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经角膜电刺激在视网膜疾病治疗中的研究进展

Research progress of transcorneal electrical stimulation in the treatment of retinal diseases

来源期刊： 眼科学报 | 2023年10月 第38卷 第10期： 708-714 发布时间：2023-10-15 收稿时间：2024/2/19 15:41:42 阅读量：1903
作者：
董雨璐,
蒲思源,
张富文,
关键词：
经角膜电刺激 视网膜疾病 神经调节 治疗方法 安全性
Transcorneal electrical stimulation retinal diseases neuromodulation treatment safety
DOI：
10.12419/2307240001
近年来，眼部电流刺激(electrical stimulation,ES)在不同方向的研究中逐渐揭示了其在多种视网膜疾病中的潜在治疗价值。其中，经角膜电刺激(transcorneal electrical stimulation,TES)作为一种非侵入性的治疗方法，能对视网膜、视神经、眼底血管及其相关结构产生积极的影响。TES能够改善视力，在保护感光细胞和减缓疾病进展方面显示出积极效果，提高患者的生存质量，还能够在不损伤眼球的情况下调节大脑中的神经元活动，为视网膜疾病的治疗提供一种新的选择。该文对近年来TES在视网膜色素变性(retinitis pigmentosa,RP)、年龄相关性黄斑变性(age-related macular degeneration,AMD)、视网膜血管病、青光眼以及视神经病变等疾病中的应用研究进行了综述。研究发现，TES治疗是一种安全且无需手术的辅助治疗工具，具有广泛的应用前景。该文旨在为临床医师提供一个全面的TES研究概述，并深入探讨其在眼科学领域的潜在应用价值。然而，TES治疗的具体机制仍需进一步探讨，以便更好地应用于临床实践。同时，未来研究还应关注TES与其他治疗方法相结合的效果，以期为患者提供更多有效的治疗选择。
In recent years, electrical stimulation of the eye (ES) has gradually revealed its potential therapeutic value in a variety of retinal diseasesin different directions. Among them, transcorneal electrical stimulation (TES), as a non-invasive treatment, can have a positive effect on the retina, optic nerve, fundus vessels and related structures. TES can improve vision, show positive effects in protecting photoreceptor cells and slowing disease progression, improve the quality of life of patients, and can regulate neuronal activity in the brain without damaging the eyeball, providing a new option for the treatment of retinal diseases. The research on the application on TES on retinitis pigementosa (RP), age-related macular degeneration (AMD), retinal angiopathy, glaucoma and optic neuropathy are reviewed in this article. It is found in the study that TES therapy is a safe and surgery-free adjuvant therapy tool, and has a wide application prospect. The purpose of this article is to provide clinicians with a comprehensive overview of TES research,and to explore its potential application value in the field of ophthalmology. However, the specific mechanism of TES therapy still needs to be further explored in order to better apply in clinical practice. At the same time, future studies should also focus on the effect of combining TES with other treatment methods, in order to provide more effective treatment options for patients.
视力障碍和失明会对个人的生活质量产生直接而深远的影响。据估计，全球有超过20亿人存在各种程度的视力损害，其中约2亿人存在中到重度的视力损害甚至失明[1]，而视网膜色素变性(retinitis pigmentosa,RP)、年龄相关性黄斑变性(age-related macular degeneration,AMD)、视网膜血管病、青光眼和视神经病变等是导致不可逆视力丧失的主要原因。这些疾病通常伴随着视网膜神经元和支持细胞的不可逆性损失，进而导致神经元的凋亡和视力的不可逆损害。最近的研究表明，经角膜电刺激(transcorneal electrical stimulation,TES)作为一种新兴的非侵入性治疗方法，在这些视网膜疾病的治疗中显示出潜在的效果。本文将对TES在视网膜疾病中的临床应用及安全性进行综述，探讨其在眼科学领域的前景。

1 经角膜电刺激的介绍

电刺激(electrical stimulation,ES)在19世纪就已在眼部康复领域的应用[2]。20世纪70年代，日本的Morimoto等[3]首次报道了TES对RP患者的治疗效果。Hanif[4]等的研究表明，低水平的ES对人类和动物的视网膜具有明显的神经保护效果。Huang等[5]进一步指出，短暂的ES(3V，20Hz，持续20 min)能够促进延迟性神经损伤的修复，并改善其功能。此后，TES在视网膜疾病的治疗中逐渐引起关注，尤其是在RP、青光眼、黄斑变性等方面。近年来，TES的应用范围扩展到了神经精神疾病，如抑郁症和阿尔茨海默病[6-7]，这显示出TES的广阔前景。目前普遍认为，ES主要通过五种不同方式向患有视网膜或视神经疾病的眼睛输送微量电流，这包括侵入性视网膜下电刺激(subretinal electrical stimulation,SES)、微创经角膜电刺激(transcorneal electrical stimulation,TcES)以及非侵入性经皮电刺激(眼睑电刺激)(transpalpebral electrical stimulation,TpES)、经皮电刺激(transdermal electrical stimulation,TdES)和重复经眶交流电刺激(repetitive transorbital alternating current stimulation,rtACS)[8]。TES可激活视网膜及其下游结构，仅触及皮肤和角膜，微创且不良反应少。其作用原理尚不完全清楚，目前认为主要涉及以下几个方面：TES可以激活视网膜神经元，如视网膜神经节细胞(retinal ganglion cells,RGCs)和光感受器，增加其活性和存活率，抑制其凋亡[9]；可以促进视网膜神经元的突触重塑，增强其可塑性和适应性，改善视网膜的功能[10]；可以调节视网膜和大脑的神经递质，如内源性阿片肽、大麻素等，产生抗炎、抗氧化、抗凋亡、抗兴奋性毒性、抗抑郁等效应[11-12]；可以激活视网膜和大脑的神经生长因子，如脑源性神经营养因子、胰岛素样生长因子1等，促进神经元的生长、分化和修复[12-14]。
TES作为一种非侵入性的电刺激技术，安全性是考量的关键。Schatz等[15]进行的一项52例患者的随机试验中，31例患者在试验结束时出现了暂时性干眼症状，但这些症状在使用人工泪液不到1d后即得到解决。Jolly等[16]也指出，干眼症是TES治疗中最常见的不良事件(发生率为37.5%)，但未观察到由TES引起的严重不良事件。大多数不良事件都是轻微的，未见后遗症。据报道，TES还可能引起异物感[17]和轻度浅表点状角膜病变[18]，但这些反应通常是短暂的，不会影响视力。经裂隙检查和检眼镜检查无明显变化，可通过使用人工泪液改善或自然恢复。在一项针对原发性开角型青光眼(primary open angle glaucoma,POAG)患者的干预性试验中，唯一的不良事件是使用0%的电阈进行假刺激组出现的视盘出血，而TES治疗组未引发任何不良或严重不良事件[19]。根据不同的治疗方案接受电流刺激的动物和临床试验较多，但其不良事件的报道频率和关注程度较低，TES的可应用性和安全性得到了证实。

2 经角膜电刺激的应用

2.1 在视网膜色素变性中的应用

2.1.1 基础研究
RP是一种进行性、遗传性退行性视网膜病变，其特征是感光细胞死亡和视网膜色素上皮萎缩[20-21]。现有研究表明，经TES能够直接影响感光细胞的电活动，在退行性视网膜病变中发挥神经保护作用。例如，Schatz等[15]的研究发现，TES能够保护成年雄性Sprague Dawley(SD)大鼠的视网膜细胞，减少轻度光诱导的视网膜变性和感光细胞死亡。视紫红质Pro 347 Leu (P347L)转基因(Tg)兔,与人类常染色体显性RP (adRP)患者的 P347L突变相似，在该兔模型中，TES同样被证实能够提高视网膜感光细胞的存活率[22]。这些证据表明，TES可以防止光感受器退化，从而发挥对RP的神经保护作用。
随着疾病的进展，视网膜小胶质细胞(R et ine microglial cells,RMGs)被激活并释放多种促炎因子，这些因子改变了视网膜的微环境并加速了感光细胞的凋亡[24-26]。因此，抑制小胶质细胞的促炎分泌是阻止RP进一步发展的关键。研究表明，电刺激可以减弱中风大鼠模型的周围区域肿瘤坏死因子-α(tumor necrosis factor-α,TNF-α)和白介素-1α等炎症细胞因子的表达[27]。而Lennikov等[28]的研究中提到，双相斜坡波形(100μA，20Hz，1h)的电流刺激能够有效抑制小胶质细胞的活性，同时不影响细胞存活。此外，一项使用TES的研究发现，TES能够通过抑制视神经损伤后大鼠模型中RMGs的活化，降低TNF-α的表达，从而抑制小胶质细胞的促炎作用[29]。上述研究结果支持TES对小胶质细胞中抗炎基因表达的直接调节作用，表明经角膜途径的应用可能改善RP患者的炎症反应。然而，这些可能性仍需通过进一步的临床研究加以证实。
2.1.2 临床研究
关于电刺激在治疗R P患者中有效性的最新研究，SinimKahraman和Oner[30]对101例RP患者进行了为期2个月的TES治疗研究，每周进行一次，每次持续30 min，在治疗前的平均最佳矫正视力(best corrected visual acuity,BCVA)在Snellen视力表中为0.19±0.23，视野平均缺损值为-27.46±7.49，经TES治疗1个月后，Snellen线提高至0.25±0.27，比较差异有统计学意义(P < 0.05) ，视野平均缺损值为-25.79±8.69，与基线值相比差异有统计学意义(P< 0.01)。在治疗结束4个月后的随访中，Snellen线为0.24±0.26，视野平均缺损为-26.21±8.5 ，尽管改善程度有所减弱，但仍高于治疗前的基线水平。另一项小规模研究[31]中，21例RP患者在接受12次TES治疗后，BCVA和色觉水平有所提高，且多焦点视网膜电图和25项低视力者生活质量量表(low vision quality of life questionnaire,LVQOL)评分也得到改善。在这项研究中，有95.24%的患者表示对TES治疗感到满意。Stett等[32]在2023年进行的一项随机研究中，对52例RP患者进行了为期一年的每周1次、每次持续30 min的单眼TES治疗(电流幅度0.1~1.0 mA)。研究发现，接受TES治疗的患者的平均视野面积(VFA)减少量比对照组少64%。其他相关研究表明，TES治疗可以增加RP患者视网膜的耗氧量[33]，改善b波振幅[23]、缩短视网膜电图的潜伏期，增加血流量[34]。因此，TES治疗可能是一种有效且安全的方法，有助于减缓RP的进展。然而，为了验证这些初步发现，还需要在更大样本量的患者群体中进行长期随访研究。

2.2 在年龄相关性黄斑变性中的应用

早期研究表明，电刺激能够安全地应用于治疗干性AMD。在一项涉及17例患者(25眼)的研究中，患者每周接受一次微电流刺激治疗(150μA，每次35 min)，25个月后52%的患者矫正视力评分有显著变化(P=0.012)[35]。近年对电刺激治疗AMD的系统评价认为，这种治疗方式对于AMD具有很大的潜力[36]。例如，波兰国家数据库的一项研究对使用玻璃体内治疗湿性AMD的患者进行了为期一年的随访，研究涵盖了2 828例患者，他们接受了阿柏西普或雷珠单抗注射，1年后这些患者的BCVA从基线的58.86个字母增加到65.1个字母[37]。这与2023年的一项TES相关临床试验形成对比，该试验中的治疗组在30周内视力从19.6个字母增加到27.8个字母[38]。更多研究证实，TES能够改善黄斑变性患者的视力和视觉功能[19，39]。然而，为了更准确地验证TES对AMD的直接效果并确定最佳治疗方案，仍需进一步研究。

2.3 电刺激在视网膜血管病的应用

3例视网膜中动脉闭塞(central retinal artery occlusion, CRAO)接受了TES(20 Hz 双相脉冲，1000~1100 μA，每月一次，每次30 min，持续3个月)治疗，2例视力提高0.2 LogMAR单位以上，3例视野均得到改善[40]。此外，临床研究还显示，TES明显改善了和视网膜分支动脉阻塞(retinal branch artery occlusion,BRAO)患者的视功能[41]。更重要的是，多焦视网膜电图(multifocal electroretinogram,mfERGs)显示 TES 治疗后各成分波的内隐时间和振幅均有显著改善，提示TES 对RVO患者的视网膜内外神经元均有良好的作用[41]。Kurimoto等[42]发现，在正常受试者中，TES治疗后3 h和24 h脉络膜视网膜血流量显著增加，这可能是经TES后RAO患者视力改善的原因之一。Morimoto等[43]通过眼底相机观察不同参数TES诱发的血管神经偶联的反应发现，在4s-TES下的反应振幅比在1s-TES下的反应振幅大5倍。由此谨慎地推测，血管反应对刺激持续时间的变化非常敏感，而具体的参数需要进一步的研究。

2.4 在青光眼中的应用

多年来，青光眼的治疗主要集中在控制眼压上[44]。虽然降眼压药物能够减缓病情，但无法防止RGCs的变性[45]。最近在急性高眼压损伤沙鼠模型中进行的一项研究，应用脉冲持续时间为1 ms/相、强度为100μA、频率为20Hz的双极矩形电流进行了每周2次、连续4周的TES治疗后，TES治疗组比对照组的RGC细胞存活率高出39.2%[46]。Assraa等[45]在DBA2/j小鼠青光眼模型中应用对称双相方波(100μA，1 ms脉冲宽度，20 Hz，10 min)，每3 d 1次，持续8周的TES治疗后，发现TES组的视神经退变程度较对照组轻，同时，他们在RGC轴突中观察到了TES的保护作用，表明TES治疗能够恢复视网膜和视神经中的能量稳态，并减少炎症反应。2018年，Naycheva 等[47]将14例POAG患者随机分为3组，并接受TES治疗(正向双向脉冲，0.15~0.90 mA, 20 Hz，每次30 min，每周1次，连续6周)，治疗后患者的眼压和视野无变化。而Ota等[48]进行的另一项研究报告称，经双相脉冲(10 ms)，100%EPT，20 Hz，每次30 min，每3个月1次，共11~68个月的TES干预后，BCVA、视网膜电图、眼压无显著变化，但视野缺损有所改善。这些研究表明，青光眼患者可能从TES治疗中受益，尤其是在RGCs保护方面。然而，青光眼患者目前应仅在研究条件下接受TES治疗，大规模的临床研究是进一步验证TES疗效和安全性的必要条件。

2.5 在视神经病变中的应用

在一项非动脉缺血性视神经病变(non-ar terial ischemic optic neuropathy,NAION)大鼠模型研究中，使用1 ms/相、100μA、20Hz频率的双相方形脉冲进行了60 min的TES治疗。实验在第1、4、7、14、28 d进行，在治疗的第28 d，TES组大鼠的暗视阈值反应振幅优于对照组，且TES组在第14天和第28天的RGCs存活率高于对照组[49]。另一项研究也有类似的发现[50]。Fujikado等[18]对5例外伤性视神经病变(traumatic optic neuropathy, TON)患者进行了一次TES治疗(600 - 800 μA, 20 Hz,30 min)后，3月后的随访中2例TON患者的外周视野面积仍有所增加。该研究还对3例NAION患者进行TES治疗，2例患者的视力提高至少0.3 LogMAR，尽管在停止TES治疗几个月后患者的视力有所下降，但在第二次TES治疗后，视力再次得到提高。这些发现暗示了TES治疗与视力改善之间的因果关系。尽管在短期病例系列中TES治疗被报道为有效，但目前它还未被广泛认可。为了确认TES治疗的有效性和安全性，还需要进行更多的临床试验。

3 小结与展望

TES作为一种创新的治疗方法，已在RP、AMD、视网膜血管病、青光眼及视神经病变等疾病中展现出潜在的治疗效果。研究表明，TES能够改善视力和视网膜功能，通过刺激视网膜及其神经元的电活动，提高患者的视觉质量。尤其在RP和AMD治疗中，TES不仅改善了视力，还在保护感光细胞和减缓疾病进展方面显示出积极效果。在视网膜血管病和青光眼治疗中，TES通过提高RGCs的存活率和改善视网膜血流，为这些疾病的管理提供了新的方向。此外，TES在视神经病变的治疗，特别是非动脉缺血性视神经病变和外伤性视神经病变的患者中同样表现出潜在的益处。TES在其他相关神经退行应用中，发现其显示出抗抑郁样行为效果，表明它不仅能改善视力，还可能对整个神经系统产生积极影响[6]。因此，TES作为一种非侵入性神经调节工具，在神经科学相关领域的应用前景值得进一步研究和探讨。关于TES治疗的安全性，研究表明，当适当控制电流强度时，TES是一种安全的治疗方式。尽管某些患者可能经历轻微的不良反应，如暂时性干眼症、异物感、一过性浅表角膜炎，但大多数不良事件都是轻微且无后遗症的。
综上所述，TES作为一种新兴的治疗方法，在多种视网膜疾病中展示了其潜在的治疗价值和良好的安全性，但仍需要更多的研究来进一步验证其长期效果和最优治疗参数。

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1、四川省自然科学基金项目(2023NSFSC0690)。
This work was supported by the Sichuan Natural Science Foundation project(2023NSFSC0690) .()
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