Diaphragm and Accessory Respiratory Muscle Stimulation Using Intramuscular Electrodes

Transcription

1 266 Diaphragm and Accessory Respiratory Muscle Stimulation Using Intramuscular Electrodes Robert B. Dunn, PhD, James S. Walter, Phi), John Walsh, AID ABSTRACT. Dunn RB, Walter JS, Walsh J. Diaphragm and accessory respiratory muscle stimulation using intramuscular electrodes. Arch Phys Med Rehabil 1995;76: We tested the hypothesis that electrical stimulation of respiratory muscles can be obtained from intramuscular electrodes. In acute anesthetized dogs, suture-type intramuscular electrodes were placed in each hemidiaphragm and needle electrodes were placed in various intercostal regions of the thorax. During a hyperventilation induced period of apnea a 2-second stimulation was applied to the diaphragm or to the thoracic electrodes, followed by a combined thoracic-diaphragm stimulation period, Thoracic expansion and tidal volumes were measured as indices of inspiratory effort. We found that diaphragm stimulation produced tidal volumes between 104% and 180% of spontaneous breathing. Electrodes in the upper thorax produced chest expansion and when combined with diaphragm stimulation increased tidal volumes (p <.05). We conclude that intramuscular electrodes represent a feasible method for long-term electrogenic ventilation. Also, thoracic support for diaphragm pacing in quadriplegics could produce a more effective long-term system that is less prone to fatigue and failure by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation Upper cervical spinal cord transection produces a loss of respiratory control with management of respiration typically requiring permanent mechanical ventilation.l Recently, phrenic nerve stimulation has been a useful clinical technique to support ventilation in these patients. 2'3 Stimulating electrodes are placed in the neck or thorax adjacent to the phrenic nerve to activate the diaphragm. Although technical improvements have provided for long-term diaphragm stimulation, the lack of coordinated contractions from supporting accessory muscles has severely limited this technique. In most cases tidal volumes are sufficient to maintain a basal state, but there is little reserve. Normally, the enlargement of the chest wall acts synergistically with the downward displacement of the diaphragm to inflate the lungs, and the magnitude of this synergism increases with increasing tidal volumes. 4 In many patients with lower cervical spinal cord injury with spontaneous diaphragm-driven respiration and all those receiving phrenic pacing, the lack of motor input to the intercostals causes an inspiratory collapse of the chest wall. 5 This inward thoracic movement produces poor respiratory mechanics, decreases the efficiency of breathing, and overburdens the diaphragm. Thoracic inspiratory muscles do not lend themselves to the techniques currently applied to stimulate the diaphragm. Small diverse nerves to select intercostal muscles precludes the use of phrenic-type electrodes. However, stimulation is possible from electrodes placed close to the ventral roots in From the Rehabilitation Research and Development Center, VA Hines Hospital; and Department of Medicine, Loyola University Stritch School of Medicine, Maywood, IL. Submitted for publication August 18, Accepted in revised form November 1, Supported by funds from Veterans Administration, Rehabilitation R&D Merit Review (B91-235AP), and the VA Hines Hospital, Rehabilitation R&D Center. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Robert B. Dunn, PhD, Rehabilitation R&D Center (151L), VA Hines Hospital, PO Box 20, Hines, IL by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation /95/ /0 thoracic segments of the spinal cord. 6'7 When spinal stimulation is combined with diaphragm stimulation, tidal volumes are always greater than with diaphragm stimulation alone. The fact that nonrespiratory muscles are also stimulated by this technique coupled with the complex invasive procedures required for electrode placement creates problems for clinical applications. We believe a more feasible and selective approach is to place intramuscular electrodes in intercostal regions adjacent to rib margins. The electrodes would be close to but not in direct contact with the ventral branches of thoracic nerves serving intercostal muscles. Advantages over spinal cord ventral root stimulation include more localized contractions from specific muscle groups and a less invasive implantation procedure. Intramuscular electrodes could also be used to stimulate the diaphragm. Although the newer phrenic electrodes are well designed, placement around the nerve still creates the risk of nerve damage and a thoracotomy is required for their initial placement and subsequent adjustments. An intramuscular diaphragm electrode has many advantages and may be a viable alternative to direct phrenic stimulation. Implantation is simpler, requiring only a small abdominal incision, and direct contact with the phrenic is avoided. Peterson and coworkers 8'9 showed that an intramuscular diaphragm electrode strategically placed is capable of complete muscle activation. This occurred as long as the electrode was within 2cm of the phrenic trunk entering the muscular diaphragm and several designs have undergone animal testing. We have developed a suture-type intramuscular electrode that provides a large surface area along a long segment, is easily inserted, and seems permanent. Our data shows the feasibility of these intramuscular electrodes as an alternative approach to functional electrical stimulation of the diaphragm and their use in localized stimulations of accessory support muscles in the thoracic wall. They may provide a practical, minimally invasive method to stimulate accessory respiratory muscles to support the diaphragm and their use could expand the use of neuroprosthetics for respiratory control and greatly improve its capabilities.

2 RESPIRATORY MUSCLE STIMULATION, Dunn 267 Knoted Wire 4--~ 5.5cm Bare wire ~ 6c m,~f ~ End of insulation bonded with cyanoacry[ate wire Fig l--intramuscular suture electrode. METHODS 21 Gage needle Animal Preparation Eighteen fasted mongrel dogs weighing between 20 and 26kg were anesthetized with an intravenous injection of pentobarbital sodium (30mg/kg). Additional doses were administered, as needed, to maintain a level of anesthesia that supressed the corneal reflex. The trachea was intubated and respiration was maintained with a Harvard ventilator. Treacheal air movement was recorded with a pneumotach a (A. Fleisch) connected to the endotracheal tube. The signal was integrated (Gould) b to give tidal volume. Body temperature was maintained close to 38 degrees C by the use of a heating pad. Pressure in the arch of the aorta was monitored via a polyethylene catheter passed retrograde from the femoral artery, and a catheter in the accompanying femoral vein was used for injection. A low pressure respiratory belt surrounding the chest and connected to a pressure transducer provided changes in thoracic dimensions. Esophageal pressure was monitored from a balloon-tipped catheter placed in the midthoracic region and abdominal pressure was monitored from a similar catheter placed in the abdominal cavity. All pressures were recorded by means of Statham pressure transducers (P23Db) and amplified by Gould preamplifiers. Parameters were displayed on an 8-channel recorder, c Electrodes The intramuscular suture electrode was initially designed to stimulate the phrenic nerve trunks as they entered the diaphragm. Ease of placement, complete phrenic activation without direct contact, and potential for chronic use were the major considerations in electrode design. The electrode (fig 1) was made of multistranded 316 LVM teflon coated stainless steel wire (Cooner). d Fifty-five millimeters of teflon was stripped about 6cm in from the end of the wire and a knot placed at the point between the teflon and bare wire as shown in figure 1. At the other end of the bare wire cyanoacrylate was applied to bond the insulation. The insulated wire tip was slipped into the blunt end of a curved 22-gauge needle and the needle crimped to secure the wire. The electrode can be sutured into the muscle with the knot acting as a stop for the bare wire. The other end can be secured much like a regular suture. This electrode provides a large surface area along its entire noninsulated length within the muscle mass. A suture electrode was placed in each hemidiaphragm through a small incision in the abdominal wall. Because it was not possible to directly observe the phrenic tracts from the abdominal side, specific landmarks were used to direct electrode placement and a test probe was used to find the optimum electrode location. This was usually about 2cm in length and close to the junction between the muscle and central tendon. On the right side it was just lateral to the penetration of the vena cava. Suturing of the electrode was started in the muscle below and continued above the region of activation. In this manner complete activation of the phrenic is possible without direct contact between electrode and nerve. In later experiments the test probe was not necessary and only anatomical landmarks were used. The suture electrode also seems ideal for intercostal muscle stimulation. The electrode can be woven into the superficial muscle between rib margins through a small skin incision. However, in mapping the chest wall for motor stimulation points needle electrodes, because of their simplicity, were used. These consisted of single-stranded stainless steel wire with a small hooked end which projected through a 27-gauge needle, e For intramuscular implantation, the needle containing the electrode was pushed through the skin and into the superficial thoracic muscle layer. The angle of penetration was approximately 30 to prevent overpenetration of the chest wall. Electrical Stimulation Stimulation was conducted using a Master-8 AMPI 8 channel constant current pulse generator, f Stimulations were monopolar with an indifferent positive electrode. Placement of the indifferent electrode varied and in some cases bipolar stimulation was performed and compared to monopolar stimulation. Various combinations of frequency (10 to 40 pps), pulse durations (80 to 150 #s) and current were examined to show optimum parameters. Each stimulation was applied for a 2-second interval. Stimulation of the intercostal muscles and diaphragm was always bilateral and performed during a hyperventilation induced period of apnea. There was a 2 to 5 minute recovery period following each stimulation episode. Because intercostal stimulations were performed close to the myocardium, there was the possibility that current from the stimulating electrodes could induce cardiac arrhythmias. In some cases, to estimate a safety factor the electrocardiogram (EKG) was monitored during a stepwise increase in current at optimum parameters until fusion of adjoining muscle groups occurred. Protocol Following implantation of the suture electrodes in each hemidiaphragm the abdomen was closed and monitored respiratory parameters were evaluated during diaphragm stimulation. Electrodes were then inserted into the thoracic wall as previously described. Placement was made between the 4th and 12th intercostal spaces. Within each interspace electrodes were designated as ventral, lateral, or posterior in position. The major emphasis was to locate motor points producing maximum thoracic movement. Initially, single bilateral pairs were tested for thoracic expansion. Then various combinations were simultaneously stimulated. Finally, diaphragm stimulation alone was compared with combinations of simultaneous thoracic and diaphragm stimulations. In three animals a pair of piezoelectric transducers, 15 to

3 268 RESPIRATORY MUSCLE STIMULATION, Dunn Tracheal Air Flow Spontaneous Respiration INSP ]~ I Dlaphra m Stlmu~n Volume --~ j. ml 400 ] Thoracic = Expansion ~ ~ ~ ] l~-.--- P,ess.roES phsg'a' 4 2w... -~- ~ mm Hg Stlmuictlon Parameters ~ Frequency 25 pps Duration 150 Current t0 ma 2 sec Fig 2--Record of the spontaneous breathing animal on the left is compared with that of diaphragm stimulation during apnic period. 20mm apart, were placed on the abdominal side of the right costal diaphragm in the midaxillary line close to the insertional tendons. The transducers were attached to a sonomicrometer, g Changes in shortening during diaphragm stimulation was expressed as a percentage change from the initial resting length at functional residual capacity. The possibility exists that with direct costal stimulation some of the muscle responses may be caused by reflex activity. To distinguish these from direct respiratory responses to stimulation, paraspinal anesthesia was performed in some trials to inhibit reflexes. Four milliliters of 2% lidocaine with epinephrine was injected adjacent to the spinal cord bilaterally from T 1 to L 1. A decrease in respiratory responses to electrical stimulation caused by anesthesia was attributed to inhibition of the reflex effect. In other animals, reflex activity was determined by stimulating thoracic muscles before and after transsection of the cervical spine. Statistics Statistical comparisons of the many groups were performed by nonparametric statistical methods. Data was first compared using the Kruskal-Wallis analysis of variance, and if significant differences were found, data were then compared using the Wilcoxon rank sum test. Differences were considered significant at the 0.05 level. RESULTS The initial preparations were used to test a number of intramuscular electrode designs, implantation techniques and to find the range of optimum stimulation parameters. After implantation of the suture electrodes monopolar stimulation of both hemidiaphragms was performed at various stimulation parameters. A frequency of 25pps was required for mechanical fusion of the diaphragm. Using parameters listed in figure 2 bilateral diaphragm stimulation produced tidal volumes between 104% and 180% (159 _+ 9.2 SEM, n = 8) of spontaneous breathing. In all cases diaphragm stimulation, without the support of thoracic intercostals, always produced a collapse of the chest wall. The needle electrodes were found to be the most convenient to map the chest wall for stimulation points that produced chest expansion. To minimize the chances for overpenetration of the chest wall, electrodes were inserted within the superficial intercostal muscles. Various combinations of stimulating frequency and duration were found to produce effective muscle contractions. For consistency in mapping the chest wall we settled on the following parameters: frequency 35pps, pulse duration 150#sec, current 10ma. Within each intercostal space, needle electrodes were placed in dorsal (superior), lateral, and ventrolateral (just lateral to the sternum) regions. Electrodes placed in the dorsal region were found to be ineffective in preliminary testing and were abandoned in all further studies. Chest expansion was taken as an index of effort supporting inspiration, but this method is somewhat qualitative when measured with a respiratory belt. Consequently, the response of each test location was scored (table 1) on a sliding scale based on the greatest single response obtained in each animal. The best locations to obtain chest expansion seems to be ventrolateral electrodes in interspaces 3 through 5 and in approximately 60% of the cases a small inspired volume occurred along with expansion. This volume generally did not exceed 50% of the animals spontaneous tidal volume. A comparison of the responses from ventrolateral electrodes in two interspaces is shown in figure 3. Laterally placed electrodes would usually produce results that were qualitatively similar but less in magnitude. Electrodes placed in the lower intercostal spaces consistently showed chest compression usually combined with a small expired volume. Table 2 summarizes the data for the chest ventrolateral electrodes. In some animals monopolar versus bipolar stimulation was compared. Pairs of electrodes within an intercostal space were placed 2 to 3mm apart and then the distance was progressively increased. At constant stimulation parameters chest expansion increased as the distance between the electrode pair increased to approximately lcm. With further separation the response remained constant. It was concluded that monopolar stimulation is more appropriate and occurs after the electrode pair exceeds a separation of lcm. Combined stimulation from two intercostal spaces was also performed. Those sites chosen included the ventrolateral electrodes between intercostal spaces 3 to 6. Our reference was the chest expansion obtained from bilateral stimulation in the third space. The data (table 3) shows that combined stimulations usually produced a greater chest expansion. From the data just presented, the best locations for chest expansion seem to overly the myocardium. The possibility Table 1: Scoring System for Chest Expansion Response (% of Max Chest Expansion) Score (0 to 4)

4 RESPIRATORY MUSCLE STIMULATION, Dunn 269 Tracheal Air Flow Tidal Thoracic Expansion INSP ~ ~ + J 4th interspace ~ i~i~ ~ii: E=ophage., 1 ~, ~ Pressure 4 mm.,. i 6th Interspace SUmulaUon Parametem 2 s~ Fig 3--Shows the response from bilateral electrodes placed ventrolaterally in two intercostal spaces. Stimulation of electrodes in the fourth interspace produced thoracic expansion and an inspired volume 52 % of that obtained during spontaneous breathing. Ventrolateral electrodes placed in the sixth interspace produced less chest expansion and no inspired volume. exists that current spread from these electrodes could adversely affect myocardial electrical activity. To test this, a stepwise increase in current was performed in interspaces 3 to 6 until fusion of several muscle groups was obtained (100pps, lms pulse duration, maximum current 50ma). No abnormalities in the EKG were observed during or immediately after the current increases. In each animal a coordinated contraction of intercostal muscles and the diaphragm was compared with diaphragm stimulation alone. The results of a single experiment with electrodes in the third interspace are shown in figure 4 but similar results were obtained between the third and sixth interspaces. Combining thoracic with diaphragm stimulation produced an expanding chest and increased tidal volumes 28% ( 1.3 SEM, n = 7) over diaphragm stimulation alone. The sonomicrometer data showed that the shortening characteristics of the diaphragm did not change when thoracic was Table 2: Thoracic Electrode Stimulation Table 3: Combined Thoracic Electrode Stimulation Increase in Chest Increase in Tidal Thorax Electrode Location Expansion (%) Volume (%) Frequency 36 pps. 3 and 4 15 ± 1.1 < 10 Duration Current I SO ~. 10ma. 3 and 5 21 _ and 6 18 _ ±.71 The data shows the response to combined activation of intercostal spaces. Data are expressed as percentage of increase (±SEM, n = 5) in chest expansion and tidal volume compared with a single bilateral electrode pair in the third intercostal space. combined with diaphragm stimulation. In either case diaphragm shortening was 39% (_+ 1.2 SEM, n -- 3). In many cases stimulation of two intercostal spaces along with diaphragm stimulation further increased tidal volumes (32% to 38%) but in others very little difference was noted. In animals that received paraspinal lidocane or cervical spinal transsection the responses to stimulation remained intact, thus they were not caused by reflex activity. DISCUSSION Our study shows the feasibility of intramuscular electrodes to stimulate muscles that support inspiration. The suture electrode when woven through the diaphragm consistently provided activation of the muscle and produced inspired volumes in excess of spontaneous ventilation. Also, an intramuscular diaphragm electrode may have advantages over the current clinical technique of using phrenic nerve electrodes, usually implanted in the upper thorax. Despite the recent technical advances contributed by several groups, Thonut Stlmuallon / Tracheal Air INSP ] Tidal VOlUUle ml mtpmaoo Electrode Location (intercostal Space) Score Comment prmm wanh9 1 and _+.14 Minimal chest expansion, usually with some limb movement _+.14 Locations 3 to 5 seem best for chest expansion ± ± _ to 11 0 Associated with chest compression Represent mean data (_+SEM, n = 7) for the ventrolateral thoracic electrodes. Score for chest expansion based on the scheme listed in table 1. Initial experiments testing various electrode designs and stimulation parameters were not included. Esophageal r r 8Umulation Parametem Diaph.rl~lm Thorax Plus Stlmuw,,JOn Diaphragm Thorax Frequency 35 ppi Duration 160 )*ll Current 10 ma! ts01~ ----q -r-- 2 SeC Fig 4--Shows the effect of combining thoracic and diaphragm stimulation. Thoracic stimulation shown on the left represents bilateral stimulation of the third intercostal space. This was accompanied by a small tidal volume and chest expansion. Diaphragm stimulation produced a tidal volume greater than spontaneous breathing but was accompanied by a collapsing chest wall. Thoracic combined with diaphragm stimulation increased tidal volume over diaphragm stimulation alone and was accompanied by an expanding chest wall.

5 270 RESPIRATORY MUSCLE STIMULATION, Dunn potential nerve damage is still an issue with phrenic electrodes. This concern, the great expense involved, and an inconsistent long-term performance of phrenic electrodes has produced only a few patients who depend on phrenic stimulation for continuous ventilatory support. An intramuscular diaphragm electrode, on the other hand, is simpler to implant, and with guidance from a laproscope, requires only a small abdominal incision. More importantly, the electrode does not come in direct contact with the phrenic nerves and thus the chances of permanent nerve injury are reduced to a minimum. Peterson and colleagues 8'9 were the first to report the use of intramuscular electrodes for diaphragm stimulation. They found that if a stimulating electrode was within 2cm of the phrenic trunk entering the diaphragm, full activation of all motor units was produced. However, their wire electrode, anchored by a series of barbes, provided a single-point stimulation so that placement became crucial for complete diaphragm activation. Also, additional electrodes needed to be inserted in case of electrode displacement. A suture electrode, on the other hand, provides a large surface area over a long length. This makes exact placement less crucial and the technique of weaving the electrode through the muscle mass should provide permanence. Even though diaphragm stimulation alone can provide adequate tidal volumes to maintain a basal level of activity, the lack of a significant reserve makes long-term support unreliable. Also, electrical stimulation of nerves is inefficient and more fatiguing than natural stimulation where sequential activation of different motor units enhances muscle endurance and protects it from fatigue. Any partial muscle fatigue or system failure becomes threatening and supplementary assistance must be available. At low respiratory rates (10 to 15 breathes per minute) diaphragm stimulation provided tidal volumes between 140% and 180% of spontaneous levels. This is similar to that reported by Peterson 8'9 for intramuscular diaphragm stimulation. The lack of support from accessory muscles of inspiration and the paradoxical collapse of the chest wall most likely combined to limit the effectiveness of the diaphragm under these conditions. Peterson 8 estimated that the collapse of the chest wall alone accounted for 14% to 33% of the volume displaced by the diaphragm. Our study further shows that intramuscular electrodes are capable of stimulating thoracic muscles that support inspiration. Upper thoracic intercostals and parasternal muscles shorten during inspiration and are now considered true agonists of inspiration, 7'1 whereas those of the lower chest seem to collapse the thorax and support expiration. 11 This is consistent with our findings. Upper thoracic electrodes produced chest expansion, whereas electrodes in the lower intercostal regions compressed the chest and produced a slight expired volume. Stimulation of the upper thoracic muscles can also be produced from an electrode placed on the ventral surface of the spinal cord. 6'v With the electrode between T2 and T3, stimulation produced strong upper thoracic contractions and a significant tidal volume. However, along with inspiratory agonists additional muscle groups unrelated to inspiration were stimulated. Also, current spread from the electrode activated phrenic motor rootlets in cervical segments. This lack of specificity may create problems with clinical application. Thoracic intramuscular electrodes seemed to work best in the third to the fifth interspaces and when placed just lateral to the sternum although from this location full activation of all potential inspiratory groups is not possible. This is reflected in the fact that large inspired volumes were not produced by thoracic stimulation alone, even when combining bilateral pairs. But in combination with phrenic stimulation a single bilateral pair of thoracic electrodes was able to reverse the chest wall collapse of phrenic stimulation into an expansion and a 28% increase in tidal volumes. Chest expansion did not compromise diaphragm shortening as equal decreases were recorded with or without thoracic expansion. Thoracic stimulation could also function as an assist in quadriplegics with an intact phrenic system. These individuals tend to show a rapid shallow breathing pattern and thus have a significantly higher dead space ventilation than normal. 12 Under these conditions thoracic stimulation to assist the diaphragm could produce an even greater increase in alveolar ventilation than would occur with a normal breathing pattern. If necessary separate pairs of electrodes could receive alternate stimulation to reduce fatigue problems. This application would recruit a new larger patient pool to benefit from neuroprothetics. Because stimulations in the chest wall are close to the heart, it is expected that some current will spread to the myocardium. This current potentially could produce arrhythmias. In our dog studies we found that no arrhythmias could be induced even when the current was increased up to 50mA. Also it has been reported that thoracic electrodes placed directly over the heart could not induce cardiac arrhythmias, even at excessive currents, provided the stimulus duration was at or below 100#sec. 13'14 This was because of the differences in membrane time constant between motoneurons and cardiac muscle. Thus, in clinical applications, short-duration stimulation of intercostal muscles should eliminate concerns of induced myocardial arrhythmias. Recently, an electrically induced cough has been reported independently by two investigators.15'16 In both cases muscular contractions induced from surface electrodes applied to the abdominal wall created sufficiently high expiratory flow rates to assist the expulsion of airway secretions. Implant systems should be equally effective and do not suffer from the limitations imposed by current spread to the myocardium. In summary, we have shown that intramuscular electrodes are not only capable of phrenic stimulation but can produce local inspiratory support from thoracic muscles. Thoracic support for diaphragm-driven respiration should provide a more effective capable system in which over the long-term is less prone to fatigue and failure. References 1. Yernault JC. Mechanical assistance in chronic respiratory insufficiency due to neuromuscular disease. Bull Eur Physiopathol Respir 1984; 20: Glenn WL, Phelps ML. Diaphragm pacing by electrical stimulation of the phrenic nerve. Neurosurgery 1985; 17: Glenn WL, Phelps ML, Elefteriades JA, Dentz B, Hogen JF. Twenty

6 RESPIRATORY MUSCLE STIMULATION, Dunn 271 years of experience in phrenic nerve stimulation to pace the diaphragm. PACE 1986;9: DiMarco AF, Supinski GS, Budzinska K. Inspiratorymuscle interaction in the generation of changes in airway pressure. J Appl Physiol 1989; 66: Danon J, Druz WS, Goldberg NB, Sharp JT. Function of the isolated paced diaphragm and the cervical accessory muscl g in the C1 quadriplegic. Am Rev Respir Dis 1979; 119: DiMarco AF, Altose MD, Cropp A, Durand D. Activation of the inspiratory intercostal muscles by electrical stimulation of the spinal cord. Am Rev Respir Dis 1987; 136: Budzinska K, Supinski G, DiMarco AF. Inspiratory action of separate external and parasternal intercostal muscle contraction. J Appl Physiol 1989;67: Peterson DK, Nochomovitz M, DiMarco AF, Mortimer JT. Intramuscular electrical activation of the phrenic nerve. IEEE Trans Biomed Eng 1986;33: Peterson DK, Stellato T, Nochomovitz ML, DiMarco AF. Electrical activation of respiratory muscles by methods other than phrenic nerve cuff electrodes. PACE 1989; 12: DeTroyer A, Kelly S, Macklem PT, Zin WA. Mechanics of intercostal space and actions of external and internal intercostal muscles. J Clin Invest 1985;75: DeTroyer A, Ninane V. Respiratory function of intercostal muscles in supine dog: an electromyographic study. J Appl Physiol 1986; 60: Loveridge BM, Dubo HI. Breathing pattern in chronic quadriplegia. Arch Phys Med Rehabil 1990;71: Riscili CE, Foster KS, Voorhees WD, Bourland JD, Geddes LA. Electroventilation in the baboon. Am J Emerg Med 1988;6: Voorhees CR, Voorhees WD, Geddes LA, Bourland JD, Hinds M. The chronaxie for myocardium and motor nerve in the dog with chestsurface electrodes. IEEE Trans Biomed Eng 1992;39: Linder SH. Functional electrical stimulation to enhance cough in quadriplegia. Chest 1993; 103: Jaeger RJ, Turba RM, Yarkony GM, Roth EJ. Cough in spinal cord injured patients: comparison of three methods to produce cough. Arch Phys Med Rehabil 1993;74: Suppliers a. Fleisch pneumotachograph, OEM Medical Inc., 8741 Landmark Rd, PO Box 27604, Richmond, VA b. Gould Inc., 8333 Rockside Rd, Valley View, OH c. Astro-Med Incorporated, Astro-Med Industrial Park, West Warwick, RI d. Cooner Wire, 9186 Independence, Chatsworth, CA e. Life Tech Incorporated, Kinghurst, Houston, TX f. A.M.P.I., 123 Uziel Street, PO Box 16477, Jerusalem 91163, Israel. g. model 120, Triton Technology, Inc., PO Box 99185, San Diego, CA