FEASIBILITY OF MUSCLE ACTIVITY ASSESSMENT WITH SURFACE

ELECTROMYOGRAPHY DURING BED CYCLING EXERCISE IN INTENSIVE

CARE UNIT PATIENTS
JUULTJE SOMMERS, MSC, PT,1 MICHELLE VAN DEN BOORN, MSC,2 RAOUL H.H. ENGELBERT, PROF, PT,1,3
FRANS NOLLET, MD,1 MARIKE VAN DER SCHAAF, PHD, PT,1,3 and JANNEKE HORN, PHD, MD2
1
Department of Rehabilitation Medicine, Amsterdam Movement Sciences, Amsterdam UMC, University of Amsterdam, Meibergdreef
9, P.O. Box 22660, 1100DD, Amsterdam, The Netherlands
2
Department of Intensive Care, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
3
ACHIEVE–Centre of Applied Research, Faculty of Health, Amsterdam University of Applied Sciences, Amsterdam, The Netherlands
Accepted 26 August 2018

ABSTRACT: Introduction: Intensive care unit (ICU) patients often investigate and document the training intensity.5
develop weakness. Rehabilitation is initiated early to prevent Therefore, a tool to assess muscle activity during exer-
physical deterioration, but knowledge of optimal training sched-
ules is lacking. A reliable method to assess muscle activity during cise would be helpful to identify the optimal level of
exercise is needed. In this study we explored the feasibility of exercise intensity for an individual. Such information
electrical activity measurement by surface electromyography would allow the development of a personalized train-
(sEMG) during bed cycling in ICU patients. Methods: SEMG was
performed in 9 ICU patients and 6 healthy controls. A standard- ing schedule. Surface electromyography (sEMG)
ized 1-minute incremental resistance bedside cycle ergometer monitoring of muscle activity has been described in
protocol was used. Results: The median cycle time was healthy volunteers to assess muscle activity and fatigue
5.3 minutes in patients and 12.0 minutes in controls. The maxi-
mum sEMG increased in both groups; the minimal sEMG activity during exercise.6–9 sEMG detects the electrical activity
remained the same in patients, whereas an increase in the con- of the motor units that are involved in muscle con-
trol group was found. Discussion: sEMG is feasible and can tractions and can be considered a surrogate measure
detect muscle activity during bed cycling in ICU patients. It may
be a useful monitoring tool. Repeated measurements could possi- of the effort of the muscles. sEMG has been used for
bly provide information on the effects of training. diaphragm monitoring in (mechanically ventilated)
Muscle Nerve 58:688–693, 2018 pre-term infants,10,11 but monitoring of leg muscles
during bed cycling in patients in the ICU is new and
In critically ill patients who are admitted to the could provide useful information.
intensive care unit (ICU), muscle weakness often The aim of this pilot study was to determine
develops, which is referred to as ICU-acquired weak- whether sEMG is a feasible method for muscle moni-
ness (ICU-AW).1 Limiting bed rest and inactivity in toring during bed cycling in ICU patients.
early rehabilitation has a positive effect on muscle
strength, walking ability, and functional outcome.2,3 METHODS
However, the optimal frequency, intensity, and type Between January 2015 and March 2016, we conducted a
of exercise for ICU patients is unknown.3,4 prospective pilot study in the ICU of the Academic Medical
To achieve training effects on muscle strength and Center, Amsterdam, The Netherlands, a 34-bed, mixed medi-
cal–surgical ICU and medium care unit. The study was
cardiorespiratory fitness, the training load should be
approved by the medical ethics review committee
sufficient, but not excessive, for the cardiac, respira- (NL50006.018.14), and informed consent from each study
tory, and musculoskeletal systems. Monitoring of subject was obtained.
these systems during exercise is required to Adult ICU patients mechanically ventilated for > 48 hours
who could cycle were eligible for the study. To enable active
bed cycling, a muscle strength score ≥ 3 on the Medical
Additional supporting information may be found in the online version of Research Council (MRC) scale for the legs (hip flexion, knee
this article. extension, and dorsal flexion of the feet) was required. Exclu-
Abbreviations: APACHE, Acute Physiology and Chronic Health Evalua- sion criteria were contraindications to perform physical exer-
tion; DEMMI, De Morton Mobility Index; HR, heart rate; ICU, intensive care cise according to the safety criteria of the Evidence Statement
unit; ICU-AW, ICU-acquired weakness; MRC, Medical Research Council; for Physiotherapy in the ICU,4 a score of < 3 (as measured
RMS, root mean square; RPE, rating of perceived exertion; RPM, revolu-
tions per minute; sEMG, surface electromyography; S5Q, Short 5-item
using the Short 5-item Questionnaire [S5Q]) for inability to
Questionnaire; sEMGmax, maximum sEMG; sEMGmin, minimum sEMG; follow instructions,12–14 and insufficient knowledge of Dutch.
ΔsEMG, change of sEMG; MDF, median frequency; MFCV, muscle fiber The control group consisted of healthy subjects.
conduction velocity

Conflicts of Interest: None of the authors have any conflict of interest to Measurements. The patients and controls were tested
disclose. once. They were placed in the semi-recumbent position in
This is an open access article under the terms of the Creative Commons
Attribution-NonCommercial-NoDerivs License, which permits use and dis- bed with both legs placed in a motorized cycling exercise
tribution in any medium, provided the original work is properly cited, the device (MOTOmed letto2; RECK-Technik, Betzenweiler, Ger-
use is non-commercial and no modifications or adaptations are made. many). The cycling protocol started with 1 minute of passive,
Correspondence: J. Sommers; e-mail: j.sommers@amc.nl unloaded cycling at 20 revolutions per minute (RPM). Next,
active cycling started, in which the resistance was gradually
© 2018 The Authors. Muscle & Nerve published by Wiley Periodicals, Inc.
Published online 30 August 2018 in Wiley Online Library increased according to the fixed levels of resistance (steps) of
(wileyonlinelibrary.com). DOI 10.1002/mus.26330 the bed cycle. The capacity of the bed cycle consisted of

688 Surface Electromyography in ICU MUSCLE & NERVE November 2018

20 increasing levels of resistance with the lowest resistance at balance items). The score range is 0–100, where 0 represents
0 (step 0). Resistance was increased at 1 step per minute in poor mobility and 100 indicates high levels of independent
the patient group and 2 steps per minute in the control mobility. From the control group, we obtained data on age,
group, leading to a total protocol duration of 22 minutes and gender, Borg RPE scale, and muscle fatigue.
12 minutes, respectively. The bed cycle provided detailed data
of the maximal workload (watts), duration of cycling
Data and Statistical Analysis. Patients’ characteristics and
(minutes), and RPM. When RPM was reduced to <10, the
continuous variables are described using descriptive statistics
cycling was stopped. Throughout the exercise test, hemody-
and are presented as mean and standard deviation, or, in the
namic parameters (heart rate [HR] and mean arterial pres-
case of a skewed distribution, as median and interquartile
sure) and respiratory parameters (oxygen saturation and
range (25th–75th percentile, IQR). Normality was checked
respiratory frequency) of the patients were collected to assess
using the Kolmogorov–Smirnov test. Categorical variables are
safety. When the HR was >80% of the maximum predicted
expressed as proportion with percent.
HR (using the Fox formula), or the patient’s safety was threat-
The sEMG signals were transformed using root-mean-
ened in any other way, the cycling was stopped.2,4,15
square (RMS) analysis, and the curves were analyzed offline in
The Borg Rating of Perceived Exertion (RPE) scale (range
MATLAB (MATrix LABoratory, The Mathworks, Natick,
6–20 points)16,17 was used directly after the exercise. The Borg
Massachusetts).
RPE scale is a reliable and valid measurement to assess exer-
Stable signals were selected from at least 10 cycling cycles
tion perceived by patients during and after exercise,18 with
immediately after an increase of resistance. The maximum
higher scores indicating higher perceived exertion.17 Further-
sEMG (sEMGmax) and minimum sEMG (sEMGmin) were
more, the patients and controls were asked whether they expe-
determined using a peak detection (high and low) algorithm
rienced muscle fatigue (yes/no) in the legs. The sEMG
in MATLAB. If peak detection identified 2 consecutive peaks
(microvolts) recordings were performed using the Dipha-16
or troughs, only the first peak or trough was used for analy-
device (Inbiolab BV, Groningen, The Netherlands). Four elec-
sis.11 From the selected 10 cycling cycles, the mean was calcu-
trodes (H59P Cloth Electrode; Kendall) were placed on the
lated and used for group analysis.11
muscle rectus femoris in both legs (refer to Fig. S1 in Supple-
Three parameters, sEMGmax, sEMGmin, and change in
mentary Material online). Without analog filtering, the sEMG
sEMG (ΔsEMG), were analyzed for each step.7,11 The peaks
data were digitized and sent wirelessly to the Dipha-16 system
(sEMGmax) represent the number of motor units recruited
connected to a laptop with a Polybench (Applied Biosignals,
during muscle contraction, and the troughs (sEMGmin) repre-
Weener, Germany) application.
sent the number of motor units still active during relaxation
The following data were obtained from the patients’ medi-
of the muscle within each revolution cycle (see Fig. S2 in Sup-
cal records: age; gender; reason for ICU admission; disease
plementary Material online). By subtracting the troughs from
severity according to the Acute Physiology and Chronic Health
the peaks, the ΔsEMG was calculated. P < 0.05 for overall dif-
Evaluation (APACHE) II19; duration of mechanical ventilation
ference between groups (ICU patients and controls) was con-
and ICU stay at moment of testing; muscle strength (MRC
sidered significant using the linear mixed model.
sum score); and the level of mobility (on the testing day), as
assessed by the De Morton Mobility Index (DEMMI).20,21 The
APACHE score measures the severity of illness on ICU admis- RESULTS
sion, with a range of 0–71. A higher score corresponds to Nine patients and 6 healthy volunteers were
more severe disease and a higher risk of death. The MRC sum included in this pilot study. The reason for ICU
score for the assessment of ICU-AW was defined as a score admission were medical (4 patients), planned
obtained from bilateral testing of 6 muscle groups (shoulder
(3 patients), and unplanned surgical (2 patients).
abduction, elbow flexion, wrist extension, hip flexion, knee
extension, and ankle dorsiflexion).22,23 This leads to a range
Further characteristics are presented in Table 1. The
for the MRC sum score of 0–60 points.24 The DEMMI scale patients had decreased levels of physical function.
measures the full range of mobility within the ICF activity The patients cycled for a shorter duration than
domain.20,21 It consists of 15 hierarchical mobility items the healthy controls (see Table 2). The increases in
(3 beds, 3 chairs, 4 static balances, 2 walking and 3 dynamic resistance and maximal workload were lower. During

Table 1. Patients’ characteristics at the moment of testing.*

ICU patients (n = 9) Healthy persons (n = 6)

Age, in years 70 (53–77) 59 (47–63)

Gender, women (n) 3 3
ICU stay to inclusion, in days 45 (14–59) —
Patients with mechanical ventilation during 4 —
measurement (n)
Mechanical ventilation, in days 18 (6–40) —
APACHE II score 17.5 (14–21) —
MRC sum score 42 (37–43) 60 (60–60)
DEMMI 24 (18–32) 100 (100–100)

IQR, interquartile range; ICU, intensive care unit; APACHE, Acute Physiology and Chronic Health Evaluation score; MRC, Medical Research Council scale;
DEMMI, De Morton Mobility Index.
*Data presented as median (interquartile range), unless noted otherwise.

Surface Electromyography in ICU MUSCLE & NERVE November 2018 689

 Table 2. Results of bed cycling.*

ICU patients (n = 9) Healthy persons (n = 6)

Duration of the test (min:s) 5:3 (4:6–8:2) 12:0 (12:0–12:0)

Maximal workload (W) 3 (2.5–5) 34.5 (32.5–54.5)
RPM 33.5 (26–38.3) 60 (53.3–73.8)
Maximum steps 4 (4–5) 20 (20–20)
Borg score 13 (12–15) 13 (9–13)
Reason to stop (n)
Muscle fatigue 7
Dyspnea 1
Other 1 6 (end of program)

ICU, intensive care unit; RPM, revolutions per minute.

*Data presented as median (interquartile range), unless noted otherwise.

the exercise test, there were no changes in the The methods used to analyze the results of sEMG
hemodynamic and respiratory safety parameters recordings during cycling differ substantially in the
monitored. Therefore, cycling was never stopped literature.6,7 Martin-Valdez et al. and Macdonald et al.
due to safety reasons. All controls completed the used the median frequency (MDF), muscle fiber
12-minute program with 20 steps of increasing conduction velocity (MFCV), and amplitude (RMS)
resistance. to investigate muscle fatigue.6,7 Both studies recom-
mended the use of RMS amplitude as the most suit-
Surface Electromyography. At the start of cycling,
able and sensitive variable to observe muscle activity
during the passive period, sEMG activity was able to during incremental exercise and fatigue.6,7 In our
be recorded. Evaluation of sEMG during active pilot study, we evaluated the amplitude (in the RMS
cycling showed an increase in ΔsEMG in the ICU signal) found in 10 subsequent rotations directly
and control groups. This reflected primarily an after each increase in resistance. This straightforward
increase in sEMGmax. The trough values (sEMGmin) method was also used to assess diaphragm weakness
showed no change in the patient group but an at our hospital.11
increase in the control group (Fig. 1.). We also found sEMG activity in both groups during
The overall difference between the peaks (sEMGmax) the passive period of cycling. This indicates that
of the ICU and control groups was not significant motor units were already activated in this phase.
(0.27 μV [95% confidence interval –4.41 to 4.96]; P = These results seem to support the observations by
0.9). For trough (sEMGmin), a statistically significant dif- Kayambu et al. of the benefits of passive cycling in
ference of 1.8 μV (95% confidence interval 0.05 to ICU populations. In those studies, they found that
3.53) was found (P = 0.047). passive cycling reduced muscle wasting and prevented
muscle atrophy, improved muscle strength and physi-
cal function, and reduced length of hospital stay in
DISCUSSION
medical and surgical ICU populations.2,27–29
In this pilot study we have shown that muscle activ- In most ICU patients, termination of bed cycling
ity from the rectus femoris can be monitored during was caused by patients reporting muscle fatigue in the
bed cycling by sEMG in ICU patients. With increas- legs. None of the controls stopped for this reason. We
ing resistance, a clear increase in muscle activity was also evaluated general exertion using the Borg RPE
observed. These findings indicate that sEMG is feasi- scale immediately after the exercise.16,17,30 Both ICU
ble and may be useful to monitor muscle activity in patients and controls reported a Borg RPE score of
ICU patients during exercise. In addition, during 13 defined as “somewhat hard,” indicating that there
passive cycling, limited muscle activity was detected. was no difference in perceived exertion.16,17
Recording of sEMG for the assessment of muscle
activity during cycling in healthy persons has already
been described.6–9 In these populations, the Limitations. Our study has some limitations that
method was found to be a useful tool to investigate need to be acknowledged. Due to the strict inclusion
muscle fatigue. sEMG during cycling was also used in criteria we used, our study population was small and
patients with chronic low back pain or cerebral palsy training was done at a rather late phase of the ICU
to detect muscle activation and fatigue.25,26 Because admission. Another limitation of our study was the
all these studies were performed on normal training software of the bedside cycle ergometer used. The
bikes instead of cycles used at the bedside, we decided increased power during the test could not be set on
to explore our method in healthy subjects to compare a fixed wattage per minute. The software selected its
and validate our method of cycling in the ICU. own increase in resistance based on the RPM and
690 Surface Electromyography in ICU MUSCLE & NERVE November 2018
FIGURE 1. (A) Peak values (sEMGmax) from patients in the ICU and controls. Numbers of participants are given on boxplot (EMG
expressed in microvolts). Peak values of the left quadriceps are shown. (B) Trough values (sEMGmin) for patients in the ICU and con-
trols. Numbers of participants given on boxplot (EMG expressed in microvolts). Trough values of the left quadriceps are shown. (C) Delta
values (ΔsEMG) from patients in the ICU and controls. Numbers of participants are given on boxplot (EMG expressed in microvolts).
Delta values of the left quadriceps are shown.

steps algorithm of the bed cycle. Nevertheless, the following a strict protocol, we could increase the
bed cycle was preferred because it has been recom- steps in a similar manner.
mended and widely used in ICU patients for practi- In conclusion, our pilot study has shown that
cal and safety reasons.2 The program of the bed sEMG is feasible and may be a useful monitoring
cycle provided detailed data of the wattage and num- tool to detect muscle activity during bed cycling in
ber of RPMs after completion of the exercise. By ICU patients. This investigation is a first step toward
Surface Electromyography in ICU MUSCLE & NERVE November 2018 691
 FIGURE 1C Continues

bedside monitoring of muscle exercise and fatigue 8. Camata TV, Altimari LR, Bortolotti H, Dantas JL, Fontes EB,
Smirmaul BP, et al. Electromyographic activity and rate of muscle
in ICU patients during bed cycling. With multiple fatigue of the quadriceps femoris during cycling exercise in the severe
measurements in single patients over a longer period domain. J Strength Cond Res 2011;25:2537–2543.
9. Coelho AC, Cannon DT, Cao R, Porszasz J, Casaburi R, Knorst MM,
of time, more knowledge can be achieved on fatigue et al. Instantaneous quantification of skeletal muscle activation, #power
and training effects. Ideally, in such future projects, |production, and fatigue during cycle ergometry. J Appl Physiol 2015;
118:646–654.
sEMG monitoring should be combined with oxygen 10. Hutten GJ, van Eykern LA, Latzin P, Thamrin C, van Aalderen WM,
uptake and heart rate measurements during incre- Frey U. Respiratory muscle activity related to flow and lung volume in pre-
term infants compared with term infants. Pediatr Res 2010;68:339–343.
mental bed cycle exercises. Such studies could help
11. Kraaijenga JV, de Waal CG, Hutten GJ, de Jongh FH, van Kaam AH. Dia-
to determine the optimal dose and timing of exer- phragmatic activity during weaning from respiratory support in preterm
cise for individual patients. infants. Arch Dis Childhood Fetal Neonatal Ed 2017;102:F307–311.
12. De Jonghe B, Sharshar T, Lefaucheur JP, Authier FJ, Durand-Zaleski I,
The authors thank J.M. Binnekade, E. Witteveen, J. Jurgens, Boussarsar M, et al. Paresis acquired in the intensive care unit: a pro-
G.J. Glas, and A.S. van Bergen for their assistance. spective multicenter study. JAMA 2002;288:2859–2867.
Ethical Publication Statement: We (the authors) confirm that 13. Gosselink R. Physiotherapy in the intensive care unit. Netherlands J Crit
we have read the Journal’s position on issues involved in ethical Care 2011;66–75.
publication and affirm that this report is consistent with those 14. Gosselink R, Bott J, Johnson M, Dean E, Nava S, Norrenberg M, et al.
Physiotherapy for adult patients with critical illness: recommendations
guidelines. of the European Respiratory Society and European Society of Intensive
Care Medicine Task Force on Physiotherapy for Critically Ill Patients.
REFERENCES Intensive Care Med 2008;34:1188–1199.
1. Herridge MS, Tansey CM, Matte A, Tomlinson G, Diaz-Granados N, 15. Fletcher GF, Ades PA, Kligfield P, Arena R, Balady GJ, Bittner VA, et al.
Cooper A, et al. Functional disability 5 years after acute respiratory dis- Exercise standards for testing and training: a scientific statement from
tress syndrome. N Engl J Med 2011;364:1293–1304. the American Heart Association. Circulation 2013;128:873–934.
2. Burtin C, Clerckx B, Robbeets C, Ferdinande P, Langer D, Troosters T, 16. Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Cli-
et al. Early exercise in critically ill patients enhances short-term func- nician’s guide to cardiopulmonary exercise testing in adults: a scientific
tional recovery. Crit Care Med 2009;37:2499–2505. statement from the American Heart Association. Circulation 2010;122:
3. Tipping CJ, Harrold M, Holland A, Romero L, Nisbet T, Hodgson CL. 191–225.
The effects of active mobilisation and rehabilitation in ICU on mortality 17. Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports
and function: a systematic review. Intensive Care Med 2017;43:171–183. Exerc 1982;14:377–381.
4. Sommers J, Engelbert RH, Dettling-Ihnenfeldt D, Gosselink R,
18. Chen MJ, Fan X, Moe ST. Criterion-related validity of the Borg ratings
Spronk PE, Nollet F, et al. Physiotherapy in the intensive care unit: an
of perceived exertion scale in healthy individuals: a meta-analysis. J
evidence-based, #expert |driven, practical statement and rehabilitation
Sports Sci 2002;20:873–899.
recommendations. Clin Rehabil 2015;29:1051–1063.
5. American College of Sports Medicine. Resource manual for guidelines for exercise 19. Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a
testing and prescription, 7th ed. Baltimore: Lippincott Williams & Wilkins; severity of disease classification system. Crit Care Med 1985;13:818–829.
2012. 20. de Morton NA, Davidson M, Keating JL. The de Morton Mobility Index
6. Macdonald JH, Farina D, Marcora SM. Response of electromyographic (DEMMI): an essential health index for an ageing world. Health Qual
variables during incremental and fatiguing cycling. Med Sci Sports Life Outcomes 2008;6:63.
Exerc 2008;40:335–344. 21. Sommers J, Vredeveld T, Lindeboom R, Nollet F, Engelbert RH, van
7. Martinez-Valdes E, Guzman-Venegas RA, Silvestre RA, Macdonald JH, der Schaaf M. Morton Mobility Index is feasible, reliable, and valid in
Falla D, Araneda OF, et al. Electromyographic adjustments during con- patients with critical illness. Phys Ther 2016;96:1658–1666.
tinuous and intermittent incremental fatiguing cycling. Scand J Med Sci 22. Hermans G, van den Berghe G. Clinical review: intensive care unit
Sports 2016;26:1273–1282. acquired weakness. Crit Care 2015;19:274.

692 Surface Electromyography in ICU MUSCLE & NERVE November 2018

23. Stevens RD, Marshall SA, Cornblath DR, Hoke A, Needham DM, de 27. Griffiths RD, Palmer TE, Helliwell T, MacLennan P, MacMillan RR.
Jonghe B, et al. A framework for diagnosing and classifying intensive Effect of passive stretching on the wasting of muscle in the critically ill.
care unit-acquired weakness. Crit Care Med 2009;37(suppl):S299–308. Nutrition 1995;11:428–432.
24. Hermans G, Clerckx B, Vanhullebusch T, Segers J, Vanpee G, 28. Kayambu G, Boots R, Paratz J. Early physical rehabilitation in intensive
Robbeets C, et al. Interobserver agreement of Medical Research Council care patients with sepsis syndromes: a pilot randomised controlled trial.
sum-score and handgrip strength in the intensive care unit. Muscle Intensive Care Med 2015;41:865–874.
Nerve 2012;45:18–25. 29. Winkelman C, Johnson KD, Hejal R, Gordon NH, Rowbottom J, Daly J,
25. Mohseni Bandpei MA, Rahmani N, Majdoleslam B, Abdollahi I, Ali SS, et al. Examining the positive effects of exercise in intubated adults in
Ahmad A. Reliability of surface electromyography in the assessment of ICU: a prospective repeated measures clinical study. Intensive Crit Care
paraspinal muscle fatigue: an updated systematic review. J Manipulative Nurs 2012;28:307–318.
Physiol Ther 2014;37:510–521. 30. Dawes HN, Barker KL, Cockburn J, Roach N, Scott O, Wade D. Borg’s
26. Alves-Pinto A, Blumenstein T, Turova V, Lampe R. Altered lower leg Rating of Perceived Exertion scales: do the verbal anchors mean the
muscle activation patterns in patients with cerebral palsy during cycling same for different clinical groups? Arch Phys Med Rehabil 2005;86:
on an ergometer. Neuropsychiatr Dis Treat 2016;12:1445-1456. 912–916.

Surface Electromyography in ICU MUSCLE & NERVE November 2018 693