New perspectives for chest physical therapy in spinal cord injury - a systematic review

Macedo, Felipe Soares; Paz, Clarissa Cardoso dos Santos Couto; Rocha, Adson Ferreira da; Miosso, Cristiano Jacques; Carvalho, Hellen Batista de; Mateus, Sergio Ricardo Menezes

doi:10.1590/1982-0194201700077

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Systematic Review • Acta Paul Enferm. 30 (5) • Sep-Oct 2017 • https://doi.org/10.1590/1982-0194201700077 copy

New perspectives for chest physical therapy in spinal cord injury - a systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective:

To describe and analyze parameters and effects of surface electrical stimulation on the respiratory muscular function among individuals with spinal cord injuries, especially while coughing.

Methods:

A systematic literature review was developed based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses. The search was conducted in the PubMed, PEDro, and LILACS databases, using the following descriptors: “functional electrical stimulation,” “electrostimulation, electrical stimulation,” “coughing,” “bronchial hygiene,” “quadriplegia,” “spinal cord injury”, “tetraplegia”, and “individual with tetraplegia” - in Spanish, English and Portuguese, with no restrictions on year of publication. Inclusion criteria were: articles describing studies with samples of individuals with spinal cord injuries treated with electrical stimulation and outcomes related to the respiratory system. Articles containing studies with invasive cough stimulation trials were excluded.

Results:

The 12 selected articles revealed the heterogeneity of electrostimulation protocols for expiratory function, which can include frequencies ranging from 30 to 50 Hz; pulse from 25 to 400 μs; applied in up to eight electrodes distributed across the expiratory and accessory muscles. Time of administration also varied, and the current amplitude was usually estimated by the patient's perception, reaching values higher than 100mA.

Conclusion:

Even though the review did not find rigorous parameters for physical therapy using electrical stimulation, because of the shortage and low-quality of the studies that systematically compare stimulation parameters among subgroups, positive changes were observed in the assessed respiratory muscle function variables, such as peak expiratory and cough flow in individuals with cervical and thoracic spinal cord injury.

Keywords
Cough; Physical therapy modalities; Electric stimulation

Study	Sample	Assessed respiratory variables	Electrostimulation parameters	Respiratory function outcomes
Linder S H., (1993)⁽¹⁷17. Linder SH. Functional electrical stimulation to enhance cough in quadriplegia functional electrical stimulation enhance cough in quadriplegia. Chest. 1993; 103(1):166-9.⁾	8 male subjects Classification: traumatic and complete Level: C4 – 5	Variables of pulmonary function and maximum expiratory pressure (MEP) at baseline and electrical stimulation in supine position.	Modality: Functional electrical stimulation (FES) Frequency: 50 Hz Pulse width: 300 μs Pulse duration: 2-3 s Amplitude: 100% Time on/off: - Rise: 0s Wave: asymmetrical biphasic Time: Up to 30 min Electrodes: 4 – 8 electrodes on abdominal wall	MEP increased an average of 33 cm H₂0 when electrostimulation was applied in relation to baseline values. No differences were observed regarding the use of belts and patient position.
Jaeger R J. et al., (1993)⁽¹⁸18. 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; 72(12):1358-61.⁾	14 male and 5 female subjects Classification: complete and incomplete Level: C4 – 7	Baseline, manual, and electrostimulation peak expiratory flow (PEF).	Modality: Electrical stimulation Frequency: 50 Hz Pulse width: 300 μs Pulse duration: 0.75s Amplitude: Up to 110 V Time on/off: - Rise: - Wave: - Time: Up to 30 min. Electrodes: Self-adhesive, round and 7.62 cm in diameter, placed on the abdomen	Electrostimulation significantly increased PEF, reaching a peak of 230 L/min ± 64 L/ min; however, values were lower than those for manually assisted coughing.
Sorli J. et al., (1996)⁽¹⁹19. Sorli J, Kandare F Jaeger RJ, Stanic U. Ventilatory assistance using electrical stimulation of abdominal muscles. IEEE Trans Rehabil Eng. 1996; 4(1):1-6.⁾	1 female subject with SCI Classification: traumatic and complete Level: C6 – 7	Trunk volume (chest and thorax) by optical tracking system, measured in supine position before and during electrostimulation.	Modality: Electrical stimulation Frequency: 50 Hz Pulse width: 25-300 μs Pulse duration: 1s Current amplitude: 20-100 mA Time on/off: - Wave: - Rise: - Time: 2 × 1 min Electrodes: a pair or rectangular electrodes (3 × 8 cm) on the abdomen, along the midline (6 cm above and the second 5 cm below the umbillicus)	Thoracic volume varied with electrostimulation, suggesting increased tidal volume.
Zupan A. et al., (1997)⁽²⁰20. Zupan A, Savrin R, Erjavec T, Kralj A, Karcnik T, Skorjanc T, Benko H, Obreza P. Effects of respiratory muscle training and electrical stimulation of abdominal muscles on respiratory capabilities in tetraplegic patients. Spinal cord. 1997; 35(8):540-5.⁾	11 male and 3 female subjects Classification: complete and incomplete Level: C4 – 7	Forced vital capacity (FVC) and forced expiratory volume in the first second (FEV₁) assessed before and after protocol in sitting and supine position. Electrostimulation associated with muscle training was applied by a physical therapist and by the patient.	Modality: Electrical stimulation Frequency: 50 Hz Pulse width: 300 μs Pulse duration: 0.75 s Voltage amplitude: up to 110 V Time on/off: - Wave: - Rise: - Time: 20 – 30 min. Electrodes: 4 electrodes on the abdomen	Average increase of 19% in VC in sitting position and 17.5% in supine position. Average increase of 20.5% in FEV₁ in sitting position and 16% in supine position. One month post-intervention, the average increase was 9.5% in FCV and 7% in FEV₁.
Cheng et al., (2006)⁽²¹21. Cheng P, Chen C, Wang C, Chung C. Effect of neuromuscular electrical stimulation on cough capacity and pulmonary function in patients with acute cervical cord injury. J Rehabil Med. 2006; 38(1):32-6.⁾	Trial group: 11 male and 2 female subjects Levels: C4 – 7 Classification: complete. Control group: 10 male and 3 female Level: C4 – 7 Classification: complete	Pulmonary function variables measured in supine position before and after (3 weeks, 3 months and 6 months) each protocol (physical therapy protocol vs. physical therapy protocol associated with stimulation).	Modality: Neuromuscular electrical stimulation Frequency: 30 Hz Pulse width: 300 μs Pulse duration: - Current amplitude: 0 – 100 mA Time on/off: 4s/4s Wave: symmetric biphasic wave Rise: 0.5 s Time: 30 min Electrodes: placed on motor points of the clavicular part of the bilateral pectoral and abdominal muscles (3 cm above umbillicus)	Pulmonary function variables, such as vital capacity, forced vital capacity, forced expiratory volume in 1 second and peak flow improved after physical therapy intervention, however, these data were more favorable when physical therapy was associated with electrostimulation. Six months post-intervention, 6 of the 13 individuals in the control group presented pulmonary complications, whereas only one person presented complications in the experimental group. Still in the control group, one subject was submitted to a tracheostomy and invasive ventilation.
Golle et al., (2006)⁽²²22. Gollee H, Hunt KJ, Allan DB, Fraser MH, McLean NA. A control system for automatic electrical stimulation of abdominal muscles to assist respiratory function in tetraplegia. Med Eng Phys. 2006; 29(7):799-80.⁾	3 male and 1 female subjects Level: C4 – 6 Classification: complete	Peak cough flow (PCF) and tidal volume (TV) measured in sitting or supine position, during calm breathing and stimulated cough through electrostimulator controled by an algorithm that identifies respiratory flow.	Modality: Electrical stimulation Frequency: 50 Hz Pulse width: 100 – 400 μs Pulse duration: - Current amplitude: 30-100 mA Time on/off: - Wave: Balanced monophasic Rise: - Time: - Electrodes: 4 on the rectus abdominis, 2 on the transverse abdominal (33 mm × 53 mm rectangular), 2 on the external and 2 on the internal oblique muscles (50 mm round)	Automated electrical stimulation increased CV in 71% and PCF in 54%. The greatest variation of tidal volume was 0.35 L to 0.6 L, and the lowest difference, 0.32 L to 0.35 L, respectively. The highest variation rate of cough was from 2.2 L/s to 3.4 L/s with stimulation.
Spivak et al., (2007)⁽²³23. Spivak E, Keren O, Niv D, Levental J, Steinberg F, Barak D, et al. Electromyographic signal-activated functional electrical stimulation of abdominal muscles: the effect on pulmonary function in patients with tetraplegia. Spinal Cord. 45(7):491-5.⁾	10 male subjects Level: C4 – 7 Classification: complete.	Assessed pulmonary function variables: unassisted, with manual physical therapy, with electrostimulation administered by caregiver, with electrostimulation administered by patient, and stimulation activated by EMG signals measured in supine position.	Modality: Functional electrical stimulation Frequency: 50 Hz Pulse width: 300 μs Pulse duration: - Current amplitude: 0 – 100 mA Time on/off: - Wave: - Rise: - Time: - Electrodes: 4 electrodes on the left and 4 on the right of the abdomen	Peak expiratory flow, forced vital capacity, and maximum voluntary ventilation increased in all interventions, except in self-administered electrostimulation. Manual physical therapy presented the best results when compared to other forms of cough assistance.
Golle et al., (2008)⁽²⁴24. Gollee H, Hunt KJ, Allan DB, Fraser MH, McLean N. Automatic electrical stimulation of abdominal wall muscles increases tidal volume and cough peak flow in tetraplegia. Technol Health Care. 2008; 16(4):273-81.⁾	3 male and 1 female subjects Level: C4 – 6 Classification: complete	Peak cough flow (PCF), tidal volume (TV), expiratory reserve volume (VER), minute ventilation (MV), respiratory frequency and partial CO2 pressure of exhaled air measured in sitting position during calm respiration and automatically electrostimulated cough through a respiratory flow controller.	Modality: Functional electrical stimulation Frequency: 50 Hz Pulse width: 400 μs Pulse duration: - Current amplitude: 30 – 100 mA Time on/off: - Wave: - Rise: - Time: - Electrodes: 8 self-adhesive electrodes distributed in 2 pairs on the rectus abdominis muscle,1 pair on the transversal abdominal muscle, 1 on the external oblique muscle, and 1 on the internal oblique muscle	An increase of up to 50% was observed in the number of coughs during electrostimulation, with an increase in PCF in all subjects. Maximum increase was 0.49 L/s (p < 0.05). CV varied up to + 0.23L. Forced vital capacity improved up to + 0.49 L/s and PCF improved in all subjects, as well as CV. The other assessed variables presented heterogenous data.
Butler et al., (2010)⁽²⁵25. Butler JE, Lim J, Gorman RB, Boswell-Ruys C, Saboisky JP, Lee BB, Gandevia SC. Posterolateral surface electrical stimulation of abdominal expiratory muscles to enhance cough in spinal cord injury. Neurorehabil Neural Repair. 2011; 25(2):158-67.⁾	8 male and 3 female subjects Level: C3 - T6 Classification: complete and incomplete	Inspiratory capacity (IC), vital capacity (VC), forced vital capacity (FVC), forced expiratory volume in 1 second (FEV1) measured in sitting position during cough with occlusion of the glottis with and without electrostimulation. Stimulation was controlled and automatically triggered in 6 subjects and self-controlled by 5.	Modality: Functional electrical stimulation Frequency: 50 Hz Pulse width: - Pulse duration: 1 s Current amplitude 50-350 mA Time on/off: - Wave: - Rise: - Time: 3 applications Electrodes: 2 pairs of electrodes (4 × 18 cm) bilaterally placed on the lateral-posterior part of the trunk	Pulmonary function variables increased in individuals submitted to electrical stimulation while coughing. Peak cough flow increased 36%, whereas mean expiratory flow increased 80%, and expiratory pulmonary volume, 41%. Occlusion of the glottis during maneuvers also contributed to improving pulmonary function variables; however, the best results were presented when electrostimulation was administered automatically by the system.
McLachlan et al., (2013)⁽¹²12. McLachlan AJ, McLean AN, Allan DB, Gollee H. Changes in pulmonary function measures following a passive abdominal functional electrical stimulation training program. J Spinal Cord Med. 2013; 36(2):97-103.⁾	11 male and 1 female subjects Level: C3 – 6 Classification: complete and incomplete	Forced vital capacity (FVC), forced expiratory volume in 1 second (FEV1), peak expiratory flow (PEF), maximum expiratory pressure (MEP), forced expiratory volume in 1 second (FEV1), measured during voluntary cough before, during and after a respiratory muscle rehabilitation program using functional electrical stimulation.	Modality: Functional electrical stimulation Frequency: 30 Hz Pulse width: 50 μs Pulse duration: - Current amplitude: 0-120 mA Time on/off: - Wave: Biphasic Rise: - Time: 6 weeks, 5 days per week, 11 – 230 min Electrodes: 8 self-adhesive electrodes distributed in 2 pairs of oblique abdominal muscles (bilateral) and 2 pairs on rectus abdominis muscle	Stimulation did not produce vigorous contractions in all subjects; neither was it tolerated by the entire group. The repercussions of the protocol on pulmonary function were heterogeneous, with slight positive changes in peak cough flow, maximum expiratory pressure, and tidal volume during training. However, after training, no statistically significant differences were found in FEV1 in the relation FEV1/FVC and PEF.
McBain et al., (2013)⁽²⁶26. Mcbain RA, Boswell-Ruys CL, Lee BB, Gandevia SC, Butler JE. Abdominal muscle training can enhance cough after spinal cord injury. Neurorehabil Neural Repair. 2013; 27(9):834-43.⁾	Group A: 7 male subjects Level: C4 - T5 Classification: complete and incomplete Group B: 8 male subjects Level: C4 – 7 Classification: complete	Inspiratory capacity (IC), vital capacity (VC), forced vital capacity (FVC), forced expiratory volume in 1 second (FEV1), peak expiratory flow (PEF) measured in sitting position during baseline state, voluntary cough, and expulsion phase of cough, both submitted to electrical stimulation.	Modality: Functional electrical stimulation Frequency: 50 Hz Pulse width: - Pulse duration: 3 s Current amplitude: Up to 250 mA Time on/off: - Wave: - Rise: - Time: 6 weeks, 5 days per week (5 series of 10 coughs per day) Electrodes: 2 electrodes (5 × 18 cm) placed bilaterally on the lateral-posterior part of the abdomen	Stimulation improved acute cough in patients with high SCI. During voluntary coughs, cough stimulation increased PEF in 50%. After 6 weeks of cough training, there was a significant increase in PEF (3.1 ± 0.1 to 3.6 ± 0.1 L/s) and in expiratory cough flow during non-stimulated voluntary cough among the assessed subjects. Pulmonary function measures improved after training. FEV1 increased from 1.3 ± 0.1 to 1.4 ± 0.1 L (P = 0.002), FVC increased from 1.7 ± 0.2 to 1.9 ± 0.2 L (P = 0.03), PEF increased from 2,1 ± 0.1 to 2.4 ± 0.2 L / s (P = 0.03), VC increased from 1.5 ± 0.1 to 1.8 ± 0.1 L (P = 0.009) and IC increased from 1.4 ± 0.1 to 1.6 ± 0.1 L (P = 0.04).
McBain et al., (2015)⁽²⁷27. Mcbain RA, Boswell-Ruys CL, Lee BB, Gandevia SC, Butler JE. Electrical stimulation of abdominal muscles to produce cough in spinal cord injury: effect of stimulus intensity. Neurorehbil Neural Repair. 2015; 29(4):1-8.⁾	7 male subjects Level: C4 – 7 Classification: complete and incomplete	Pulmonary function variables measured in sitting position during baseline state, voluntary cough, and expulsion phase of cough, both submitted to electrical stimulation.	Modality: Functional electrical stimulation Frequency: 50 Hz Pulse width: - Pulse duration: 1 s Current amplitude: 50 – 360 mA Time on/off: - Wave: - Rise: - Time: - Electrodes: 2 pairs of electrodes (4 × 18 cm) placed bilaterally on the lateral-posterior part of the abdomen	The greatest percentage of patients submitted to electrical stimulation while coughing had an increase in cough flow simultaneously with the increase of the current amplitude applied. Peak cough flow reached 4.0 ± 0.4 L /s with parameters of 80 to 240 mA and was significantly higher than in voluntary cough without electrostimulation, which was 2.2 ± 0.1 L / s, p <0.05. Total expiratory volume was also higher during stimulating, reaching 2.1 L whereas no stimulation had 1.3 L with the same parameters.

Article	STROBE items																						Total items
Article	1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16	17	18	19	20	21	22	Total items
Linder S H., (1993)⁽¹⁷17. Linder SH. Functional electrical stimulation to enhance cough in quadriplegia functional electrical stimulation enhance cough in quadriplegia. Chest. 1993; 103(1):166-9.⁾	0	1	1	1	0	1	0	1	0	0	1	0	1	0	1	0	0	1	0	1	1	0	11/22
Jaeger R J. et al., (1993)⁽¹⁸18. 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; 72(12):1358-61.⁾	0	1	0	1	0	0	0	1	1	0	1	1	1	1	1	1	0	1	0	1	1	0	13/22
Sorli J. et al., (1996)⁽¹⁹19. Sorli J, Kandare F Jaeger RJ, Stanic U. Ventilatory assistance using electrical stimulation of abdominal muscles. IEEE Trans Rehabil Eng. 1996; 4(1):1-6.⁾	0	1	1	1	0	1	0	1	0	0	1	0	1	1	1	1	0	1	0	1	1	0	13/22
Golle et al., (2006)⁽²²22. Gollee H, Hunt KJ, Allan DB, Fraser MH, McLean NA. A control system for automatic electrical stimulation of abdominal muscles to assist respiratory function in tetraplegia. Med Eng Phys. 2006; 29(7):799-80.⁾	0	1	1	1	0	0	0	1	0	0	1	0	1	1	1	0	0	1	0	1	1	0	11/22
Spivak et al., (2007)⁽²³23. Spivak E, Keren O, Niv D, Levental J, Steinberg F, Barak D, et al. Electromyographic signal-activated functional electrical stimulation of abdominal muscles: the effect on pulmonary function in patients with tetraplegia. Spinal Cord. 45(7):491-5.⁾	1	1	1	1	0	0	0	1	0	0	1	1	1	1	1	1	0	1	1	1	0	0	13/22
Golle et al., (2008)⁽²⁴24. Gollee H, Hunt KJ, Allan DB, Fraser MH, McLean N. Automatic electrical stimulation of abdominal wall muscles increases tidal volume and cough peak flow in tetraplegia. Technol Health Care. 2008; 16(4):273-81.⁾	0	1	1	1	1	1	0	1	0	0	1	1	1	1	1	0	0	1	1	1	0	0	1422
Butler et al., (2010)⁽²⁵25. Butler JE, Lim J, Gorman RB, Boswell-Ruys C, Saboisky JP, Lee BB, Gandevia SC. Posterolateral surface electrical stimulation of abdominal expiratory muscles to enhance cough in spinal cord injury. Neurorehabil Neural Repair. 2011; 25(2):158-67.⁾	0	1	1	1	0	1	0	1	0	0	1	1	1	1	1	1	0	1	0	1	0	1	14/22
McLachlan et al., (2013)⁽¹²12. McLachlan AJ, McLean AN, Allan DB, Gollee H. Changes in pulmonary function measures following a passive abdominal functional electrical stimulation training program. J Spinal Cord Med. 2013; 36(2):97-103.⁾	1	1	1	1	1	1	0	1	0	0	1	1	1	1	1	1	0	1	1	1	0	0	16/22
McBain et al., (2015)⁽²⁷27. Mcbain RA, Boswell-Ruys CL, Lee BB, Gandevia SC, Butler JE. Electrical stimulation of abdominal muscles to produce cough in spinal cord injury: effect of stimulus intensity. Neurorehbil Neural Repair. 2015; 29(4):1-8.⁾	0	1	1	1	0	1	0	1	0	0	1	1	1	1	1	1	0	1	0	1	0	1	14/22

Article	PEDro scale items											Total score
Article	1^* * - Criterion not scored according to the PEDro scale recommendation	2	3	4	5	6	7	8	9	10	11	Total score
Zupan A. et al., (1997)⁽²⁰20. Zupan A, Savrin R, Erjavec T, Kralj A, Karcnik T, Skorjanc T, Benko H, Obreza P. Effects of respiratory muscle training and electrical stimulation of abdominal muscles on respiratory capabilities in tetraplegic patients. Spinal cord. 1997; 35(8):540-5.⁾	*	1	0	1	0	0	0	1	0	0	0	2/10
Cheng et al., (2006)⁽²¹21. Cheng P, Chen C, Wang C, Chung C. Effect of neuromuscular electrical stimulation on cough capacity and pulmonary function in patients with acute cervical cord injury. J Rehabil Med. 2006; 38(1):32-6.⁾	*	1	0	1	0	0	0	1	0	1	1	5/10
McBain et al., (2013)⁽²⁶26. Mcbain RA, Boswell-Ruys CL, Lee BB, Gandevia SC, Butler JE. Abdominal muscle training can enhance cough after spinal cord injury. Neurorehabil Neural Repair. 2013; 27(9):834-43.⁾	*	1	0	1	0	0	0	0	0	0	0	2/10

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[1] Corresponding author, Felipe Soares Macedo Campus, Universitário Darcy Ribeiro, 70910-900, Brasília, DF, Brazil. macedosfelipe@gmail.com