Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 5 , Pages 717-725, May 2009

Lower Thoracic Spinal Cord Stimulation to Restore Cough in Patients With Spinal Cord Injury: Results of a National Institutes of Health–Sponsored Clinical Trial. Part I: Methodology and Effectiveness of Expiratory Muscle Activation

Presented in part to the Congress of Neurological Surgeons, October 7–12, 2006, Chicago, IL; the American Spinal Injury Association, May 30–June 2, 2007, Tampa, FL; the International Spinal Cord Society, June 27–July 1, 2007, Reykjavik, Iceland; the American Paraplegia Society, August 27–29, 2007, Orlando, FL; the American Academy of Physical Medicine and Rehabilitation, September 27–30, 2007, Boston, MA; the American Thoracic Society, May 16–21, 2008, Toronto, ON, Canada; and the American Spinal Injury Association, August 8–11, 2008, Orlando, FL.

  • Anthony F. DiMarco, MD

      Affiliations

    • Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, OH
    • Corresponding Author InformationCorrespondence to Anthony F. DiMarco, MD, MetroHealth Medical Center, Rammelkamp Center for Education and Research, 2500 MetroHealth Dr, Cleveland, OH 44109
    • ,
  • Krzysztof E. Kowalski, PhD

      Affiliations

    • Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, OH
    • ,
  • Robert T. Geertman, MD, PhD

      Affiliations

    • Department of Neurological Surgery, Case Western Reserve University, Cleveland, OH
    • Division of Neurological Surgery, MetroHealth Medical Center, Cleveland, OH
    • ,
  • Dana R. Hromyak, BS

      Affiliations

    • Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, OH

Article Outline

Abstract 

DiMarco AF, Kowalski KE, Geertman RT, Hromyak DR. Lower thoracic spinal cord stimulation to restore cough in patients with spinal cord injury: results of a National Institutes of Health–sponsored clinical trial. Part I: methodology and effectiveness of expiratory muscle activation.

Objective

Evaluation of the capacity of lower thoracic spinal cord stimulation (SCS) to activate the expiratory muscles and generate large airway pressures and high peak airflows characteristic of cough, in subjects with tetraplegia.

Design

Clinical trial.

Setting

Inpatient hospital setting for electrode insertion; outpatient setting for measurement of respiratory pressures; home setting for application of SCS.

Participants

Subjects (N=9; 8 men, 1 woman) with cervical spinal cord injury and weak cough.

Interventions

A fully implantable electrical stimulation system was surgically placed in each subject. Partial hemilaminectomies were made to place single-disk electrodes in the epidural space at the T9, T11, and L1 spinal levels. A radiofrequency receiver was placed in a subcutaneous pocket over the anterior portion of the chest wall. Electrode wires were tunneled subcutaneously and connected to the receiver. Stimulation was applied by activating a small portable external stimulus controller box powered by a rechargeable battery to each electrode lead alone and in combination.

Main Outcome Measures

Peak airflow and airway pressure generation achieved with SCS.

Results

Supramaximal SCS resulted in high peak airflow rates and large airway pressures during stimulation at each electrode lead. Maximum peak airflow rates and airway pressures were achieved with combined stimulation of any 2 leads. At total lung capacity, mean maximum peak airflow rates and airway pressure generation were 8.6±1.8 (mean ± SE) L/s and 137±30 cmH2O (mean ± SE), respectively.

Conclusions

Lower thoracic SCS results in near maximum activation of the expiratory muscles and the generation of high peak airflow rates and positive airway pressures in the range of those observed with maximum cough efforts in healthy persons.

Key Words: Cough, Electric stimulation, Quadriplegia, Rehabilitation, Respiratory muscles, Spinal cord injuries

List of Abbreviations: FRC, functional residual capacity, IC, inspiratory capacity, SCI, spinal cord injury, SCS, spinal cord stimulation, TLC, total lung capacity

 

CERVICAL AND HIGH THORACIC spinal cord injury results in paralysis of the expiratory intercostal and abdominal muscles, the major muscle groups responsible for generating the high positive airway pressures characteristic of a normal cough.1, 2, 3 The ability of patients with SCI to clear airway secretions therefore is markedly impaired, resulting in physical discomfort, inconvenience, and the development of atelectasis and recurrent respiratory tract infections.4, 5, 6, 7, 8 Consequently, these patients are dependent on caregiver assistance for the application of manual suctioning, assisted coughing maneuvers, or other methods of airway management.9, 10, 11, 12 These techniques are generally uncomfortable and cumbersome and often restrict patient mobility. Moreover, despite their use, respiratory tract infections remain a major cause of morbidity and mortality in this patient population.13, 14, 15, 16

In theory, restoration of expiratory muscle function and thereby an effective cough mechanism would improve life quality, enhance mobility, eliminate the need for artificial methods of secretion clearance, and potentially reduce the incidence of respiratory complications in SCI. Because the neuromuscular apparatus below the level of injury is generally intact, the expiratory muscles are amenable to a variety of stimulation techniques.3, 17, 18, 19, 20, 21 Based on previous investigations in animals,18, 22, 23 we hypothesized that lower thoracic SCS would result in the generation of high peak airflow rates and large airway pressures in SCI, characteristic of a normal cough.

In this study, we present the results of a clinical trial in which lower thoracic SCS was applied to activate the expiratory muscles in SCI. By this technique, single-disk electrodes are positioned in the dorsal epidural space at the lower thoracic and upper lumbar spinal levels. In this article, the capacity of this technique to activate the expiratory muscles and generate large positive airway pressures and high peak airflow rates is presented. The stimulus-output relationships and effects of stimulation of different electrode combinations are also described. In a companion article,24 we report the clinical effects of lower thoracic SCS in terms of benefits, risks, and side effects. Preliminary results of this technique were described previously in a case report.25

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Methods 

This investigation was approved by the Institutional Review Board, the National Institute of Neurological Disorders and Stroke, and the Food and Drug Administration. Informed consent was obtained from each subject before enrollment in the study.

All research subjects had some form of traumatic injury to the cervical spinal cord and were in stable condition at the time of study entrance. None of the subjects had significant lung, cardiac, or brain disease, which represent exclusion criteria. Among the inclusion criteria for study subjects were objective evidence of expiratory muscle weakness and symptoms of an inadequate cough. Each subject had significant paresis of their expiratory muscles as evidenced by markedly reduced peak expiratory airflow rates and maximum expiratory pressures less than 2.5 L/s and 30 cmH2O, respectively, measured at TLC. In addition, all subjects complained of difficulty coughing and mobilizing secretions.

Electrical Stimulation System 

In a single procedure, a fully implantable electrical stimulation system was surgically placed in each subject to activate the expiratory muscles. Each subject underwent partial hemilaminotomies to place three, 4-mm single-lead, platinum-iridium disk electrodesa at the T9, T11, and L1 spinal levels (fig 1). Electrodes were positioned in the midline in the epidural space overlying the thecal sac using fluoroscopic guidance. A single-disk, ground electrode (30mm) was placed under the surface of the thoracolumbar fascia. A radiofrequency receiver (7.6×4.6×0.85cm; 12g)b was placed in a subcutaneous pocket over the anterior portion of the chest wall, over either the lower rib cage or the upper abdominal wall. The electrode wires were tunneled subcutaneously and connected to the receiver. During electrical stimulation applied in the operating room, contraction of the expiratory muscles was confirmed by visual inspection and palpation of the chest wall.

Postoperatively, stimulation was applied by activating a small portable external control box (9.5×6×2.5cm) connected to a rubberized transmitter, which was secured to the skin with tape directly over the implanted receiver. The stimulus controller box, which is powered by a rechargeable battery, delivers a radiofrequency signal to the implanted receiver, which is converted to an electrical signal that is transmitted to the electrodes (see fig 1). The stimulator provides a biphasic stimulus over a wide range of stimulus amplitudes (10–40V), stimulus frequencies (2–105Hz), and pulse widths (16–800μs). Stimulus on-time could be adjusted between 0.2 and 50s.

Muscle Reconditioning 

Prior to use of the cough system, 2 to 3 weeks were allowed to elapse to provide time for regression of edema and hemorrhage at the electrode and receiver sites and healing of all wounds. It was assumed that the expiratory muscles were significantly atrophied secondary to disuse and would require a period of repeated muscle stimulation to restore strength. After an initial evaluation session, subjects were instructed to apply stimulation every 30 seconds for 5 to 10 minutes, 2 or 3 times a day, in the home or nursing home setting. Stimulus parameters were set at values resulting in near maximal positive airway pressure generation, as tolerated, because high intensity force generation for short periods results in the greatest increases in muscle strength.26, 27, 28 Subjects were also instructed to use the device for evacuation of secretions or pharyngeal clearance, as needed.

Measurements 

Airway pressure was monitored with a pressure transducerc to assess the force of expiratory muscle contraction. Expiratory airflow rates were monitored by use of a heated pneumotachograph.d Measurements were made with use of a tight-fitting full face mask or through tracheostomy tube, when present. Subjects with tracheostomies all had cuffless tubes. Dressings were applied around the tracheostomy, therefore, to minimize air leak. In the seated posture, airway pressure measurements were made under conditions of airway occlusion at FRC and TLC. Cheek pressure was maintained manually during SCS. In a separate maneuver, peak expiratory airflow was measured after release of airway occlusion after peak airway pressure was achieved during SCS. Pressure and flow measurements were recorded on an 8-channel recorder.e During the period of stimulation, subjects were instructed to relax completely. In instances of subject effort, evidence of glottic closure, or obvious mask leakage, data were discarded.

During the initial phase of stimulation, blood pressure, pulse rate, and oxygen saturationf were closely monitored. If absolute blood pressure exceeded 140mmHg systolic or 100mmHg diastolic, stimulation was withheld until values returned to baseline or below 140mmHg systolic and 90mmHg diastolic. Stimulation was then applied at less frequent intervals.

Repeat measurements were made during outpatient visits every 4 to 5 weeks during the first 28 weeks, then at 3-month intervals for 6 months, and then at 6-month intervals. The IC was assessed at each subject visit as an index of resting lung volume.

After 2 to 3 months of daily application of stimulation, the potential for expiratory muscle fatigue was assessed. Airway pressure generation was measured during maximum stimulation, applied every minute for a 30-minute period. A decline in pressure generation of 20% or greater was arbitrarily taken as evidence of muscle fatigue.

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Results 

The specific clinical characteristics of the 9 subjects with SCI are provided in table 1. The interval between the time of injury and study entry ranged between 1 and 34 years. The spontaneous vital capacities of each subject were variably reduced, ranging from 11% to 47% predicted (see table 1).

Table 1. Clinical Data of the Subjects
SubjectSexAge (y)Cause of InjuryLevel of InjuryElapsed Time Since Injury (y)Spontaneous Vital Capacity (L) (% predicted)Maximal Expiratory Pressure (cmH2O) (% predicted)Peak Expiratory Airflow (L/s) (% predicted)
1M52MVAC5/C671.96(39)21(10)2.1(21)
2F28MVAC3220.36(11)16(10)0.7(12)
3M42GSWC4191.22(29)21(10)1.4(16)
4M28SportC4/C522.64(45)26(11)2.2(21)
5M50ViolenceC5/C6122.40(47)24(11)2.0(21)
6M23DivingC4/C510.90(17)24(11)1.8(19)
7M45TrampolineC5/C621.40(23)20(9)2.1(20)
8M49DivingC3/C4341.70(30)22(10)2.0(18)
9M52MVAC3191.70(30)28(13)2.4(23)

Abbreviations: F, female; GSW, gunshot wound; M, male; MVA, motor vehicle accident.

Using maximum stimulus parameters, the effects of lower thoracic SCS at the T9, T11, and L1 spinal levels alone and during combined stimulation at T9+L1, T9+T11, T11+L1 and combined stimulation of all 3 electrodes on airflow rates and airway pressure generation are shown for 1 subject in figure 2. The effects of stimulation at TLC and FRC are shown in panels A and B, respectively. Stimulation at each individual site alone resulted in high peak airflow rates and large airway pressures in the range of 5.8 to 8.6L/s and 120 to 144cmH2O at TLC, respectively. Combined stimulation with any 2 electrodes resulted in substantially greater values in the range of 10.1 to 10.6L/s and 162 to 206cmH2O at TLC, respectively. At total lung capacity, mean maximum peak airflow rates and airway pressure generation were 8.6±1.8L/s and 137±30cmH2O, respectively. Stimulation with 3 electrodes, however, resulted in no significant increases in these parameters. As expected, peak airflow rate and airway pressure generation were smaller at FRC than TLC during single and multisite stimulation. Nonetheless, these values were still substantial. Combined stimulation with 2 electrodes, for example, resulted in peak airflow rates and airway pressures in the range of 6.7 to 7.7L/s and 107 to 134cmH2O.

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  • Fig 2. 

    Effects of lower thoracic SCS for 1 subject on airflow and airway pressure generation during stimulation at the T9, T11, and L1 spinal levels alone and in combinations at TLC (A) and at FRC (B). Large airflow rates and airway pressures were generated during single site stimulation. These parameters were greater with combined stimulation at any 2 sites. Combined stimulation at all 3 sites did not result in further increases in these parameters.

The mean changes in peak airflow rates and airway pressure generation at these same stimulation sites are provided in figure 3. During stimulation at individual spinal levels, the mean changes in peak airflow rates at TLC ranged between 6.1 and 6.9L/s, while the mean airway pressure ranged between 94 and 105cmH2O. While qualitatively similar results were observed during SCS at FRC, the magnitude of peak airflow rates and airway pressures were significantly smaller. During single site stimulation at FRC, mean peak flow rates ranged between 3.6 and 4.5L/s, while mean airway pressure generation ranged between 62 and 75cmH2O (P<.05 compared with each FRC value). There were no significant differences in peak airflow rate or airway pressure generation between individual sites at either FRC or TLC.

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  • Fig 3. 

    Mean peak airflow rates (upper panel) and mean airway pressures (lower panel) during SCS at the T9, T11, and L1 spinal levels alone and in combinations at TLC (solid bars) and at FRC (dotted bars). Mean spontaneous peak expiratory flow rates and airway pressure are shown for comparison (empty bars). Large peak airflow rates and airway pressures of similar magnitude were generated during SCS during single site stimulation. Combined stimulation of 2 sites, however, resulted in significantly greater peak airflow rates and airway pressures (P<.05 for each). There were no significant differences in either peak airflow rates or airway pressure generation between any 2 sites. Combined stimulation of 3 sites did not result in further increases in these parameters.

SCS at 2 sites resulted in significant increases in peak airflow rate and airway pressure generation to 7.8 to 8.8L/s and 124 to 150cmH2O, respectively, at TLC, and to 5.0 to 6.2L/s and 85 to 98cmH2O, respectively, at FRC. These values were significantly greater than those achieved with any single site stimulation alone (P<.05). The effects of SCS at all 3 sites in combination, however, were not significantly different than those achieved with SCS at 2 sites, at either TLC or FRC (P>.05). There were no significant differences between any of the 2 site combinations in terms of peak airflow or airway pressure generation at TLC or FRC.

The relationships between stimulus frequency (10–50Hz) and airway pressure generation (at maximal stimulus amplitude and pulse width of 200μs) at TLC and FRC, expressed as a percentage of control values, are shown in figure 4. With increases in stimulus frequency, there were significant increases in airway pressure generation both during single site stimulation and with a 2-electrode combination. A plateau in pressure generation developed between 40 and 50Hz.

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  • Fig 4. 

    Relationship between stimulus frequency and mean airway pressure generation (expressed as a percent maximum) during single site SCS and combined stimulation of 2 sites at FRC and at TLC. There were progressive increases in airway pressure generation with increases in stimulus frequency. There was a plateau between 40 and 50Hz, because there were only small changes in pressure generation between these stimulus frequencies. There were no significant differences between responses at TLC and FRC.

The relationships between stimulus amplitude (10–40V) and airway pressure generation (stimulus frequency 50Hz and pulse width 200μs) at TLC and FRC, expressed as a percentage of control values, are shown in figure 5. During stimulation at each individual site, there were progressive increases in airway pressure with increasing stimulus amplitude with no apparent plateau in pressure generation. With the 2-electrode combination, there were also progressive increases in pressure generation with increasing stimulus amplitude. However, there were no significant differences between 30 and 40V (P>.05), suggesting the development of a plateau in pressure generation at these amplitude levels.

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  • Fig 5. 

    Relationship between stimulus amplitude and mean airway pressure generation (expressed as a percent maximum) during single site SCS and combined stimulation of 2 sites at FRC and at TLC. There were progressive increases in airway pressure generation with increasing stimulus amplitude. With 2-site stimulation, a plateau developed between 30 and 40V, because there were no significant differences in pressure generation between these amplitude levels (P>.05). There were no significant differences between responses at TLC and FRC.

The relationship between pulse width and airway pressure generation (at 40V and 50Hz) is shown in figure 6. Mean airway pressure generation did not increase with the application of pulse widths exceeding 150μs.

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  • Fig 6. 

    Relationship between pulse width and mean airway pressure generation (expressed as a percent maximum) during combined stimulation at 2 sites at TLC. There was a significant increase in pressure generation between 100 and 150 μs (P<.05). However, there were no further increases in pressure generation with increasing pulse duration as high as 250μs.

Based on these measurements, supramaximal stimulus parameters—that is, stimulus frequency, amplitude and pulse width values above which there were no further significant increases in pressure generation—were determined for each subject. While there was some variation between subjects, supramaximal parameters ranged between 30 and 40V, 30 to 40Hz, with a pulse width of 150 to 200μs.

As shown in figure 7, there was a close relationship between peak airflow and airway pressure generation during supramaximal SCS at TLC and FRC. Airway pressure generation during SCS therefore could be used as a reliable indicator of peak expiratory airflow, a parameter that is often used to assess cough efficacy.

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  • Fig 7. 

    Relationship between airway pressure and peak airflow generation for each subject at FRC and at TLC. There was a highly significant linear relationship between these parameters (P<.01). By this relationship, peak airflow rates could be predicted based on the magnitude of airway pressure generation.

The effects of supramaximal stimulation applied every minute for 30 minutes are shown in figure 8. Pressure generation was maintained at or above control values throughout this period, indicating the absence of significant system fatigue.

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  • Fig 8. 

    Mean changes in airway pressure (expressed as a percent maximum) with 2-site SCS applied every 1 minute over a 30-minute period. There were no significant decrements in airway pressure generation over this period, indicating no evidence of system fatigue during the chronic application of SCS.

Procedurally related complications included mild edema at the receiver site in 5 subjects that generally resolved over several weeks. In 1 subject, revision of the receiver placement was necessary because of skin folds. In 2 other subjects, 1 of the 3 leads was not functional. Because only 2 leads were necessary to achieve maximal pressure development, this failure of 1 lead did not interfere with overall function of the system. No other complications were observed.

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Discussion 

In a previous case report,25 we presented the results of our initial subject with tetraplegia in whom lower thoracic SCS was applied to restore an effective cough mechanism. In this article, additional clinical experience with this technique is provided. Consistent with our previous report,25 the results of this investigation demonstrate that lower thoracic SCS results in the generation of large peak airflow rates and airway pressures, which in several subjects approach values observed during a maximum cough effort in healthy persons.29, 30, 31, 32 While mean maximum pressure generation during SCS (137 cmH2O) was less than the maximum expiratory pressure generating capacity of healthy persons (∼200cmH2O for males and ∼150cmH2O for females),33 this most likely occurred as a result of the reductions in IC in our research subject group. The expiratory muscles are positioned at their greatest length and achieve their greatest force-generating capacity at TLC; expiratory muscle force generation falls progressively with decreases in lung volume.18 Despite the reduced IC, several subjects achieved maximum airway pressure generation in the normal range. Taken together, these data suggest that lower thoracic SCS results in near maximal activation of the expiratory muscles.

The magnitude of peak flow necessary to maintain an effective cough is not clear. However, in patients with Duchenne muscular dystrophy during periods of upper respiratory tract infection and therefore increased secretions, a peak airflow of at least 4.5L/s was necessary to avoid the development of respiratory failure.34 With the exception of 1 subject with kyphoscoliosis, each of our research subjects achieved peak airflow rates above this value with SCS. In fact, the mean peak airflow rate was substantially greater than this value, indicating a significant margin of reserve.

Mechanism of Expiratory Muscle Activation 

In contrast to prior animal studies,22, 23 the magnitude of pressure development was similar at each of the 3 stimulation sites. In dogs, maximum pressure development occurred with dorsal epidural stimulation at the T9 spinal level.18, 22, 23 At the T11 and L1 spinal levels, pressure generation fell to 72% and 40% of the values obtained at the T9 level, respectively.23 The reasons for these differences are not clear but may relate to anatomic differences between species. For example, the human thorax is much more compressed in the anteroposterior dimension, whereas the quadruped thorax is more compressed in the transverse dimension.35, 36 Conceivably, these shape differences may have altered the mechanical advantage of the expiratory muscles or the transmission of intra-abdominal pressure to the airway.

The mechanism of expiratory muscle activation during lower thoracic SCS has been evaluated extensively in animal studies.18, 22, 23, 37 In dogs, epidural dorsal SCS at the T9 spinal level resulted in direct activation of motor roots in the vicinity of the electrode (∼2 segments cephalad and ∼2 segments caudal). In addition, more caudal roots were activated via spinal cord pathways.22, 23 SCS at the T9 level alone, however, resulted in incomplete expiratory muscle activation, as stimulation with a second electrode at the L1 spinal level resulted in significantly greater changes in airway pressure. Stimulation with a third electrode at sites between T9 and T13/L1, however, did not result in any further increases in pressure generation.22, 23 Despite these results in animal studies, a 3-electrode system was implanted at the T9, T11, and L1 spinal levels in our clinical trial because of size differences between species. Like the animal studies, however, a 2-electrode system resulted in similar airway pressures as those generated with a 3-electrode system. While initial results obtained from our first subject25 suggested that the combination of T9 and L1 stimulation resulted in the greatest pressure generation, the group mean data of the present study indicate that any 2-electrode combination resulted in similar airway pressure generation. Consistent with the close correlation between airway pressure generation and peak airflow rates (see fig 6), similar relationships were observed between sites of stimulation and peak airflow rate generation.

Methodologic Concerns 

The accurate measurement of airway pressure and airflow was highly dependent on operator technique and subject cooperation. During data collection, several factors often led to an underestimation of actual airflow and pressure generation. First, given the very high airway pressures resulting from SCS, mask leakage was a frequent occurrence. To obtain accurate results, therefore, technical assistance was required to hold the mask in place and prevent mask displacement. Manual pressure was also applied to the cheeks during SCS. Mask leakage was usually obvious secondary to associated high-pitched sounds; in these instances, SCS was repeated until mask leakage was minimized or eliminated. Second, while subjects were instructed to relax completely and maintain an open glottis during SCS, reflex glottic closure was a frequent occurrence, resulting in inaccurately low airway pressure measurement. Large differences in airflow and pressure generation with similar expiratory muscle activation can also occur as a result of differential narrowing of the glottis. With frequent practice maneuvers and training, however, each of the subjects was able to coordinate the maintenance of glottic opening with SCS.

Because maximum spontaneous airway pressure generation was small relative to pressures generated by SCS, there was much less concern about the potential for overestimation of airway pressure generation. Nonetheless, subjects were instructed to relax completely during SCS, and subjects were carefully observed for any signs of effort.

Comparison With Other Methods of Expiratory Muscle Activation 

Other stimulation techniques have also been proposed to activate the expiratory muscles. These include high-frequency magnetic stimulation20, 21, 38, 39 and surface abdominal muscle stimulation.17, 19, 40, 41

Magnetic stimulation of the expiratory muscles requires placement of a stimulating coil over the back at the T10 spinal level.20, 21, 39 Previous investigations have shown that this method results in the generation of large positive airway pressures in healthy subjects.21, 38 When applied in subjects with tetraplegia, however, airway pressures and airflow rates were not significantly different than those generated during spontaneous maximum expiratory efforts.39 Muscle atrophy may have been responsible, in part, for the generation of smaller airway pressures. The major advantages of magnetic stimulation are that it results in only mild discomfort, activates a large portion of the expiratory muscles, and can be applied noninvasively.21, 39 Limiting clinical application, however, are several significant disadvantages. The device is bulky and expensive and requires an external power source, which is likely to restrict patient mobility. In addition, the device carries some risk of thermal injury because it generates considerable heat at the stimulating coil. Significant adipose tissue may also interfere with expiratory muscle activation because of the greater distance between the stimulating coil and motor roots.

Several investigations have assessed the potential of surface abdominal muscle stimulation to activate the expiratory muscles.17, 19, 40, 41 In previous studies in subjects with tetraplegia in which electrodes were placed over the anterior abdominal wall, stimulation resulted in only modest increases (∼30cmH2O) in maximum expiratory pressure to ∼55 to 60cmH2O.17, 19, 40 Moreover, peak airflow rates with this technique were not significantly different than volitional cough. Importantly, significant abdominal muscle contraction could not be achieved in more than 20% of subjects. In a more recent study in healthy subjects, however, surface electrodes (with much larger surface areas) placed over the posterolateral portion of the abdominal wall resulted in twitch pressures comparable to those achieved with magnetic stimulation.41 While also noninvasive, this method has significant disadvantages. Repeated application of electrodes to the skin surface is likely to be quite tedious and cumbersome and may lead to skin irritation and breakdown, a common problem in patients with SCI. Moreover, the presence of adipose tissue in obese patients may prevent successful application because of the high electrical resistance of fatty tissue.

The SCS technique presented in this study is highly portable and does not require the repeated application and removal of electrodes. Moreover, the degree of expiratory muscle activation should not be affected by the presence of significant adipose tissue. While this method does require an invasive procedure, the surgical technique for electrode placement is standard; SCS has been in clinical use for over 35 years in the treatment of chronic back pain and spasticity.42, 43, 44, 45 Most complications of the procedure relate to equipment failure, which can range as high as 20% to 25%. In this study, 2 of 27 leads were nonfunctional. However, this did not interfere with the function of the system. The incidence of operative complications such as infection and bleeding, however, is quite low.42, 43, 44, 45 While deep infection is rare,42 superficial infections have been observed in 4% to 6% of patients.42, 43, 44, 45 No infections were observed in the present study. Future development of this technique should include the evaluation of wire electrodes that can be implanted much less invasively and may also achieve adequate expiratory muscle activation.

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Conclusions 

In conclusion, lower thoracic SCS results in near maximal activation of the expiratory muscles with the consequent generation of high peak airflow rates and airway pressures, characteristic of a normal cough. Restoration of an effective cough by this method has the potential to facilitate removal of secretions and reduce the incidence of respiratory tract infections and atelectasis and associated morbidity and mortality in subjects with SCI.

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Acknowledgments 

We acknowledge the technical assistance in data analysis of Tomasz Kowalski.

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References 

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  • a Freehand Epimysial Electrode; NeuroControl Corp, 8333 Rockside Rd, Valley View, OH 44125.
  • b Finetech Medical Ltd, 13 Tewin Court, Welwyn Garden City, Hertfordshire, United Kingdom AL7 1AU.
  • c MP45; Validyne Co, 8626 Wilbur Ave, Northridge, CA 91324.
  • d 3700 Series; Hans Rudolph, 7200 Wyandotte, Kansas City, MO 64114.
  • e DASH8; AstroMed Inc, 600 East Greenwich Ave, West Warwick, RI 02893.
  • f N-200; Nellcor, 6135 Gunbarrel Ave, Boulder, CO 80301.

 Supported by the National Institute of Neurological Disorders and Stroke (grant no. R01 NS049516) and the National Center for Research Resources (grant no. M01 RR 00080 and UL1 RR024989). Clinical Trial Registration Number: NCT00116337.

 We certify that we have affiliations with or financial involvement (eg, employment, consultancies, honoraria, stock ownership or options, expert testimony, grants and patents received or pending, royalties) with an organization or entity with a financial interest in, or financial conflict with, the subject matter or materials discussed in the article. Dr. DiMarco is a founder of and has a significant financial interest in Synapse BioMedical, Inc, a manufacturer of diaphragm pacing systems.

 Reprints are not available from the author.

PII: S0003-9993(09)00123-3

doi:10.1016/j.apmr.2008.11.013

Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 5 , Pages 717-725, May 2009

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