552527

research-article2014

NNRXXX10.1177/1545968314552527Neurorehabilitation and Neural RepairMcBain et al

Original Research Articles

Electrical Stimulation of Abdominal Muscles to Produce Cough in Spinal Cord Injury: Effect of Stimulus Intensity

Neurorehabilitation and Neural Repair 1­–8 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1545968314552527 nnr.sagepub.com

Rachel A. McBain, PhD1,2, Claire L. Boswell-Ruys, PhD1,2,3, Bonsan B. Lee, MBBS1,2,3, Simon C. Gandevia, MD1,2, and Jane E. Butler, PhD1,2

Abstract Background. Surface electrical stimulation of the abdominal muscles, with electrodes placed in the posterolateral position, combined with a voluntary cough can assist clearance of airway secretions in individuals with high-level spinal cord injury (SCI). Objective. To determine whether an increase in stimulus intensity of the trains of electrical stimuli delivered to the expiratory muscles has an increasing effect on a stimulated voluntary cough and to determine at which stimulus intensity a plateau of cough peak expiratory flow occurs. Methods. In 7 healthy individuals with a SCI at and above C7, gastric pressure (Pga), esophageal pressure (Pes), peak expiratory cough flow (PEFcough), and expiratory volume were measured as participants coughed voluntarily with simultaneous trains of electrical stimuli delivered over the abdominal muscles (50 Hz, 1-s duration). The intensity of the stimulation was increased incrementally. Results: A plateau in PEFcough occurred in all 7 individuals at a mean of 211 ± 29 mA (range 120-360 mA). Peak values reached for Pga, Pes, and PEFcough were 83.0 ± 8.0 cm H2O, 66.1 ± 5.6 cm H2O, and 4.0 ± 0.4 l/s respectively. Conclusions. The plateau in expiratory cough flow that was associated with increasing expiratory pressures is indicative of dynamic airway compression. This suggests that the evoked cough will be effective in creating more turbulent airflow to further assist in dislodging mucus and secretions. Keywords functional electrical stimulation, spinal cord injury, abdominal muscles, stimulated cough

Introduction For people with a cervical or high thoracic spinal cord injury (SCI), paralyzed or weakened abdominal muscles result in a reduced ability to cough effectively.1-3 Their ability to clear airway secretions is reduced, and the risk of atelectasis and pneumonia is increased. Respiratory complications, such as pneumonia, remain a major cause of death in people with SCIs.4-6 Stimulation of the abdominal muscles, timed with a voluntary cough, enhances cough in people with SCI. The abdominal muscles can be stimulated using various methods, including surface electrical,3,7-11 magnetic,12-16 or implanted spinal cord stimulation.17-19 Implanted spinal cord stimulation at combined thoracic and lumbar levels in people with SCI produces the largest expiratory pressures (as high as 200 cm H2O) and flows (up to 10 L/s) in cough from total lung capacity (TLC).17,19 However, large abdominal pressures (66 cm H2O) and expiratory flows (5 L/s) also can be produced in people with SCI by trains of magnetic stimulation over T10 to activate the ventral roots that innervate the abdominal muscles.16

Recently, we have shown that surface electrical stimulation of the abdominal muscles, with electrodes positioned posterolaterally to activate a large number of the intercostal nerves, that innervate the abdominal muscles, can produce large cough pressures (50 - 60 cm H2O) and flows (4 L/s) in SCI.3,8,20 This method is much more effective than surface electrical stimulation with electrodes placed over the anterior abdominal wall.7,10,11,21-23 Surface electrical stimulation is a feasible, accessible, affordable, and portable method to evoke a functional cough. To date, the stimulus intensities that we have used for the posterolateral electrical stimulation in people with SCI have been deliberately limited to those that produce a gastric pressure of 40 cm H2O at functional residual capacity 1

Neuroscience Research Australia, Randwick, NSW, Australia University of New South Wales, Randwick, NSW, Australia 3 Prince of Wales Hospital, Randwick, NSW, Australia 2

Corresponding Author: Jane E. Butler, PhD, Neuroscience Research Australia, Barker Street, Randwick NSW 2031, Sydney, Australia. Email: [email protected]

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Table 1.  Participant Data and Lung Function.a Participant

Age (years)

1 2 3 4 5 6 7 Mean (SEM)

73 60 60 58 57 40 42 56  4

SCI Level

TSI

C4 C C4/C5 A C5 A C5 A C5/C6 A C5/C7 A C6/C7 B

8.1 0.4 42 42.1 32.3 0.4 0.8 18 (7.5)

BMI MEP Respiratory FVC FEV1 FEV1/FVC (kg/m2) (cm H2O) Health FVC (l) (% pred.) FEV1 (l) (% pred.) (%) IC (l) 32.4 24.1 21.6 17.8 34.0 24.8 31.8 26.6 (2.3)

1.5 1.7 0.8 1.3 0 2.0 1.6 1.3 (0.3)

Noneb OSAb OSAb Asthmab OSAb OSAc OSAb

1.4 1.9 1.1 1.5 2.3 0.9 2.1 1.6 (0.2)

32 28 20 36 52 19 48 34 (5)

1.1 1.5 1.1 1.2 1.7 1.5 1.6 1.4 (0.1)

36 30 24 35 49 21 43 34 (4)

81 76 95 81 73 72 73 79 (3)

1.1 1.5 1.0 1.4 1.8 2.0 2.1 1.6 (0.2)

Abbreviations: SCI, spinal cord injury; TSI, time since injury; BMI, body mass index; MEP, maximal expiratory pressure; FVC, forced vital capacity; % pred, % predicted; FEV1, forced expiratory volume in 1 s; IC, inspiratory capacity; OSA, obstructive sleep apnea; SEM, standard error of the mean. a Individual patient data showing, age (years), SCI level (including American Spinal Injury Association classification), TSI (years), BMI, MEP (measured at total lung capacity from increase in mouth pressure above baseline at rest), respiratory health, FVC, FVC (% pred.), FEV1, FEV1 (% pred.), and IC. Only 1 patient had preexisting lung disease (asthma); 5 had OSA. b Ex-smoker. c Current smoker.

(FRC).3,8,24 The mean intensity used to do this was ~125 mA.3 This intensity is about a third of that which produces a maximal twitch pressure and is estimated to produce a twitch pressure of ~30% maximal twitch pressure. Therefore, there is potential to further enhance cough by increasing the stimulus intensity for the trains of stimuli applied during voluntary cough. Therefore, the current study aimed to examine the effect of increases in stimulus intensity on the expiratory pressures, flow, and expiratory volume during stimulated coughs in individuals with cervical SCI. We hypothesized that as stimulus intensity increased, expiratory pressures and flow would also increase and that peak expiratory flow would eventually plateau.

Methods A total of 7 healthy male patients with a SCI and motor impairment at and above C7 were studied. Clinical assessment of their neurological impairment was assessed in accordance with the American Spinal Injury Association25; see Table 1. Participants were screened to check that they could tolerate the stimulation. All patients had a reduced cough (assessed by their unstimulated voluntary cough) and impaired lung function (Table 1). All procedures were approved by the University of New South Wales and the South Eastern Sydney Illawarra Area Health Service Human Research Ethics Committees and conformed with the Declaration of Helsinki. The experimental setup was similar to that published previously3,8 (see Figure 1). Patients were seated in their wheelchair, and measures of lung function were performed prior to cough testing (Table 1). Patients breathed through a mouthpiece, and air flow was measured using a pediatric

pneumotachometer (model 3813, Hans Rudolph, Kansas City, MO). This signal was integrated online to give volume. A gastroesophageal catheter, mounted with 2 pressure transducers (CTG-2, Gaeltec Ltd, Dunvegan, UK), was inserted via the nose to measure gastric (or abdominal) pressure (Pga) and esophageal (or thoracic) pressure (Pes) through transducers located in the stomach and 20 cm rostral in the esophagus, respectively. Two or 3 sprays of local anesthetic (5% lignocaine hydrochloride) were delivered to the nose and back of the throat before insertion of the catheter. A thin smear of gel (2% lignocaine hydrochloride) was also applied to the tip of the catheter before insertion. In addition, beat-to-beat blood pressure was monitored continuously via a Portapres system (FMS, Finapres Medical Systems BV, Amsterdam, Netherlands) with the pressure cuff around the left middle finger. All signals were digitized (1401 Plus, CED Limited, Cambridge, UK) and stored on computer (sampling rate 2000 Hz).

Stimulation Electrical stimulation was applied through 2 flexible, reusable multistick gel electrodes (10 × 18 cm2, multistick gel electrodes, Axelgaard Manufacturing Co, Ltd, Fallbrook, CA) that were halved (5 × 18 cm2); their corners were rounded, and they were then placed bilaterally over the thoracoabdominal wall, in the posterolateral position optimal for abdominal muscle stimulation3,8,24 (see Figure 1A). Stimulus Trains.  To assess the effect of stimulus on cough, trains of 50-Hz stimuli (1-s duration) were applied bilaterally to tetanically contract abdominal muscles while patients attempted a maximal voluntary cough from near TLC. The

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intensity of the stimulus train applied during voluntary coughs was increased in 40-mA increments. Two maximal coughs were performed at each stimulus intensity, starting from 40 mA, then 80 mA, then 120 mA and so on, up to 1 or 2 increments beyond the point at which peak expiratory flow had reached a plateau (excluding points that were at or below the peak expiratory flow achieved in a cough without stimulation, Figure 1B). The range of highest intensities used across patients was 160 to 480 mA. Stimulated coughs were compared with maximal voluntary coughs without stimulation.

Figure 1.  Experimental setup and protocol. A. Experimental setup showing patient seated in wheelchair, breathing through a mouthpiece attached to a pneumotachometer. A gastroesophageal catheter was positioned such that a pressure transducer located in the stomach measured Pga, and the proximal transducer located in the esophagus measured Pes. Blood pressure was monitored continuously. B. Upper panel shows typical flow trace during a cough (breath in to total lung capacity is also shown). Stimulation was applied at 50 Hz for 1 s during a voluntary cough. Increasing intensities of stimulation up to 240 mA were applied. Stimulation was delivered just prior to the onset of the expulsive phase of cough (timed with verbal cues). C. Raw data from a single patient (C5, American Spinal Injury Association C) depicting 3 voluntary coughs: 1 without (left panel) and 2 with superimposed trains of stimuli (middle and right panels, 50 Hz, 1 s duration, 200 and 360 mA). Expiratory flow, lung volume, abdominal pressure (Pga), and thoracic pressure (Pes) traces are shown. Gray bars and vertical dashed line indicate the onset and duration of the stimulus train. Short horizontal dashed lines on flow traces indicate PEFcough for the unstimulated cough effort. Long horizontal dashed lines indicate zero flow, end-tidal volume, and baseline pressures. With electrical stimulation superimposed on a voluntary cough, there are increases in PEFcough, expiratory volume below endtidal volume, and expiratory pressures (indicated by positive deflections). In B and C, flow returns to zero during the cough when there is glottic closure.

expulsive phase of the cough was timed by verbal cues to occur just after the onset of stimulation (~250 ms).3,8 The

Single Stimuli.  To assess the maximal force production of the abdominal muscles, twitch pressures were evoked with single stimuli delivered through the same posterolaterally placed electrodes at end expiratory volume (an estimate of FRC), so that the inspiratory and expiratory muscles were relaxed at the time of the single stimuli. The single pulses (rectangular, 0.2 ms duration) were delivered bilaterally in pairs (4 s apart) at increasing intensities (from 40 to 700 mA) in either 40- or 50-mA increments and increased until the gastric twitch pressure reached a plateau at its maximum (Figure 2). We defined the maximal Pga twitch as the highest twitch pressure produced (average of the response to 2 stimuli at each intensity) and when a further increase in stimulus intensity did not produce further increases in twitch pressure or produced a decrease in twitch pressure. In 1 patient, we did not increment the intensity beyond 700 mA, at which point, we had reached a plateau in Pes but not Pga.

Analysis Measurements were made during each cough of the Pga, Pes, peak expiratory flow produced in the cough (PEFcough), and the total expiratory volume from near TLC. The expiratory volume below the usual end-expiratory volume was also calculated. For Pga and Pes, the active change in pressure produced by the expiratory muscles was measured from a baseline pressure taken midway between the inspiratory and expiratory pressure swings in the quiet breaths taken prior to the cough. All data were averaged for 2 similar trials at each stimulus-train intensity. Data were compared across stimulus intensities with a repeated-measures 1-way ANOVA with post hoc multiple comparisons versus control (Dunnett’s method), in which the control was taken as a cough with no stimulation. Only data from stimulation trains up to 240 mA were included in the statistical analysis, because only 3 patients were stimulated at higher intensities. The stimulus intensities used in the trains applied during cough (from TLC) were compared with the stimulus intensities required to produce a maximal Pga twitch at rest (at FRC) with a single pulse. Unless indicated, data are shown as mean ± standard error of the mean in the text and

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Results

Figure 2.  Individual recruitment curves of twitch pressures (Pes and Pga) with single electrical stimuli. Recruitment curves of twitch pressures evoked by single stimuli during relaxation at FRC (40- to 50-mA increments) for both Pes (A) and Pga (B) for each of the 7 patients. The filled circles indicate the stimulus intensity at which peak expiratory flow reached a plateau for that patient when trains of stimuli were applied during a voluntary cough, and the open circle indicates the stimulus intensity at which Pes reached a plateau (in only 1 patient). C. Average twitch pressures across patients at each stimulus intensity (Pes, open bars; Pga, filled bars). The black arrow (at left) indicates the mean stimulus intensity at which a plateau of peak expiratory flow occurred across all 7 patients. The gray arrow (at right) indicates mean stimulus intensity to produce the maximal Pga twitch in each patient. Note that after 550 mA, patient numbers decrease to n = 5, 4, and then 3. For 3 patients, the Pga twitch pressure did not reach a plateau by our criteria, but the last increment in stimulus intensity produced only small changes in pressure in 2 patients (by 2.5% and 5.7% above the size of the pressure twitch with the previous stimulus intensity). For the patient who did not reach a plateau, the increase in pressure was 9.0%. However, for each of these 3 patients, the Pes twitch pressure reached a plateau.

figures. A P value of

Electrical stimulation of abdominal muscles to produce cough in spinal cord injury: effect of stimulus intensity.

Surface electrical stimulation of the abdominal muscles, with electrodes placed in the posterolateral position, combined with a voluntary cough can as...
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