International Journal of Gerontology 11 (2017) 41e45

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International Journal of Gerontology

journal homepage: www.ijge-online.com

Original Article

Electric Muscle Stimulation for Weaning from Mechanical Ventilation

in Elder Patients with Severe Sepsis and Acute Respiratory Failure e A
Pilot Study*
Sheng-Yeh Shen 1, Chao-Hsien Lee 2, Rong-Luh Lin 1, Kuang-Hua Cheng 1, 3 *
1
Division of Chest Medicine, Departments of Internal Medicine, Mackay Memorial Hospital, 2 Critical Medicine Department, Mackay Memorial Hospital,
Taipei, 3 National Taiwan University College of Medicine, Graduate Institute of Clinical Medicine, Taiwan

a r t i c l e i n f o s u m m a r y

Article history: Background: Patients with severe sepsis and acute respiratory failure often developed muscle weakness
Received 13 January 2017 because of their critical illness and immobility. We hypothesized electric muscle stimulation (EMS) may
Accepted 13 January 2017 prevent the weakness and shorten the duration of mechanical ventilation (MV).
Available online 17 February 2017
Methods: Elderly patients with severe sepsis and acute respiratory failure were enrolled and randomized
to EMS or control group on the third day of MV. The EMS was applied to both quadriceps 32 minutes in
Keywords:
weekdays with minimal voltage to induce visible muscle contraction (device: HELEX 573, programmed
mechanical ventilation,
strength aggravating mode). Control group had passive exercise of extremities. Duration of MV support
electric muscle stimulation,
sepsis,
was compared.
weaning Results: 545 patients were screened and 25 patients were randomized in 2:1 ratio. (18 patients into EMS
and 7 into control group). 64% of the acute respiratory failures resulted from pneumonia. Both group had
similar demographic data and median age of all participants was 78 years-old (interquartile range 72
e82). The mean duration of ventilator dependence was 6 days (IQR 6e15) in control group and 6.5 days
(IQR 5e10) in EMS group (P 0.85).
Conclusion: EMS did not help critical-ill septic elderly to reduce the duration of mechanical ventilation in
our pilot study. Further larger study is warranted with adequate study power and identical weaning
strategy to test the EMS benets.
Copyright 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier
Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).

1. Introduction
Critical-ill patients may have muscle wasting and general
weakness when they are bed-bound in intensive care unit (ICU)
with acute severe disease. The intensive care unit acquired weak-
ness (ICUAW) typically affects proximal limb muscles symmetrically
and respiratory muscles. The main risk factors for ICUAW include
*
Disclosure of conicts of interest: I certify that all my afliations with or
nancial involvement in, within the past 5 years and foreseeable future, any or-
ganization or entity with a nancial interest in or nancial conict with the subject
matter or materials discussed in the manuscript are completely disclosed (e.g.,
employment, consultancies, honoraria, stock ownership or options, expert testi-
mony, grants or patents received or pending, royalties).
* Correspondence to: Dr. Kuang-Hua Cheng, Critical Medicine Department,
Mackay Memorial Hospital. No. 92, Sec. 2, Zhongshan N. Rd., Taipei City 10449,
Taiwan.
E-mail address: jeff01@mmh.org.tw (K.-H. Cheng).
high severity of illness upon admission, sepsis, multiple organ fail-
ure, prolonged immobilization, and hyperglycemia, and also older
patients have a higher risk1. After described in early 1980, critical
illness polyneuropathy and myopathy (CIPM) are increasingly
recognized as one of important causes in ICUAW2. The muscle
weakness was reported in 32e100% of critically ill adult patients
ventilated for longer than 3 days3 and 69% in critical primary
neurological diseases4. Administration of glucocorticoids and non-
depolarizing muscle relaxants, sepsis and multi-organ failure per
se as well as elevated levels of blood glucose and muscular immo-
bilization are the risk factors of CIPM5. Diaphragm was affected in
CIPM and weaning from mechanical ventilation could be delayed4,6.
In management of CIPM and ICUAW, no specic pharmaco-
therapy was validated. Infection control and early mobilization are
the cornerstone of the management. The earlier the physical
rehabilitation started, the better improvement was observed in
body functions7,8. However, active rehabilitation is not always

http://dx.doi.org/10.1016/j.ijge.2017.01.001
1873-9598/Copyright 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier Taiwan LLC. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
42
eligible for ICU patients because of the stupor consciousness,
sedation or restraint in ICU. Electric muscle stimulation (EMS) in-
duces muscle contraction without patient's cooperation and was
proposed as an adjunctive rehabilitation modality. In 2003, Zanotti
et al reported EMS in addition to active limb mobilization signi-
cantly improved peripheral muscles strength in bed-bound pa-
tients with mechanical ventilation for chronic obstructive
pulmonary disease9. For septic patients requiring mechanical
ventilation and having 1 or more organ failure other than respira-
tory dysfunction enrolled in the intensive care unit, Rodriguez
et al reported EMS was associated with an increase in strength of
the stimulated muscle10. Further research showed early EMS
applied to legs in critically ill patients with an Acute Physiology and
Chronic Health Evaluation (APACHE) score  13 prevented the
development of CIPM and also resulted in shorter duration of
weaning11. Two system-review also reported EMS was an effective
means of improving muscle weakness in adults with progressive
diseases such as COPD, chronic heart and critical illness12,13.
Previous EMS studies did not focus in acute respiratory failure
following severe sepsis. However, the most acute respiratory failure
acquiring mechanical ventilation in my constitution resulted from
elderly patients with severe sepsis and multiple comorbidities.
Mean age of the ICU patients were increasing globally, and severe
sepsis and septic shock remain leading cause of respiratory failure
in the elderly. Age itself may not predict mortality14, and adequate
therapy should be given to the elderly. Therefore, we conducted the
pilot study to investigate the feasibility and effect of early EMS in
the elderly with sepsis and acute respiratory failure. Optimal
setting of EMS (muscle site, daily duration, electric voltage and
frequency) was not clearly dened so far, and we also want to
evaluate the effect of a programed electric stimulation device
(HELEX 573) applied in weekdays. The aim of our study was to
assess the effect of EMS on muscle power preservation and dura-
tion of mechanical ventilation (MV) in critically septic patients.
2. Materials and methods
2.1. Study design
The study was a prospective randomized control study
approved by institutional Review Board in Mackay Memorial hos-
pital (13MMHIS060) in June, 2013 (ClinicalTrials.gov ID:
NCT01895647A). Informed consent was explained and obtained
from all of the participants' surrogates before the enrollment. The
primary end-point was duration of mechanical ventilation. Suc-
cessful weaning was dened as spontaneous breath without
inspiratory pressure support more than 6 hours. The second out-
comes were mortality after randomization and hand grip strength
measured by digital handgrip dynamometer every three day after
randomization.
Mackay Memorial Hospital is a teaching hospital in Taipei, and
the adult medical ICU had 28 beds. The ICU had patientenurse ratio
2:1, patienterespiratory therapist ration 10:1, and patient-
ephysician ratio 8:1. The weaning strategy was driven by the crit-
ical care physicians.
2.2. Participants
Adult patients (20e90 years-old) admitted with mechanical
ventilator were daily screened and recorded as eligible If they ful-
lled criteria of sepsis according to denition of 1992 American
College of Chest Physicians and the Society of Critical Care Medi-
cine15. The randomization was performed when the eligible pa-
tients required mechanical ventilation longer than 72 hours
(dened as need of inspiratory mechanical support in ventilator
S.-Y. Shen et al.
setting). They were randomly assigned to electric muscle stimula-
tion (Intervention group, arm biceps or thigh quadriceps) or passive
arm biceps or thigh quadriceps limb mobilization (Control group)
in 1:1:1 ratio.
The exclusion criteria were following:
1. Skin defect or infection around the thighs
2. Acute myocardial infarction within one week
3. Life-threatening cardiac arrhythmia
4. Pregnancy
5. Dying patient with life expectance shorter than one month.
6. Severe encephalopathy with coma and no spontaneous
breath drive
7. Uncontrolled seizure
8. Patient is fully awake and has adequate muscle power to
cooperate active limb exercise
9. Air-born contagious diseases. eg. Tuberculosis and Inuenza
virus infection
10. Moderate to severe adult respiratory distress syndrome with
requirement of neuromuscular blocker.
11. Patients with Extracorporeal Membrane Oxygenation
2.3. Intervention protocol
The patients in the intervention group received EMS on both
quadriceps (vastus medialis) and biceps, 32 minutes per day, 5 days
per week (Monday to Friday). EMS was conducted with a com-
mercial stimulator (HELEX 573, EverProsperous company, Taiwan)
with adhesive electrode (4.7 cm  4.7 cm). The stimulator output
current was 0e75 mA in biphasic waves with carrier frequency of
1500 Hz. We used its strength aggravation mode which protocol
consisted with warm-up, exercise and cool-down. The lowest
stimulation current was given to induce visible muscle contraction.
Bilateral hands grip strengths were measured and recorded by
digital hand dynamometer (CAMRY, model: EH101, China, (range
0e90 Kg)) before EMS and every 3 days. The test was performed
with the arm at right angles and the elbow by the side of the body.
Three trials were allowed for each hand alternatively, with a pause
of 60 seconds between each test.
The control group had active or passive exercise of extremities.
the extent of exercise was decided and performed by the physical
rehabilitation therapist after the consultation. The actual exercise
was individualized clinically.
2.4. Statistical analyses
All continuous variables were presented by median (25e75%
quartile range). Categorical data were presented in exact ratio. The
differences between groups were evaluated by nonparametric test
(Two-sample Wilcoxon rank-sum (ManneWhitney) test) for
continuous variable and Fisher's exact test for categorical variables.
The statistical signicance of P value was set at 0.05. The
KaplaneMeier method was used to compare the duration of
ventilator support between patients assigned to the EMS and
control groups. All analyses were done with small STATA 12.1
(StataCorp, Texas USA).
3. Result
From 1st Aug, 2013 to 30 Sept 2015, 545 patients were screened
as eligible at their ICU admission. The major cause of their sepsis
and acute respiratory failure resulted from pneumonia and urinary
tract infection. After three days of mechanical ventilation, 288 pa-
tients (52.84%) could be weaned from bi-level ventilator support, 17
Electric Muscle Stimulation for Weaning
patients (3.12%) expired, 84 patients (15.41%) refused the study and
131 patients (24.04%) met the exclusion criteria. The owchart of
screening and exclusion were listed in Fig. 1. Eventually, 25 patients
underwent randomization and 17 patients were assigned to EMS
group and 8 patients were allocated to control group. The baseline
demographic data of the participants were comparable and were
shown in Table 1. The median age of all participants was 78 years-
old (IQR 72e82). The sources of infection in 16 (64%) participants
were pulmonary infections; 4 (16%) were urinary tract infections; 3
(12%) were blood stream infections and 2 (8%) were intra-
abdominal infections.
We used handgrip dynamometer to assess the change of muscle
power during the study. But 17/25 (68%) of participants were too
weak, stupor or reluctant to cooperate the handgrip strength test.
Eight participants could perform the test, and 2e5 kg hand strength
were measured. The handgrip result was much lower than normal
reference (20e33 Kg for population older than 70 years-old)16. Six
patients dropped out in the EMS group because 2 patients (11.1%)
died and 4 patients (22.2%) refused further muscle stimulation.
Among the dropped-out group, only 1 patient survived at his
discharge. One patient (14.29%) expired in the control group before
Fig. 1. Results of screening, exclusion and randomization. ECMO: Extracorporeal Membrane Oxygenation.
43
the ventilator weaning. Adverse effects of EMS were closely
monitored during the muscle stimulation sessions, and neither skin
damage nor arrhythmia was observed.
The mean duration of ventilator dependence was 6 (IQR 6e15)
days in control group and 6.5(IQR 5e10) days in EMS group
(P 0.85). The hospital mortality was also similar in both groups.
Due to the censored data, The KaplaneMeier surviving method was
used to compare the time-to-weaning probability (Fig. 2), and the
probability of ventilator dependence was not signicantly different
in the two groups (Log rank P 0.82).
4. Discussion
Our pilot study revealed EMS were feasible and safe in elderly
ventilated patients, but the duration of mechanical ventilation was
not signicantly shorten compared to passive limb rehabilitation.
Drowsiness and muscle weakness were common in elder patients
with severe sepsis and acute respiratory failure, and handgrip
dynamometer measurement was often impracticable. For the
elderly patient could cooperate the handgrip test, the results were
much lower than predicted and ICUAW should be considered.
44 S.-Y. Shen et al.

Table 1 barrier to adequate exercise in ICU included sedation, restrain,

The demographic characteristic and clinical outcomes of patients in EMS and endotracheal tube, femoral catheters and delirium. EMS may
control groups (median (25the75th percentiles)).
generate visible muscle contraction in such condition and increase
Parameter Control group EMS group P value microcirculation, oxygen consumption25, prevent the inactivity
(N 7) (n 18) diaphragm atrophy26 and CIPM in critical ill patients10e12,18. Many
Age 78 (73e83) 77.5 (72e81) 0.69 studies reported EMS help muscle strength12 and may have sys-
Gender, male/female 2/5 12/6 0.18 temic effect in the strength of muscles not stimulated18,27. The
Coma scale 8 (6e10) 9 (7e10) 0.78
systemic effect of EMS could be partially explained by peripheral
APACHE II on admission 25 (21e27) 23.5 (19e28) 0.86
Charson score on admission 3 (2e4) 3 (2e3) 0.71 cytokine change (Increased interleukin-6 and reduced interleukin-
Blood glucose (mg/dL) 161 (112e210) 157 (129e222) 0.93 1/tumor necrosis factor alpha20,28).
Creatinine (mg/dL) 2.2 (1.3e2.8) 1.35 (0.9e1.8) 0.13 Compared to the single study reported positive effect of EMS on
Bilirubin (T) (mg/dL) 1.1 (0.8e1.6) 0.8 (0.6e1.2) 0.15
MV weaning by Routsi et al11, our participants were older with
Albumin (g/dL) 2.7 (2.5e3.5) 2.65 (2.3e2.9) 0.32
Septic shock 4/7 11/18 1.0
higher APACHE II score (Age 77 46.7 vs 61 19; APACHE II
Fever days 3 (1e7) 4 (2e10) 0.52 24.67 6.19 vs 18 4). Our participants were limited to severe
COPD 2/7 4/18 1.0 sepsis with acute respiratory failure in contrast to critical-illness
CHF 5/7 10/18 0.66 with or without ventilator. The two studies both have low rate of
Malignancy 2/7 6/18 1.0
enrollment. Routsi et al excluded patients died after randomization
Steroid use 3/7 7/18 1.0
Steroid days 0 (0e5) 0 (0e2) 0.73 and the APACHE II score became signicantly incomparable and
Outcome measurement higher in the control group. On the contrary, we did nal analysis
Hospital mortality 2/7 (28.57%) 5/18 (27.78%) 1.0 including participant died after randomization to compare mor-
MV days 6 (6e15) 6.5 (5e10) 0.85 tality, and the APACHE II score kept similar in the two groups. EMS
Successful spontaneous breath 6/7 14/18 1.0
intervention was 55 minutes daily in Routsi study, and 32 minutes/
Coma scale: Glasgow coma scale, only including eye (1e4) and motor response weekdays in our protocol. This may be another explanation of the
(1e6).
different outcome.
APACHEII Acute Physiology and Chronic Health Evaluation II. COPD: chronic
obstructive pulmonary disease. CHF: congestive heart failure. MV: mechanical Potential hazard of electric stimulation, e.g. skin burn, cardio-
ventilation. vascular, respiratory and, hemodynamic interaction was not
observed in previous29 and our study. We believe EMS may be safe
and effective exercise in ICU. But only Routsi et al had reported EMS
The gold standard for the diagnosis of ICUAW remains electro-
shorten duration of mechanical ventilation. No study demonstrated
myography (EMG), but it seldom was used in screening. The clinical
EMS effect on mortality so far.
guideline suggested manual muscle strength to identify the dis-
Weaning from ventilator for a patient t with severe sepsis is a
tribution and degree of muscle weakness17. The handgrip dyna-
complex process involving sepsis control, cardiopulmonary func-
mometry performance correlated well with the Medical Research
tion and CIPM recovery30. Muscle strength is important, but
Council (MRC) score for clinical assessment of muscle strength18.
effective and timely antimicrobial treatment, adequate infection
However, only approximately to 25 to 29 percent of patients are
source control, baseline cardiopulmonary function, and the wean-
adequately awake to assess muscle strength19. The nding was
ing strategy may inuence the duration of mechanical ventilation.
consistent with our study.
Thus one limitation of our study was lacking records of baseline
Early rehabilitation/mobilization in the ICU has been shown to
heart and lung function such as ventricular ejection fraction and
prevent and treat ICUAW1,7,8. Exercise with muscle contraction was
forced expiratory volume in one second. Another weakness of our
believed to have benecial effect on anti-inammatory
trial was the weaning strategy dependent on the ICU physicians.
cytokines20e22, glucose metabolism and diminish protein break-
Some physicians in our hospital used intermittent T-piece
down23. Mechanical ventilation 18 to 69 hours would result in
method when the patients are weak, and the mechanical ventila-
diaphragmatic inactivity and marked atrophy of human diaphragm
tion was resumed at night. After gradually prolonging T-piece trial
myobers because of increased diaphragmatic proteolysis24. But
were gradually prolonged and the extubation was subsequently
performed several days later. Thus we arbitrarily decided the six
hours for criterial of successful spontaneous breath trial.
Poor control of sepsis hindered weaning. Thus initial duration of
fever more than 38.3  C was recorded to stand for the infection
control, and the fever duration were comparable in our two groups.
Nevertheless, heterogeneous source and severity of infection may
still affect the comparison of ventilation weaning. And ICU-ac-
quired infection may happen and had negative impact on EMS ef-
fect and mortality.
The major limitation is the small sample size after high rate of
exclusion/dropout. We had to pool arm biceps and thigh quadriceps
stimulation group into EMS arm. According to Routsi trial, we want
to enroll 60 patients initially. Based on our available result, if we
want to conrm one-day difference in the two groups (standard
deviation 5e6; type I error rate 0.05; power 0.8), the estimated
sample size is 393e566 in each group. Thus further recruitment
was stopped because of slow recruitment. Further study is war-
ranted to conrm EMS effect with larger sample size, multi-center
enrollment, antibiotic guideline-adherence, heart/lung function
Fig. 2. KaplaneMeier curve comparing probability of ventilator-dependent days in recording, stratied sepsis source/severity and standardized
patient with or without EMS. (Log-rank test: P 0.82). weaning protocol.
Electric Muscle Stimulation for Weaning
5. Conclusion
EMS could be the only way to induce active muscle contraction
and prevent the inactivity muscle weakness in uncooperative or
sedated ICU patients. For the patients with severe sepsis and acute
respiratory failure, our study demonstrated general weakness was
frequent complication. EMS was feasible but did not shorten the
duration of ventilation support.
Nevertheless, further larger study with adequate power is
warranted to examine the impact of EMS in bedridden ICU patients
who are mechanically ventilated. The cardiopulmonary function,
weaning protocol, infection severity and guideline-adherence
should be clearly elucidated in further study design.
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