Safety and effectiveness of neuromuscular electrical stimulation in cardiac surgery: A systematic review

Table 1 Quality assessment of the included studies using the physiotherapy evidence database

	Fischer et al[19]	Schardong et al[20]	Kitamura et al[21]	Fontes Cerqueira et al[22]	Fontes Cerqueira et al[23]	Sumin et al[24]	Rengo et al[25]	Cerqueira et al[26]	Takino et al[27]	Sumin et al[28]
Eligibility criteria1	√	√	√	√	√	√	√	√	√	√
Random allocation	√	√	√	√	√	√	√	√	√	√
Concealed allocation	√	√			√			√	√
Baseline comparability	√	√	√	√	√	√		√	√	√
Blinded subjects	√	√			√				√
Blinded therapists
Blinded assessors		√	√	√		√		√	√
Adequate follow-up	√	√	√						√	√
Intention-to-treat analysis	√	√	√	√	√	√		√	√	√
Between-group comparisons	√	√	√	√	√	√	√	√	√	√
Point estimates and variability	√	√	√	√	√	√	√	√	√	√
Total score	8/10	9/10	7/10	6/10	7/10	6/10	3/10	7/10	9/10	6/10

¹Eligibility criteria item does not contribute to total score.

Table 2 The main baseline characteristics among patients after cardiac surgery in each study included in the systematic review

Ref.	Groups	Males/Females (N)	Age (yr)	Weight (kg)	Height (cm)	BMI (kg/m2)	Type of surgery
Fischer et al[19]	NMES (n = 27); CG (n = 27)	18/9; 20/7	63.3 ± 15.5; 69.7 ± 13.1	NA	NA	27.6 ± 3.7; 27.7 ± 4.6	Aortic valve replacement; CABG; Heart transplantation; Other cardiothoracic surgery; Mitral valve replacement; Mitral valve reconstruction; Tricuspid valve reconstruction; Bentall surgery
Schardong et al[20]	FES (n = 10); CG (n = 10)	7/3; 7/3	60 ± 7.3; 63.5 ± 5	NA	NA	27.3 ± 3.1; 29.1 ± 6.2	CABG; Heart valve surgery
Kitamura et al[21]	NMES (n = 60); CG (n = 59)	39/21; 37/22	67 (55-74); 70 (61-77)	NA	NA	25.5 (20.4-24.8); 22.3 (20.4-24.9)	CABG; Valvular surgery; Thoracic Aorta
Fontes Cerqueira et al[22]	NMES (n = 26); CG (n = 33)	18/8; 23/10	41.8 ± 13.17; 42.21 ± 14.36	66.12 ± 13.29; 61.85 ± 12.69	160 ± 6; 165 ± 8	25. ± 4.72; 21.96 ± 4.2	Mitral valve replacement; Aortic valve replacement; Mitral valve reconstruction; Aortic valve reconstruction; Mitral valve replacement + Aortic valve reconstruction
Fontes Cerqueira et al[23]	NMES (n = 15); CG (n = 15)	9/6; 5/10	49.87 ± 14.37; 50.93 ± 14.56	NA	NA	NA	CABG; Valve replacement; CABG + Valve replacement
Sumin et al[24]	NMES (n = 18); CG (n = 19)	12/6; 13/6	61.5 [52-70]; 64 [60-68]	NA	NA	28.4 [25.2-30.9]; 28.4 [25.8-32.5]	CABG; Aortic valve replacement; Mitral valve replacement; CABG + valve replacement; Multivalve operations; Bentall surgery; Aortic dissection; Heart transplantation
Rengo et al[25]	NMES (n = 18); CG (n = 19)	16/2; 17/2	66.5 ± 1.6; 66.2 ± 1.4	89.4 ± 2.7; 90.9 ± 3.8	173 ± 1; 176 ± 3	29.7 ± 0.8; 29.0 ± 0.8	CABG; CABG + Valve replacement
Cerqueira et al[26]	NMES (n = 23); CG (n = 22)	12/11; 15/7	47.8 ± 13.9; 46.4 ± 13.5	72.3 ± 14.8; 68.5 ± 13.6	163.1 ± 10.4; 165.2 ± 7.2	27.2 ± 4.9; 25.1 ± 4.5	CABG; Aortic valve replacement; Mitral valve replacement; Mitral valve replacement; + Aortic valve reconstruction
Takino et al[27]	NMES (n = 90); CG (n = 90)	61/29; 63/27	74 ± 5; 74 ± 5	NA	NA	19.8 (18.0-21.8); 19.3 (18.2-20.8)	CABG; Valvular surgery; Thoracic aorta; Other surgery; Combined surgery
Sumin et al[28]	NMES n = 62); CG (n = 60)	44/18; 39/21	62.0 [57.5-66.6]; 63.5 [59.0-69.0]	NA	NA	27.4 [25.4-31.5]; 28.7 [25.9-33.3]	Prehabilitation (before cardiac surgery)

Values are presented as a mean ± SD or median (interquartile range). CABG: Coronary artery bypass grafting; CG: Control group; FES: Functional electrical stimulation; NMES: Neuromuscular electrical stimulation group; NA: Not available.

Table 3 Population, intervention, comparison, outcomes, and study design of each study included in the systematic review

Ref.	Interventions by group	Frequency	Session duration	Intervention Duration	Outcomes	Main results	Adverse events
Fischer et al[19]	NMES: biphasic rectangular pulses at 66 Hz, pulse duration 0.4 ms, duty cycle 3.5 s on and 4.5 s off to quadriceps muscle bilaterally. CG: stimulator electrodes were applied but no electricity was delivered	2 times/d for 7 d/wk	30 min	From POD 1 until ICU exit or POD 14	Muscle layer thickness, Muscle strength; Functional capacity	No significant effect on MLT. ↑ 4.5 times in recovering muscle strength to NMES group during ICU stay. Positive correlation between change in MLT and cumulative fluid balance (r = 0.43, P = 0.01) the first 3 PODs. No significant effect on functional ability	5 patients in the NMES group mentioned a feeling of discomfort
Schardong et al[20]	1FES: symmetric biphasic rectangular pulses at 15 Hz, pulse duration 0.5 ms, duty cycle 5 s on and 10 s off to vastus medialis and lateralis muscle bilaterally. CG: Stimulator electrodes were applied but no electricity was delivered	2 times/wk	40 min	8 wk	Functional capacity; Muscle strength; Muscle endurance; Muscle mass	↑ Distance to 6MWT in the FES group by 11.0% (49.6 m, 95%CI: 15.9-83.3) and in the CG by 10.4% (41.5 m, 95%CI: 7.8-75.2) with no significant between-groups. ↑ muscle strength (7.2 kg, 95%CI: 0.2-14.2). ↑ Muscle endurance (2.2 repetitions, 95%CI: 1.0-3.4)	No complications
Kitamura et al[21]	NMES: Symmetric biphasic square pulses, duty cycle 0.4 s on and 0.6 s off, 10 pulse trains (10 s) with 30 s intervals to quadriceps femoris and triceps surae muscle bilaterally. Usual postoperative rehabilitation program. CG: Usual postoperative rehabilitation program	1 time/d	30 min	3 d before surgery and from POD 1 to POD 5 (8 sessions)	The mean concentration of 3-MH/Cre; Physical function; Walking speed; Grip strength	No significant difference in the mean 3-MH/Cre from POD 1 to POD 6 between groups (225.3 [204.0-248.3] μmol/g vs 227.3 [206.3-259.9] μmol/g, P = 0.531). No significant difference in the KEIS on POD 7 between groups (0.44 ± 0.13 kgf/kg vs 0.41 ± 0.12 kgf/kg, P = 0.149. No significant difference in walking speed between groups (1.04 ± 0.24 m/s vs 0.99 ± 0.23 m/s, P = 0.294). No significant difference in grip strength between groups (29.1 ± 10.5 kg vs 26.9 ± 8.7 kg, P = 0.213)	1 patient mentioned muscle soreness
Cerqueira et al[22]	NMES: Stimulation at 50 Hz, duration 400 ms duty cycle 3 s on and 9 s off, to quadriceps and gastrocnemius muscle bilaterally. Regular physiotherapy care. CG: Usual physiotherapy care twice a day	2 times/d	60 min	from POD 1 to POD 5	Ambulation ability; Muscle strength; Functional independence; Quality of life	No significant difference in distance walked (95%CI: -64.87 to 65.97) and walking speed (95%CI: -0.55 to 0.57) between groups. No significant difference in muscle strength in the upper- limb, lower limb, and total MRC values, functional independence, and quality of life between groups	2 patients reported hypotension, and 1 patient complained of pain
Cerqueira et al[23]	NMES: Stimulation at 50 Hz, duration 200 ms duty cycle 3 s on and 9 s off, to quadriceps and gastrocnemius muscle bilaterally. Regular physiotherapy care. CG: stimulator electrodes were applied but no electricity was delivered	Once during the first 48 h of ICU stay	60 min	60 min	Hemodynamic responses; Respiratory responses	No difference in heart rate, systolic blood pressure, diastolic blood pressure, mean blood pressure respiratory rate, and oxygen saturation between groups	No complications
Sumin et al[24]	NMES: biphasic rectangular pulses at 45 Hz, duty cycle 12 s on and 5 s off to quadriceps muscle bilaterally. CG: Usual postoperative rehabilitation program	1 time/d	90 min	from POD 3 to exit the hospital (12 sessions or more)	Knee extensors strength; Handgrip strength; Knee flexor strength CSA of quadriceps femoris	↑ Knee extensors strength in the NMES group [28.1 (23.8; 36.2) kg on the right and 27.45 (22.3; 33.1) kg on the left] vs CG [22.3 (20.1; 27.1) and 22.5 (20.1; 25.9) kg, respectively; P < 0.001]. No difference in handgrip strength, knee flexor strength, quadriceps CSA, and 6MWT at discharge between groups	Non mentioned
Rengo et al[25]	2NMES: biphasic rectangular pulses at 25 Hz, pulse duration 400 ms, duty cycle 10 s on and 30 s off to quadriceps muscle bilaterally. CG: no intervention	1 times/d for 5 d/wk	45 min	4 wk	Physical function Mental and physical health	From discharge to 4-wk post-discharge: No significant interaction effect for total SPPB score (P = 0.11; ηp2 = 0.073; CG: 2.89 ± 0.50 vs NMES: 4.11 ± 0.54 units). Time effects for 6MWT distance (P < 0.01; ηp2 = 0.207; CG: 194 ± 18 vs NMES: 267 ± 16 m) and 6MWT power output (P = 0.01; ηp2 = 0.168; CG: 0.4 ± 0.1 vs NMES: 0.6 ± 0.1 W; P = 0.01)	No complications
Cerqueira et al[26]	NMES: Stimulation at 50 Hz, duration 400 ms duty cycle 3 s on and 9 s off, to rectus femoris and gastrocnemius muscle bilaterally. Regular physiotherapy care twice a day. CG: Usual physiotherapy care twice a day	2 times/d	60 min	From POD 1 to POD 5	Distance walked; Gait speed; Lactate levels Muscle strength Electromyographic activity of the rectus femoris; Functional Independence Measure	No significant difference in the distance walked (P = 0.650) between NMES group (239.06 ± 88.55) and CG (254.43 ± 116.67) as well as gait speed (P = 0.363), lactate levels (P = 0.302), knee extensor strength (P = 0.117), handgrip strength (P = 0.882), global muscle strength (P = 0.104), electromyographic activity (P = 0.179) and Functional Independence Measure (P = 0.059)	No complications
Takino et al[27]	NMES: Biphasic symmetric square pulses at 20 and 200 Hz, duty cycle 0.4 s on and 0.6 s off to vastus lateralis, vastus medialis and triceps surae muscle bilaterally. Standard post- surgical rehabilitation. CG: Standard post- surgical rehabilitation.	1 time/d	60 min	from POD 1 to POD 7	% change in isometric knee strength; % change in usual and maximum walking speed; % change in grip strength	↓ %ΔIKES in the NMES than CG [NMES: Mean -2%, 95% confidence interval (CI) -6 to 1; CG: -13%, 95% CI -17 to -9, P < 0.001]. ↓ %ΔMWS (P = 0.04). ↓ %ΔUWS and %ΔGS in the NMES compare to CG but not statistically significant	Non mentioned
Sumin et al[28]	NMES: rectangular pulses at 45 Hz, duty cycle 12 s on and 5 s off to quadriceps muscle bilaterally. Standard preoperative rehabilitation program; CG: Standard preoperative rehabilitation program	1 time/d	90 min	from the 2nd day of hospital stay until the day before surgery (7–10 sessions)	Exercise capacity; Muscle strength	↑ in KES, KFS, and 6MWT distance (all P < 0.001) in the NMES group compared to the CG. Slight ↑ in HS to the NMES group and slight ↓ to the CG but not statistically significant (P = 0.054 on the right hand and P = 0.062 on the left)	No complications

¹Patients were discharged from hospital and submitted to phase I of cardiac rehabilitation.

²Home-based intervention after hospital discharge.

CG: Control group; CSA: Cross-sectional area; FES: Functional electrical stimulation; ICU: Intensive care unit; KEIS: Knee extensor isometric strength; MLT: Muscle layer thickness; NMES: Neuromuscular electrical stimulation POD: Post operative day; SPPB: Short physical performance battery; 3-MH/Cre: 3-methylhistidine concentration corrected for urinary creatinine content; 6MWT: Six minutes walking test; KFS: Knee flexor strength; KES: Knee extensor strength; NA: Not available.