Heart & Lung 47 (2018) 1e9

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Heart & Lung

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Care of Critically Ill Patients

Influence of muscle strength on early mobility in critically ill adult

patients: Systematic literature review
Audrey R. Roberson, MS, RN a, *, Angela Starkweather, PhD, RN b,
Catherine Grossman, MD c, Edmund Acevedo, PhD d, Jeanne Salyer, PhD, RN a
a
School of Nursing, Department of Adult Health and Nursing Services, Virginia Commonwealth University, Richmond, VA, USA
b
Center for Advancement in Managing Pain, School of Nursing, University of Connecticut, Storrs, CT, USA
c
School of Medicine, Internal Medicine, Virginia Commonwealth University, Richmond, VA, USA
d
School of Kinesiology and Human Science, Virginia Commonwealth University, Richmond, VA, USA

a r t i c l e i n f o a b s t r a c t

Article history: Background: Muscle strength may be one indicator of readiness to mobilize that can be used to guide
Received 17 December 2016 decisions regarding early mobility efforts and to progressively advance mobilization.
Received in revised form Objectives: To provide a synthesis of current measures of muscle strength in the assessment of early
18 September 2017
mobilization in critically ill adult patients who are receiving MV therapy.
Accepted 4 October 2017
Methods: Research studies conducted between 2000-2015 were identified using PubMed, CINHAL,
MEDLINE, and the Cochrane Database of Systematic Reviews databases using the search terms “muscle
strength”, “intensive care”, “mechanical ventilation” and “muscle weakness”.
Keywords:
Muscle strength
Results: Nine articles used manual muscle testing, the Medical Research Council scale and/or hand-held
Intensive care dynamometer to provide objective measures for assessing muscle strength in the critically ill adult
Mechanical ventilation patient population.
Muscle weakness Conclusions: Further research is needed to examine the application of standardized measures of muscle
Early mobility strength for guiding decisions regarding early and progressive advancement of mobility goals in adult
ICU patients on MV.
Ó 2017 Elsevier Inc. All rights reserved.

Introduction care. Neuromuscular dysfunction has been identified as an eti-

ology of muscle weakness due to disease processes found in the
Immobility in the critically ill adult patient ICU patient population, such as sepsis, multiple organ dysfunc-
tion syndromes, and acute respiratory distress syndrome.11,15
Muscle weakness, prevalent in the critically ill patient, is Further complicating muscle weakness in critically ill patients
multi-factorial in its causes and may be compounded by neuro- are possible neurosensory impairments (e.g., tactile, auditory,
muscular, cardiovascular, pulmonary, psychological, pharmaco- visual) and localized barriers/injuries (e.g., invasive lines/tubes,
logical and equipment barriers.9,21,27 Intensive care unit (ICU) pressure ulcers) frequently experienced during critical illness.
patients may experience deficits in their attention, arousal and Reduced venous return resulting in deep vein thrombosis8,23
cognitive abilities26, especially if neuromuscular blocking agents and pulmonary complications, such as atelectasis and pneu-
and sedatives have been administered as part of their plan of monia, are unfortunate sequelae of muscle weakness and
immobility.8,23
Persistent muscle weakness and immobility due to muscle
deconditioning can be unfortunate consequences of mechanical
This research did not receive any specific grant from funding agencies in the
ventilation therapy. Mechanical ventilation, the process of
public, commercial, or not-for-profit sectors.
Disclaimer: The views expressed in this manuscript represent those of the authors exchanging oxygen and carbon dioxide using a device, may
and are not the opinions of Virginia Commonwealth University. impact early mobilization and lengthen the ICU stay. It is well
* Corresponding author. Virginia Commonwealth University Health, 1213 E. Clay established that the implementation of an early mobilization
Street, Critical Care Hospital, 4th floor, 4-132, Richmond, VA 23298, USA. program improves patient outcomes, to include functional sta-
E-mail addresses: [email protected] (A.R. Roberson), angela.starkweather@
uconn.edu (A. Starkweather), [email protected] (C. Grossman),
tus, patients getting out of the bed sooner in the ICU setting, and
[email protected] (E. Acevedo), [email protected] (J. Salyer). decreased hospital and ICU days.2,6,19,28 However, health care

0147-9563/$ e see front matter Ó 2017 Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.hrtlng.2017.10.003
2 A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9

team members are often hesitant to initiate early mobility in- The peripheral neuromyopathy weakness component of CINM,
terventions for patients who require MV because of perceptions which has come to be described as ICU-acquired weakness (ICU-
that they may put the patient at increased risk of accidental AW),10 has raised awareness of its clinical significance in the criti-
extubation or injury. In recent years, several research studies cally ill adult. The prevalence of muscle weakness in patients who
have concluded that mobilizing patients on MV therapy is safe, regain normal consciousness after greater than one week of MV
feasible and minimizes the long-term effects of immobiliza- therapy is 25%e60%.10 These patients have demonstrated muscle
tion.2,6,19,28 Muscle strength is often assessed in other patient waste peaking during the first three weeks of ICU stay, indicating
populations to guide the delivery of activity interventions and early physical activity in this patient population can benefit overall
determine rehabilitation needs. Less attention, however, has muscle health and minimize muscle deconditioning.14 Patients
been focused on identifying the influence of muscle strength on experiencing ICU-AW often have a diagnosis of sepsis leading to
early mobilization in the critically ill adult patient on MV ther- multiple organ and respiratory failure requiring prolonged MV
apy. Equally important is determining how muscle strength can therapy.22 Patients exhibiting both limb and respiratory weakness
be measured in this patient population at the bedside. Under- are at risk of experiencing clinically significant decline in their
standing and recognizing the influence of muscle strength on muscle strength, requiring purposeful interventions to support
decreasing muscle deconditioning has the potential to increase early mobility. While there has been a significant focus on respi-
early mobilization in this patient population. Muscle strength is ratory muscle weakness, less emphasis has been placed on
an important measure for predicting and evaluating early measuring limb strength as a potential influence of mobility
mobilization in the critically ill adult patient on MV therapy. readiness.
Therefore, a literature review was performed to provide a syn-
thesis of current measurements of muscle strength used in the Methods
assessment of readiness to mobilize in critically ill adult patients
who are receiving MV therapy. The questions guiding the sys- Eligibility criteria and sources
tematic literature review were:
Using the preferred reporting items for systematic reviews and
(a) What measurements have been used to assess muscle strength meta-analyses (PRIMSA) guidelines,18 the PubMed/MEDLINE,
in adult critically ill patients receiving mechanical ventilation CINAHL, and the Cochrane Database of Systematic Reviews data-
therapy? bases were searched to access research studies published between
(b) Which measurements demonstrate readiness for early mobi- the years 2000e2015 to reflect current best practice. The articles
lization in adult critically ill patients receiving mechanical were primary research conducted in an adult ICU setting on pa-
ventilation therapy? tients receiving MV therapy, assessing muscle strength and re-
ported in the English language. This literature review was
Muscle strength in the critically ill adult patient conducted from May 2014eNovember 2015 using the search terms
“muscle strength”, “intensive care”, “mechanical ventilation” and
Despite the dissemination of literature promoting the impor- “muscle weakness”. Although this literature search started in May
tance of early mobilization in the critically ill patient receiving MV 2014, it was not completed until November 2015 due to time
therapy, there is a lack of research that has explored the influence constraints in completing the search.
of muscle strength on early mobilization in this patient popula-
tion. Numerous patients admitted to an ICU setting acquire a Search and study selection
syndrome described as a neuromuscular dysfunction, which is
characterized as generalized limb and respiratory muscle weak- Using the PubMed database, the above-mentioned search terms
ness.5 This syndrome, which has come to be known as critical were used with a search date range of “01/01/2000 through 11/14/
illness neuromyopathy (CINM), occurs in critically ill patients 2015”, “humans”, “English language”, and “adults: 19þ years” as
without previous neuromuscular disease, indicating its simulta- additional limiters. The results yielded a total of 97,848 articles.
neous development with the critical illness and/or treat- Each search term was added to the search builder section of the
ments.11,21,22 CINM has a respiratory neuromuscular weakness and advanced search method using the “AND” operator, yielding (34)
peripheral neuromyopathy components.9 The respiratory neuro- articles. This same process was used for each of the other database
muscular component of CINM has been shown to be a predictor of searches. Screening of the articles was independently performed by
delayed weaning in patients receiving MV therapy as well as the primary author. Using the inclusion and exclusion criteria,
associated with peripheral myopathy weakness.9 Although the initial screening included a review of each article’s title, which
respiratory component of CINM is not the focus of this literature eliminated (17) articles due to the title having a different patient or
review, it is a vital assessment area in the overall outcome of disease foci, such as red blood cells, neurologic disease, electrical
critically ill adults being able to perform activities during and stimulation and heart transplantation. An additional (11) articles
following their ICU stay. were eliminated after reading the title, full abstract, introduction

Table 1
Literature search inclusion and exclusion criteria.

Inclusion criteria Exclusion criteria

U Adults >18 years old U Patients not in the ICU setting during study
U Admitted to an ICU setting U Patients with pre-existing neuromuscular disorders, trauma, missing limbs, orthopedic
U Receiving mechanical ventilation for duration of their disorders, unable to ambulate independently or with an assist device during their admission
participation in study and patients with cardiac dysfunctions
U Assessing muscle strength U Patients using nerve stimulation
U English language, spoken and comprehended by the patient U Patients not awake, currently on sedation, paralyzed or that require stimulated muscle force
U Original Study (not a review, editorial)
 A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9 3

and methodology sections of the articles due to alternate focus of included in the analysis were evaluated as low bias. Criteria for
research, to include rehabilitation therapy, glycemic control and inclusion are listed in Table 1 and were identified based on desired
MV weaning. The remaining (6) articles were read in their entirety patient population (adults greater than 18-years old), location of
based on meeting the inclusion criteria and were included in this the patient (ICU setting), patients receiving MV therapy during the
systematic review. Ancestry searches (review of references in study, study was focused on assessing muscle strength, patients
selected articles) were performed on the six publications acquired comprehended the English language and the study was an original
and two additional publications were identified that fit the inclu- study. Exclusion criteria, also listed in Table 1, included patients not
sion and exclusion criteria and were added to this systematic re- in the ICU setting during the study and patients with pre-existing
view. One additional article was included in this review upon neuromuscular disorders, any missing limbs, unable to ambulate
receiving this article in a journal subscription as it, too, also met the upon ICU admission with or without an assistive device, any nerve
inclusion and exclusion criteria. A total of nine articles were stimulation needs and patients not awake, sedated or paralyzed at
included in this literature review. Risk of bias was determined by the time of the study. Refer to Fig. 1 for a descriptive flowchart of
evaluating the methodological quality of all articles that met the the literature search in the PubMed database.
inclusion criteria to the extent to which these studies could be
replicated. Publication bias was minimized by using a variety of Data collection process and data items
databases to search for relevant research articles. All articles
Using Garrard’s Matrix Method13, a table was developed to sys-
tematically summarize the eight articles. Topics for abstraction from
each article included: (a) the authors’ name and year of publication;
97,848 articles (b) the research design, which included the timeframe of the study;
(c) sample and setting; (d) method(s)/devices used to measure
initially found strength; (e) statistical analysis, and; (f) the main outcomes of the
using limiters study. The principal summary measures reported in each manu-
script were identified and include descriptive analysis and tests of
significance. A summary of this process can be found in Table 2.

Results

(34) articles found using Nine publications between the years 2008e2015 were included
in this systematic review. Eight were prospective design studies
search terms and one was a randomized controlled trial (RCT) design. The age
range of the subjects was 23- to 93-years and 56% of the studies had
more male than female subjects. In four of the studies (44%), there
were more female patients enrolled than male patients.1,7,20,29 The
settings for the studies varied between Medical ICUs (MICU), Sur-
gical ICUs (SICU), and a Medical-Surgical ICU. Three articles did not
specify the type of ICU setting their study was conducted4,7,29 and
one study identified using only surgical ICU patients.16 Seven arti-
(17) eliminated due to patient cles reported MV measurements using median and interquartile
ranges (IQR) for the days spent on MV.1,3,4,7,9,16,20 With the excep-
population diagnosis tion of one publication,6 articles included subjects with sepsis or
infection and respiratory disease as a diagnosis. One study included
subjects with a diagnosis of sepsis but not respiratory disease3 and
another study identified a history of cardiac and respiratory dis-
ease6 in its subjects.
All the studies assessed the patients’ ability to focus their
attention to perform simple commands following enrollment.
Three studies1,3,4 used the Attention Screening Exam, a valid
(11) eliminated due to alternate method for ICU patients and two studies used a screening method
research focus for assessing awakening and comprehension.9,16 One study used
both methods to assess attention to commands. Another study
enrolled patients who received intravenous sedation and/or
neuromuscular blocking agents in the ICU, however, did not assess
the participants’ ability to follow commands. Two studies did not
identify a specific method for determining comprehension or
ability to follow simple commands.
There were two measures predominately used in the nine
(6) articles + (2) ancestry articles + studies to determine muscle strength. The Manual Muscle Test
(MMT), as measured by the Medical Research Council (MRC) 0e5
(1) printed article included in summated score was used in seven studies.1,3,4,9,16,20,29 The MMT
compares the patient’s muscle strength in six different muscles
review
groups in the upper and lower extremities bilaterally and is
measured to determine the Medical Research Council (MRC) 0e5
summated score, which has been deemed a reliable and valid test
Fig. 1. Systematic literature search in PubMed database flowchart. to assess muscle strength.11 The lower MRC scores, grades 0e3,
Table 2

4
Studies using influential factors of muscle strength in critically ill adults on mechanical ventilation.

Research study Research design Sample and setting Methods/devices for Statistical analysis Main outcomes
measurement
Ali, N.A., O’Brien, J.M., Hoffman, Prospective, multicenter, cohort (5) medical ICUs in academic Muscle strength measured with Spearman’s r ¼ 0.90, p- Hospital mortality higher in
S.P., Phillips, G., Garland, A., study medical centers (AMC) affiliated Medical Research Council (MRC) value<0.001 between ICU- patients with ICU-AP than
Finley, J.C., Almoosa, K., . May 2005eApril 2007 with the Midwest Critical Care scale acquired paresis (ICU-AP) and without weakness, per MRC
Midwest Critical Care Consortium Dominant hand-held device MRC exam and HHD
Consortium, 20081 174 subjects enrolled and 136 (HHD) using the JAMAR device Using sex-specific thresholds for HHD may provide rapid, simple
Objective: (a) ICUAP is in- completed study Assessments repeated next day handgrip, handgrip strength had alternative to MRC exam for ICU-
dependently associated with Adults  18 years old, on MV Maximum total MRC score and good test performance when AP diagnosis
increased mortality; (b) for  5 days handgrip from either compared with an ICU-AP Number of ICU- and hospital-free
determine if HHD is a concise day ¼ subject’s strength diagnosis by MRC (sensitivity days were significantly reduced
measure of global strength and 80.6%, specificity 83.2%) in ICU-AP subjects per MRC
is independently associated Odds of hospital mortality higher exam, with strong correlation
with mortality in subjects with ICU-AP Odds with handgrip strength
Ratio (OR) ¼ 7.8, 95% confidence No reference to mobility; perfect
interval (CI), 2.4e25.3, p ¼ 0.001 agreement of interobservers for
12 pts but didn’t state timing or
location of evaluations (all in
ICU?)
Baldwin, C.E. and Bersten, A.D., Prospective, cross-sectional with 16 subjects for both critically ill HHD used to determine isometric Mean (SD) or median (IQR), (13) subjects limited to limb

A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9

20143 a case-controlled element and healthy group hand-grip, elbow flexion, and Independent esamples t-test, exercises in bed with “some”
Objective: concurrently November 2010eDecember 2011 Consecutive patients 18 years knee extension forces (Jamar, Pearson r, z-scores for muscle stable for fully assisted transfer to
investigate relative differences old, requiring 12 h MV, with Illinois; Lafayette manual muscle thickness and strength with chair; (3) subjects able to
in both thickness and strength sepsis, in a single tertiary ICU test system, Indiana) reference values obtained from perform standing transfer to
or respiratory and peripheral MRC sum score graded 3 upper the control group for within- chair from up to 2-person
muscles during routine care limb and 3 lower limb groups group analysis by repeated physical assistance
bilaterally to ascertain meeting measures analysis of variance Subjects weaker than control
ICU-AW criteria score of <48 out MRC sum score median ¼ 48 (42 group (p  0.001) in respiratory
of 60 e54 IQR); MRC sum score < 48 and limb muscle strength
Measurements done when (indicating ICU-AW) n ¼ 8 (50%) measures
subjects able to perform all Mean difference (95% CI) Future studies should investigate
measures between critically ill and healthy unexplained variances in muscle
subjects force: elbow flexion 14.4 strength, (e.g., severity of illness)
(10.2e18.5, p  0.001); handgrip other than size and mass
23.5 (16.0e30.5, p  0.001); knee Only 20% of subjects able to
extension 19.0 (14.0e23.9, return to their pre-admission
p  0.001) residence on discharge
Baldwin, C.E., Paratz, J.D., and Repeated measures (17) critically ill patients and (12) Interrater reliability assessed Descriptive statistics High interrater agreement of
Bersten, A.D., 20134 November 2009eDecember 2010 healthy volunteers using (2) physiotherapists; Test- Triplicate force readings for each hand grip and knee extension
Objective: (a) investigate test- Single tertiary ICU retest assessed by one examiner muscle group were averaged and forces but wide-ranging 95% CIs
retest and interrater reliability Patients  18 years old with an 2-days later logarithmically transformed for for bilateral elbow flexion in
of a muscle strength ICU length of stay of  5days and Peak isometric hand grip, elbow reliability analysis, reported as critically ill patients
assessment with portable anticipated hospital admission of flexion, and knee extension force the geometric mean (95% CI) High test-retest agreement of
dynamometry in survivors of a further 3 days measured in modified recumbent Interrater and test-retest hand grip and knee extension
critical illness; (b) examine the Protocol initiated at 13- days positions (3) times bi- laterally, reliability analyzed with a 2-way forces in the critically ill patients
minimal detectable difference (IQR, 10e16) of ICU admission over 6-sec intervals mixed model intraclass and greater reliability right
force required to mitigate MV 240-h (IQR, 107e355) Grip strength measured with correlation coefficient (ICC, [95% elbow flexion than left
measurement error; (c) depict JAMAR hydraulic hand CI]) There was overlap of force values
peak forces per MRC scale dynamometer in the 2nd handle Scatter plots used to represent between MRC grades of all
position to the nearest 0.5 kg range of forces contained within muscle groups in critically ill
Elbow flexion and knee corresponding MRC scale grades sample and considerable range of
extension strength measured for each muscle action, measured forces represented within MRC
with Lafayette manual muscle by examiner A on the initial test grades 4 and 5.
test system in high range to the day
nearest 0.1 kg
MRC score given for each muscle
action after HHD testing for each
muscle group
Burtin, C., Clerckx, B., Robbeets, Randomized Controlled Trial (90) critically ill patients in the Allocation to treatment or control Descriptive statistics, 95% CI (37/71) patients (52%) in surgical
C., Ferdinande, P., Langer, D., December 2005eFebruary 2007 medical and surgical ICU at group using sealed opaque Differences between groups ICU; (8/19) patients (42%) in
Troosters, T, Hermans, G . University Hospital Gasthuisberg, envelopes in random block sizes evaluated using unpaired medical ICU; 84% patients were
Gosselink, R., 20096 Belgium (45 ¼ treatment group, Assessments taken at both day of Student’s t tests, Wilcoxon, intubated
Objectives: (a) investigate 45 ¼ control group) ICU discharge and day of hospital Mann-Whitney U test (variables Quadricep force improved more
whether daily training, using discharge not normally distributed) or between ICU discharge and
bedside cycle ergometer, is Treatment group received Fisher’s exact tests (comparing hospital discharge in treatment
safe/effective intervention in control group interventions plus proportions) group than control group
preventing or attenuating the cycling exercise session (5) days/ Spearman’s correlation Handgrip force not different
decrease in functional exercise week, using bedside cycle coefficients (95% CI) between treatment and control
capacity, functional status, and Isometric quadriceps force group at ICU discharge and
quadriceps force associated quantified using HHD in supine hospital discharge
with longer ICU stay position with 30 knee flexion; Handgrip force was not
instructions given to extend correlated with other outcome
knees maximally over 3-secs measures
with three repetitions At hospital discharge, quadricep
Berg Balance Scale (“from sit to force and SF-36 correlated
stand”) (r ¼ 0.46, p < 0.001) and the 6-
Physical Functioning item of the Minute Walking Distance test
Short Form-36 (SF-36) Health correlated with quadriceps force
Survey questionnaire (r ¼ 0.55, p < 0.001)
Chlan, L.L, Tracy, M.F., Prospective, descriptive, 120 subjects in (12) ICUs at (5) JAMAR Hydraulic Hand Descriptive statistics, graphing Median baseline grip strength

A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9

Guttormson, J. and Savik, K, correlational study hospitals in the Minneapolis-St Dynamometer (Patterson and mixed effects modeling diminished, ranging from 1 to
20157 September 2006eMarch 2011 Paul, Minnesota, area Medical) e serial measurements 102 pounds-force
Objective: (a) describe daily (participants were a subset from over time Pattern of grip strength indicated
peripheral muscle strength a randomized clinical trial on Used Mathiowetz et al.’s subjects either started at a higher
measurements in subjects self-management of anxiety standardized protocol to assess grip strength and their strength
receiving MV therapy; and, (b) using preferred, relaxing music, hand grip, using the mean of (3) declined or they started at a low
describe the relationships in patients receiving MV therapy) grip trials level of strength and either
among factors that influence Occupational Therapist consulted stayed low or further declined
ICU-AW to modify protocol for this Females grip strength was lower
study’s subjects than males
The older the patient, the grip
strength diminished
The longer on MV therapy, grip
strength was decreased
Did not have data on subjects’
activity level prior to ICU
admission nor on respiratory
muscle strength
De Jonghe, B., Bastuji-Garin, S., Prospective, observational study 2-medical ICUs, 1-surgical ICU, Maximal inspiratory/expiratory Categorical variables ¼ n (%) and Bedside measurement of muscle
Durand, M-C., Malissin, I., June 2003eJune 2005 1-medico-surgical ICU in two pressures and vital capacity compared using chi-square or strength at awakening revealed
Rodrigues, P., Cerf, C., Outin, H university hospitals and one Muscle strength measured in the Fisher’s exact test severed respiratory muscle
.. Group de Reflexion et university-affiliated hospital four limbs with MRC scale Median (IQR) used and compared weakness associated with limb
d’Etude des Neuromyopathies 116 consecutive patients after using the Mann-Whitney test weakness (median MRC
En Re; animation, 20079  7-days of MV Associations between MRC score ¼ 41 for 115 patients
Objective: (a) Assess severity of score’s and other inspiratory/ [99.1%]; IQR ¼ 21e52).
respiratory neuromuscu-lar expiratory pressures and vital Significant correlations between
function; (b) correlation capacity outcome measures MRC score inspiratory pressures
between respiratory and limb analyzed using Spearman’s (rho ¼ 0.35, p ¼ 0.001),
muscle strength. correlations and analysis of expiratory pressures (rho ¼ 0.49,
variance p < 0.0001), and vital capacity
(rho ¼ 0.31, p ¼ 0.007)
Low MRC score was an
independent predictor of delayed
successful extubation (odds ratio,
3.03; 95% CI, 1.23e7.43; p ¼ 0.02)
(continued on next page)

5
Table 2 (continued )

6
Research study Research design Sample and setting Methods/devices for Statistical analysis Main outcomes
measurement
Lee, J.L., Waak, K., Grosse- Prospective, observational study (95) patients in the 20-bed SICU Manual Muscle Testing (MMT), Multivariant logistic regression MMT reliably predicted in-
Sundrup, M., Xue, F., Lee, J., July 2011eOctober 2011 in a large tertiary AMC, who had JAMAR handgrip dynamometry used to identify which hospital mortality, number of
Chipman, D., Ryan, C . surgery and relatively low (Sammons, Illinois), sum score on independent variables (MMT and vent days, SICU length of stay
Eikermann, 201216 disease severity level the MRC scale to quantify MMT HHD) were associated with (LOS) and hospital LOS.
Objective: (a) evaluate the MV days varied from median 1.5 MMT completed in 95 patients mortality Logistic regression demonstrated
predictive value of strength (IQR, 0 to 4.5) to 3 (IQR, 1.5 to 8.4) (88.8%), 44 (46.3%) met cutoff for Spearman’s correlation used to as strength increased, mortality
measured by MMT and HHD at 18 years old ICU-AP (MRC < 48) median ¼ 48 identify indepen-dent variables decreased
ICU admission for in-hospital (IQR, 39.8 to 56.6) associated with SICU LOS, Grip strength and MMT-derived
mortality, SICU LOS; (b) MMT 80/94 patients (85.1%) ¼ ICU-AP hospital LOS and MV days strength measurements r ¼ 0.55,
and handgrip strength (12) muscle groups measured Lower level of disease severity p < 0.0001, but grip strength
measurements would be and lower grip strength than Ali didn’t predict patient outcomes
associated with hospital LOS study and in SICU
and MV days Sedation paused for exams for Handgrip strength was not
how long? independently associated with
Median time until strength mortality, LOS, MV days
testing could be reliably Global muscle weakness predicts
performed ¼ 3days (IQR, 2e5 mortality and MV duration in the
days) ICU
SICU and MICU data differ,

A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9

suggesting HHD strength is a
viable tool for predicting
mortality
Nordon-Craft, A., Schenkman, M., Case Series study 19 patients with ICU- AW who PT was provided by a therapist 5 Median (IQR), frequencies Lines/tubes temporarily
Ridgeway, K., Benson, A., and March 2008eFebruary 2009 required MV for at least 7-days,  days/week for 30 mins/session disconnected for mobility
Moss, M., 201120 18 years; 12 (63%) in MICU and 6 MRC scoring system, MMT, Criteria for progression of activity
Objective: (a) described safety (32%) SICU FTSST, FIM, TUG, 2MWT, based on the clinician’s judgment
and feasibility of participation FIM (Functional Independence of the patients’ physiological
in PT intervention for patients Measure) components measured response and cognitive status,
with ICU-AW with MV for at bed mobility, transfers, and gait). and patients’ subjective report of
least 7-days; (b) characterize Reliability of individual items of fatigue
the exam and intervention the FIM has not been established PT driven for initiating and early
procedures with sufficient FTSST, TUG and 2MWT tests used termination
detail that can be implement a to measure activity and balance PT intervention is safe and
similar strategy 2MWT correlates with the 6MWT feasible for patients with ICU-AW
(r ¼ 0.94) requiring MV for at least 7-days
PT exam and interventions done Team approach is necessary and
with PT, RN, RT and MD team critically ill patients can tolerate
members earlier mobilization than what
typically occurs
Most participants limited to
perform functional activities w/
baseline median FIM 2
Yosef-Brauner O, Adi N, Ben Prospective, single-blinded study (18) ICU subjects with MV > 48-h Subject’s family members were Descriptive statistics, change in No statistical difference found
Shahar T, Yehezkel E and June 2011eFebruary 2012 and expected to remain questioned regarding subject’s parameters between both groups between the two groups at
Carmeli E., 201529 ventilated  48 additional hours pre-hospital functional and between T1 and T2 and T1 baseline for MRC, dynamometry,
Objectives: evaluate the effect of (most were surgical subjects), parameters, Subjects were tested and T3. maximum inspiratory pressure
an intensive physical therapy randomly divided into (2) at (3) time periods: baseline (T1) Chi-square for nominal variables; and SB
protocol in subjects who groups: control and treatment for right and left hand grip Mann-Whitney for ordinal T1 and T2 demonstrated a
contract ICU-AW, in terms of >18-years old, independent strength using a Jamar variables and between groups; t- statistically significant
muscle strength, breathing and before admission, able to perform dynamometer (Lafayette, test for ratio variables and improvement (P < 0.05) for MIP
functional indices. simple commands, and had a IN), passive range of motion in between groups; and MRC in the treatment group;
 A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9 7

provide reliability in the assessment of strength in patients expe-

Coefficient; FTSST ¼ Five Times Sit to Stand Test; AMC ¼ Academic Medical Center; TUG ¼ Time Up to Go; 2MWT ¼ 2-Minute Walk Test; RN ¼ Registered Nurse; RT ¼ Respiratory Therapist; MD ¼ Medical Doctor; SB ¼ Sitting
Abbreviations: SD ¼ Standard Deviation; SICU ¼ Surgical Intensive Care Unit; IQR ¼ Interquartile Range; MICU ¼ Medical Intensive Care Unit; CI ¼ Confidence Interval; PT ¼ Physical Therapy; ICC ¼ Intraclass Correlation
only MIP parameter for T1 and T3

between MRC and MIP in T1 and

riencing weakness.4 However, grades 4e5 has been noted to not
Statistically significant decrease

between MRC and SB and MRC

and right hand dynamometry
demonstrate a similar reliability, especially in the critically ill pa-
Strong positive relationship

Strong negative correlation

tient population, requiring another assessment tool to validate
Trend towards decrease

findings regarding strength.4 Hand-held dynamometry (HHD), a

in the number of ICU
hospitalization days

standard method used to quantify the force or strength of hand grip

ventilation time

muscle strength, was used in seven studies in this review.1,3,4,6,7,16,29

This device measures handgrip strength and quadriceps force and
has been used in studies involving the critically ill patient popu-
lation6,24,25 and it has demonstrated high interrater reliability.17
tests

T2

Due to the difficulty in differentiating between the MRC 4e5

scores in the critically ill patient, HHD measurement was used in
Spearman’s rho for ratio variables
average differences between T1
Wilcoxon and t-test to describe

conjunction with the MRC scores in five out of the seven

and Pearson’s rho for ordinal
Correlations described using

studies.1,3,4,16,29 The MRC score was not used in two studies, how-
ever, the HHD measure was used in these studies.6,7 Three studies
and T2 and T1 and T3

used the MRC score along with maximum inspiratory pressure

(MIP) measurements.3,9,29 Measurement of MIPs, in addition to
using the MRC scale to measure muscle strength, revealed severe
respiratory muscle weakness associated with limb weakness.9
variables

The only randomized controlled trial (RCT) article included in

this review focused on safety and efficacy using a prescriptive cycle
ergometer (MOTOmed Letto 2, Germany) intervention to prevent
the decrease in functional exercise capacity, functional status (us-
the upright position, manual lung

breathing exercises, manual lung

and trunk exercises; (T3) done at

suctioning; (T2), performed after

measuring the same parameters

48e72 h, included subjects who
were 1 on the manual muscle

suctioning, sitting balance (SB)

ing the Berg Balance Scale), and quadriceps force in critically ill
hyperinflation and bronchial

subjects, measured at ICU and/or hospital discharge. Isometric

test, active joint exercises,

hyperinflation, bronchial

quadriceps force was quantified using a HHD (Microfet 2,

discharge from the ICU

Netherlands) and it was determined that quadriceps force

improved more between ICU discharge and hospital discharge in
as done in T2.

the treatment group (1.83  0.91 N kg1 vs. 2.37  0.62 N kg1,
p < 0.01) than in the control group (1.86  0.78 N kg1 vs.
2.03  0.75 N kg1, p ¼ 0.11).
There was one study that used three measurements, MMT, MRC
and HHD, to determine muscle strength in the SICU setting.16
Recognizing data from the SICU varied from findings in the MICU
examination score < 48 points.

in other studies, this study suggested that the HHD was a viable tool
for predicting mortality in the ICU setting.16 Another study used
MRC physical strength

four measures, MRC, HHD, maximum inspiratory pressure (MIP)

and sitting balance (SB), mainly in the SICU setting, over three time
intervals. In this study, the authors described no significant differ-
ence of these measures at baseline, however, Time 1 (T1, baseline)
and Time 2 (T2, after 48e72 h) demonstrated a statistically sig-
nificant improvement (p < 0.05) for MIP and MRC in the treatment
group, while only the MIP parameter for T1 and Time 3 (T3, time of
discharge from the ICU) tests showed a statistically significant
difference for T1 and T3. This study was also able to demonstrate a
statistically significant decrease in the number of ICU hospitaliza-
tion days and a trend towards decrease ventilation time.
There was only one study in which a measurement of physical
activity (i.e., bed mobility, transfers and gait) and muscle strength
was summarized, noting that patients who were discharged home
showed higher initial MMT and functional independence measure
(FIM) scores. In addition, this study used the MMT-summary score
instead of the MRC sum score because the MMT had a greater
incidence of detecting small and significant changes in patients
with ICU-AW. This was also the only article in this review that
identified criteria for progression of activity that included neuro-
muscular and cognitive status assessment, as well as the patient’s
subjective report of their fatigue.
The studies identified for the systematic review focused on
measurements of muscle strength in critically ill adults receiving
MV therapy, however, only one study examined the relationship
between muscle strength and the development of criteria for pro-
gression of activity. The outcome measures of the studies did not
Balance.

include active mobilization initiation, frequency or duration out of

the bed.
8 A.R. Roberson et al. / Heart & Lung 47 (2018) 1e9

Discussion with critical thinking skills and support of an interprofessional

team may provide safe and feasible early and progressive mobility
In the critically ill adult patient, several factors can be measured for the ICU patient, as demonstrated by the patient’s activity out of
that may identify the degree at which one will be able to determine the bed while on MV therapy. There is a need to develop a stan-
muscle strength. First, assessing patients’ ability to focus their dardized method for quantifying muscle strength and applying
attention on simple commands appears to be a principle factor to these results to determine the patient’s activity level (e.g., sitting on
determine prior to the initiation of any muscle strength measure- the edge of the bed, out of bed to chair or out of room ambulating a
ment. Each of the measurements used in the above studies requires specific distance). Evaluation of the relationship between muscle
that the patient comprehend how to perform the measurements to strength and mobility could provide translational tools to improve
provide an accurate return demonstration. Determining a patient’s early and progressive mobilization in this patient population.
comprehension abilities to accurately follow directions is impera- Of note, there were a range of different diagnoses and comor-
tive in scoring the measurements precisely. Whether using the bidities across the studies that are common across different ICU
Attention Screening Exam or a set of questions, identifying the settings. This supports the use of a standardized method to mea-
patient’s ability to accurately respond to commands is relevant in sure muscle strength and exploration of strength thresholds that
determining their ability to follow such commands related to may be related to, and possibly predict, mobilization readiness.
muscle activities. It is also worth considering using the CAM-ICU Standardizing the method to measure muscle strength in this pa-
(Confusion Assessment Method for the ICU) in its entirety to tient population also provides an opportunity for health care team
assess the overall mentation status.12 The CAM-ICU tool, a step- members to more clearly communicate the patients’ plan of care as
wise process that assesses multiple facets of a patient’s menta- it relates to early and progressive mobility.
tion, including determining if there are any acute mental status
changes, the patient’s attention to details/instruction, their level of
consciousness, and if any disorganized thinking exists.12 This tool Conclusions
will provide objective data to assess the patient’s readiness to
comprehend instructions given on how to perform the various While the purpose of this literature review was to identify fac-
muscle strength measures and it has demonstrated high interrater tors that influence muscle strength in the adult, critically ill patient
reliability.12 receiving MV therapy, it is quite clear that this is an area of science
Second, based on this literature review, muscle strength in the that requires additional research. There are very few articles
patient located in the medical and/or surgical ICU receiving MV addressing muscle strength in the critically ill adult patient
therapy can be measured using the MRC, MMT, HHD and MIP receiving MV therapy with the purpose of guiding their early and
measures. Although the MRC has limitations in the ICU patient progressive mobility activities. MMT, MRC and HHD appear to have
population, using the MRC in conjunction with a HHD and/or the positive benefits in quantifying these patients’ muscle strength
MIP techniques provides the objective measurements needed to with predictive value on their functional abilities. Additional
address these limitations. The HHD and MIP measurements can studies measuring muscle strength and its impact on early mobi-
also vary based on the patient’s strength during their acute phase of lization are needed in the adult intensive care settings with pa-
critical illness. However, these measures may better indicate the tients requiring MV therapy.
level of strength an acutely ill adult patient may be experiencing
and how this strength is improving over time during this phase of
their illness, further indicating the patient’s readiness to perform References
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