co-authors
- #24 This is one of the retinal detachment with PVR cases where ILM peeling was attempted and done. This was a 56 year old male patient who presented with vision loss. This was combined with a buckle. As in all surgeries which will involve removing the ILM, I have previously stained the ILM with Brilliiant Blue and rpceeded to start the maculorrhexis from the temporal area, attempting to free as much ILM up to the arcades. ILM fragments when done on PVR complicated retinal detachments, and is difficult to remove on detached retina, as we all have experienced.
- #25 One of the diseases that ILM may play a role is myopic foveoschisis. Our Japanese colleagues have one of the highest data on surgical management of myopic foveoschisis. There are proponents of removing the ILM completely, but Shimada and co-authors reported the formation of a full thickness macular hole in 17% of cases where a full ILM peel was done. Compared to when a “fovea sparring ILM peel was done, no macular hole formation was noted.
- #26 In conclusion, ILM peeling has become an integral part of our skill sets when we do vitrectomy surgery, and is one of the most important things we have to teach our fellows during training. The debate whether to remove the ILM during vitrectomy surgery may depend on the surgeon, but for most macular holes, removing the ILM or creating a flap with it far outweigh non-removal especially in macular hole cases, and in retinal detachments with macular hole or in PVR surgery. Histopathologically, the ILM acts as a scaffold when used with a flap technique on large holes, RD with macular holes, creating an environment to seal the hole. However, this may also hold contrary on uncomplicated retinal detachments, or myopic foveoschisis where an ILM peel can result in poorer visual or functional results.
- #27 So, in the conclusion of this short lecture, the ILM can either be both your “FRIEND OR YOUR FOE”.