Impulse modulating therapeutic electrical stimulation (IMTES) increases visual field size in patients with optic nerve lesions

Impulse modulating therapeutic electrical stimulation (IMTES) increases visual field size in patients with optic nerve lesions

International Congress Series 1282 (2005) 525 – 529 www.ics-elsevier.com Impulse modulating therapeutic electrical stimulation (IMTES) increases vis...

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International Congress Series 1282 (2005) 525 – 529

www.ics-elsevier.com

Impulse modulating therapeutic electrical stimulation (IMTES) increases visual field size in patients with optic nerve lesions A.B. Fedorova,*, A.N. Chibisovab, J.M. Tchibissovac a

The Centre of Clinical Electrical stimulation, Grazhdansky pr. 114-1-402, 195267, Saint-Petersburg, Russia b The Centre of Clinical Electrical stimulation, Saint-Petersburg, Russia c State Medical Academy of Iy. Mechnikov, Saint-Petersburg, Russia

Abstract. Objective: The restoration of visual functional loss that results from optic nerve lesions is still considered an unsolved problem. Despite the large number of the optic nerve fibers, their capacity of plasticity to achieve recovery is rather limited. In these conditions, it seems appropriate to activate intact visual cortex of blind or partial sight patients to rehabilitate vision. Methods: We applied impulse modulating therapeutic electrical stimulation (IMTES) to activate visual pathway structure and striate cortex, where small electrical currents are applied to the eye ball non-invasively. Efficacy of this treatment was studied clinically with perimetry and physiologically using EEG, VEP and PET data. The recordings were compared between different etiologies, degrees of initial vision loss and the type of visual field (VF) defects. Subjects: We analyzed the outcomes of 874 patients, which has sustained either severe or partial optic nerve lesion of traumatic, inflammatory and post-tumour origin. Results: Before treatment, most patients had severe vision loss ranging from to total blindness to severe or mild VF defects. The best clinical effect was seen in the group of patients with severe visual impairment. Here, 62.6% of the cases responded positively to IMTES as evidence by perimetric and/or physiological recordings. Repeated perimetry revealed enlargement of peripheral visual field (mean 27.5% from background), visible as contraction or decreased absolute scotoma size. Of the patients with legal blindness (visual acuity not exceed sense of light or small remnant of residual vision was still), 16% showed benefits. In groups of the patients with blindness or slight vision, the recovery of visual function was achieved in 49.7% and 58.2% of the cases, respectively. In some cases, striate cortex activation as documented with EEG and PET confirmed these observations. Conclusions: We propose that IMTES-induced restoration of vision is not only mediated by

* Corresponding author. Tel.: +7 812 5318052; fax: +7 812 5318052. E-mail address: [email protected] (A.B. Fedorov). 0531-5131/ D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2005.05.007

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improved optic nerve function but it also activates striate and extrastriate cortex in which plasticity is physiologically induced. D 2005 Elsevier B.V. All rights reserved. Keywords: Electrical stimulation; Optic nerve; Brain lesion; Visual field; Restoration; Striate cortex; Plasticity

1. Introduction According to various authors, the prevalence of pregeniculate visual disturbances in case of brain injury of traumatic, vascular and tumoural pathological processes is widely varied and reach more than 40% [1–6]. Severe visual function loss in patients with brain injury adversely affects neurorehabilitation process because vision provides for such major functions as space orientation, visual control of movements and focussing attention [3]. It proves high medical and social importance of this problem. The recent 15 years the method of impulse modulating therapeutic electrical stimulation (IMTES) successfully is used for vision rehabilitation in patients with optic neuropathy (ON), retina diseases and amblyopia [7,8]. The goal of this study was to estimate the efficiency of IMTES application for sight recovery in patients with optic neuropathy. 2. Subjects and methods We have studied 874 patients with visual function loss caused by pregeniculate visual optic pathway, which were treated by using IMTES method. Patients were distributed depending on etiology of visual impairment; an amount of the surveyed eyes, sex, age and visual disturbances duration are presented in Table 1. Neuroophthalmological, neurological and neurophysiological examinations for every patient, compared with CT or MRI data, were performed. Neuroophthalmological examination included measurements of VA, visual fields defects (VFD) identification. According to background of visual acuity, all patients were divided into five groups based on the criteria of visual impairments established by WHO [9]. Visual field defects (VFD) were evaluated by using Goldman perimetry. The results of sight loss were compared with brain injury and the level of visual system impairment. Neurophysiological examinations included EEG and VEP (flash and reverse pattern) examinations. The IMTES was carried out using special multichannel device by weak currents impulses generated in blocks of forms 2 to 9 impulses with frequency from 5 up to 30 Hz. An active multichannel electrode was placed in the eyeball area and a passive electrode was located either inside the arm or at Table 1 The characteristics of patients examined depend on optic nerve damage etiology, sex, age and disease duration Etiology

Brain trauma CNS inflammation Post-tumour Glaucoma

Persons

Sex

Age

Disease duration

Patients, n =874

Eye, n =1576

Male, n =577

Female, n =297

Range

M FS.D.

Range

M FS.D.

375 185 158 156

568 370 326 312

277 148 56 96

98 37 102 60

14–68 14–55 14–74 39–87

32.4F 8.7 31.8F 8.5 33.7F 9.3 67.5F 9.8

0.6–12 1–9 1–14 3–10

5.9F2.5 5.5F2.7 6.6F3.2 5.7F2.2

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back of the head (in the projection of occipital lobe). The amplitude of pulse currents was no more than 1000 mkA. The treatment, which was conducted continuously, took 10 days. Under moderate visual function improvements, we meant VA increase of more than 50% from the initial value and VF enlargement in the range from 25% to 75% from the initial degree. By significant visual function improvement, we meant two-fold increase of VA as compared with background and/or of VF expansion more than 75% from the initial stage. If VF was enlarged less than 25% from the reference value, such effect was considered to be insignificant expansion. The reliability VA and VF dynamics were based on paired t-criterion for dependent samples. To determine the strengths of linear associations between VA and VF values and different variables such as age, sight loss duration and the number courses of the treatment were performed based on the Pearson product-moment correlation. 3. Results All patients had deep visual acuity decrease and significant visual field defects as the result of visual pathway injury including prechiasmal one-sided or bilateral optic nerve lesion, chiasm lesion and postchiasmal optic tract injury. More than 40% of all patients examined had total blindness or blindness. Severe visual impairment was revealed in 29.8% of all cases. And only in 29.2% of VA cases was more than 6/60 and above. The following types of VFD were defined: (1) only contraction of the peripheral borders (30%), (2) combination of peripheral borders contraction with central scotoma (26.9%), (3) only central or pericentral absolute scotoma (24.4%) and (4) residual areas in temporal or nasal field parts (18.7%). The degree of VF contraction highly correlated with the type of VFD (r =0.49, p = 0.001). Visual function recovery after IMTES application was compared with initial degree of visual impairment and separated with type of improvements (Fig. 1). As shown on Fig. 1, the best clinical effect was seen in the group of patients with severe visual impairment—62.6% positive results. Patients with total blindness could achieve VA increase only in 16% (appearance of object sight). In patient’s group, bvisual impairmentQ effect of VF restoration (28.9%) clearly prevailed. In groups of the patients with slight vision, visual function recovery was revealed in 58.2%. The evidence of the stability of clinical effects was considered. As mentioned above, visual function improvement depended not only on initial VA, but also on the origin of optic nerve lesion.

Fig. 1. Visual functions dynamics of after IMTES application. (A) No effects, (B) only visual acuity increasing, (C) VA increasing in the combination with VF enlargements, (D) only VF enlargements.

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Fig. 2. Visual field examination and visual acuity value before (I) and after (II) treatment course for a patient with optic nerve lesion after inflammatory process. Recovery of vision. Significant reduction of the central scotoma size and considerable visual acuity increase. Normal VF borders are shown by black contour lines. The area of grey color corresponds to zones of VF loss—absolute central scotoma. The hatching shows the zone of VF with relative scotoma.

Maximum efficiency after the IMTES course was observed in patients with ION—55.4% positive results. Similar results were obtained in TON and GON patients group—48.2% and 45.2% vision recovery, respectively. In the case of post-tumour ON, the positive effects were observed in 26.4% of the cases. The clear correlation between type of VF defects and the degree of the enlargement was revealed (r = 0.48, p b0.001). In patients group with residual field in 26% cases was observed the improvement of more than 75% from background. In patients with absolute central scotoma and peripheral border contraction, the degree of VF improvement was moderate (25% to 75% from initial value) and was observed in 34% and 27% cases correspondingly. In cases where central scotoma and the contraction of peripheral border were combined, 82% cases revealed VF expansion of less than 25% from the initial value. The analysis of the correlation between VF enlargement degree and the initial defect degree has shown that maximum frequency of VF improvements was observed in the case of moderate narrowing (from 1008 up to 3008). An example of clinical improvement is shown in Fig. 2. Taking into account the data concerning the direct relationship between sight and alpha rhythm in EEG, which are confirmed by our research of patients with optic nerve and retina diseases [8], our special interest was to compare vision recovery in patients with a optic nerve injury with brain bioelectrical activity reorganization. After the treatment in patient’s EEG in cases of the initial absence of alpha rhythm in primary visual cortex projection, alpha range groups started to appear ( p b 0.01), which gradually formed steady patterns of alpha rhythm. In the case of relatively intact alpha rhythms in rear brain areas were not only more modulated, but had a tendency to spreading into the projection of parietal lobe.

4. Discussion and conclusion Investigation of the clinical application of the IMTES in patients with severe visual impairment including blindness has shown the possibility to achieve visual functions recovery. The degree of visual acuity loss and type of visual field defects were leading criteria affecting to the result of the treatment (based on correlation analysis). As for the

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dependences of positive results of the duration of vision loss and patient’s age, no good correlation was revealed. Groups of patients included into the category of blind or severe visual impairment, according to WHO classification [9], seem to be more promising in terms of sight recovery. In visual system, the most considerable reserve of plasticity is associated with visual cortex, the least—with the neurons of lateral geniculate nucleus and retina [10–14]. It is suggested that, during IMTES directed at afferent inputs of visual system, there occurs activation of classical visual pathway (retino-geniculate-striate way) involving parallel visual pathways, which pass through superior calliculus and pulvinar to extrastriate cortex zones [15], and also along retinohypothalamic pathway ensuring functional relationship between retina with suprachiasmatic nuclei of hypothalamus [12,16]. The result of neurophysiological investigations has shown that visual function recovery is combined with the activation of not only striate, but also extrastriate cortex zone. Such functional brain cortex reorganization involving nonspecific (parietal) cortical areas is likely to be associated with the mechanisms of the cortex plasticity. References [1] M.S. Fowler, et al., Squints and diplopia seen after brain damage, J. Neurol. 243 (1996) 86 – 90. [2] R. Gianutsos, Vision rehabilitation following acquired brain injury, in: M. Gentile (Ed.), Functional Visual Behavior. A Therapists Guide to Evaluation and Treatment Options, American Occupational Therapist Organization, Bethesda, MD, 1997, pp. 267 – 294. [3] G. Kerkhoff, Neurovisual rehabilitation: recent developments and future directions, J. Neurosurg. Psychiatry 68 (2000) 691 – 706. [4] A. Munier, et al., Causes of blindness in the adult population of the Republic of Ireland, Br. J. Ophthalmol. 6 (1998) 630 – 633. [5] M. Yap, J. Weatherill, Causes of blindness and partial sight in the Bradford Metropolitan District from 1980 to 1985, Ophthalmic Physiol. Opt. 9 (1989) 289 – 292. [6] J. Zihl, D. Von Cramon, Visual field recovery from scotoma in patients with postgeniculate damage, Brain 108 (1985) 335 – 365. [7] A.N. Chibisova, A.B. Fedorov, The method of vision rehabilitation under optic nerves atrophy, retina diseases and amblyopia. Patent of Russian Federation (1996) N 2102046. [8] A.N. Chibisova, A.B. Fedorov, N.A. Fedorov, Neurophysiologic features of compensatory brain process at the rehabilitation of sensoneural disturbances of visual and hearing system, Hum. Physiol. 3 (2001) 14 – 21. [9] World Health Organization, International Statistical Classification of Diseases and Related Health Problems, Tenth Revision, vol. 1, World Health Organization, Geneva, 1992. [10] U.Th. Eysel, F. Gonzalez-Aguilar, U. Mayer, A functional sign of reorganization in the visual system of adult cats: lateral geniculate neurons with displaced receptive fields after lesions of the nasal retina, Brain Res. 181 (1980) 285 – 300. [11] C.D. Gilbert, T.N. Wiesel, Receptive field dynamics in adult primary visual cortex, Nature 356 (1992) 150 – 152. [12] B. Rusak, Photic enthronement routes in mammals, Discuss. Neurosci. 8 (1992) 38 – 43. [13] B.A. Sabel, Restoration of vision I: neurobiological mechanisms of restoration and plasticity after brain damage—a review, Restor. Neurol. Neurosci. 15 (1999) 177 – 200. [14] J. Kaas, Plasticity of sensory and motor maps in adult mammals, Annu. Rev. Neurosci. 14 (1991) 137 – 167. [15] D.C. Van Essen, Behind the optic nerve: an inside view of the primate visual system, Trans. Am. Ophthalmol. Soc. 93 (1995) 123 – 133. [16] T.G. Youngstrom, M.L. Weiss, A.A. Nunez, Retinofugal projections to the hypothalamus, anterior thalamus and basal forebrain in hamsters, Brain Res. Bull. 26 (1991) 403 – 411.