Effects of galvanic stimulation of the mastoid process on the gastric motility induced by caloric stimulation

Effects of galvanic stimulation of the mastoid process on the gastric motility induced by caloric stimulation

Auris Nasus Larynx 26 (1999) 263 – 268 Effects of galvanic stimulation of the mastoid process on the gastric motility induced by caloric stimulation ...

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Auris Nasus Larynx 26 (1999) 263 – 268

Effects of galvanic stimulation of the mastoid process on the gastric motility induced by caloric stimulation Byung Rim Park a,*, Min Sun Kim a, Moon Young Lee a, Yong Ki Kim b, Suck Chei Choi c, Yong Ho Nah c a Department of Physiology, Wonkwang Uni6ersity School of Medicine, Iksan 570 -749, South Korea Department of Otolaryngology, Chosun Uni6ersity School of Medicine, Kwangju 501 -759, South Korea c Department of Internal Medicine, Wonkwang Uni6ersity School of Medicine, Iksan 570 -749, South Korea b

Received 5 June 1998; received in revised form 7 December 1998; accepted 22 January 1999

Abstract The effects of galvanic stimulation to the mastoid portion on the vestibuloautonomic symptoms induced by caloric stimulation, such as nausea, vomiting, and vertigo, were evaluated in this study. Gastric motility was measured by electrogastrography (EGG) in 20 healthy volunteers (11 male and nine female) aged 20 – 30 (average: 25.4) years. Electrical stimulation of the mastoid process with 1.0– 3.0 mA, 1.0 ms, 100 Hz was applied using a bipolar-biaural method during caloric stimulation of the external auditory canal. The dominant frequency and power of EGG were determined using running spectral frequency analysis and the time-course of EGG was evaluated in a pseudo three dimensional graphic. Frequency of EGG was classified into normogastria with 3 cpm, bradygastria with lower than 3 cpm, and tachygastria with higher than 3 cpm. At quiescent period, normogastria was 78.7 9 3.7%, bradygastria 5.0 9 1.1%, and tachygastria 16.4 93.7%. Caloric stimulation with warm water in the unilateral ear and cold water in the contralateral ear elicited vestibuloautonomic symptoms, with accompanied decreases in normogastria (57.7 9 4.6%, PB0.01) and increases in tachygastria (34.8 9 4.8%, PB 0.01). Cathodal stimulation to the mastoid process ipsilateral to cold water irrigation during caloric stimulation restored normal pattern of gastric motility: normogastria in 77.195.3% and tachygastria in 19.39 4.7%, and relieved vestibuloautonomic symptoms. Cathodal stimulation to the inhibited vestibular system ameliorates the vestibular symptoms induced by caloric stimulation. © 1999 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Vestibuloautonomic symptom; Electrogastrography; Caloric stimulation; Galvanic stimulation

* Corresponding author. Tel.: +82-653-850-6773; fax: + 82-653-842-6373. E-mail address: [email protected] (B. R. Park) 0385-8146/99/$ - see front matter © 1999 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 3 8 5 - 8 1 4 6 ( 9 9 ) 0 0 0 1 3 - 9

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1. Introduction

2.1. Recordings and analysis of EGG

In recent years, galvanic stimulation has been introduced as a useful means for recovery of vestibular symptoms after unilateral vestibular lesion (ULX) in animals [1 – 3], in which galvanic stimulation caused a faster compensation in nystagmus and head deviation. However, little has been known on the effects of electrical stimulation on vestibuloautonomic symptoms, such as nausea and vomiting. Nor have etiology and treatment of the autonomic symptoms caused by vestibular dysfunctions been elucidated. Vestibuloautonomic reflex is different from vesitbuloocular or vestibulospinal reflex since it contains more synapses than the other reflexes [4] and has no reciprocal antagonism, such as excitation by ipsilateral stimulation and inhibition by contralateral stimulation. Many basic studies have been performed to examine salivary secretion, heart rate, and respiration after ULX [5,6], and the gastric motility by means of cutaneous electrogastrography (EGG) was recorded for investigating vestibuloautonomic symptoms [7]. The twofold purposes of the present study were to investigate the changes of EGG by caloric stimulation and to evaluate the effects of galvanic stimulation to the mastoid process on the recovery of gastric motility induced by caloric stimulation in healthy adults.

EGG was recorded by using electrogastrography (Microdigitrapper, Synetics Medical, USA) with Ag–AgCl cutaneous electrodes in supine position. A cutaneous electrode as a reference was placed on the skin at 2 cm above the umbilicus, and a pair of exploring electrodes were placed at 5 cm above the reference and at 5 cm left from the reference, respectively [8]. EGG was recorded continuously during 60-min, 20 min after placing electrodes in darkness; 30 min for baseline and 30 min for caloric stimulation of the vestibular system. The dominant frequency and power of EGG were determined using running spectral frequency analysis and the time-course of EGG was evaluated in a pseudo three dimensional graphic [7]. The dominant frequency of EGG was divided into three types: normogastria with three cycles per minute (cpm; normal range of 2.5–3.5), bradygastria with lower than 3 cpm, tachygastria with higher than 3 cpm [9]. More than 10 cpm was discarded in analyzing EGG since it represented the motility of small intestine. The control EGG was obtained from the baseline recordings for 30 min in all subjects.

2. Material and methods Twenty volunteers (11 male and nine female) aged 20–30 (average: 25.4) years were tested. Each subject was given a brief physical and ENT examination before experiment; none was found to be abnormal, nor had past history of neurological disorders. Subjects were applied with caloric stimulation to elicit vestibuloautonomic symptoms, in which galvanic stimulation was applied during caloric stimulation. Subjects fasted for at least 4 h before the experiment. The procedure used was approved by the Institutional Ethical Committee on Experimental Use of Human Subjects.

2.2. Caloric stimulation of the 6estibular system Each subject was laid supine with head tilted 30° above horizontal and was kept awake. To evoke vestibuloautonomic symptoms by excitation of the unilateral vestibular system and inhibition of the contralateral system, 250 ml warm water at 44°C was applied to the unilateral external auditory canal for 30 s and 250 ml cold water at 30°C was applied to the contralateral ear for 30 s, with a 2-min interval in between.

2.3. Gal6anic stimulation of the 6estibular system Galvanic stimulation was applied to the mastoid process by square pulses with 1.0 ms, 100 Hz through a pair of Ag–AgCl cutaneous bipolar electrodes. Intensity of electrical stimulation was at the range of 1–3 mA which could abolish caloric stimulation-induced nystagmus. In order to evaluate the effects of electrical stimulation on

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vestibuloautonomic symptoms induced by caloric stimulation, a cathodal electrode was positioned on the mastoid process of cold water irrigated side and an anodal electrode was on the warm water side. Electrical stimulation was continued for 3 min during caloric stimulation.

2.4. Statistical analysis All data are presented as mean9SE. The statistical significance of difference was assessed using analysis of variance (ANOVA). The statistical difference was defined significant at P B 0.05 for all analyses.

3. Results

3.1. EGG at quiescent period Each subject showed stable and regular patterns of EGG at rest without stimulation. Each subject had three types of gastric motility, normogastria with 3 cpm, bradygastria with lower than 3 cpm, and tachygastria with higher than 3 cpm. In all subjects with recording for 30 min as a baseline (control), 3 cpm was in 78.79 3.7%, bradygastria was in 5.091.1%, and tachygastria

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was in 16.4 9 3.7% (Fig. 1). These results indicated that normal EGG with 3 cpm was the most dominant and bradygastria was the least.

3.2. EGG in response to caloric stimulation Warm water irrigation of unilateral ear and cold water irrigation of contralateral ear elicited nystagmus (100%), dizziness (50%), nausea (45%), and vomiting (5%). The caloric stimulation produced changes of EGG at 0.5–4 min, and the symptoms were abolished after 10–20 min of stimulation. These results also showed that normogastria (57.79 4.6%) decreased (PB 0.01), and tachygastria (34.89 4.8%) increased (PB 0.01). The percentage of bradygastria (7.59 2.1%) was not significantly altered (Figs. 2 and 3). Amplitude in EGG was not proportional to the changes in frequency. However, subjects with the large amplitude produced by caloric stimulation complained severe symptoms in a few cases. Nystagmus induced by caloric stimulation which was observed by video-camera preceded changes in EGG. The severity of vestibuloautonomic symptoms was proportional to intensity of tachygastria in all subjects. Especially, one subject who had higher rate of tachygastria (65.3%) experienced severe vertigo and vomiting during caloric stimulation.

3.3. Effects of gal6anic stimulation on EGG induced by caloric stimulation

Fig. 1. Regular pattern of EGG at rest over 30 min before either caloric or electrical stimulation in 20 normal adults. Each subject had three types of gastric motility. 3CPM (normal range with 3 cpm), tachygastria (TACHY) with higher than 3 cpm, and bradygastria (BRADY) with lower than 3 cpm. Each bar represents mean 9SE.

To determine the effects of galvanic stimulation on the recovery of vestibuloautonomic symptoms induced by caloric stimulation, EGG was measured during electrical stimulation of the mastoid process. When the cathodal stimulation was applied to the mastoid process of the ear inhibited by cold water irrigation and the anodal stimulation was applied to the mastoid process in warm water irrigated side, EGG restored normal pattern by increase in 3 cpm (77.1 9 5.3%, PB 0.01) and decrease in tachygastria (19.394.7%, PB 0.05) compared with data obtained by caloric stimulation only, which were similar to control values without stimulation (Fig. 3). In parallel with recovery of gastric motility, nausea, vomiting, dizzi-

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Fig. 2. Three dimensional analysis of EGG during caloric stimulation. After baseline recording for 30 min, right ear was irrigated by cold water for 30 sec and left ear by warm water for 30 s with 2 min interval in between. Power (dB) represents the amplitude of gastric motility. CAL indicates the duration of caloric stimulation.

ness and nystagmus were also ameliorated by galvanic stimulation.

4. Discussion The present results demonstrate that galvanic stimulation to the mastoid process facilitates recovery of vestibuloautonomic symptoms occurred during caloric stimulation. This is also manifested by the restoration of gastric motility to control level. Considering that tachygastria is closely related to motion sickness [7], EGG may be useful as an index for evaluating vestibuloautonomic symptoms. Moreover, EGG using cutaneous electrodes is not only closely correlated with direct EMG of gastric wall muscle [10], but also is easily recorded. The dominant frequency of EGG in quiescent period was 3 cpm, higher frequency than 3 cpm was tachygastria, and lower frequency was bradygastria [9]. Although the neurohumoral mechanisms that mediate nausea and tachygastria in caloric vestibular stimulation are unknown, imbalance of electrical activities in bilateral VN could have more important role in occurrence of vestibuloautonomic symptoms than sympathetic dominance

induced by stress. The imbalance of electrical activities in VN induced by caloric stimulation is indirectly identified by the appearance of nystagmus of which direction corresponded to excitation of the vestibular system. The mechanism of vestibuloautonomic symptoms induced by caloric stimulation was also similar to that of vestibuloocular response induced by sinusoidal electrical stimulation to the mastoid process in human subjects [11]. Electricity has been widely used for treatment as well as diagnosis because it has a thermal, chemical, and physiological effects in vivo [12]. Cathodal stimulation of the vestibular system increased afferent signals by depolarizing the vestibular nerve, whereas anodal stimulation decreased afferent signals by hyperpolarizing the nerve [13]. Park et al. [2] reported that cathodal stimulation with 1.0 ms and 100 Hz to the lesioned vestibular system promoted recovery of spontaneous nystagmus, and restored vestibuloocular reflex induced by sinusoidal rotation and postural imbalance after unilateral labyrinthectomy in rabbits. Taken together, chronic electrical stimulation of the lesioned vestibular system may facilitate neuronal plasticity at the level of the vestibular nuclei or higher centers by expansion of

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the peripheral innervation, unmasking existing connections, functioning blind axonal endings, increasing nerve growth factor, or development of supersensitivity and/or up-regulation of receptors for neurotransmitters [14]. Moreover, the vestibuloocular reflex induced by sinusoidal rotation during cathodal stimulation restored normal pattern in unilateral labyrinthectomized rabbits [2] and rats [3], suggesting that the vestibular symptoms caused by unilateral vestibular lesion could be recovered by restoration of electrical activity in the lesioned vestibular system. In this case, it is clear that electrical stimulation acts directly on the vestibular nuclei instead of peripheral vestibular inputs of the lesioned side. Therefore, galvanic stimulation to the lesioned vestibular system may be useful for treatment of vestibuloautonomic symptoms assuming that the symptoms would be caused by imbalance of afferent signals in bilateral VN [15,16]. The present study demonstrated that the cathodal, but not the anodal, stimulation restored normal level of gastric motility by reducing tachygastria induced by caloric stimulation. Elec-

Fig. 3. Effects of electrical stimulation to the mastoid process on EGG induced by caloric stimulation. CON, control (n= 20); CAL, caloric stimulation (n=14); CAL +ES, electrical stimulation with cathodal current to the cold water-irrigated side during caloric stimulation (n=7). ** Significantly different from control, **PB 0.01. †,‡ Significantly different from caloric stimulation, †P B 0.05, ‡PB 0.01.

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trical stimulation may be a useful tool to diminish vestibuloautonomic symptoms at acute stage as well as to facilitate plasticity in the central nervous system following vestibular lesions. In addition, EGG could be used as a useful index to monitor vestibuloautonomic symptoms. Acknowledgements This research was supported by Braintech 97N1-02-03-A-01 and Wonkwang University (1998). References [1] Masumitsu Y, Sekitani T. Effect of electric stimulation on vestibular compensation in guinea pigs. Acta Otolaryngol (Stockh) 1991;111:807 – 12. [2] Park BR, Suh JS, Kim MS, Jeong JY, Chun SW, Lee JH. Influence of sensory deprivation or electrical stimulation on acute vestibular symptoms following unilateral labyrinthectomy in rabbits. Acta Otolaryngol (Stockh) 1995;Suppl. 519:62 – 7. [3] Park BR, Park SK, Kim MS, Lee MY. Modification of vestibuloocular reflex by electrical stimulation following unilateral labyrinthectomy in rats. Exp Neurobiol 1995;4:53 – 60. [4] Yates BJ, Goto T, Bolton PS. Responses of neurons in the caudal medullary raphe nuclei of the cat to stimulation of the vestibular nerve. Exp Brain Res 1992;89:323 – 32. [5] Igarashi M, Chae S, MacDonald S, Himi T, Takeda N. Autonomic indexes during the vestibulo-visual conflict exposure: a squirrel monkey study. Auris Nasus Larynx 1990;17:69 – 76. [6] Miller AD, Yates BJ. Vestibular effects on respiratory activity. In: Yates BJ, Miller AD, editors. Vestibular autonomic regulation. New York: CRC Press, 1996:113 – 44. [7] Stern RM, Koch KL, Stewart WR, Lindblad IM. Spectral analysis of tachygastria recorded during motion sickness. Gastroenterology 1987;92:92 – 7. [8] Pfaffenbach B, Adamek RJ, Kuhn K, Wegener M. Electrogastrography in healthy subjects. Evaluation of normal values, influence of age and gender. Dig Dis Sci 1995;40:1445 – 50. [9] Atanassova E, Daskalov I, Dotsinsky I, Christov I, Atanassova A. Non-invasive electrogastrography. Part 2: Human electrogastrogram. Arch Physiol Biochem 1995;103:436 – 41. [10] Kajimoto T. Relation between electrogastrography and gastric electromyogram, mechanical activity. J Smooth Muscle Res 1995;31:93 – 107. [11] Moore DM, Hoffman LF, Beykirch K, Honrubia V, Baloh RW. The electrically evoked vestibulo-ocular

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reflex. 1. Normal subjects. Otolaryngol Head Neck Surg 1991;104:219 – 24. [12] Cummings J. Electrical stimulation of healthy muscle. In: Nelson RM, Currier DP, editors. Clinical electrotherapy. Norwalk: Appleton & Lange, 1987:81–96. [13] Goldberg JM, Fernandez C, Smith CE. Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents. Brain Res 1982;252:156–60. [14] Mendell LM. Modifiability of spinal synapses. Physiol Rev 1984;64:260 – 324.

[15] Lee MY, Kim MS, Park BR. Effect of electrical stimulation of the vestibular system on neuronal activity of the ipsilateral medial vestibular nuclei following unilateral labyrinthectomy in rats. Korean J Physiol Pharmacol 1997;1:263 – 73. [16] Park BR, Hwang HR, Lee MY, Kim MS. Effect of electrical stimulation of the vestibular system on vestibuloocular reflex and c-Fos expression in the medial vestibular nuclei of unilateral labyrinthectomized rats. Korean J Physiol Pharmacol 1997;1:275 – 84.

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