Ann Otol Rhinol Laryngo/lOO:1991
ELECTRICAL PACING FOR DYNAMIC TREATMENT OF UNILATERAL VOCAL CORD PARALYSIS EXPERIMENT IN LONG-DENERVATED MUSCLE HISAYOSHI KOJIMA, MD IWAO
HONIO,
MD
KOICHI OMORI, MD
MITSUHARU NONOMURA, MD
NOBUHIKO ISSHIKI, MD
YASUHIKO SHIMIZU, MD
KYOTO, JAPAN
In order to explore the possibility of clinical application of laryngeal pacing as a treatment for unilateral vocal cord paralysis, we examined the reactivity of atrophic muscle to electrical stimulation in dogs whose recurrent laryngeal nerves were damaged by crushing, dissection followed by resuturing, or a 3-cm neurectomy. The threshold level to induce enough vocal cord adduction reached the maximum at 2 weeks after nerve injury, decreased with time, and never surpassed 7 V in each case. On the basis of results of these preliminary probings, laryngeal pacing was conducted on a dog 15 months after resection of the laryngeal nerve. Adduction of the paralyzed vocal cord for synchrony with the intact cord was achieved by 7 V of electrical stimulation of the thyroarytenoid muscle that was triggered by signals from the cricothyroid muscle.
KEY WORDS - electrical laryngeal pacing, muscle atrophy, recurrent laryngeal nerve paralysis.
INTRODUCTION
study. Under Nembutal sodium intravenous anesthesia, unilateral recurrent laryngeal nerves were exposed through a midline neck incision and damaged by crushing, dissection followed by resuturing, or a 3-cm neurectomy. The thyroarytenoid muscles of the damaged side of these dogs were subjected to electrical stimulation immediately and 1, 2, 4, 8, and 12 weeks after the injury. The optimal threshold level that gave adequate adduction of paralyzed cords was measured at each point of time.
Unilateral vocal cord paralysis leads to various degrees of hoarseness or swallowing difficulty. To eliminate these symptoms, the glottal gap caused by the adductive dysfunction of the paralyzed cord should be corrected. Currently, cordal injection or various thyroplasties have been applied generally with good results. As compared with these static treatments, remobilization of the paralyzed cord is more physiologic in nature. Although many attempts to restore dynamic function of the paralyzed vocal cord using a nerve-to-nerve anastomosis':" or neuromuscular transplantation technique':" have been reported, they have failed in wide clinical applications.
As shown in Fig 1, each dog exhibited enough vocal cord adduction immediately after the injury even with 3 V of stimulation. However, the threshold level was raised to 7 to 10 V 2 weeks after the injury and declined slowly thereafter. The threshold decline was the slightest in the dog with nerve resection: to a threshold of 7 V.
As a new approach to remobilizing the paralyzed cord, the authors reported an electrical laryngeal pacing system that was triggered by a signal from the cricothyroid muscle." Acute phase experiments revealed fair adduction of the paralyzed vocal cord, which synchronized with the movement of the intact cord during phonation. However, several problems must be solved for the final aim, clinical application of laryngeal pacing, to be fulfilled. The most serious problem seems to be muscle atrophy after denervation. This research was designed to examine the reactivity of atrophic muscle to electrical stimulation. In addition, the availability of muscle contraction in response to laryngeal pacing after prolonged denervation was also studied in canine vocal cords denervated 15 months prior to the study.
Experiment 2. Long-term observation was further performed in three dogs with 3-cm resection of the recurrent laryngeal nerves. The thyroarytenoid Volts - - resection ----- suture _._.- compression
15 10 5
OL..-----.L-----..L-----..a.-5
METHOD AND RESULTS
10
15 Weeks
Fig 1. Stimulation voltage for optimal adduction in various types of recurrent laryngeal nerve injuries.
Experiment 1. Three adult dogs were used in the
From the Departments of Otolaryngology (Kojima, Omori, Nonomura, Honjo) and Plastic Surgery (Isshiki) and the Research Center for Biomedical Engineering (Shimizu), Kyoto University, Kyoto, Japan. Presented at the meeting of the American Laryngological Association, Palm Beach, F1orida, April 28~29, 1990. REPRINTS - Hisayoshi Kojima, MD, Dept of Otolaryngology, Kyoto University, Sakyo-ku, Kyoto 606, Japan.
15
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
Kojima et al, Electrical Pacing of Larqnx
16
nation and during respiration was used for setting the threshold. The waveform of the electrical stimulation used was monophasic and rectangular, with a frequency of 50 Hz, a duration of 5 milliseconds, and a voltage of 7 V (Fig 2). In addition, the larynx after the laryngeal pacing experiment was submitted to histologic examination (Fig 3).
LARYNX paralyzed side
intact side
In contrast to the intact side, muscle atrophy of the paralyzed side was obvious. This experiment, which was designed to examine the availability of laryngeal pacing in such severely atrophic muscle, revealed that remobilization of the paralyzed cord in synchrony with the intact cord was possible even 15 months after denervation.
Fig 2. Block diagram of pacing system.
muscle of each dog was subjected to electrical stimulation IO, 14, or 15 months after the injury. The optimal threshold level that gave enough adduction of the paralyzed vocal cord was examined. In each case it exhibited enough adduction with 7 V of stimulation. Experiment 3. The possibility of laryngeal pacing was examined in the dog used in experiment 2 whose thyroarytenoid muscle had been denervated for 15 months. Under Nembutal anesthesia, the larynx was exposed and a stimulation electrode was inserted into the thyroarytenoid muscle of the paralyzed side through the thyroid cartilage. To attain the trigger signal that synchronized with phonation, a wire electrode was set in the cricothyroid muscle of the intact side. After integration of the electrical discharge from the cricothyroid muscle, the difference in the level of the signal during pho-
One cycle of adduction-abduction during electrical pacing is shown in Fig 4. The paralyzed side is on the left. Slight asynchrony was noted between the two cords. Although the intact cord has apparently started adducting already, the paralyzed one appears not yet to be initiating any movement in Fig 4, part 2. In Fig 4, part 3, adduction of the paralyzed cord is observed and complete closure is obtained. On glottal opening, the paralyzed side also lagged behind the intact one. DISCUSSION
Although a number of research and clinical attempts that aim at remobilizing the paralyzed vocal cord have been proposed, the methods of nerve-tonerve anastomosis and neuromuscular transplantation are still far from clinical application. On the other hand, electrical stimulation has recently been used to treat muscle palsy, 6 and it is being experimentally applied in the larynx. 1.8 We previously reported" on the electrical pacing of vocal cord adduction triggered by electrical discharge from the cricothyroid muscle, with some
Fig 3. Histologic findings of thyroarytenoid muscle. A) At 15 months after denervation, distinct muscle atrophy is observed. B) Intact side.
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
Kojima et al, Electrical Pacing oj Larynx
17
Fig 4. One cycle of adduction and abduction during electrical pacing.
promising results in the acute experiment. This procedure, however, involves several unsolved problems concerning, for example, miniaturization of the tools, biocompatible material for long-term implantation, and muscle atrophy after denervation. Among these problems, here discussed are atrophic muscle after denervation and its reactivity to electrical stirn ulation. According to Sate's" report, the level of stimulation voltage for the maximum contraction of the thyroarytenoid muscle reached the maximum in 2 or 3 weeks after the denervation, and it would be 30 V. Such a high stimulation voltage could be painful, making it impossible to apply the laryngeal pacing. Even if it were possible, such stimulation would cause a leak of electrical current into the trigger electrode placed in the intact cricothyroid muscle, thereby disrupting the synchrony between the two vocal cords. We investigated the threshold voltage of stimulation to induce enough glottic closure under various conditions of nerve palsy. The results were almost in agreement with Sato's, with the threshold level reaching the maximum at 2 weeks after nerve injury. However, the level decreased with time, and it never sur-
passed 7 V even in the worst case of nerve resection. In order to reveal the stimulation voltage required for long-denervated atrophic muscle, laryngeal pacing was conducted on a dog 15 months after resection of the recurrent laryngeal nerve. Adduction of the paralyzed cord for phonation in synchrony with the intact cord was induced by 7 V stimulation. Concerning the time lag between the two cords, we observed that the stimulated vocal cord lagged slightly behind the intact one, as we had reported previously in the acute-phase experiment. This time lag may be attributable to the integrating time of the action potential of the cricothyroid muscle in the closing phase, and to the passive glottic movement in the opening phase. Muscle atrophy in the chronic-phase experiment seemed to have no effect on this time lag. Taking into consideration the ability of continuous electrical stimulation to prevent muscle atrophy as reported by Lomo and Rosenthal.!" Westgaard;!' and Pachter et al ;" we can conclude that the result of this chronic experiment would indicate laryngeal pacing as being one of the potential treatments for unilateral vocal cord paralysis.
REFERENCES 1. Dedo HH. Electromyographic and visual evaluation of recurrent laryngeal nerve anastomosis in dogs. Ann Otol Rhinol LaryngolI971;80:664-8.
5. Kojima H, Omori K, Shoji K, et al. Laryngeal pacing in unilateral vocal cord paralysis. Arch Otolaryngol Head Neck Surg 1990;116:74-8.
2. Sato F, Ogura JH. Neurorraphy of the recurrent laryngeal nerve. Laryngoscope 1978;88:1034-41. 3. Tucker HM, Harvey J, Ogura JH. Vocal cord remobilization in the canine larynx. Arch OtolaryngoI1970;92:530-3.
6. Liberson WT, Holmquest HJ, Scott D, Dow M. Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase on the gait of hemiplegic patients. Arch Phys Med Rehabil 1961;42:101-5.
4. Sato F, Ogura JH. Functional restoration for recurrent laryngeal nerve paralysis. An experimental study. Laryngoscope 1978;88:855-77.
7. Broniatowski M, Ilyes LA, Jacobs GB, Nose Y, Tucker HM. Artificial reflex arc: a potential solution for chronic aspiration. II. A canine study based on a laryngeal prosthesis. Laryngo-
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
18
Kojima et al, Electrical Pacing of Larynx
scope 1988;98:235-7.
activity in the rat. J Physiol (Lond) 1972;221:493-513.
8. Kim GR, Kim KM, Choi HS. Magnetic control for the vocal cord adduction in the canine. Auris Nasus Larynx 1989;16: 65-70.
11. Westgaard RH. Influence of activity on the passive electrical properties of denervation soleus muscle fibers in the rat. J Physiol (Lond) 1975;251:683-97.
9. Sato I. Function of the intrinsic laryngeal muscles after regeneration of the recurrent laryngeal nerve. J Otolaryngol Jpn 1974;77:444-52. 10. Lomo T, Rosenthal J. Control of ACh sensitivity by muscle
12. Pachter BR, Eberstein A, Goodgold J. Electrical stimulation effect on denervated skeletal myofibers in rats: a light and electron microscopic study. Arch Phys Moo Rehabil 1972;63: 427-30.
INTERNATIONAL HEARING AID CONFERENCE: SIGNAL PROCESSING, FITTING, & EFFICACY The International Hearing Aid Conference: Signal Processing, Fitting, & Efficacy will be held June 21-23, 1991, at The University of Iowa, Iowa City, Iowa. The organizing committee includes Richard S. Tyler, PhD (Signal Processing), Chaslav V. Pavlovic, PhD (Fitting), and Ruth A. Bentler, PhD (Efficacy). Further information may he obtained from any member of the organizing committee at the Department of Speech Pathology and Audiology, The University of Iowa, Iowa City, IA 52242; (319) 335-8726, FAX (319) 335-8851.
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
ELECTRICAL PACING FOR DYNAMIC TREATMENT OF UNILATERAL VOCAL CORD PARALYSIS EXPERIMENT IN LONG-DENERVATED MUSCLE HISAYOSHI KOJIMA, MD IWAO
HONIO,
MD
KOICHI OMORI, MD
MITSUHARU NONOMURA, MD
NOBUHIKO ISSHIKI, MD
YASUHIKO SHIMIZU, MD
KYOTO, JAPAN
In order to explore the possibility of clinical application of laryngeal pacing as a treatment for unilateral vocal cord paralysis, we examined the reactivity of atrophic muscle to electrical stimulation in dogs whose recurrent laryngeal nerves were damaged by crushing, dissection followed by resuturing, or a 3-cm neurectomy. The threshold level to induce enough vocal cord adduction reached the maximum at 2 weeks after nerve injury, decreased with time, and never surpassed 7 V in each case. On the basis of results of these preliminary probings, laryngeal pacing was conducted on a dog 15 months after resection of the laryngeal nerve. Adduction of the paralyzed vocal cord for synchrony with the intact cord was achieved by 7 V of electrical stimulation of the thyroarytenoid muscle that was triggered by signals from the cricothyroid muscle.
KEY WORDS - electrical laryngeal pacing, muscle atrophy, recurrent laryngeal nerve paralysis.
INTRODUCTION
study. Under Nembutal sodium intravenous anesthesia, unilateral recurrent laryngeal nerves were exposed through a midline neck incision and damaged by crushing, dissection followed by resuturing, or a 3-cm neurectomy. The thyroarytenoid muscles of the damaged side of these dogs were subjected to electrical stimulation immediately and 1, 2, 4, 8, and 12 weeks after the injury. The optimal threshold level that gave adequate adduction of paralyzed cords was measured at each point of time.
Unilateral vocal cord paralysis leads to various degrees of hoarseness or swallowing difficulty. To eliminate these symptoms, the glottal gap caused by the adductive dysfunction of the paralyzed cord should be corrected. Currently, cordal injection or various thyroplasties have been applied generally with good results. As compared with these static treatments, remobilization of the paralyzed cord is more physiologic in nature. Although many attempts to restore dynamic function of the paralyzed vocal cord using a nerve-to-nerve anastomosis':" or neuromuscular transplantation technique':" have been reported, they have failed in wide clinical applications.
As shown in Fig 1, each dog exhibited enough vocal cord adduction immediately after the injury even with 3 V of stimulation. However, the threshold level was raised to 7 to 10 V 2 weeks after the injury and declined slowly thereafter. The threshold decline was the slightest in the dog with nerve resection: to a threshold of 7 V.
As a new approach to remobilizing the paralyzed cord, the authors reported an electrical laryngeal pacing system that was triggered by a signal from the cricothyroid muscle." Acute phase experiments revealed fair adduction of the paralyzed vocal cord, which synchronized with the movement of the intact cord during phonation. However, several problems must be solved for the final aim, clinical application of laryngeal pacing, to be fulfilled. The most serious problem seems to be muscle atrophy after denervation. This research was designed to examine the reactivity of atrophic muscle to electrical stimulation. In addition, the availability of muscle contraction in response to laryngeal pacing after prolonged denervation was also studied in canine vocal cords denervated 15 months prior to the study.
Experiment 2. Long-term observation was further performed in three dogs with 3-cm resection of the recurrent laryngeal nerves. The thyroarytenoid Volts - - resection ----- suture _._.- compression
15 10 5
OL..-----.L-----..L-----..a.-5
METHOD AND RESULTS
10
15 Weeks
Fig 1. Stimulation voltage for optimal adduction in various types of recurrent laryngeal nerve injuries.
Experiment 1. Three adult dogs were used in the
From the Departments of Otolaryngology (Kojima, Omori, Nonomura, Honjo) and Plastic Surgery (Isshiki) and the Research Center for Biomedical Engineering (Shimizu), Kyoto University, Kyoto, Japan. Presented at the meeting of the American Laryngological Association, Palm Beach, F1orida, April 28~29, 1990. REPRINTS - Hisayoshi Kojima, MD, Dept of Otolaryngology, Kyoto University, Sakyo-ku, Kyoto 606, Japan.
15
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
Kojima et al, Electrical Pacing of Larqnx
16
nation and during respiration was used for setting the threshold. The waveform of the electrical stimulation used was monophasic and rectangular, with a frequency of 50 Hz, a duration of 5 milliseconds, and a voltage of 7 V (Fig 2). In addition, the larynx after the laryngeal pacing experiment was submitted to histologic examination (Fig 3).
LARYNX paralyzed side
intact side
In contrast to the intact side, muscle atrophy of the paralyzed side was obvious. This experiment, which was designed to examine the availability of laryngeal pacing in such severely atrophic muscle, revealed that remobilization of the paralyzed cord in synchrony with the intact cord was possible even 15 months after denervation.
Fig 2. Block diagram of pacing system.
muscle of each dog was subjected to electrical stimulation IO, 14, or 15 months after the injury. The optimal threshold level that gave enough adduction of the paralyzed vocal cord was examined. In each case it exhibited enough adduction with 7 V of stimulation. Experiment 3. The possibility of laryngeal pacing was examined in the dog used in experiment 2 whose thyroarytenoid muscle had been denervated for 15 months. Under Nembutal anesthesia, the larynx was exposed and a stimulation electrode was inserted into the thyroarytenoid muscle of the paralyzed side through the thyroid cartilage. To attain the trigger signal that synchronized with phonation, a wire electrode was set in the cricothyroid muscle of the intact side. After integration of the electrical discharge from the cricothyroid muscle, the difference in the level of the signal during pho-
One cycle of adduction-abduction during electrical pacing is shown in Fig 4. The paralyzed side is on the left. Slight asynchrony was noted between the two cords. Although the intact cord has apparently started adducting already, the paralyzed one appears not yet to be initiating any movement in Fig 4, part 2. In Fig 4, part 3, adduction of the paralyzed cord is observed and complete closure is obtained. On glottal opening, the paralyzed side also lagged behind the intact one. DISCUSSION
Although a number of research and clinical attempts that aim at remobilizing the paralyzed vocal cord have been proposed, the methods of nerve-tonerve anastomosis and neuromuscular transplantation are still far from clinical application. On the other hand, electrical stimulation has recently been used to treat muscle palsy, 6 and it is being experimentally applied in the larynx. 1.8 We previously reported" on the electrical pacing of vocal cord adduction triggered by electrical discharge from the cricothyroid muscle, with some
Fig 3. Histologic findings of thyroarytenoid muscle. A) At 15 months after denervation, distinct muscle atrophy is observed. B) Intact side.
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
Kojima et al, Electrical Pacing oj Larynx
17
Fig 4. One cycle of adduction and abduction during electrical pacing.
promising results in the acute experiment. This procedure, however, involves several unsolved problems concerning, for example, miniaturization of the tools, biocompatible material for long-term implantation, and muscle atrophy after denervation. Among these problems, here discussed are atrophic muscle after denervation and its reactivity to electrical stirn ulation. According to Sate's" report, the level of stimulation voltage for the maximum contraction of the thyroarytenoid muscle reached the maximum in 2 or 3 weeks after the denervation, and it would be 30 V. Such a high stimulation voltage could be painful, making it impossible to apply the laryngeal pacing. Even if it were possible, such stimulation would cause a leak of electrical current into the trigger electrode placed in the intact cricothyroid muscle, thereby disrupting the synchrony between the two vocal cords. We investigated the threshold voltage of stimulation to induce enough glottic closure under various conditions of nerve palsy. The results were almost in agreement with Sato's, with the threshold level reaching the maximum at 2 weeks after nerve injury. However, the level decreased with time, and it never sur-
passed 7 V even in the worst case of nerve resection. In order to reveal the stimulation voltage required for long-denervated atrophic muscle, laryngeal pacing was conducted on a dog 15 months after resection of the recurrent laryngeal nerve. Adduction of the paralyzed cord for phonation in synchrony with the intact cord was induced by 7 V stimulation. Concerning the time lag between the two cords, we observed that the stimulated vocal cord lagged slightly behind the intact one, as we had reported previously in the acute-phase experiment. This time lag may be attributable to the integrating time of the action potential of the cricothyroid muscle in the closing phase, and to the passive glottic movement in the opening phase. Muscle atrophy in the chronic-phase experiment seemed to have no effect on this time lag. Taking into consideration the ability of continuous electrical stimulation to prevent muscle atrophy as reported by Lomo and Rosenthal.!" Westgaard;!' and Pachter et al ;" we can conclude that the result of this chronic experiment would indicate laryngeal pacing as being one of the potential treatments for unilateral vocal cord paralysis.
REFERENCES 1. Dedo HH. Electromyographic and visual evaluation of recurrent laryngeal nerve anastomosis in dogs. Ann Otol Rhinol LaryngolI971;80:664-8.
5. Kojima H, Omori K, Shoji K, et al. Laryngeal pacing in unilateral vocal cord paralysis. Arch Otolaryngol Head Neck Surg 1990;116:74-8.
2. Sato F, Ogura JH. Neurorraphy of the recurrent laryngeal nerve. Laryngoscope 1978;88:1034-41. 3. Tucker HM, Harvey J, Ogura JH. Vocal cord remobilization in the canine larynx. Arch OtolaryngoI1970;92:530-3.
6. Liberson WT, Holmquest HJ, Scott D, Dow M. Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase on the gait of hemiplegic patients. Arch Phys Med Rehabil 1961;42:101-5.
4. Sato F, Ogura JH. Functional restoration for recurrent laryngeal nerve paralysis. An experimental study. Laryngoscope 1978;88:855-77.
7. Broniatowski M, Ilyes LA, Jacobs GB, Nose Y, Tucker HM. Artificial reflex arc: a potential solution for chronic aspiration. II. A canine study based on a laryngeal prosthesis. Laryngo-
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
18
Kojima et al, Electrical Pacing of Larynx
scope 1988;98:235-7.
activity in the rat. J Physiol (Lond) 1972;221:493-513.
8. Kim GR, Kim KM, Choi HS. Magnetic control for the vocal cord adduction in the canine. Auris Nasus Larynx 1989;16: 65-70.
11. Westgaard RH. Influence of activity on the passive electrical properties of denervation soleus muscle fibers in the rat. J Physiol (Lond) 1975;251:683-97.
9. Sato I. Function of the intrinsic laryngeal muscles after regeneration of the recurrent laryngeal nerve. J Otolaryngol Jpn 1974;77:444-52. 10. Lomo T, Rosenthal J. Control of ACh sensitivity by muscle
12. Pachter BR, Eberstein A, Goodgold J. Electrical stimulation effect on denervated skeletal myofibers in rats: a light and electron microscopic study. Arch Phys Moo Rehabil 1972;63: 427-30.
INTERNATIONAL HEARING AID CONFERENCE: SIGNAL PROCESSING, FITTING, & EFFICACY The International Hearing Aid Conference: Signal Processing, Fitting, & Efficacy will be held June 21-23, 1991, at The University of Iowa, Iowa City, Iowa. The organizing committee includes Richard S. Tyler, PhD (Signal Processing), Chaslav V. Pavlovic, PhD (Fitting), and Ruth A. Bentler, PhD (Efficacy). Further information may he obtained from any member of the organizing committee at the Department of Speech Pathology and Audiology, The University of Iowa, Iowa City, IA 52242; (319) 335-8726, FAX (319) 335-8851.
Downloaded from aor.sagepub.com at OAKLAND UNIV on July 6, 2015
