Efficacy of internal limiting membrane peeling combined with vitreous injection of mouse nerve growth factor for the treatment of macular hole in high myopia_Chinese Journal of Ocular Fundus Diseases

Authors：

Yu Xiao , You Zhipeng ,  Wang Shiwang

Department of Ophthalmology, The Affiliated Hospital of Nanchang University, Nanchang 330006, China;

Corresponding author：

Wang Shiwang, Email: 2393934300qq.com

Keywords：

Myopia, degenerative; Retinal perforations; Nerve growth factor; Intravitreal injections; Vitrectomy; Internal limiting membrane peeling

DOI：

10.3760/cma.j.cn511434-20211008-00562

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To observe the efficacy of pars plana vitrectomy (PPV) combined with internal limiting membrane (ILM) peeling and vitreous injection of mouse never growth factor (mNGF) in the high myopia macular hole (HMMH). Methods A prospective study. Thirty-one patients (33 eyes) with HMMH diagnosed in Affiliated Eye Hospital of Nanchang University from August 2020 and February 2021 were selected. Before surgery, all included patients were subjected to a complete ophthalmologic evaluation including best corrected visual acuity (BCVA), optical coherence tomography (OCT), macular microperimetry and axial length measurement. The BCVA examination was carried out using the international standard visual acuity chart, which was converted into logarithm of minimum resolution angle (logMAR) visual acuity during statistics. The included subjects were accepted the treatment of PPV combined with ILM peeling and vitreous injection of mNGF (combined group) or PPV united with ILM peeling (simple group), 15 cases with 16 eyes, 16 cases with 17 eyes, respectively. There were no significant differences in logMAR BCVA (t=0.836), macular hole (MH) diameter (t=0.657), visual acuity (VA) (t=0.176), the missing length of external limting membrane (ELM) and ellipsoid zone (EZ) (t=1.255, 0.966) between two groups (P＞0.05). The follow-up time was at least 6 months. The BCVA, closure rate of MH, integrity of ELM and EZ and recovery of VA in macular area were compared and observed between the two groups after surgery. The logMAR BCVA, VA, the deficient lengths of ELM and EZ at different time points were compared by independent-samples t-test between two groups and analysis of variance was used to compare the repeated measurement data of each group. Fisher test was performed for comparison of count data. Results Six months after surgery, MH closure rates in the simple group and the combined group were 88.24% (15/17) and 93.75% (15/16), respectively, with no significant difference (P=0.523). At 3 and 6 months after surgery, the integrity recovery of ELM in the combined group was better than that in the simple group, and the difference was statistically significant (t=2.282, 3.101; P＜0.05). At 1, 3 and 6 months after surgery, EZ deletion length in the combined group was lower than that in the simple group, and the difference was statistically significant (t=1.815, 2.302, 2.784; P＜0.05). Compared with 1 week after surgery, VA in macular area of the combined group increased at 1, 3 and 6 months, and the difference was statistically significant (P=0.007, ＜0.001, ＜0.001). At 3 and 6 months after surgery, VA in macular area of affected eyes in the combined group was higher than that in the simple group, and the difference was statistically significant (t=1.897, 2.250; P＜0.05). There was an interaction effect between the surgical method and the follow-up time. The postoperative time was prolonged, and the VA in macular area was decreased in the simple group and increased in the combined group, with statistical significance (F=12.963, P＜0.001). The BCVA and BCVA changes in the two groups increased with the extension of postoperative time. The improvement of BCVA and the difference of BCVA changes in the combined group were significantly higher than those in the simple group at different time points after surgery, with statistically significant differences (F=12.374, 21.807, 5.695, 4.095; P＜0.05). Conclusion PPV combined with ILM peeling and vitreous injection of mNGF is more effective than PPV with ILM peeling for HMMH, improving both anatomical and functional outcomes.

Citation： Yu Xiao, You Zhipeng, Wang Shiwang. Efficacy of internal limiting membrane peeling combined with vitreous injection of mouse nerve growth factor for the treatment of macular hole in high myopia. Chinese Journal of Ocular Fundus Diseases, 2022, 38(6): 484-490. doi: 10.3760/cma.j.cn511434-20211008-00562 Copy

1.	Ohno-Matsui K, Lai TY, Lai CC, et al. Updates of pathologic myopia[J]. Prog Retin Eye Res, 2016, 52: 156-187. DOI: 10.1016/j.preteyeres.2015.12.001.
2.	Johnson MW. Myopic traction maculopathy: pathogenic mechanisms and surgical treatment[J]. Retina, 2012, 32 (Suppl 2): S205-210. DOI: 10.1097/IAE.0b013e31825bc0de.
3.	Spiteri Cornish K, Lois N, Scott NW, et al. Vitrectomy with internal limiting membrane peeling versus no peeling for idiopathic full-thickness macular hole[J]. Ophthalmology, 2014, 121(3): 649-655. DOI: 10.1016/j.ophtha.2013.10.020.
4.	Michalewska Z, Michalewski J, Cisiecki S, et al. Correlation between foveal structure and visual outcome following macular hole surgery: a spectral optical coherence tomography study[J]. Graefe's Arch Clin Exp Ophthalmol, 2008, 246(6): 823-830. DOI: 10.1007/s00417-007-0764-5.
5.	Mesentier-Louro LA, Rosso P, Carito V, et al. Nerve growth factor role on retinal ganglion cell survival and axon regrowth: effects of ocular administration in experimental model of optic nerve injury[J]. Mol Neurobiol, 2019, 56(2): 1056-1069. DOI: 10.1007/s12035-018-1154-1.
6.	Németh J, Tapasztó B, Aclimandos WA, et al. Update and guidance on management of myopia. European society of ophthalmology in cooperation with international myopia institute[J]. Eur J Ophthalmol, 2021, 31(3): 853-883. DOI: 10.1177/1120672121998960.
7.	张英, 韩方媛, 金长辉, 等. 不同黄斑内界膜手术联合空气填充治疗特发性黄斑裂孔[J]. 国际眼科杂志, 2022, 22(3): 505-508. DOI: 10.3980/j.issn.1672-5123.2022.3.32.Zhang Y, Han FY, Jin CH. Clinical observation of different internal limiting membrane surgeries combined w ith sterile air tamponade in the treatment of idiopathic macular hole[J]. Int Eye Sci, 2022, 22(3): 505-508. DOI: 10.3980/j.issn.1672-5123.2022.3.32.
8.	Kelly NE, Wendel RT. Vitreous surgery for idiopathic macular holes. Results of a pilot study[J]. Arch Ophthalmol, 1991, 109(5): 654-659. DOI: 10.1001/archopht.1991.01080050068031.
9.	Wu YJ, Rao J, Wu KR, et al. Vitrectomy with internal limiting membrane peeling versus its flap insertion for macular hole in high myopia: a meta-analysis[J]. Int J Ophthalmol, 2020, 13(1): 141-148. DOI: 10.18240/ijo.2020.01.21.
10.	Wakabayashi T, Ikuno Y, Shiraki N, et al. Inverted internal limiting membrane insertion versus standard internal limiting membrane peeling for macular hole retinal detachment in high myopia: one-year study[J]. Graefe's Arch Clin Exp Ophthalmol, 2018, 256(8): 1387-1393. DOI: 10.1007/s00417-018-4046-1.
11.	Tsai D, Huang YH, Chen SJ. Parafoveal atrophy after human amniotic membrane graft for macular hole in patients with high myopia[J]. Br J Ophthalmol, 2021, 105(7): 1002-1010. DOI: 10.1136/bjophthalmol-2019-315603.
12.	Figueroa MS, Mora Cantallops A, Virgili G, et al. Long-term results of autologous plasma as adjuvant to pars plana vitrectomy in the treatment of high myopic full-thickness macular holes[J]. Eur J Ophthalmol, 2021, 31(5): 2612-2620. DOI: 10.1177/1120672120960340.
13.	李巧林, 周云帆, 徐向忠, 等. 玻璃体切割联合内界膜填塞及鼠神经生长因子注射治疗大直径特发性黄斑裂孔[J]. 国际眼科杂志, 2021, 21(10): 1798-1802. DOI: 10.3980/j.issn.1672-5123.2021.10.27.Li QL, Zhou YF, Xu XZ. PPV combined w ith internal limiting membrane tamponade and rat nerve grow th factor injection in the treatment of large diameter IMH[J]. Int Eye Sci, 2021, 21(10): 1798-1802. DOI: 10.3980/j.issn.1672-5123.2021.10.27.
14.	Zhang L, Li X, Yang X, et al. Internal limiting membrane insertion technique combined with nerve growth factor injection for large macular hole[J]. BMC Ophthalmol, 2019, 19(1): 247. DOI: 10.1186/s12886-019-1258-z.
15.	刘丹宁. 玻璃体腔注射鼠神经生长因子治疗视网膜色素变性的临床前研究[D]. 重庆: 第三军医大学西南医院, 2009.Liu DN. Preclinical study of intravitreal injection of mouse nerve growth factor for retinitis pigmentosa[D]. Chongqing: The South West Hospital, Third Military Medical University, 2009.
16.	Zhang L, Li X, Lin X, et al. Nerve growth factor promotes the proliferation of Müller cells co-cultured with internal limiting membrane by regulating cell cycle via Trk-A/PI3K/Akt pathway[J]. BMC Ophthalmol, 2019, 19(1): 130. DOI: 10.1186/s12886-019-1142-x.
17.	Zhang L, Li X, Shen Y, et al. Transdifferentiation effects and related mechanisms of nerve growth factor and internal limiting membrane on Müller cells[J]. Exp Eye Res, 2019, 180: 146-154. DOI: 10.1016/j.exer.2018.12.005.
18.	Garcia TB, Hollborn M, Bringmann A. Expression and signaling of NGF in the healthy and injured retina[J]. Cytokine Growth Factor Rev, 2017, 34: 43-57. DOI: 10.1016/j.cytogfr.2016.11.005.
19.	Sacchetti M, Mantelli F, Rocco ML, et al. Recombinant human nerve growth factor treatment promotes photoreceptor survival in the retinas of rats with retinitis pigmentosa[J]. Curr Eye Res, 2017, 42(7): 1064-1068. DOI: 10.1080/02713683.2017.1279634.
20.	Kaluzny JJ, Zabel P, Kaluzna M, et al. Macular sensitivity in area of internal limiting membrane (ILM) peeling in eyes after pars plana vitrectomy with temporal inverted ILM flap technique for full thickness macular hole[J]. Retina, 2021, 41(8): 1627-1634. DOI: 10.1097/IAE.0000000000003096.
21.	Viana KÍS, Gordilho CT, Almeida FPP, et al. Combined pars plana vitrectomy (PPV) and phacoemulsification (phaco) versus PPV and deferred phaco for phakic patients with full-thickness macular hole (FTMH) and no significant cataract at baseline: 1-year outcomes of a randomized trial combined PPV/phaco vs PPV/deferred phaco for MH[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(1): 29-36. DOI: 10.1007/s00417-020-04731-7.
22.	Avci R, Mavi Yildiz A, Yilmaz S. Conventional internal limiting membrane peeling versus temporal inverted internal limiting membrane flap for large macular holes[J]. Eur J Ophthalmol, 2021, 31(2): 679-687. DOI: 10.1177/1120672119892427.
23.	Giannelli SG, Demontis GC, Pertile G, et al. Adult human Müller glia cells are a highly efficient source of rod photoreceptors[J]. Stem Cells, 2011, 29(2): 344-356. DOI: 10.1002/stem.579.
24.	Lin B, Zhang X, Xu X. Nerve growth factor protects retinal ganglion cells related to inhibiting endoplasmic reticulum stress by inhibiting IRE1-JNK-CHOP signaling pathway[J]. Ocul Immunol Inflamm, 2021, 1: 1-6. DOI: 10.1080/09273948.2021.1872651.

1. Ohno-Matsui K, Lai TY, Lai CC, et al. Updates of pathologic myopia[J]. Prog Retin Eye Res, 2016, 52: 156-187. DOI: 10.1016/j.preteyeres.2015.12.001.
2. Johnson MW. Myopic traction maculopathy: pathogenic mechanisms and surgical treatment[J]. Retina, 2012, 32 (Suppl 2): S205-210. DOI: 10.1097/IAE.0b013e31825bc0de.
3. Spiteri Cornish K, Lois N, Scott NW, et al. Vitrectomy with internal limiting membrane peeling versus no peeling for idiopathic full-thickness macular hole[J]. Ophthalmology, 2014, 121(3): 649-655. DOI: 10.1016/j.ophtha.2013.10.020.
4. Michalewska Z, Michalewski J, Cisiecki S, et al. Correlation between foveal structure and visual outcome following macular hole surgery: a spectral optical coherence tomography study[J]. Graefe's Arch Clin Exp Ophthalmol, 2008, 246(6): 823-830. DOI: 10.1007/s00417-007-0764-5.
5. Mesentier-Louro LA, Rosso P, Carito V, et al. Nerve growth factor role on retinal ganglion cell survival and axon regrowth: effects of ocular administration in experimental model of optic nerve injury[J]. Mol Neurobiol, 2019, 56(2): 1056-1069. DOI: 10.1007/s12035-018-1154-1.
6. Németh J, Tapasztó B, Aclimandos WA, et al. Update and guidance on management of myopia. European society of ophthalmology in cooperation with international myopia institute[J]. Eur J Ophthalmol, 2021, 31(3): 853-883. DOI: 10.1177/1120672121998960.
7. 张英, 韩方媛, 金长辉, 等. 不同黄斑内界膜手术联合空气填充治疗特发性黄斑裂孔[J]. 国际眼科杂志, 2022, 22(3): 505-508. DOI: 10.3980/j.issn.1672-5123.2022.3.32.Zhang Y, Han FY, Jin CH. Clinical observation of different internal limiting membrane surgeries combined w ith sterile air tamponade in the treatment of idiopathic macular hole[J]. Int Eye Sci, 2022, 22(3): 505-508. DOI: 10.3980/j.issn.1672-5123.2022.3.32.
8. Kelly NE, Wendel RT. Vitreous surgery for idiopathic macular holes. Results of a pilot study[J]. Arch Ophthalmol, 1991, 109(5): 654-659. DOI: 10.1001/archopht.1991.01080050068031.
9. Wu YJ, Rao J, Wu KR, et al. Vitrectomy with internal limiting membrane peeling versus its flap insertion for macular hole in high myopia: a meta-analysis[J]. Int J Ophthalmol, 2020, 13(1): 141-148. DOI: 10.18240/ijo.2020.01.21.
10. Wakabayashi T, Ikuno Y, Shiraki N, et al. Inverted internal limiting membrane insertion versus standard internal limiting membrane peeling for macular hole retinal detachment in high myopia: one-year study[J]. Graefe's Arch Clin Exp Ophthalmol, 2018, 256(8): 1387-1393. DOI: 10.1007/s00417-018-4046-1.
11. Tsai D, Huang YH, Chen SJ. Parafoveal atrophy after human amniotic membrane graft for macular hole in patients with high myopia[J]. Br J Ophthalmol, 2021, 105(7): 1002-1010. DOI: 10.1136/bjophthalmol-2019-315603.
12. Figueroa MS, Mora Cantallops A, Virgili G, et al. Long-term results of autologous plasma as adjuvant to pars plana vitrectomy in the treatment of high myopic full-thickness macular holes[J]. Eur J Ophthalmol, 2021, 31(5): 2612-2620. DOI: 10.1177/1120672120960340.
13. 李巧林, 周云帆, 徐向忠, 等. 玻璃体切割联合内界膜填塞及鼠神经生长因子注射治疗大直径特发性黄斑裂孔[J]. 国际眼科杂志, 2021, 21(10): 1798-1802. DOI: 10.3980/j.issn.1672-5123.2021.10.27.Li QL, Zhou YF, Xu XZ. PPV combined w ith internal limiting membrane tamponade and rat nerve grow th factor injection in the treatment of large diameter IMH[J]. Int Eye Sci, 2021, 21(10): 1798-1802. DOI: 10.3980/j.issn.1672-5123.2021.10.27.
14. Zhang L, Li X, Yang X, et al. Internal limiting membrane insertion technique combined with nerve growth factor injection for large macular hole[J]. BMC Ophthalmol, 2019, 19(1): 247. DOI: 10.1186/s12886-019-1258-z.
15. 刘丹宁. 玻璃体腔注射鼠神经生长因子治疗视网膜色素变性的临床前研究[D]. 重庆: 第三军医大学西南医院, 2009.Liu DN. Preclinical study of intravitreal injection of mouse nerve growth factor for retinitis pigmentosa[D]. Chongqing: The South West Hospital, Third Military Medical University, 2009.
16. Zhang L, Li X, Lin X, et al. Nerve growth factor promotes the proliferation of Müller cells co-cultured with internal limiting membrane by regulating cell cycle via Trk-A/PI3K/Akt pathway[J]. BMC Ophthalmol, 2019, 19(1): 130. DOI: 10.1186/s12886-019-1142-x.
17. Zhang L, Li X, Shen Y, et al. Transdifferentiation effects and related mechanisms of nerve growth factor and internal limiting membrane on Müller cells[J]. Exp Eye Res, 2019, 180: 146-154. DOI: 10.1016/j.exer.2018.12.005.
18. Garcia TB, Hollborn M, Bringmann A. Expression and signaling of NGF in the healthy and injured retina[J]. Cytokine Growth Factor Rev, 2017, 34: 43-57. DOI: 10.1016/j.cytogfr.2016.11.005.
19. Sacchetti M, Mantelli F, Rocco ML, et al. Recombinant human nerve growth factor treatment promotes photoreceptor survival in the retinas of rats with retinitis pigmentosa[J]. Curr Eye Res, 2017, 42(7): 1064-1068. DOI: 10.1080/02713683.2017.1279634.
20. Kaluzny JJ, Zabel P, Kaluzna M, et al. Macular sensitivity in area of internal limiting membrane (ILM) peeling in eyes after pars plana vitrectomy with temporal inverted ILM flap technique for full thickness macular hole[J]. Retina, 2021, 41(8): 1627-1634. DOI: 10.1097/IAE.0000000000003096.
21. Viana KÍS, Gordilho CT, Almeida FPP, et al. Combined pars plana vitrectomy (PPV) and phacoemulsification (phaco) versus PPV and deferred phaco for phakic patients with full-thickness macular hole (FTMH) and no significant cataract at baseline: 1-year outcomes of a randomized trial combined PPV/phaco vs PPV/deferred phaco for MH[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(1): 29-36. DOI: 10.1007/s00417-020-04731-7.
22. Avci R, Mavi Yildiz A, Yilmaz S. Conventional internal limiting membrane peeling versus temporal inverted internal limiting membrane flap for large macular holes[J]. Eur J Ophthalmol, 2021, 31(2): 679-687. DOI: 10.1177/1120672119892427.
23. Giannelli SG, Demontis GC, Pertile G, et al. Adult human Müller glia cells are a highly efficient source of rod photoreceptors[J]. Stem Cells, 2011, 29(2): 344-356. DOI: 10.1002/stem.579.
24. Lin B, Zhang X, Xu X. Nerve growth factor protects retinal ganglion cells related to inhibiting endoplasmic reticulum stress by inhibiting IRE1-JNK-CHOP signaling pathway[J]. Ocul Immunol Inflamm, 2021, 1: 1-6. DOI: 10.1080/09273948.2021.1872651.

Chinese Journal of Ocular Fundus Diseases

Efficacy of internal limiting membrane peeling combined with vitreous injection of mouse nerve growth factor for the treatment of macular hole in high myopia

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content