262 Full
262 Full
262 Full
study was performed in accordance with the Declaration Table 1. Medical Research Council Scale Score
of Helsinki. Written informed consent was obtained from
Point Description
the subjects or their relatives before inclusion.
0 No muscular contraction detected
Electrical Muscle Stimulation Intervention 1 Barely detectable flicker or trace of contraction
2 Active movement with gravity eliminated
3 Active movement against gravity
The electrical muscle stimulation intervention involved 4 Active movement against gravity and some resistance
two 30-min electrical muscle stimulation sessions per day, 5 Active movement against gravity and full resistance
5 d/wk for 2 wk. During each session, rectangular elec-
trodes were placed on motor points of the vastus lateralis
and rectus femoris of both legs. Electrical muscle stimu-
lation was performed by using a commercial stimulator Primary Outcomes Measurement
(Omnistm 500, ZMI, Taipei, Taiwan) with biphasic waves
at a simulation frequency of 50 Hz and pulse width of Pulmonary Function Measurement. The subjects were
400 s, cycling 2 s on and 4 s off. Electrical muscle required to maintain the semi-Fowler position during mea-
stimulation intensity was gradually increased until a visi- surement of weaning profiles. During measurement, sub-
ble muscle contraction was observed. The subjects in the jects’ endotracheal or tracheostomy tubes were temporar-
control group received similar electrode placement and ily disconnected from the ventilator and connected to a
intervention duration, except that the stimulator power was spirometer (Respiradyne II, Sherwood, St. Louis, Mis-
off. souri). Once the subjects were stable, the investigator
(HSF) activated the spirometer and measured minute
volume and breathing frequency. To measure the mouth’s
Study Procedure
maximum inspiratory pressure, the investigator con-
nected the endotracheal or tracheostomy tube with a T
This study followed a prospective and randomized de- tube and placed a manometer (Boehringer Ingelheim,
sign. Before subject recruitment, sequential sealed enve- Norristown, Pennsylvania) to one end of the T tube by
lopes were prepared by an independent investigator (CYH), using a nipple adapter and a 1-way valve. After the
with one chosen randomly by another investigator for each inspiratory port was manually occluded, the investigator
subject. The subjects were then assigned to an electrical coached the subject to inhale actively against the oc-
muscle stimulation group or a control group according to cluded airway during breathing cycles for 20 to 25 s; the
the label in the envelope. Age, sex, body weight, height, most negative value was recorded as the maximum in-
and diagnosis at respiratory care center admission were spiratory pressure.
recorded for each subject. Disease severity was assessed
within 24 h of respiratory care center admission by using Muscle Function Measurement. Muscle function was
the APACHE (Acute Physiology and Chronic Health Eval- assessed by skin-fold thickness, leg circumference, and
uation) II score. The subjects assigned to the electrical quadriceps muscle strength. To measure skin-fold thick-
muscle stimulation group received daily electrical muscle ness, the investigator pinched the skin at the middle of the
stimulation starting from the day after completion of base- bilateral thigh and pulled the skin fold away from the
line data collection. The subjects in the control group re- underlying muscle; therefore, only skin and fat tissue were
ceived similar medical treatment except for the electrical held. Lange calipers (Cambridge Scientific Industries,
muscle stimulation therapy. Cambridge, Maryland) were used to measure the skin-fold
thickness (in mm). Two measurements were recorded and
Primary and Secondary Outcomes averaged. Leg circumference was measured at the level of
the middle thigh. Quadriceps muscle strength, an indicator
Primary outcomes, which included pulmonary function, of knee extension, was assessed according to modified
muscle function, and physical function, were measured on procedures of manual muscle testing. In brief, the subjects
the day before the intervention (day 0) and the day after maintained a semi-Fowler position with the knee bent and
completion of the intervention (day 11). After completing were asked to perform a knee extension. The strength was
the intervention program, the subjects were followed up scored according to the Medical Research Council (MRC)
until they were discharged from the respiratory care cen- scoring system (Table 1).12 These scores are widely used
ter. Secondary outcomes were defined as the subject’s to evaluate ICU-acquired paresis.13,14
hospitalization outcomes, which included survival status,
weaning outcomes, duration of ventilation in the respira- Physical Functional Status Measurement. Physical
tory care center, and respiratory care center length of stay. functional status was assessed before and after the study
Excluded
66
Did not meet inclusion criteria: 43
Declined to participate: 23
Subjects enrolled
37
Analyzed Analyzed
16 17
period by using the Functional Independence Measure. pital mortality and 30 – 40% dropouts, the sample size was
The subjects were scored from totally dependent to com- increased to 19 subjects. Analysis was conducted by using
pletely independent, with lower scores representing greater SPSS v.17 (SPSS, Chicago, Illinois). The normality of
disability. The reliability and validity of these question- distribution was examined by using the Shapiro-Wilk test.
naires have been demonstrated.13 The results were expressed as the mean ⫾ SD for nom-
inal distributions, and as median and interquartile range
Secondary Outcomes Measurement (25th-75th percentiles) for nonparametric distributions.
Baseline characteristics, pre-intervention and post-inter-
Respiratory Care Center (RCC) Hospitalization Out- vention measurements, and continuous-variable hospital-
comes. RCC hospitalization outcomes were followed up ization outcomes of the electrical muscle stimulation group
until the subjects were discharged from the respiratory and the control group were compared by using an unpaired
care center to ward or home. Survival status, weaning Student t test or Mann–Whitney U test in case of nonpara-
outcomes, duration of ventilation in the respiratory care metric distribution. A paired t test or Wilcoxon signed-
center, and respiratory care center stay were recorded from rank test was used to examine intervention effects on pul-
the subjects’ medical records. Weaning off the mechanical monary function and muscle function within groups.
ventilator was considered successful if the subject was Pearson and Spearman correlation coefficients were used
continuously free of the mechanical ventilator for ⬎5 con- to examine the relationship between baseline variables and
secutive days. parametric or nonparametric distributions, respectively. A
chi-square test was used to analyze differences in the fre-
Statistical Analysis quency distributions of mechanical ventilator weaning and
survival rates between the groups. P ⬍ .05 indicated sta-
The main outcome was taken as quadriceps muscle power tistical significance.
measured in the subjects on the day after completion of
electrical muscle stimulation. The sample size was calcu- Results
lated according to a previous study,12 with assuming an
SD of ⫾1 and an ␣ error of .05, a sample size of 11 From August 2012 to July 2013, a total of 103 consec-
subjects would have 90% power to detect an increase of utive eligible patients were screened (Fig. 1). Sixty-six
1 MRC scale point on one of the stimulated muscles com- patients were excluded because they did not meet inclu-
pared with baseline. When allowing for 10 –20% in-hos- sion criteria (n ⫽ 43) or declined to participate (n ⫽ 23).
Thus, 37 subjects were randomized into the electrical mus- Comparisons of Primary Outcomes Between the
cle stimulation group (n ⫽ 18) and the control group Electrical Muscle Stimulation and Control Groups
(n ⫽ 19). During the study period, 2 subjects in each group
had acute pulmonary infection and dropped out of the
In the measurements of pulmonary function, no signif-
study, which left 16 (electrical muscle stimulation group) icant difference existed in both pre-intervention and post-
and 17 (control group) for analysis. intervention measurements between the electrical muscle
stimulation and control groups (Table 3). In the measure-
Demographic Characteristics ments of muscle function, no significant differences in
skin-fold thickness or leg circumference were revealed
between the groups in pre-intervention and post-interven-
A summary of the demographic and clinical charac- tion measurements. The muscle strength was assessed by
teristics of the subjects is presented in Table 2. Prob- MRC scale. Subjects were scored from “0 point - no mus-
lems at admission to the respiratory care center were cular contraction”, “1 point -Barely detectable trace of
mostly diseases that involved the respiratory system. No contraction”, “2 points -active movement with elimination
significant differences existed between the electrical of gravity”, “3 points -active movement against gravity”,
muscle stimulation and control groups in terms of age “4 points - active movement against gravity and some
(mean ⫾ SD, 77.7 ⫾ 14.3 vs 73.8 ⫾ 17.8 years, re- resistance”, “5 points -active movement against gravity
spectively, P ⫽ .49), BMI (mean ⫾ SD, 22.9 ⫾ 5.6 vs and full resistance”.12 The MRC points of right quadri-
23.1 ⫾ 3.9 kg/m2, respectively, P ⫽ .71), severity ceps muscle in the electrical stimulation muscle group
(APACHE II score mean ⫾ SD, 20.8 ⫾ 7.4 vs 20.3 ⫾ 6.3, were significantly higher than those in the control group
respectively, P ⫽ .82), or diagnosis. In baseline mea- after the intervention (median [IQR], 2[1-4] points vs 1[1-2]
surements, muscle strength was significantly associated points, respectively, P ⫽ .024). The MRC points of left
with Functional Independence Measure scores (r ⫽ 0.79, quadriceps muscle in the electrical muscle stimulation
P ⫽ .001). The subjects who had higher muscle strength group increased by a median of 0.5 points (IQR, 0 –1
were associated with higher independence in daily ac- points) from the enrollment to the end of the program,
tivities. A significant inverse relationship also existed which were significantly higher than those in the control
between muscle strength and APACHE scores group (median [IQR], 0 [0-0] points) (P ⫽ .046) (Table 5).
(r ⫽ ⫺0.41, P ⫽ .031) at baseline. Physical functional status was assessed by using Func-
Table 3. Comparisons of Pulmonary Function in Electrical Muscle Table 4. Comparisons of Quadriceps Skin-Fold Thickness, Leg
Stimulation and Control Groups Circumference, and Quadriceps Muscle Power in the
Electrical Muscle Stimulation and Control Groups
Electrical
Muscle Electrical
Variable Control Group P Muscle Control
Stimulation Variable P
Group Stimulation Group
Group
VT , median (25th–75th Skin-fold thickness, median
percentiles) mL (25th–75th
Pre 190 (170–220) 205 (150–250) .84 percentiles) mm
Post 210 (170–245) 180 (170–215) .38 Right side
Pre 10.2 (6–13.3) 13 (7–20) .19
P .07 .69
Post 8 (5.5–14.3) 14 (7.5–24.3) .02
f, mean ⫾ SD breaths/min
P .31 .78
Pre 24.6 ⫾ 7.8 23.6 ⫾ 8.6 .90 Left side
Post 23.6 ⫾ 8.2 25.9 ⫾ 8.0 .50 Pre 10.5 (6.8–15.8) 13.0 (6–19) .30
P .86 .49 Post 10.0 (5.8–14) 14.5 (8.5–19.3) .03
Minute volume, P .034* .92
mean ⫾ SD L Leg circumference,
Pre 5.3 ⫾ 2.0 4.9 ⫾ 2.4 .63 mean ⫾ SD cm
Right side
Post 4.7 ⫾ 0.9 5.3 ⫾ 1.8 .38
Pre 39.8 ⫾ 5.6 46.0 ⫾ 6.9 .71
P .80 .80
Post 39.3 ⫾ 5.5 45.1 ⫾ 5.6 .051
RSBI, mean ⫾ SD P .51 .13
Pre 133.7 ⫾ 64.6 115.4 ⫾ 68.5 .45 Left side
Post 126.8 ⫾ 81.5 135.9 ⫾ 59.1 .77 Pre 39.7 ⫾ 5.6 47.5 ⫾ 8.3 .99
P .24 .35 Post 38.8 ⫾ 5.1 44.6 ⫾ 5.7 .47
PIamx, mean ⫾ SD cm H2O P .38 .004*
Pre 35.0 ⫾ 9.6 36.0 ⫾ 14.9 .58 Quadriceps muscle strength,
MRC scale median
Post 38.3 ⫾ 15.1 35.0 ⫾ 17.7 .77 (25th–75th
P .33 .35 percentiles) point
Right side
VT ⫽ tidal volume Pre 2 (1–3.5) 1 (1–2) .09
Pre ⫽ pre-intervention Post 2 (1–4) 1 (1–2) .02
Post ⫽ post-intervention
f ⫽ breathing frequency
P .08 .56
RSBI ⫽ rapid shallow breathing index Left side
PIamx ⫽ maximal inspiratory pressure Pre 2 (1–3.5) 1 (1–2) .068
Post 2 (1–4) 1 (1–2.5) .53
P .034* ⬎.99
Medical Research Council scale score points are 0 point- no muscular contraction; 1 point-
tional Independence Measure scores. No significant dif- Barely detectable trace of contraction; 2 points-active movement with elimination of gravity; 3
ferences were found in pre- or post-measurements of Func- points-active movement against gravity; 4 points-active movement against gravity and some
resistance; 5 points-active movement against gravity and full resistance.12
tional Independence Measure scores between the electrical Pre ⫽ pre-intervention
muscle stimulation and control groups. Post ⫽ post-intervention
Table 5. Comparison of Changes of Muscle Function Between the ference in respiratory care center length of stay (median
Groups [IQR], 25 [18-49] d vs 24 [18-47] d; P ⫽ .74) and the
Electrical
duration of ventilation in the respiratory care center (me-
Variable Muscle Control Group P dian [IQR], 21.5[11-42.8] d vs 20 [12.5-43] d; P ⫽ .89)
Stimulation
Group between the electrical muscle stimulation and control
groups (Table 6).
Skin-fold thickness,
median
(IQR) mm
Right side ⫺0.75 (⫺3–1) ⫺0.5 (⫺1–2.5) .71 Discussion
Left side ⫺1 (⫺3–0.25) 0 (0–4.5) .34
Leg circumference,
median This study examined the effects of electrical stimulation
(IQR) cm
Right side ⫺1 (⫺2.25–1.5) ⫺0.5 (⫺3.6–2.25) .92
on the muscle function and hospitalization outcomes in the
Left side ⫺1 (⫺2.5–0.25) ⫺1.75 (⫺2.75–1.75) .66 subjects who received PMV. We discovered that the elec-
Quadriceps MRC trical muscle stimulation program improved muscle func-
scale, median
(IQR) point tion in the subjects who received PMV by increasing mus-
Right side 0 (0–1) 0 (0–0) .033 cle strength, but no significant improvement was revealed
Left side 0.5 (0–1) 0 (0–0) .046 in pulmonary function or hospitalization outcomes. The
subjects in the control group had significant reductions in
leg circumference (from 47.5 cm to 44.6 cm, P ⫽ .004).
This indicated that the subjects who received PMV were at
Table 6. Comparison of Hospitalization Outcomes Between the risk of muscle atrophy. Prolonged bed rest leads to de-
Groups creased muscle protein synthesis, increased muscle catab-
olism, and decreased muscle mass, particularly in the lower
Electrical extremities,15,16 and interactions among critical illness, in-
Muscle Control
Variable
Stimulation Group
P vasive ventilation, and immobility may lead to further mus-
Group cle function impairment.
Weaning rate, n/N (%) 9/16 (56.3) 8/17 (47.0) .72
The majority of the subjects in the present study were
Mortality, n/N (%) 3/16 (18.8) 2/17 (11.8) .67 diagnosed with pneumonia, often associated with elevated
Length of stay in RCC, 25 (18–49) 24 (18–47) .74 inflammatory mediators, cytokines, an abnormal metabolic
median (IQR) d state, and increased oxidative stress. These factors induce
Ventilator days in RCC, 21.5 (11–42.8) 20 (12.5–43) .89 changes in microvascular permeability, and increased glu-
median (IQR) d cose uptake and subsequent reactive oxygen species gen-
RCC ⫽ respiratory care center
eration may result in decreased oxygen and nutrient de-
livery to muscles, protein catabolism upregulation, and
muscle-fiber structure alteration.17,18 In our study, the sub-
jects in the electrical muscle stimulation group demon-
the left leg circumference decreased, from 47.5 ⫾ 8.3 cm strated a significant increase in muscle strength, whereas
to 44.6 ⫾ 5.7 cm (P ⫽ .004). No change was found in no change was found in the control group. In addition, the
skin-fold thickness in the subjects in the control group subjects had a reduction in skin-fold thickness without
(from 13.0 [6-19] to 14.5 [8.5-19.3] cm; P ⫽ .92). In the changes in leg circumference after receiving electrical mus-
measurement of physical function, the Functional Inde- cle stimulation.
pendence Measure scores increased, from 29.0 ⫾ 14.5 to Electrical muscle stimulation creates passive (nonvoli-
32.0 ⫾ 18.6 (P ⫽ .12) in the electrical muscle stimulation tional) contraction of skeletal muscles through the use of
group. In the control group, the Functional Independence low-voltage electrical impulses delivered by using surface
Measure scores decreased, from 25.6 ⫾ 7.9 to 25.2 ⫾ 14.5 electrodes through the skin to the underlying muscles,19
(P ⫽ .65). which may enhance muscle-fiber recruitment and reduce
atrophy due to immobility or critical illness.20 Previous
Comparisons of Secondary Outcomes Between studies reported that the application of high-frequency neu-
the Groups romuscular electrical stimulation caused muscle contrac-
tion and resulted in an increase in the size and cross-
For weaning outcomes, neither the weaning rate (56.3% sectional area of muscle fibers in healthy individuals21 and
vs 47.0%, P ⫽ .72) nor the mortality rate (18.8% vs 11.8%, subjects in the ICU.22 Vieira et al23 also reported an in-
P ⫽ .67) was significantly different between the electrical crease in fat-free mass in subjects with COPD. Our study
muscle stimulation and control groups. There was no dif- findings were consistent with previous findings,20 –22 which
indicated the potential role of electrical muscle stimulation found in the control group. In addition, leg circumference
in improving muscle function in PMV populations. was significantly decreased in the control group, whereas
Studies reported that exercise training can increase pe- no changes in leg circumference were found in the elec-
ripheral muscle function and exercise tolerance, thereby trical muscle stimulation group. The above-mentioned data
improving physical function.7,8,24 electrical muscle stimu- indicated that the application of electrical muscle stimu-
lation can, not only improve muscle function, but also lation prevents the progression of muscle dysfunction in
provide systemic effects that are similar to exercise. Gero- patients with PMV. However, no significant difference
vasili et al25 reported that electrical muscle stimulation in was found in hospitalization outcomes.
subjects who are critically ill induced an acute systemic This study had several limitations. First, because muscle
effect on microcirculation, and Perez et al26 demonstrated strength was the primary outcome in this study, the sample
that electrical muscle stimulation in healthy individuals size was calculated based on detecting a difference in
improved oxygen-uptake kinetics and work efficiency. Cen- the MRC scale score. However, this sample size may have
tral command and activation of the metaboreflex during been insufficient to reveal a between-group difference in
electrical muscle stimulation may even increase sympa- other outcomes, for example, hospitalization. In addition,
thetic discharge and contribute to changes in heart rate, we did observe a slight but significant reduction in the
systolic blood pressure, blood volume, and cardiac output, limb circumference of the control group, which may indi-
which thereby affect skeletal muscle metabolism in a sys- cate that subjects with PMV had a high risk of muscle
temic manner that may include respiratory muscles. How- atrophy. Future studies with larger sample sizes are re-
ever, in the present study, no significant differences in quired to confirm this finding and the effects of electrical
physical function were found between the groups. The stimulation on hospitalization outcomes. Second, the tim-
primary reason for this discrepancy may relate to differ- ing and total duration of our study may have been con-
ences in subject characteristics and electrical muscle stim- founding factors that attenuated the results. In a previous
ulation protocol. In a previous study, subjects with mod- study of subjects in the ICU, electrical muscle stimulation
erate-to-severe COPD but capable of ambulation sessions were initiated early (on the second day of admis-
demonstrated significant improvements in muscle strength sion) to prevent possible complications associated with
and 6-min walking test distance after a 6-wk home-based being bedridden and were continued until the subjects were
electrical muscle stimulation program.27 In this study, the discharged from the ICU.23
subjects who received PMV who had been bedridden for However, to ensure subject safety in our study and elec-
⬎21 d demonstrated more-severe impairment in pulmo- trical muscle stimulation session consistency, we began
nary muscle function than subjects in previous studies. electrical muscle stimulation when the subjects were he-
Electrical muscle stimulation duration, which was shorter modynamically stable, and it was performed for only 10 d.
in our study than reported elsewhere, may also have a role The delay may have predisposed the subjects to a higher
in determining its effects. Our 2-wk electrical muscle stim- risk of deconditioning and muscle wasting; therefore, they
ulation session may have been too short to induce suffi- may have required longer interventions to produce signif-
cient muscle strength to achieve significant improvement icant improvement. Also, we did not include any mecha-
in physical function. In a study that involved subjects with nistic evaluation of the effects of electrical muscle stimula-
COPD who were bedridden and received mechanical ven- tion, electrophysiologic measures of muscle function, or
tilation, 4 wk of electrical muscle stimulation resulted in histologic muscle evaluations, which might have produced
an increase in muscle strength and the capability to trans- more objective results.33 Although it has been widely used
fer from bed to chair.28 Whether a longer duration would for evaluating muscle strength, the MRC scale remains a
produce greater improvement in physical function requires subjective measure and has been questioned for its interob-
further study. server variability. However, in our study, muscle strength
Muscle strength and muscle mass have been reported to was assessed by a single-blinded observer, and potential in-
be negatively correlated with the stay in the hospital.29-31 terobserver variability was reduced by performing muscle
The greater the muscle strength that patients regain during strength comparisons among subjects. Nevertheless, from a
their hospitalization, the shorter the days they stay in the clinical perspective, the MRC scale is a convenient and use-
hospital.29-31 In our study, we also found that the subjects ful measure in an respiratory care center setting.
who had greater muscle strength were associated with To the best of our knowledge, this was the first study
greater independence in daily activities. The increase in that examined the effects of electrical muscle stimulation
MRC scale has been reported to be associated with changes on subjects who received PMV. Electrical muscle stimu-
of mortality rate.32 For each 1 unit increase in muscle lation is a simple, noninvasive method of muscle strength-
strength, there was a 5% relative decrease in the odds of ening that is well tolerated, without adverse effects, as
mortality.32 In our study, electrical muscle stimulation in- previously described. It produces effects similar to exer-
duced more improvement in the MRC scale score than that cise and does not require cooperation from patients. Elec-
trical muscle stimulation could be easily implemented in 6. Topp R, Ditmyer M, King K, Doherty K, Hornyak J III. The effect
patients who receive PMV without major interference to of bed rest and potential of prerehabilitation on patients in the in-
tensive care unit. AACN Clin Issues 2002;13(2):263-276.
the routine care in respiratory care centers and with no
7. Casaburi R, ZuWallack R. Pulmonary rehabilitation for management
apparent increase to staff work load. Because a previous of chronic obstructive pulmonary disease. N Engl J Med 2009;
study observed slight skin injury in some subjects,34 elec- 360(13):1329-1335.
trical muscle stimulation should be performed with care by 8. Nici L, Raskin J, Rochester CL, Bourbeau JC, Carlin BW, Casaburi
trained personnel. R, et al. Pulmonary rehabilitation: what we know and what we need
to know. J Cardiopulm Rehabil Prev 2009;29(3):141-151.
The strength of our study was that all the subjects re-
9. Maffiuletti NA. Physiological and methodological considerations for
ceived the same number of electrical muscle stimulation the use of neuromuscular electrical stimulation. Eur J Appl Physiol
sessions before primary outcome measurements; thus, in- 2010;110(2):223-234.
terference due to different electrical muscle stimulation 10. Snyder-Mackler L, Delitto A, Bailey SL, Stralka SW. Strength of the
sessions could be ruled out. In other studies, subjects re- quadriceps femoris muscle and functional recovery after reconstruc-
ceived electrical muscle stimulation sessions until discharge tion of the anterior cruciate ligament. A prospective, randomized
clinical trial of electrical stimulation. J Bone Joint Surg Am 1995;
from the clinical setting; consequently, electrical muscle 77(8):1166-1173.
stimulation duration and time to primary outcome varied 11. Sillen MJH, Speksnijder CM, Eterman RA, Janssen PP, Wagers SS,
among subjects and may have affected the objectiveness Wouters EFM5, et al. Effects of neuromuscular electrical stimulation
of outcome comparisons.27,30 We further ensured objec- of muscles of ambulation in patients with chronic heart failure or
tiveness by using a control group and concealed treatment COPD: a systematic review of the English-language literature. Chest
2009;136(1):44-61.
allocation, and we blinded the caregivers.
12. Rodriguez PO, Setten M, Maskin LP, Bonelli I, Vidomlansky SR,
Attie S, et al. Muscle weakness in septic patients requiring mechan-
Conclusions ical ventilation: Protective effect of transcutaneous neuromuscular
electrical stimulation. J Crit Care 2012;27(3):319.e1-e8.
In this randomized trial with a blinded outcome assess- 13. Paternosto-Sluga T, Grim-Stieger M, Posch M, Schuhfried O, Vacariu
ment, electrical muscle stimulation increased muscle strength G, Mittermaier C, et al. Reliability and validity of the medical research
council (MRC) scale and a modified scale for testing muscle strength in
in the subjects who received PMV, but it was ineffective in patients with radial palsy. J Rehabil Med 2008;40(8):665-671.
improving physical function and hospitalization outcomes. 14. Dodds TA, Martin DP, Stolov WC, Deyo RA. A validation of the
Because our trial involved only 2 weeks of electrical muscle functional independence measurement and its performance among re-
stimulation sessions, the beneficial effects may have been habilitation inpatients. Arch Phys Med Rehabil 1993;74(5):531-536.
underestimated. electrical muscle stimulation was well toler- 15. Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of
10 days of bed rest on skeletal muscle in healthy older adults. JAMA
ated and seemed to be promising as a preventive strategy for 2007;297(16):1772-1774.
muscle weakness in subjects receiving PMV. Future inter- 16. Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR. Pro-
ventional studies should be conducted to examine whether longed bed rest decreases skeletal muscle and whole body protein
earlier or longer duration electrical muscle stimulation pro- synthesis. Am J Physiol 1996;270(4 Pt 1):E627-E633.
vides more favorable outcomes. 17. Bolton CF. Neuromuscular manifestations of critical illness. Muscle
Nerve 2005;32(2):140-163.
18. Druschky A, Herkert M, Radespiel-Tröger M, Druschky K, Hund E,
REFERENCES Becker CM, et al. Critical illness polyneuropathy: clinical findings
1. MacIntyre NR, Epstein SK, Carson S, Scheinhorn D, Christopher K, and cell culture assay of neurotoxicity assessed by a prospective
Muldoon S, et al; National Association for Medical Direction of study. Intensive Care Med. 2001;27(4):686-93.
Respiratory Care. Management of patients requiring prolonged me- 19. Needham DM, Truong AD, Fan E. Technology to enhance physical
chanical ventilation: Report of a NAMDRC Consensus Conference. rehabilitation of critically ill patients. Crit Care Med 2009;37(10
Chest 2005;128(6):3937-3954. Suppl):S436-S441.
2. Zilberberg MD, Shorr AF. Prolonged acute mechanical ventilation 20. Segers J, Hermans G, Bruyninckx F, Meyfroidt G, Langer D, Gos-
and hospital bed utilization in 2020 in the United States: implications selink R. Feasibility of neuromuscular electrical stimulation in crit-
for budgets, plant and personnel planning. BMC Health Serv Res ically ill patients. J Crit Care 2014;29(6):1082-1088.
2008;8:242. 21. Nuhr M, Crevenna R, Gohlsch B, Bittner C, Pleiner J, Wiesinger G, et
3. Chen YH, Lin HL, Hsiao HF, Huang CT, Kao KC, Li LF, et al. al. Functional and biochemical properties of chronically stimulated hu-
Effects of additional pressure support level on exercise duration in man skeletal muscle. Eur J Appl Physiol 2003;89(2):202-208.
patients on prolonged mechanical ventilation. J Formos Med Assoc 22. Dirks ML, Hansen D, Van Assche A, Dendale P, Van Loon LJ. Neu-
2015;114(12):1204-1210. romuscular electrical stimulation prevents muscle wasting in criti-
4. Scheinhorn DJ, Hassenpflug MS, Votto JJ, Chao DC, Epstein SK, cally ill comatose patients. Clin Sci (Lond) 2015;128(6):357-365.
Doig GS, et al; Ventilation Outcomes Study Group. Ventilator-de- 23. Vieira PJ, Chiappa AM, Cipriano G Jr., Umpierre D, Arena R, Chiappa
pendent survivors of catastrophic illness transferred to 23 long-term GR. Neuromuscular electrical stimulation improves clinical and physi-
care hospitals for weaning from prolonged mechanical ventilation. ological function in COPD patients. Respir Med 2014;108(4):609-620.
Chest 2007;131(1):76-84. 24. Chen YH, Lin HL, Hsiao HF, Chou LT, Kao KC, Huang CC, Tsai
5. Gogia P, Schneider VS, LeBlanc AD, Krebs J, Kasson C, Pientok C. YH. Effects of exercise training on pulmonary mechanics and func-
Bed rest effect on extremity muscle torque in healthy men. Arch tional status in patients with prolonged mechanical ventilation. Re-
Phys Med Rehabil 1988;69(12):1030-1032. spir Care 2012;57(5):727-734.
25. Gerovasili V, Tripodaki E, Karatzanos E, Pitsolis T, Markaki V, outcome in patients with SIRS and acute respiratory failure. Inten-
Zervakis D, et al. Short-term systemic effect of electrical muscle sive Care Med 2010;36(1):66-74.
stimulation in critically ill patients. Chest 2009;136(5):1249-1256. 31. Ali NA, O’Brien JM Jr, Hoffmann SP, Phillips G, Garland A, Finley
26. Pérez M, Lucia A, Santalla A, Chicharro JL. Effects of electrical J, et al; Midwest Critical Care Consortium. Acquired weakness,
stimulation on VO2 kinetics and delta efficiency in healthy young handgrip strength, and mortality in critically ill patients. Am J Respir
men. Br J Sports Med 2003;37(2):140-143. Crit Care Med 2008;178(3):261-268.
27. Nápolis LM, Dal Corso S, Neder JA, Malaguti C, Gimenes AC, Nery 32. Lee JJ, Waak K, Grosse-Sundrup M, Xue F, Lee J, Chipman D, et al.
LE. Neuromuscular electrical stimulation improves exercise toler- Global muscle strength but not grip strength predicts mortality and
ance in chronic obstructive pulmonary disease patients with better length of stay in a general population in a surgical intensive care unit.
preserved fat-free mass. Clinics 2011;66(3):401-406. Phys Ther 2012;92(12):1546-1555.
28. Zanotti E, Felicetti G, Maini M, Fracchia C. Peripheral muscle strength 33. Kho ME, Truong AD, Zanni JM, Ciesla ND, Brower RG, Palmer
training in bed-bound patients with COPD receiving mechanical ven- JB, Needham DM. Neuromuscular electrical stimulation in me-
tilation: effect of electrical stimulation. Chest 2003;124(1):292-296. chanically ventilated patients: a randomized, sham-controlled pi-
29. Connolly BA, Jones GD Curtis AA, Murphy PB, Douiri A, Hopkin- lot trial with blinded outcome assessment. J Crit Care 2015;30(1):
son NS, et al. Clinical predictive value of manual muscle strength 32-39.
testing during critical illness: an observational cohort study. Crit 34. Routsi C, Gerovasili V, Vasileiadis I, Karatzanos E, Pitsolis T, Tri-
Care 2013;17(5):R229-R237. podaki E, et al. Electrical muscle stimulation prevents critical illness
30. Brunello AG, Haenggi M, Wigger O, Porta F, Takala J, Jakob SM. polyneuromyopathy: a randomized parallel intervention trial. Crit
Usefulness of a clinical diagnosis of ICU-acquired paresis to predict Care 2010;14(2):R74-R84.