The Open Ophthalmology Journal


ISSN: 1874-3641 ― Volume 11, 2017

Pars Plana Vitrectomy with Internal Limiting Membrane Peeling for Nontractional Diabetic Macular Edema



Jan Niklas Ulrich*
Department of Ophthalmology, University of North Carolina at Chapel Hill, United States

Abstract

Background:

Diabetes mellitus remains the leading cause of blindness among working age Americans with diabetic macular edema being the most common cause for moderate and severe vision loss.

Objective:

To investigate the anatomical and visual benefits of pars plana vitrectomy with inner limiting membrane peeling in patients with nontractional diabetic macular edema as well as correlation of integrity of outer retinal layers on spectral domain optical coherence tomography to visual outcomes.

Methods:

We retrospectively reviewed the charts of 42 diabetic patients that underwent vitrectomy with internal limiting membrane peeling for nontractional diabetic macula edema. The integrity of outer retinal layers was evaluated and preoperative central macular thickness and visual acuity were compared with data at 1 month, 3 months and 6 months postoperatively. The student t-test was used to compare the groups.

Results:

31 eyes were included. While no differences were seen at 1 and 3 months, there was significant improvement of both central macular thickness and visual acuity at the 6 months follow up visit compared to preoperatively (357, 427 microns; p=0.03. 20/49, 20/82; p=0.03) . Patients with intact external limiting membrane and ellipsoid zone had better preoperative vision than patients with outer retinal layer irregularities (20/54, 20/100; p=0.03) and greater visual gains postoperatively (20/33, p<0.001 versus 20/81; p=non-significant).

Conclusion:

Pars plana vitrectomy with internal limiting membrane peeling can improve retinal anatomy and visual acuity in patients with nontractional diabetic macular edema. Spectral domain optical coherence tomography may help identify patients with potential for visual improvement.

Keywords: Diabetic macular edema, Ellipsoid zone, Internal limiting membrane peeling, Pars plana vitrectomy.


Article Information


Identifiers and Pagination:

Year: 2017
Volume: 11
First Page: 5
Last Page: 10
Publisher Id: TOOPHTJ-11-5
DOI: 10.2174/1874364101711010005

Article History:

Received Date: 09/9/2016
Revision Received Date: 22/12/2016
Acceptance Date: 03/1/2017
Electronic publication date: 10/1/2017
Collection year: 2017

© Jan Niklas Ulrich; Licensee Bentham Open

open-access license: This is an open access article licensed under the terms of the Creative Commons Attribution-Non-Commercial 4.0 International Public License (CC BY-NC 4.0) (https://creativecommons.org/licenses/by-nc/4.0/legalcode), which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.


* Address correspondence to this author at the Department of Ophthalmology, University of North Carolina at Chapel Hill, United States; Tel: (919) 966-5296; Fax: (919) 966-1908; E-mail: jnulrich@med.unc.edu




INTRODUCTION

Diabetes mellitus remains the leading cause of blindness among working age Americans with diabetic macular edema (DME) being the most common cause for moderate and severe vision loss [1Klein R, Klein BE, Moss SE, Cruickshanks KJ. The wisconsin epidemiologic study of diabetic retinopathy. XV. The long-term incidence of macular edema. Ophthalmology 1995; 102(1): 7-16.
[http://dx.doi.org/10.1016/S0161-6420(95)31052-4] [PMID: 7831044]
-3Klein BE. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol 2007; 14(4): 179-83.
[http://dx.doi.org/10.1080/09286580701396720] [PMID: 17896294]
]. The use of anti-vascular endothelial grow factor (anti-vegf) medications has become the first line treatment for DME [4Brown DM, Nguyen QD, Marcus DM, et al. Long-term outcomes of ranibizumab therapy for diabetic macular edema: the 36-month results from two phase III trials: RISE and RIDE. Ophthalmology 2013; 120(10): 2013-22.
[http://dx.doi.org/10.1016/j.ophtha.2013.02.034] [PMID: 23706949]
-9Elman MJ, Qin H, Aiello LP, et al. Intravitreal ranibizumab for diabetic macular edema with prompt versus deferred laser treatment: three-year randomized trial results. Ophthalmology 2012; 119(11): 2312-8.
[http://dx.doi.org/10.1016/j.ophtha.2012.08.022] [PMID: 22999634]
] with macular laser and steroids as adjuvant agents for non-responders [10Photocoagulation for diabetic macular edema. Early treatment diabetic retinopathy study report number 1. Early Treatment Diabetic Retinopathy Study research group. Arch Ophthalmol 1985; 103(12): 1796-806.
[http://dx.doi.org/10.1001/archopht.1985.01050120030015] [PMID: 2866759]
-14Sanford M. Fluocinolone acetonide intravitreal implant (Iluvien®): in diabetic macular oedema. Drugs 2013; 73(2): 187-93.
[http://dx.doi.org/10.1007/s40265-013-0010-x] [PMID: 23335133]
]. Despite these improvements there is no standardized approach for the treatment of chronic or recurrent DME and repeated intraocular injections pose a significant burden on patients, physicians and the healthcare system.

Pars plana vitrectomy (PPV) has been suggested as a potential alternative to intravitreal injections and macular laser. Multiple studies showed reduction in central macular thickness (CMT) and visual gains in patients with abnormalities of the vitreo-retinal interface [15Lewis H, Abrams GW, Blumenkranz MS, Campo RV. Vitrectomy for diabetic macular traction and edema associated with posterior hyaloidal traction. Ophthalmology 1992; 99(5): 753-9.
[http://dx.doi.org/10.1016/S0161-6420(92)31901-3] [PMID: 1594222]
-19Haller JA, Qin H, Apte RS, et al. Vitrectomy outcomes in eyes with diabetic macular edema and vitreomacular traction. Ophthalmology 2010; 117(6): 1087-1093.e3.
[http://dx.doi.org/10.1016/j.ophtha.2009.10.040] [PMID: 20299105]
]. More recently several papers evaluated the effects of PPV with or without internal limiting membrane (ILM) peeling in patients with nontractional DME and reported mixed effects. While some authors reported postoperative anatomic and visual improvements [20Thomas D, Bunce C, Moorman C, Laidlaw DA. A randomised controlled feasibility trial of vitrectomy versus laser for diabetic macular oedema. Br J Ophthalmol 2005; 89(1): 81-6.
[http://dx.doi.org/10.1136/bjo.2004.044966] [PMID: 15615752]
-23Doi N, Sakamoto T, Sonoda Y, et al. Comparative study of vitrectomy versus intravitreous triamcinolone for diabetic macular edema on randomized paired-eyes. Graefes Arch Clin Exp Ophthalmol 2012; 250(1): 71-8.
[http://dx.doi.org/10.1007/s00417-011-1777-7] [PMID: 21853229]
] others did not confirm gains in visual acuity [24Figueroa MS, Contreras I, Noval S. Surgical and anatomical outcomes of pars plana vitrectomy for diffuse nontractional diabetic macular edema. Retina 2008; 28(3): 420-6.
[http://dx.doi.org/10.1097/IAE.0b013e318159e7d2] [PMID: 18327133]
-28Liu DC, Wu H, Yang HQ. Clinical observation of vitrectomy for treatment of diffuse nontraditional diabetic macular edema. Zhonghua Yan Ke Za Zhi 2011; 47(6): 492-6.
[PMID: 21914262]
].

In two publications the authors preoperatively examined the status of the outer retinal layers on spectral domain OCT (sdOCT) and reported visual gains after PPV with ILM peel in patients with preserved external limiting membrane and ellipsoid zone (EZ) retinal layers [29Chhablani JK, Kim JS, Cheng L, Kozak I, Freeman W. External limiting membrane as a predictor of visual improvement in diabetic macular edema after pars plana vitrectomy. Graefes Arch Clin Exp Ophthalmol 2012; 250(10): 1415-20.
[http://dx.doi.org/10.1007/s00417-012-1968-x] [PMID: 22354371]
, 30Nishijima K, Murakami T, Hirashima T, et al. Hyperreflective foci in outer retina predictive of photoreceptor damage and poor vision after vitrectomy for diabetic macular edema. Retina 2014; 34(4): 732-40.
[http://dx.doi.org/10.1097/IAE.0000000000000005] [PMID: 24177189]
].

Due to the heterogeneity of study designs it remains unclear to this day which patients would benefit from PPV with ILM peeling for DME.

In this study we evaluated if PPV with ILM peeling could reduce the CMT and improve visual acuity in patients with nontractional DME as well as the predictive value of preoperative sdOCT.

MATERIAL AND METHODS

We retrospectively reviewed the medical records of all consecutive patients undergoing PPV with ILM peeling for DME at our institution from 2012 to 2014.

We excluded patients with less than 6 month follow up or worse than 20/400 vision preoperatively, patients with abnormalities of the vitreo-retinal interface on sdOCT and patients who had received any treatment for DME within 3 months prior to vitrectomy. We also excluded patients who had received adjuvant intraoperative or postoperative steroid or anti-vegf injections.

All patients had undergone standard 25-gauge vitrectomy with peribulbar anesthesia by a single surgeon. After induction of a posterior vitreous detachment, indocyanine green (ICG) assisted ILM peeling of an area of at least three disc diameters centered on the fovea was achieved.

Fig. (1)
Above: Patient with normal external limiting membrane (ELM) and ellipsoid zone (EZ),
Below: Normal ELM and EZ nasally (arrowhead). Absent ELM and irregular EZ in foveal area (arrow).


Patients had Heidelberg sdOCT images of the macula on the pre- and each postoperative visit (Heidelberg Engineering, Heidelberg, Germany). We evaluated OCT images for the presence of abnormalities of the vitreo-retinal interface and determined the status of the external limiting membrane (ELM) and ellipsoid zone (EZ) in the foveal area as preserved or disrupted/abnormal (Fig. 1).

Phakic status, prior number of intravitreal injections and focal/grid laser were recorded.

Visual acuity and central macular thickness were evaluated preoperatively as well as 1 month, 3 months and 6 months after the surgery. In a subgroup analysis patients with intact ELM/EZ were compared with patients with abnormal foveal anatomy and analyzed in regards to different outcome.

Pre- and postoperative data was compared using the student t-test. A p-value smaller than 0.05 was considered statistically significant.

All research adhered to the tenets of the Declaration of Helsinki and the Internal Review Board of our University had approved the study protocol.

RESULTS

We identified 42 eyes in the database and eventually included 31 eyes of 28 patients. Average age was 63 years, 17 out of 31 eyes (55%) belonged to male patients (Table 1). The average preoperative CMT was 427 microns, mean visual acuity 20/82. 10 patients (32%) had an intact ELM and ellipsoid zone in the foveal area.

Table 1
Baseline characteristics.


At 1 and 3 months postoperatively, there was no significant change in either CMT (431, 390 microns; p= 0.91, 0.29) or visual acuity (20/73, 20/60; p= 0.69, 0.21). However at 6 months postoperatively the central macular thickness had significantly decreased (357 microns; p=0.03) and the visual acuity was improved (20/49; p=0.03; Table 2). No patient had worsened visual acuity postoperatively and 10 patients (32%) improved by three lines or more.

Table 2
Changes in central macular thickness and visual acuity over course of study.


Patients with intact ELM/EZ had statistically significant better visual acuity preoperatively compared to the patients with defects on OCT (20/54 vs 20/100; p=0.03). Patients with intact foveal anatomy improved to 20/33 at the last visit (p<0.009) with 6 out of 10 patients (60%) gaining three or more lines of vision. Patients with defects in foveal anatomy improved to 20/81 (p=non-significant) with only 4 patients (20%) improving three or more lines of vision. There was no difference in foveal thickness between the groups with preserved and defective anatomy at any point in the study. (Table 3).

Table 3
Change in central macular thickness and visual acuity in patients with intact versus irregular outer retinal anatomy.


DISCUSSION

Our study was able to demonstrate a statistically significant improvement in visual acuity and decrease in foveal thickness six months after vitrectomy with ILM peel in patients with nontractional DME. The improvement in visual acuity was even more pronounced in patients with preserved foveal anatomy on sdOCT.

While the current literature appears to support vitrectomy for tractional DME [15Lewis H, Abrams GW, Blumenkranz MS, Campo RV. Vitrectomy for diabetic macular traction and edema associated with posterior hyaloidal traction. Ophthalmology 1992; 99(5): 753-9.
[http://dx.doi.org/10.1016/S0161-6420(92)31901-3] [PMID: 1594222]
-19Haller JA, Qin H, Apte RS, et al. Vitrectomy outcomes in eyes with diabetic macular edema and vitreomacular traction. Ophthalmology 2010; 117(6): 1087-1093.e3.
[http://dx.doi.org/10.1016/j.ophtha.2009.10.040] [PMID: 20299105]
], the benefit of PPV in patients with nontractional DME is much less clear. It is believed that vitrectomy can reduce DME by increasing the oxygenation in the vitreous cavity and removing proangiogenic factors like VEGF as well as cytokines and chemokines which promote a breakdown of the blood retinal barrier [31Stefansson E, Landers MB III, Wolbarsht ML. Increased retinal oxygen supply following pan-retinal photocoagulation and vitrectomy and lensectomy. Trans Am Ophthalmol Soc 1981; 79: 307-34.
[PMID: 7200671]
-33Park JH, Woo SJ, Ha YJ, Yu HG. Effect of vitrectomy on macular microcirculation in patients with diffuse diabetic macular edema. Graefes Arch Clin Exp Ophthalmol 2009; 247(8): 1009-17.
[http://dx.doi.org/10.1007/s00417-009-1062-1] [PMID: 19294405]
]. The role of ILM peeling during surgery remains unclear as well. In patients without obvious abnormalities of the vitreo-retina interface, peeling of the ILM can ensure that no residual vitreous is left behind and can reduce tangential traction [34Gandorfer A, Messmer EM, Ulbig MW, Kampik A. Resolution of diabetic macular edema after surgical removal of the posterior hyaloid and the inner limiting membrane. Retina 2000; 20(2): 126-33.
[http://dx.doi.org/10.1097/00006982-200002000-00004] [PMID: 10783944]
, 35Rice S, Madreperla SA, McCuen B. Internal limiting membrane removal in surgery for full thickness macular holes Macular Hole Pathogenesis, Diagnosis and Treatment. 2nd ed. Boston: Butterworth Heinemann 1998; pp. 125-46.].

Kumagai et al. reported visual gains in two large series of patients with nontractional diabetic macular edema with or without ILM peeling. In these studies the macular anatomy was not assessed with sdOCT and all phakic patients underwent simultaneous cataract extraction which may have contributed to visual gains [36Kumagai K, Hangai M, Ogino N, Larson E. Effect of internal limiting membrane peeling on long-term visual outcomes for diabetic macular edema. Retina 2015; 35(7): 1422-8.
[http://dx.doi.org/10.1097/IAE.0000000000000497] [PMID: 26102439]
, 37Kumagai K, Furukawa M, Ogino N, Larson E, Iwaki M, Tachi N. Long-term follow-up of vitrectomy for diffuse nontractional diabetic macular edema. Retina 2009; 29(4): 464-72.
[http://dx.doi.org/10.1097/IAE.0b013e31819c632f]
]. However, several studies were unable to demonstrate visual gains despite anatomical improvement [24Figueroa MS, Contreras I, Noval S. Surgical and anatomical outcomes of pars plana vitrectomy for diffuse nontractional diabetic macular edema. Retina 2008; 28(3): 420-6.
[http://dx.doi.org/10.1097/IAE.0b013e318159e7d2] [PMID: 18327133]
-28Liu DC, Wu H, Yang HQ. Clinical observation of vitrectomy for treatment of diffuse nontraditional diabetic macular edema. Zhonghua Yan Ke Za Zhi 2011; 47(6): 492-6.
[PMID: 21914262]
].

Two authors recently reported an association between photoreceptor damage represented by disruption of the outer retina on sdOCT and visual acuity in patients DME. Chabblani’s et al. group retrospectively studied 34 eyes with resistant DME and found pre-operative ELM integrity to be a better predictor for vision improvement than CMT or IS/OS junction integrity. While combining ELM integrity and preoperative CMT yielded the best predictive information, the addition of the IS/OS junction integrity was not beneficial. This study included patients with abnormalities of the vitreo-retinal interface (e.g. epiretinal membrane) which complicates a direct comparison to our study of nontractional DME [29Chhablani JK, Kim JS, Cheng L, Kozak I, Freeman W. External limiting membrane as a predictor of visual improvement in diabetic macular edema after pars plana vitrectomy. Graefes Arch Clin Exp Ophthalmol 2012; 250(10): 1415-20.
[http://dx.doi.org/10.1007/s00417-012-1968-x] [PMID: 22354371]
]. Nishijama et al. reported on sdOCT findings and visual outcomes in a retrospective series of 32 eyes. Ten of these eyes were found to have what is described as “hyperreflective foci” in the outer retinal layers. While it remains unclear what exactly these foci represent, they appeared to be associated with damage to the IS/OS junction and worse visual outcome after vitrectomy [30Nishijima K, Murakami T, Hirashima T, et al. Hyperreflective foci in outer retina predictive of photoreceptor damage and poor vision after vitrectomy for diabetic macular edema. Retina 2014; 34(4): 732-40.
[http://dx.doi.org/10.1097/IAE.0000000000000005] [PMID: 24177189]
].

In a recent retrospective study of 53 eyes, Browning et al. reported improved foveal thickness and visual acuity 12 months after vitrectomy for DME. The intactness of the EZ on sdOCT did not appear to be correlated with better postoperative vision. This study included patients with abnormalities of the vitreo-retinal interface, patients with proliferative diabetic retinopathy. Further, intravitreal steroids were injected in a majority of cases at the end of the surgery [38Browning DJ, Lee C, Stewart MW, Landers MB III. Vitrectomy for center-involved diabetic macular edema. Clin Ophthalmol 2016; 10: 735-42.
[http://dx.doi.org/10.2147/OPTH.S104906] [PMID: 27175056]
].

Due to significant heterogeneity among these studies including inclusion criteria, surgical technique and follow up, the visual benefit of PPV in patients with nontractional DME remains unclear.

Our study is limited by the small numbers and its retrospective nature. However, we were able to demonstrate visual and anatomical benefits in patients undergoing vitrectomy with ILM peeling for nontractional DME and suggest the integrity of the outer retina on sdOCT as possible predictor for visual potential.

Larger prospective studies may give additional insight into which patients will benefit the most from vitrectomy as well as the optimal time of surgical intervention.

CONFLICT OF INTEREST

The author confirms that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

Declared none.

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"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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