Analysis of Ganglion Cell-Inner Plexiform Layer Thickness after Internal Limiting Membrane Peeling

Jeffrey Lee; Jung Min Park

doi:10.3341/jkos.2016.57.9.1369

Journal List > J Korean Ophthalmol Soc > v.57(9) > 1010388

Go to TopGo to Top Go to BottomGo to Bottom

TOOLS

Lee and Park: Analysis of Ganglion Cell-Inner Plexiform Layer Thickness after Internal Limiting Membrane Peeling

Original Article

J Korean Ophthalmol Soc 2016;57(9):1369-1377.

Published online: 25 September 2016

DOI: https://doi.org/10.3341/jkos.2016.57.9.1369

Analysis of Ganglion Cell-Inner Plexiform Layer Thickness after Internal Limiting Membrane Peeling

Jeffrey Lee, MD, Jung Min Park, MD, PhD

Department of Ophthalmology, Maryknoll Medical Center, Busan, Korea

Address reprint requests to Jung Min Park, MD, PhD Department of Ophthalmology, Maryknoll Medical Center, #121 Junggu-ro, Jung-gu, Busan 48972, Korea Tel: 82-51-461-2540, Fax: 82-51-465-7470 E-mail: pjm1438@hanmail.net

Received 24 March 2016 Revised 20 May 2016 Accepted 7 July 2016

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Purpose

To evaluate the ganglion cell-inner plexiform layer (GCIPL) thickness after internal limiting membrane (ILM) peeling with or without intravitreal gas injection (IVGI) or surgical induction of posterior vitreous detachment (PVD).

Methods

Eighty patients who were diagnosed with epiretinal membrane (ERM) or macular hole and who received surgical intervention were retrospectively reviewed. Forty patients were treated with ILM peeling and forty patients were treated with ERM removal, but not with ILM peeling. The patients were categorized according to ILM peeling, IVGI, and surgical induction of PVD. The GCIPL thickness was measured using optical coherence tomography, and the average and sectorial thickness of GCIPL were compared.

Results

The GCIPL thickness in the ILM peeling group significantly decreased (−13.80 ± 22.63 μ m; p < 0.001), but was not significantly different in the ERM removal without ILM peeling group, compared with the preoperative GCIPL thickness (+1.21 ±22.53 μ m; p = 0.546). The difference was statistically significant between the two groups (p = 0.038). In the ILM peeling group, GCIPL thickness was not significantly different in the IVGI group (−17.41 ± 23.92 μ m vs. −7.25 ± 19.05 μ m; p = 0.109) and was significantly decreased in the surgical induction of the PVD group (−23.06 ± 23.92 μ m vs. −7.25 ± 19.05 μ m; p = 0.020). On sectorial analysis, reduction of the temporal GCIPL thickness was the largest and was significantly different compared with the nasal GCIPL thickness in ILM peeling group (−19.73 ± 28.55 μ m vs. −7.42 ± 19.90 μ m; p = 0.005).

Conclusions

ILM peeling and surgical induction of PVD may damage ganglion cells. Therefore, gentle ILM peeling and surgical induction of PVD may be needed to minimize ganglion cell damage, especially when ILM peeling is performed in glaucomatous patients.

Keywords: Ganglion cell-inner plexiform layer, Internal limiting membrane peeling, Intravitreal gas injection, Posterior vitreous detachment induction

References

1. Smiddy WE, Green WR, Michels RG, de la Cruz Z. Ultrastructural studies of vitreomacular traction syndrome. Am J Ophthalmol. 1989; 107:177–85.

2. Smiddy WE, Michels RG, Green WR. Morphology, pathology, and surgery of idiopathic vitreoretinal macular disorders. A review. Retina. 1990; 10:288–96.

3. Guyer DR, Green WR, de Bustros S, Fine SL. Histopathologic abdominals of idiopathic macular holes and cysts. Ophthalmology. 1990; 97:1045–51.

4. Kwok AK, Lai TY, Li WW, et al. Indocyanine green-assisted abdominal limiting membrane removal in epiretinal membrane surgery: a clinical and histologic study. Am J Ophthalmol. 2004; 138:194–9.

5. Brooks HL Jr. Macular hole surgery with and without internal abdominal membrane peeling. Ophthalmology. 2000; 107:1939–48. abdominal 1948–9.

6. Almony A, Nudleman E, Shah GK, et al. Techniques, rationale, and outcomes of internal limiting membrane peeling. Retina. 2012; 32:877–91.

7. Wolf S, Schnurbusch U, Wiedemann P, et al. Peeling of the basal membrane in the human retina: ultrastructural effects. Ophthalmology. 2004; 111:238–43.

8. Haritoglou C, Gass CA, Schaumberger M, et al. Macular changes after peeling of the internal limiting membrane in macular hole surgery. Am J Ophthalmol. 2001; 132:363–8.

9. Tadayoni R, Svorenova I, Erginay A, et al. Decreased retinal abdominal after internal limiting membrane peeling for macular hole surgery. Br J Ophthalmol. 2012; 96:1513–6.

10. Yamashita T, Uemura A, Kita H, Sakamoto T. Analysis of the abdominall nerve fiber layer after indocyanine green-assisted vitrectomy for idiopathic macular holes. Ophthalmology. 2006; 113:280–4.

11. Yip HK, Lai TY, So KF, Kwok AK. Retinal ganglion cells toxicity caused by photosensitising effects of intravitreal indocyanine green with illumination in rat eyes. Br J Ophthalmol. 2006; 90:99–102.

12. Kim KY, Yu SY, Kim MS, et al. Changes of parafoveal retinal nerve fiber layer thickness analyzed by spectraldomain optical abdominal tomography after pars plana vitrectomy. Retina. 2013; 33:776–84.

13. Baba T, Hagiwara A, Sato E, et al. Comparison of vitrectomy with brilliant blue G or indocyanine green on retinal microstructure and function of eyes with macular hole. Ophthalmology. 2012; 119:2609–15.

14. Baba T, Sato E, Oshitari T, Yamamoto S. Regional reduction of ganglion cell complex after vitrectomy with internal limiting abdominal peeling for idiopathic macular hole. J Ophthalmol. 2014; 2014:372589.

15. Seo KH, Yu SY, Kwak HW. Topographic changes in macular abdominal cell-inner plexiform layer thickness after vitrectomy with indocyanine green-guided internal limiting membrane peeling for idiopathic macular hole. Retina. 2015; 35:1828–35.

16. Pierro L, Iuliano L, Gagliardi M, et al. Role of ganglion cell complex in visual recovery following surgical internal limiting abdominal peeling. Graefes Arch Clin Exp Ophthalmol. 2015; 253:37–45.

17. Tan O, Chopra V, Lu AT, et al. Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography. Ophthalmology. 2009; 116:2305–14.e1–2.

18. Kinoshita T, Kovacs KD, Wagley S, Arroyo JG. Morphologic abdominals in epiretinal membranes on ocular coherence tomography as a predictive factor for surgical outcome. Retina. 2011; 31:1692–8.

19. Snead DR, James S, Snead MP. Pathological changes in the abdominal junction 1: epiretinal membrane formation. Eye (Lond). 2008; 22:1310–7.

20. Johnson RN, Gass JD. Idiopathic macular holes. Observations, stages of formation, and implications for surgical intervention. Ophthalmology. 1988; 95:917–24.

21. Yooh HS, Brooks HL Jr, Capone A Jr, et al. Ultrastructural features of tissue removed during idiopathic macular hole surgery. Am J Ophthalmol. 1996; 122:67–75.

22. Madreperla SA, Geiger GL, Funata M, et al. Clinicopathologic abdominal of a macular hole treated by cortical vitreous peeling and gas tamponade. Ophthalmology. 1994; 101:682–6.

23. Akiba J, Ishiko S, Hikichi T, et al. Imaging of epiretinal membranes in macular holes by scanning laser ophthalmoscopy. Am J Ophthalmol. 1996; 121:177–80.

24. Messmer EM, Heidenkummer HP, Kampik A. Ultrastructure of abdominal membranes associated with macular holes. Graefes Arch Clin Exp Ophthalmol. 1998; 236:248–54.

25. Gordon LW, Glaser BM, Ie D, et al. Full-thickness macular hole formation in eyes with a preexisting complete posterior vitreous detachment. Ophthalmology. 1995; 102:1702–5.

26. Fekrat S, Wendel RT, de la Cruz Z, Green WR. Clinicopathologic correlation of an epiretinal membrane associated with a recurrent macular hole. Retina. 1995; 15:53–7.

27. Blain P, Paques M, Massin P, et al. Epiretinal membranes surrounding idiopathic macular holes. Retina. 1998; 18:316–21.

28. Ezra E, Munro PM, Charteris DG, et al. Macular hole opercula. Ultrastructural features and clinicopathological correlation. Arch Ophthalmol. 1997; 115:1381–7.

29. Garretson BR, Pollack JS, Ruby AJ, et al. Vitrectomy for a abdominal lamellar macular hole. Ophthalmology. 2008; 115:884–6.e1.

30. Witkin AJ, Ko TH, Fujimoto JG, et al. Redefining lamellar holes and the vitreomacular interface: an ultrahigh-resolution optical abdominal tomography study. Ophthalmology. 2006; 113:388–97.

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

32. La Heij EC, Dieudonné SC, Mooy CM, et al. Immunohistochemical analysis of the internal limiting membrane peeled with infracyanine green. Am J Ophthalmol. 2005; 140:1123–5.

33. Sevim MS, Sanisoglu H. Analysis of retinal ganglion cell complex thickness after Brilliant Blue-assisted vitrectomy for idiopathic macular holes. Curr Eye Res. 2013; 38:180–4.

34. Nukada K, Hangai M, Ooto S, et al. Tomographic features of mac-ula after successful macular hole surgery. Invest Ophthalmol Vis Sci. 2013; 54:2417–28.

35. Curcio CA, Allen KA. Topography of ganglion cells in human retina. J Comp Neurol. 1990; 300:5–25.

36. Kawano K, Ito Y, Kondo M, et al. Displacement of foveal area toward optic disc after macular hole surgery with internal limiting membrane peeling. Eye (Lond). 2013; 27:871–7.

37. Lee HJ, Kim MS, Jo YJ, Kim JY. Ganglion cell-inner plexiform layer thickness in retinal diseases: repeatability study of abdominal-domain optical coherence tomography. Am J Ophthalmol. 2015; 160:283–9.e1.

Figure 1.

Preoperative optical coherence tomography (OCT) findings. (A) The spectral domain optical coherence tomography (SD-OCT) images of a patient showing epiretinal membrane. (B) An elliptical annulus (vertical inner and outer diameter of 1.0 mm and 4.0 mm; horizontal inner and outer diameter of 1.2 mm and 4.8 mm, respectively) around the fovea. (C) The ganglion cell anal-ysis algorithm identifies the outer boundary of the retinal nerve fiber layer (purple line) and the outer boundary of the inner plexi-form layer (yellow line). (D) The average, minimum, and sectorial (superior, superotemporal, inferotemporal, inferior, inferonasal, superonasal) thicknesses of the ganglion cell-inner plexiform layer (GCL-IPL) are measured in an elliptical annulus. OS = oculus sinister.

Table 1.

Demographic features of patients

Procedure	n	Procedure	n
ILM peeling(+)	40	PVD induced (+)	15
		PVD induced (−)	25
		IVGI (+)	24
		IVGI (−)	16
ILM peeling(−)	40	PVD induced (+)	13
		PVD induced (−)	27
		IVGI (+)	8
		IVGI (−)	32

ILM = internal limiting membrane; PVD = posterior vitreous detachment; IVGI = intravitreal gas injection.

Table 2.

Comparison of GCIPL thickness between the ILM peeling group and the ERM removal without ILM peeling group

GCIPL thickness	ILM peeling (+/−)	Preoperative (μm)	Postoperative (μm)	p-value^*	Difference (μm)	p-value^†
Average	(+)	67.67 ± 20.83	53.87 ± 19.86	<0.001	−13.80 ± 22.63	0.038
	(−)	58.05 ± 15.05	59.26 ± 20.14	0.546	1.21 ± 22.53
Superior	(+)	71.89 ± 30.56	54.40 ± 22.48	0.003	−17.49 ± 36.94	0.103
	(−)	57.11 ± 39.04	56.11 ± 25.82	0.872	−1.00 ± 37.68
Superotemporal	(+)	75.11 ± 29.99	51.89 ± 21.56	<0.001	−23.22 ± 35.06	0.027
	(−)	65.31 ± 25.77	63.47 ± 23.03	0.904	−1.84 ± 27.14
Inferotemporal	(+)	67.80 ± 29.04	51.56 ± 22.58	0.001	−16.24 ± 30.50	0.088
	(−)	60.05 ± 21.48	58.74 ± 22.92	0.931	−1.32 ± 33.98
Inferior	(+)	60.91 ± 29.06	49.80 ± 21.58	0.023	−11.11 ± 31.52	0.015
	(−)	46.68 ± 27.21	55.05 ± 23.44	0.151	8.37 ± 35.02
Inferonasal	(+)	62.71 ± 27.15	56.38 ± 21.37	0.088	−6.33 ± 24.36	0.183
	(−)	56.63 ± 13.54	60.53 ± 21.06	0.629	3.89 ± 23.48
Superonasal	(+)	67.82 ± 27.78	59.31 ± 23.82	0.032	−8.51 ± 25.70	0.328
	(−)	61.74 ± 23.42	61.32 ± 19.03	0.904	−0.42 ± 22.87
Temporal	(+)	71.46 ± 25.51	51.72 ± 21.35	<0.001	−19.73 ± 28.55	0.019
	(−)	62.68 ± 19.73	61.11 ± 21.78	0.778	−1.58 ± 27.66
Nasal	(+)	65.27 ± 23.86	57.84 ± 21.48	0.016	−7.42 ± 19.90	0.160
	(−)	59.18 ± 14.77	60.92 ± 19.33	0.673	1.74 ± 20.21

Values are presented as mean ± SD unless otherwise indicated.

GCIPL = ganglion cell-inner plexiform layer; ILM = internal limiting membrane; ERM = epiretinal membrane.

^* Paired t-test

^† Student's t-test.

Table 3.

Comparison of GCIPL thickness between with or without PVD induction in the ILM peeling group

GCIPL thickness	PVD induction (+/−)	Preoperative (μm)	Postoperative (μm)	p-value^*	Difference (μ m)	p-value^†
Average	(+)	77.06 ± 20.86	54.00 ± 22.44	<0.001	−23.06 ± 23.18	0.020
	(−)	61.41 ± 18.66	53.78 ± 18.38	0.107	−7.63 ± 20.42
Superior	(+)	81.89 ± 26.34	50.22 ± 24.34	0.002	−31.67 ± 34.09	0.036
	(−)	65.22 ± 57.19	57.19 ± 21.17	0.442	−8.04 ± 36.29
Superotemporal	(+)	83.17 ± 33.66	51.56 ± 23.19	0.009	−31.61 ± 38.90	0.281
	(−)	69.74 ± 26.58	52.11 ± 20.86	0.012	−17.63 ± 31.78
Inferotemporal	(+)	68.50 ± 28.30	52.33 ± 24.43	0.042	−16.17 ± 30.60	0.763
	(−)	67.33 ± 30.05	51.04 ± 21.73	0.013	−16.30 ± 31.01
Inferior	(+)	74.33 ± 33.39	48.89 ± 23.58	0.007	−25.44 ± 33.60	0.016
	(−)	51.96 ± 22.19	50.41 ± 20.57	0.782	−1.56 ± 26.58
Inferonasal	(+)	75.17 ± 32.13	58.17 ± 25.26	0.035	−17.00 ± 29.59	0.057
	(−)	54.41 ± 19.83	55.19 ± 18.76	0.849	0.78 ± 17.33
Superonasal	(+)	79.83 ± 29.64	62.78 ± 27.99	0.021	−17.06 ± 29.03	0.080
	(−)	59.81 ± 23.77	57.00 ± 20.84	0.866	−2.81 ± 21.97
Temporal	(+)	75.83 ± 26.88	51.94 ± 23.42	0.004	−23.89 ± 30.58	0.431
	(−)	68.54 ± 24.62	51.57 ± 20.32	0.006	−16.96 ± 27.35
Nasal	(+)	77.50 ± 26.42	60.47 ± 25.68	0.004	−17.03 ± 22.01	0.014
	(−)	57.11 ± 18.29	56.09 ± 18.49	0.904	−1.02 ± 15.71

Values are presented as mean ± SD unless otherwise indicated.

GCIPL = ganglion cell-inner plexiform layer; PVD = posterior vitreous detachment; ILM = internal limiting membrane.

^* Mann-Whitney test

^† Wilcoxon signed rank test.

Table 4.

Comparison of GCIPL thickness between with or without intravitreal gas injection in the ILM peeling group

GCIPL thickness	IVGI (+/−)	Preoperative (μm)	Postoperative (μm)	p-value^*	Difference (μm)	p-value^†
Average	(+)	69.55 ± 21.00	52.14 ± 20.51	0.001	−17.41 ± 23.92	0.109
	(−)	64.25 ± 20.75	57.00 ± 18.85	0.214	−7.25 ± 19.05
Superior	(+)	77.07 ± 29.46	51.10 ± 22.79	0.001	−25.97 ± 35.64	0.053
	(−)	62.50 ± 31.22	60.38 ± 21.30	0.959	−2.13 ± 35.22
Superotemporal	(+)	78.41 ± 30.33	48.38 ± 22.80	<0.001	−30.03 ± 35.27	0.034
	(−)	69.13 ± 29.37	58.25 ± 18.06	0.501	−10.88 ± 32.12
Inferotemporal	(+)	69.21 ± 29.88	50.72 ± 33.37	0.010	−18.48 ± 33.37	0.887
	(−)	65.25 ± 28.24	53.06 ± 21.59	0.036	−12.19 ± 24.96
Inferior	(+)	61.41 ± 26.24	50.21 ± 21.56	0.101	−11.21 ± 31.30	0.850
	(−)	60.00 ± 34.50	49.06 ± 22.30	0.244	−10.94 ± 32.96
Inferonasal	(+)	61.86 ± 24.89	55.76 ± 22.32	0.202	−6.10 ± 22.59	0.661
	(−)	64.25 ± 31.66	57.50 ± 20.17	0.589	−6.75 ± 28.07
Superonasal	(+)	69.59 ± 27.27	56.59 ± 24.08	0.013	−13.00 ± 24.94	0.038
	(−)	64.63 ± 29.30	64.25 ± 23.28	0.280	−0.38 ± 25.83
Temporal	(+)	73.81 ± 26.68	49.55 ± 22.76	<0.001	−24.26 ± 30.90	0.135
	(−)	67.19 ± 23.44	55.66 ± 18.58	0.083	−11.53 ± 22.29
Nasal	(+)	65.72 ± 22.57	56.17 ± 22.15	0.016	−9.55 ± 17.79	0.165
	(−)	64.44 ± 26.79	60.88 ± 20.55	0.093	−3.56 ± 23.38

Values are presented as mean ± SD unless otherwise indicated.

GCIPL = ganglion cell-inner plexiform layer; ILM = internal limiting membrane; IVGI = intravitreal gas injection.

^* Mann-Whitney test

^† Wilcoxon signed rank test.

Table 5.

Comparison of temporal and nasal GCIPL thickness in various groups

GCIPL thickness	Sector	Preoperative (μ m)	Postoperative (μ m)	p-value	Difference (μ m)	p-value
ILM peeling(+)	Temporal	71.46 ± 25.51	51.72 ± 21.35	<0.001^*	−19.73 ± 28.55	0.005^†
	Nasal	65.27 ± 23.86	57.84 ± 21.48	0.016^*	−7.42 ± 19.90
ILM peeling(−)	Temporal	62.68 ± 19.73	61.11 ± 21.78	0.778^*	−1.58 ± 27.66	0.573^†
	Nasal	59.18 ± 14.77	60.92 ± 19.33	0.673^*	1.74 ± 20.21
ILM peeling with PVD induction	Temporal	75.83 ± 26.88	51.94 ± 23.42	0.004^‡	−23.89 ± 30.58	0.287^§
	Nasal	77.50 ± 26.42	60.47 ± 25.68	0.004^‡	−17.03 ± 22.01
ILM peeling without PVD induction	Temporal	68.54 ± 24.62	51.57 ± 20.32	0.006^‡	−16.96 ± 27.35	0.004^§
	Nasal	57.11 ± 18.29	56.09 ± 18.49	0.904^‡	−1.02 ± 15.71
ILM peeling with IVGI	Temporal	73.81 ± 26.68	49.55 ± 22.76	<0.001^‡	−24.26 ± 30.90	0.005^§
	Nasal	65.72 ± 22.57	56.17 ± 22.15	0.016^‡	−9.55 ± 17.79
ILM peeling without IVGI	Temporal	67.19 ± 23.44	55.66 ± 18.58	0.083^‡	−11.53 ± 22.29	0.352^§
	Nasal	64.44 ± 26.79	60.88 ± 20.55	0.093^‡	−3.56 ± 23.38

Values are presented as mean ± SD unless otherwise indicated.

GCIPL = ganglion cell-inner plexiform layer; ILM = internal limiting membrane; PVD = posterior vitreous detachment; IVGI = intravitreal gas injection.

^* Paired t-test

^† Student's t-test

^‡ Mann-Whitney test; ^§ Wilcoxon signed rank test.

TOOLS

Similar articles