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doi: 10.2522/ptj.20110403Originally published online September 13, 20122012; 92:1546-1555.PHYS THER.

EikermannEdward A. Bittner, Ulrich Schmidt and MatthiasFeifei Xue, Jarone Lee, Daniel Chipman, Cheryl Ryan,Jeanette J. Lee, Karen Waak, Martina Grosse-Sundrup,Population in a Surgical Intensive Care UnitPredicts Mortality and Length of Stay in a GeneralGlobal Muscle Strength But Not Grip Strength

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Global Muscle Strength But Not Grip

Strength Predicts Mortality andLength of Stay in a General Populationin a Surgical Intensive Care UnitJeanette J. Lee, Karen Waak, Martina Grosse-Sundrup, Feifei Xue, Jarone Lee,Daniel Chipman, Cheryl Ryan, Edward A. Bittner, Ulrich Schmidt,Matthias Eikermann

Background. Paresis acquired in the intensive care unit (ICU) is common inpatients who are critically ill and independently predicts mortality and morbidity.

Manual muscle testing (MMT) and handgrip dynamometry assessments have beenused to evaluate muscle weakness in patients in a medical ICU, but similar data forpatients in a surgical ICU (SICU) are limited.

Objective. The purpose of this study was to evaluate the predictive value ofstrength measured by MMT and handgrip dynamometry at ICU admission forin-hospital mortality, SICU length of stay (LOS), hospital LOS, and duration of mechan-ical ventilation.

Design. This investigation was a prospective, observational study.

Methods. One hundred ten patients were screened for eligibility for testing in theSICU of a large, academic medical center. The Acute Physiology and Chronic Health

Evaluation (APACHE) II score, diagnoses, and laboratory data were collected. Mea-surements were obtained by MMT quantified with the sum (total) score on theMedical Research Council Scale and by handgrip dynamometry. Outcome data,

including in-hospital mortality, SICU LOS, hospital LOS, and duration of mechanicalventilation, were collected for all participants.

Results. One hundred seven participants were eligible for testing; 89% were testedsuccessfully at a median of 3 days (25th75th percentiles3 6 days) after admission.Sedation was the most frequent barrier to testing (70.6%). Manual muscle testing wasidentified as an independent predictor of mortality, SICU LOS, hospital LOS, and

duration of mechanical ventilation. Grip strength was not independently associatedwith these outcomes.

Limitations. This study did not address whether muscle weakness translates tofunctional outcome impairment.

Conclusions. In contrast to handgrip strength, MMT reliably predicted in-hospitalmortality, duration of mechanical ventilation, SICU LOS, and hospital LOS.

J.J. Lee, MD, Department of Anes-thesia, Critical Care & Pain Medi-cine, Harvard Medical School,Massachusetts General Hospital,

Boston, Massachusetts.K. Waak, PT, DPT, CCS, Depart-ment of Physical and Occupa-tional Therapy Services, Massa-chusetts General Hospital, 15Parkman St, WACC 136, Boston,MA 02114 (USA). Address all cor-respondence to Dr Waak at:[email protected].

M. Grosse-Sundrup, MD, Depart-ment of Anesthesia, Critical Care& Pain Medicine, Harvard MedicalSchool, Massachusetts GeneralHospital.

F. Xue, MD, Department of Anes-thesia, Critical Care & Pain Medi-cine, Harvard Medical School,Massachusetts General Hospital.

J. Lee, MD, Department of Anes-thesia, Critical Care & Pain Medi-cine, Harvard Medical School,Massachusetts General Hospital.

D. Chipman, RRT, Department ofRespiratory Care Services, Massa-chusetts General Hospital.

C. Ryan, RN, MSN, Department of

Clinical Nursing Services, Massa-chusetts General Hospital.

E.A. Bittner, MD, PhD, Depart-ment of Anesthesia, Critical Care& Pain Medicine, Harvard MedicalSchool, Massachusetts GeneralHospital.

Author information continues onnext page.

Critical IllnessSpecial Series

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Muscle weakness is an indepen-dent predictor of mortality inmany populations.13 This fact

is of particular interest in the intensivecare setting because patients who are

critically ill have been shown to have a50% to 80% risk of developing neuro-muscular abnormalities, includingparesis acquired in the intensive careunit (ICU).4 Paresis acquired in theICU is associated with increases inmorbidity and mortality and pro-longed mechanical ventilation5,6 andmay lead to impaired functional statuseven 1 year after hospital discharge.7,8

Modalities for quantifying musclestrength include quantitative mea-

sures of nonvolitional muscle forceand maximum voluntary contractionforce. Although nonvolitional mus-cle force assessments, including themeasurement of evoked contrac-tions of extremity muscles, may be

informative in patients with analtered level of consciousness,9 thesetechniques are not universally avail-able and require deep sedation andanalgesia.10 In contrast, maximum

voluntary contraction force can be

assessed readily at the bedsidethrough manual muscle testing(MMT) or handgrip dynamometry.

The sum (total) score on the MedicalResearch Council (MRC) Scale is a

valid and reliable method for quanti-fying MMT across a large range ofmuscles and predicts the outcomesof patients who are critically ill.11

Recent data have suggested that aless time-consuming approach to theassessment of muscle strength via

the measurement of handgripstrength may be a feasible alternativeto more comprehensive globalMMT.13,12,13

Handgrip strength has been used toapproximate total body musclestrength, but limited information isavailable on the predictive value of

MMT and handgrip strength mea-surements for the outcomes ofpatients in the surgical ICU (SICU).

Therefore, we conducted a prospec-tive study to test the hypothesis thatMMT and handgrip dynamometry

would predict in-hospital mortalityin a general population in the SICU.

Secondarily, we hypothesized thatMMT and handgrip strength mea-surements would be associated withlength of stay (LOS) and days on a

ventilator.

MethodMuscle strength testing is routinelyperformed in our 20-bed SICU at alarge, tertiary, academic medical cen-ter. The SICU admits trauma, trans-plant, and a variety of surgical pop-

ulations (thoracic, vascular,abdominal, gynecologic, and ortho-pedic surgery) from a large geo-graphic region. Between July andOctober 2011, we conducted a per-formance improvement initiative toevaluate whether grip strength orMMT assessment should be used infuture muscle strength testing in this

unit. During the 10-week period, allavailable patients in the SICU wereprospectively identified for potentialinclusion in the study. The Partners

Institutional Review Board (thehealth care system of which our facil-ity is a member) approved the obser-

vational performance improvement

Available WithThis Article atptjournal.apta.org

Listen to a special Craikcaston the Special Series on

Rehabilitation in Critical Carewith editor Patricia Ohtake.

eTable:Univariate Analysis ofOutcomes With High Versus LowManual Muscle Testing and GripStrength Measurements

eFigure 1:Predictive Value ofHandgrip Strength

eFigure 2:Scatterplot of ManualMuscle Strength Versus GripStrength

U. Schmidt, MD, PhD, Department of Anes-thesia, Critical Care & Pain Medicine, Har-vard Medical School, Massachusetts GeneralHospital.

M. Eikermann, MD, PhD, Department ofAnesthesia, Critical Care & Pain Medicine,

Harvard Medical School, MassachusettsGeneral Hospital, and Klinik fuer Anaesthesi-ologie und Intensivmedizin, Essen-DuisburgUniversity, Essen, Germany.

[Lee JJ, Waak K, Grosse-Sundrup M, et al.Global muscle strength butnotgrip strengthpredicts mortality and length of stay in ageneral population in a surgical intensivecare unit. Phys Ther.2012;92:15461555.]

2012AmericanPhysicalTherapyAssociation

Published Ahead of Print: September 13, 2012Accepted: September 4, 2012Submitted: November 14, 2011

Predictors of Mortality and Length of Stay in a Surgical Intensive Care Unit

December 2012 Volume 92 Number 12 Physical Therapy f 1547

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initiative and waived the need forinformed consent.

Demographic information, includingage, sex, and the presence of comor-bid conditions, was obtained fromthe medical records for all potentialparticipants. Additionally, the fol-

lowing data related to the currentSICU course were collected: AcutePhysiology and Chronic Health Eval-

uation (APACHE) II score, SICUadmission diagnosis, dates of hospi-tal admission and SICU admission,ICU discharge readiness date, num-ber of organs affected by the disease,and organ failure score.14 Laboratorydata recorded at SICU admissionincluded levels of hemoglobin(g/dL), albumin (g/dL), and creati-

nine (mg/dL); international normal-ized ratio (INR); and daily glucoselevels (mg/dL). These data wereselected because of published asso-ciations with the outcomes ofpatients in the intensive care set-ting.1521 Any use and duration ofmechanical ventilation wererecorded.

The participants had to be 18 yearsold or older and must have had no

known preexisting paralysis or exist-ing or new extremity amputation

(Fig. 1). Of the 110 patients screenedfor inclusion, 107 were included inthe study; 3 were excluded for thefollowing reasons (1 each): preexist-ing tetraplegia, prior amputationabove the knee, and behavioral

issues. Enrollment continued until95 participants successfully com-pleted strength testing to ensure ade-

quate power. Participant demo-graphics, comorbidities, SICUadmission diagnoses, presence oforgan failure, APACHE II scores, andlaboratory data are shown in Table 1.

All clinical testing was completed byan experienced physical therapist(K.W.) or an anesthesiologist/critical

care fellow (J.J.L.). The followingmeasurements were collected dur-ing testing: Richmond AgitationSedation Scale (RASS) score, MMT,and handgrip dynamometry. Partici-pants were typically identified

within 48 hours after ICU admission,upon which the tester examined aparticipants arousal with the RASS.

If the participant was sufficientlyalert (RASS score of at least 1),attention and the capacity to follow

instructions were screened by askingthe participant to follow a series of 1-and 2-step instructions. Using a mod-ified version of the approachdescribed by De Jonghe et al,22 we

deemed the participants ready forstrength testing if they were able torespond to 3 of 3 instructions cor-rectly. If a participants arousal orcapacity to follow instructions wasnot sufficient to complete the test-ing, then the screening was repeatedon subsequent days until 1 of 3 con-ditions was met: the participanttransferred from the unit, the partic-

ipant was able to be tested success-fully, or the participant passed away.

All strength measures for a given par-

ticipant (MMT and handgrip) werecompleted in the same session. Anybarriers to testing on a given day,including sedation, delirium, lack ofavailability of participants, andhemodynamic instability, were

noted. All bedside examinationswere completed during the SICUadmission. When clinically indicatedand appropriate, continuous seda-tion drips were paused before theexaminations. Outcome data, includ-

ing SICU LOS, hospital LOS, mechan-ical ventilation days, and in-hospitalmortality, were collected from the

medical records for all participants.

RASSThe RASS is a valid and reliable toolfor categorizing sedation and agita-tion levels in patients in the ICU;scores range from 5 (not able to bearoused) to 4 (combative).23

MMTThe MRC Scale is an MMT gradingsystem mentioned extensively in thecritical care literature, in which ithas been reported to be a valid mea-sure of strength. The scale uses ascoring system from 0 to 5: 0nomuscle contraction, 1trace con-traction, 2movement with gravity

eliminated, 3movement againstgravity, 4movement against gravityand manual resistance, and 5

110 participants eligible

107 participants screenedfor testing

95 participants completedtesting during SICU

admission

3 participants excluded:preexisting tetraplegia (n=1)prior above knee amputation (n=1)behavioral issues (n=1)

12 participants unable to completeentire SICU stay due to:deceased before testing (n=2)altered mental status (n=9)unavailable for testing (n=1)

Figure 1.Enrollment of study participants. SICUsurgical intensive care unit.



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normal strength. In accordance with apreviously validated version of thescale,24 we tested 12 muscle groups:shoulder abductor, elbow flexor, wristextensor, hip flexor, knee extensor,

and ankle dorsiflexor muscles bilater-ally. For each participant, the totalstrength score out of 60 was recorded.During the examinations, the partici-pants were repositioned as needed tofacilitate testing and to manipulate theinfluence of gravity based on perfor-mance. The MRC Scale was chosenbecause of its relative ease for bedsideadministration and its established rela-

tionship with weakness acquired inthe ICU. De Jonghe et al22 reportedthat an MRC Scale sum (total) score of

less than 48 during MMT is sensitivefor the identification of ICU-acquired

weakness.

An experienced strength examiner(K.W.) served as the reference rater

and provided the team with compre-hensive hands-on and didactic train-ing in MMT. Hermans et al25

reported excellent interrater reliabil-ity when trained examiners usedMMT with the MRC Scale grading

system to examine patients whowere critically ill.

Handgrip DynamometryA Jamar dynamometer (SammonsPreston Rolyan, Bolingbrook, Illi-nois) was used for all handgrip mea-surements. Participants were tested

with the dominant hand unless thatmethod was not feasible because offractures. Examiners demonstratedand verbally explained the task

before testing. Participants werepositioned as close to upright as pos-sible, with the shoulder in neutralrotation at the participants side andthe elbow at 90 degrees of flexion.Participants were provided verbalencouragement to squeeze the dyna-mometer tightly for 2 or 3 seconds.The highest value (in kilograms)

from 3 trials was recorded. The dyna-mometer handle was placed in thesecond position to allow comparison

Table 1.Demographics and Characteristics of Participantsa

Characteristic Value

Age, y, X (SD) 61.2 (18.3)

Male:female ratio 59:48

APACHE II score, X (SD) 15.2 (9.0)

Comorbidities

Diabetes mellitus 21 (19.6)

Coronary artery disease 22 (20.6)

Chronic obstruct ive pulmonary disease 26 (24.3)

Peripheral vascular disease 12 (11.2)

Chronic kidney disease 15 (14.0)

Psychological disease 15 (14.0)

Musculoskeletal disease 12 (11.2)

Other 37 (34.6)

Admission diagnoses

Postsurgery 70 (65.4)

Trauma 13 (12.1)

Sepsis 11 (10.3)

Respiratory failure 28 (26.2)

Acute coronary syndrome 1 (0.9)

Hemodynamic instability 25 (23.4)

Bowel obstruction 6 (5.6)

Pancreatitis 4 (3.7)

Other 7 (6.5)

Admission laboratory values, X (SD)

Hemoglobin 11.0 g/dL (2.0)

Creatinine 1.2 mg/dL (1.0)

International normalized ratio 1.2 (0.4)

Albumin 3.3 g/dL (0.8)

Daily laboratory value for glucose, X (SD) 132.0 mg/dL (36.1)

Organ failure

Any organ failure 86 (88)

Respiratory 52 (53)

Cardiovascular 53 (54)

Renal 12 (12)

Neurologic 12 (12)

Hepatic 2 (2)

Hematologic 6 (6)

Infectious 18 (18)

ODIN score, X (SD) 1.46 (1.23)

aValues are reported as number (percentage) of 107 participants unless otherwise noted.APACHEAcute Physiology and Chronic Health Evaluation, ODIN scoreorgan dysfunction and/orinfection score for people in an intensive care unit.14





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with published normative values inaccordance with published recom-mendations, such as those of the

American Society of Hand Thera-pists.2628 Handgrip dynamometers

have been shown to have very goodinterrater reliability in the ICUsetting.25

Data AnalysisA power analysis was performedbefore the initiation of the study. Onthe basis of our institutional data, weexpected a mortality rate of 18%. Wecalculated that a sample size of 95

examined participants would pro-vide 80% power to detect an associ-ation between grip strength or MMT

and mortality with a 2-tailed Pvalueof less than .05.

Data were analyzed with the SPSSstatistical software program (version13.0, SPSS Inc, Chicago, Illinois) and

STATA 10 (StataCorp LP, College Sta-tion, Texas). Our primary hypothesis

was that the measurement ofstrength through MMT and handgripdynamometry in participants who

were alert early after admission

would be associated with in-hospitalmortality (dependent variable). Sec-ondarily, we hypothesized that the

MMT and handgrip measurementswould be associated with days on aventilator, SICU LOS, and hospitalLOS (dependent variables). Simplelogistic regression was used to iden-tify which of the prospectivelydefined independent variables wasassociated with mortality. The Spear-man correlation was used to identify

independent variables associatedwith SICU LOS, hospital LOS, anddays on a ventilator. The followingindependent variables wereincluded in our prospectivelydefined, initial analysis: creatinine,INR, albumin, MMT, APACHE IIscore, hemoglobin, glucose, age,organ failure score, and grip

strength. Significant predictors(P.05) were subsequently includedin our multivariate analysis.

A multivariate analysis was under-taken to determine which of theindependent variables remainedassociated with the dependent vari-ables after controlling for other inde-

pendent variables. A forward step-wise regression approach was usedto construct the multivariate models.Zero-truncated Poisson regressionmodels were used to identify inde-pendent predictors of SICU LOS,hospital LOS, and days on a ventila-tor, and logistic regression was usedto evaluate independent predictorsof in-hospital mortality. Zero-

truncated Poisson regression is usedto model count data in conditions in

which the value 0 cannot occur,

such as LOS in a hospital or an ICU.29

The adequacy of model goodness offit was evaluated with the Hosmer-Lemeshow chi-square test for logisticregression and the Pearson chi-square test for the Poisson regression

models. Testing for multicollinearitywas performed for each multivariatemodel by calculation of a varianceinflation factor for each independent

variable in the model. A varianceinflation factor of greater than 10

was used to indicate excessive mul-ticollinearity. Receiver operatingcharacteristic curve analysis was

used to compare the predictive abil-ities of MMT and the APACHE IIscore for mortality; the areas underthe curve were compared statistically.

ResultsApproximately two thirds of ourstudy population was admitted tothe SICU for recovery after a major

surgical procedure. The most com-mon admission diagnoses wererespiratory failure (26.2%) andhemodynamic instability (23.4%).The overall in-hospital mortality ratein the cohort was 9.3%. The medianSICU LOS was 5 days (25th75th per-centiles39.5 days), and the totalnumber of days in the SICU was 970.

The median hospital LOS was 13days (25th75th percentiles824days). When all participants were

included in the analysis, a median of1.5 days (25th75th percentiles0 4.5 days) of mechanical ventilation

was required. When the analysis wasrestricted to participants requiring at

least 0.5 day of mechanical ventila-tion, the median duration of mechan-ical ventilation was 3 days (25th75th percentiles1.58.4 days).

MMT Measurements of StrengthManual muscle testing was success-fully completed in 95 participants(88.8% of 107), 44 of whom (46.3%)met the cutoff for ICU-acquired pare-

sis, as defined by an MRC Scale sumscore of less than 48.22 The medianMRC Scale sum score was 48 (mini-

mum0, maximum60; 25th75thpercentiles39.856.6). AlthoughMMT measurements were success-fully obtained in 95 participants,they typically could not be com-pleted on the day after admission.

The median time until strength test-ing could be reliably performed

was 3 days (minimum1 day, maxi-mum80 days; 25th75th percen-tiles25 days). The barriers mostfrequently contributing to observed

delays were as follows: sedation,with a RASS score of less than 1(70.6%); lack of availability of partic-

ipants, such as from additional sur-geries (14.4%); hemodynamic insta-bility (5%); and delirium, withdecreased attention or decreasedability to follow instructions (2.3%).

In the univariate analysis, mortalitywas associated with serum creati-nine, albumin, and MMT. Both SICU

LOS and hospital LOS were associ-ated with INR, albumin, APACHE IIscore, and MMT. Hospital LOS wasalso associated with hemoglobin(Tab. 2). The number of days onmechanical ventilation was associ-ated with creatinine, INR, albumin,

APACHE II score, and MMT.

The multivariate analysis demon-strated that MMT was the only vari-able that was independently associ-



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ated with mortality (P.04) and dayson a ventilator (P.01). Manual mus-cle testing and albumin indepen-dently predicted both SICU LOS

(P.001) and hospital LOS(P.001), and INR was also associ-ated with hospital LOS (P.001)(Tabs. 3 and 4, Fig. 2). No evidenceof multicollinearity was identified foreach multivariate model.

In an additional univariate analysiswith group stratification (partici-

pants with an MRC Scale sum scoreof48 and those with an MRC Scalesum score of 48), MMT remainedsignificantly associated with dayson a ventilator, hospital LOS, andSICU LOS ( eTable, available atptjournal.apta.org).

Logistic regression demonstrated

that strength was protective againstmortality; as strength increased, mor-tality decreased. For each 1 unitincrease in strength, there was a 5%relative decrease in the odds of mor-tality (Tab. 3). To better understandthe relationship between MMT andmortality, we collapsed the MRCScale sum score into quartiles and

assigned the participants to the quar-tiles on the basis of their sum scores(015, 1630, 3145, and 4660).

Table 2.Univariate Analysis of Mortality, Length of Stay (LOS) in the Surgical Intensive Care Unit (SICU), and LOS in the Hospitala

Parameter

Mortality SICU LOS Hospital LOS

OR SE P 95% CI r P 95% CI r P 95% CI

Creatinine (mg/dL) 1.73 0.41 .02b 1.07 to 2.75 .19 .05 0.001 to 0.36 .15 .13 0.04 to 0.33

INR 1.26 0.80 .72 0.36 to 4.40 .24 .02b 0.04 to 0.41 .31 .002b 0.11 to 0.47

Albumin (g/dL) 0.32 0.15 .02b 0.13 to 0.80 .25 .02b 0.44 to 0.04 .32 .004b 0.50 to 0.10

MMT 0.94 0.02 .006b 0.89 to 0.98 .31 .002b 0.48 to 0.12 .33 .001b 0.50 to 0.13

APACHE II score 1.06 0.04 .07 0.99 to 1.13 .44 .001b 0.25 to 0.59 .39 .001b 0.18 to 0.55

Hemoglobin (g/dL) 0.74 0.14 .12 0.50 to 1.07 .11 .25 0.29 to 0.07 .24 .01b 0.41 to 0.04

Glucose (mg/dL) 1.00 0.01 1.00 0.98 to 1.01 .15 .15 0.04 to 0.32 .02 .81 0.17 to 0.21

Age (y) 1.03 0.02 .14 0.98 to 1.08 .09 .33 0.28 to 0.09 .11 .29 0.29 to 0.09

Grip (kg) 1.00 0.03 .74 0.93 to 1.04 .06 .55 0.26 to 0.14 .05 .65 0.25 to 0.16

a ORodds ratio, SEstandard error, CIconfidence interval, rSpearman correlation, INRinternational normalized ratio, MMTmanual muscle testing,APACHEAcute Physiology and Chronic Health Evaluation.b Significant at P.05.

Table 3.Multivariate Analysis of In-hospital Mortalitya

Parameter OR SE zScore P 95% CI

MMT 0.95 0.02 2.02 .04b 0.900.99

Albumin (g/dL) 0.48 0.27 1.29 .19 0.151.45

aA logistic regression model for evaluating independent predictors of outcome was used. The Hosmer-Lemeshow chi-square goodness-of-fit test showed adequate model fit (P.49). ORodds ratio,SEstandard error, CIconfidence interval, MMTmanual muscle testing.b Significant at P.05.

Table 4.Multivariate Analysis of Length of Staya

Parameter IRR SE zScore P 95% CI

SICU

MMT 0.98 0.00 7.29 .001b 0.970.98

Albumin (g/dL) 0.68 0.03 6.62 .001b 0.610.76

APACHE II 0.99 0.00 0.21 .83 0.991.00

Hospital

MMT 0.97 0.00 13.63 .001b 0.970.98

Albumin (g/dL) 0.82 0.03 4.87 .001b 0.760.89

INR 1.17 0.05 3.49 .001b

1.071.29

APACHE II 1.00 0.00 1.80 .07 0.991.01

a Zero-truncated Poisson regression models for evaluating independent predictors were used. ThePearson chi-square goodness-of-fit test showed adequate model fit for the surgical intensive care unit(SICU) analysis (P.28) and the hospital analysis (P.31). IRRincidence rate ratio, SEstandard error,CIconfidence interval, MMTmanual muscle testing, APACHEAcute Physiology and Chronic HealthEvaluation, INRinternational normalized ratio.b Significant at P.05.



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This analysis confirmed that partici-

pants in the 2 lowest quartiles hadhigher mortality rates than those inthe 2 highest quartiles (40% and16.7% versus 4.2% and 3.5%). On thebasis of the initial data, receiveroperating characteristic curve analy-sis was used to compare the predic-tive abilities of MMT and the

APACHE II score for mortality given

that the latter is widely used to pre-dict mortality risk in the critical caresetting.30 There was no significant

difference in the areas under the 2

receiver operating characteristiccurves (0.73 for MMT and 0.89 forthe APACHE II score; 20.99,

P.32).

Grip StrengthGrip strength could be measured in94 participants (87.9% of 107), 52 of

whom (55.3%) had a grip strength of

0 kg. On the basis of published age-and sex-predicted normative valuesin volunteers who were healthy,28

our study participants had grip

strength measurements that, on aver-age, were 11.6% (range0%89%)of predicted values. Neither the gripstrength value nor the grip strengthderived dichotomous variable ICU-acquired paresis classification (gripstrength of11 kg of force in menand 7 kg of force in women31) wasassociated with mortality, LOS, or

days on a ventilator (Tab. 2; eTable;eFig. 1, available at ptjournal.apta.org).

Figure 2.Predictive value of theMedical Research Council (MRC) Scale. (A)Relationship between MRCScale sum score andmortality. Quartiles(boxes), medians (lines within boxes), and 10th and 90th percentiles (error bars; outliers are represented by open circles) wereplotted. The MRC Scale sum score correlated with mortality and was significantly higher in survivors. (B) Scatterplot of MRC Scalesum score versus hospital length of stay (LOS). Stepwise forward multiple regression analysis revealed that the MRC Scale sum scorewas negatively correlated with hospital LOS (z13.63, P.001). (C) Scatterplot of MRC Scale sum score versus surgical intensivecare unit (SICU) LOS. Stepwise forward multiple regression analysis revealed that the MRC Scale sum score was negatively correlatedwith SICU LOS (z7.29, P.001). MMTmanual muscle testing.



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Grip strength and MMT-derivedstrength measurements were corre-lated (r.55, P.0001), but gripstrength did not predict the out-comes of participants in the SICU.

The MRC Scale sum score in thegroup of participants who had a gripstrength of 0 kg ranged from 0 to 60;an analysis demonstrated a limitedassociation between the 2 measuresfor participants with low gripstrength measurements (eFig. 2,available at ptjournal.apta.org).Using previously published cutoff

values for the classification of ICU-

acquired paresis by handgrip dyna-mometry (Ali et al31), we categorized80 of 94 participants (85.1%) as hav-

ing ICU-acquired paresis.

Additional LOS AnalysisReliable strength measurements wereobtained later in the ICU stay in par-ticipants for whom ICU-acquired pare-

sis was suggested by MMT22 than inparticipants without weakness (6.3[SD13] days versus 2.9 [SD2]days). In response to this finding, weconducted an additional data analysis.

A regression analysis revealed that the

time between ICU admission and suc-cessful strength measurements did notexplain the independent variance of

mortality, LOS, or days on a ventilator.In addition, a subgroup analysis of par-ticipants for whom valid strength mea-surements were obtained during thefirst 3 days of their hospital stay(n64) revealed that MMT still pre-dicted the number of days on a venti-lator (P.01) and SICU LOS (P.03).In addition, there was a trend toward

the prediction of hospital LOS(r.23,P.06). These findings sup-port the view that strength predictsthe outcomes of people in the ICUrather than reflecting the conse-quences of muscle wasting in the ICU.

DiscussionFor participants in the SICU, we

found that MMT reliably predictedin-hospital mortality, the number ofdays on a ventilator, SICU LOS, and

hospital LOS. Handgrip strength wasnot independently associated withany of the outcomes measured.These results confirmed findings sug-gesting that global muscle weakness

predicts mortality13

as well as theduration of mechanical ventila-tion22,32 in people in the ICU.

Similar to our previous observationsin the SICU,33 the data from the pres-ent study are at odds with findings inthe medical ICU,31,34,35 which sug-gested that handgrip strength is a

viable tool for predicting mortality in

people in the ICU. More specifically,Ali et al31 demonstrated that bothhandgrip strength and MMT mea-

surements are independently associ-ated with outcomes, includingin-hospital mortality. The differencesin the study findings may have beendue, in part, to the different popula-tions studied. In the study of Ali et

al,31 the patients were in a medicalICU, had a high level of illness sever-ity (APACHE III score of 65.8), andreceived mechanical ventilation forat least 5 days. In the present study,the participants were in a SICU and

had a lower average level of diseaseseverity (mean APACHE II score of15.2); these data translated to a pre-

dicted mortality rate that wasapproximately 50% lower than thatof the patients studied by Aliet al.31,36,37 Although the same dyna-mometer was used in both studies,

we obtained low grip strength mea-surements; 55% of the participants inthe present study had a grip strengthof 0 kg, whereas Ali et al31 reported

that 26% of the patients in their studyhad a grip strength of 0 to 5 kg.

Interestingly, in the present study, agrip strength of 0 kg for many partici-pants in the SICU was associated withacceptable or even normal MMT mea-surements, underlining the issue ofthe low resolution of grip strength

measurements for lower levels of mus-cle strength.38 Grip strength may notalways be a valid representative of

total body strength.39 One possibleexplanation for the rather low gripstrength measurements relates to theconcept of task-specific training. Inthe present study, people in the SICU

were routinely asked to participate inMMT examinations and functionalmobility tasks, such as transfers andambulation, when possible. Task-specific training equivalent to handgrip dynamometry is not routinelyincorporated.40 In addition, it is possi-ble that the effects of drugs (eg, resid-ual neuromuscular blocking agents)compromised the tetanic force that is

tested during grip strength measure-ments but allowed sufficient musclefunction during submaximal contrac-

tions to produce comparatively higherMMT measurements. The effects ofresidual neuromuscular blockade onmuscle strength are significantlygreater during maximum (tetanic)contractions than during submaximal

contractions.41

For 46% of the participants in thepresent study, the diagnosis of ICU-acquired paresis (based on the crite-rion of an MRC Scale sum score of

less than 4822) was met, and theseparticipants had a significantly lon-ger LOS and longer duration of

mechanical ventilation than thosefor whom this criterion was not met.The overall incidence of clinical

weakness was within the range of25.3% to 50% reported in other stud-ies, including studies of patients withsepsis, multiorgan failure, orextended mechanical ventila-tion.22,31,32,42 The present study

showed that in the SICU, muscleweakness occurs early, and this tim-ing seems to be different from that inthe medical ICU. We speculate thatsurgical pain, tissue trauma, effectsof drugs, and inflammatory media-tors may have affected muscle per-formance during MMT. In previousstudies, even in the absence of a high

level of critical illness severity, weobserved muscle weakness resultingfrom residual effects of drugs.41,43



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Reliable strength measurementswere obtained later in participantsfor whom MMT measurements indi-cated ICU-acquired paresis22 than inparticipants without weakness (6.3

[SD

13] days versus 2.9 [SD

2]days). Multiple barriers to successfulstrength examinations contributedto testing delays. The barriersincluded low level of arousal; delir-ium, with inattention or inabilityto adequately follow instructions;hemodynamic instability; and lack ofavailability of participants. Thesebarriers were encountered despite

the goals in the SICU of minimizingsedation and managing delirium.Similarly, Hough et al44 noted inat-

tention as a barrier to MMT in 62 of135 eligible patients who were in theICU and received mechanical venti-lation for at least 3 days. The presentstudy showed that examination tim-ing did not represent a confounding

variable with respect to our goal ofusing muscle strength measurementsto predict outcomes. Regressionanalysis revealed that the timebetween ICU admission and success-ful strength measurements did not

explain the independent variance inoutcomes. In addition, a subgroupanalysis of participants tested within

3 days showed that MMT measure-ments obtained during this time pre-dicted the number of days on a ven-tilator as well as ICU LOS. Thesefindings support the view thatstrength predicts the outcomes ofpeople in the ICU rather than reflect-ing the consequences of muscle

wasting in the ICU.

Other instruments that can be rea-sonably used to predict mortalityearly after ICU admission include the

APACHE II score and the SICU opti-mal mobility score, both of whichhave been validated for predictingmortality in people in the ICU whenobtained at day 1 after admission.33

In the present study, the APACHE IIscore did not independently predict

mortality when MMT was added tothe model.

We found that the plasma albuminconcentration also independently pre-

dicted SICU LOS and hospital LOS.Similarly, the albumin level has beenshown to be a reliable prognostic toolfor predicting mortality and morbidityin patients after surgery and patients

with pneumonia.45,46Additionally, theINR was found to independently pre-dict hospital LOS. The INR was shownto be associated with ICU mortality inanother study.47

LimitationsThe present study was not under-

taken to diagnose ICU-acquired pare-sis or critical illness polyneuromy-opathy. We did not measure musclestrength before admission, did notobtain routine electrodiagnosticstudies, and did not conduct longitu-

dinal follow-up measurements. Itwould be interesting to evaluate thepredictive value of muscle strengthfor long-term morbidity, includingfunctional outcomes, in a surgicalpopulation. The present study

included only people who hadundergone surgery and had a rela-tively low level of disease severity;

therefore, the results of the presentstudy may not be generalizable to amedical ICU population or an ICUsubgroup with a higher level of dis-ease severity. We did not formallyestablish interrater reliability amongthe clinicians who evaluated musclestrength. However, there is suffi-cient literature stating that both

MMT and handgrip strength havegood interrater reliability.4850 Theuse of the highest grip strength valueobtained for each participant in thedata analyses may have resulted inmeasurement bias.

In summary, the present studyshowed that in the SICU, the global

assessment of muscle strength byMMT rather than grip strength mea-surements alone predicts mortality,

days on a ventilator, ICU LOS, andhospital LOS. Further studies areneeded to identify whether interven-tions that specifically target musclestrength, including physical therapy,

affect these and other outcomes ofpeople in the SICU.

Dr Jeanette J. Lee and Dr Waak contributedequally to taking measurements and writingthe article. Dr Waak, Dr Jarone Lee, DrSchmidt, and Dr Eikermann provided con-cept/idea/research design. Dr Grosse-Sundrup, Dr Xue, Dr Jarone Lee, Dr Bittner,and Dr Eikermann also provided writing. DrJeanette J. Lee, Dr Waak, Dr Grosse-Sundrup,Dr Jarone Lee, and Mr Chipman provideddata collection. Dr Grosse-Sundrup, Dr Xue,Dr Jarone Lee, Dr Bittner, and Dr Eikermann

provided data analysis. Dr Waak and Dr Eik-ermann provided project management. DrJeanette J. Lee and Dr Waak provided studyparticipants. Dr Eikermann provided institu-tional liaisons. Dr Grosse-Sundrup, Ms Ryan,Dr Schmidt, and Dr Eikermann providedconsultation (including review of manuscriptbefore submission). The authors thank John

Anderson-Dam, MD, for his technical assis-tance with data formatting.

The Partners Institutional Review Boardapproved the observational performanceimprovement initiative.

An abstract poster presentation was given at

the Annual Meeting of the American Societyof Anesthesiologists; October 1317, 2012;

Washington, DC.

DOI: 10.2522/ptj.20110403

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doi: 10.2522/ptj.20110403

Originally published online September 13, 20122012; 92:1546-1555.PHYS THER.

EikermannEdward A. Bittner, Ulrich Schmidt and MatthiasFeifei Xue, Jarone Lee, Daniel Chipman, Cheryl Ryan,Jeanette J. Lee, Karen Waak, Martina Grosse-Sundrup,Population in a Surgical Intensive Care UnitPredicts Mortality and Length of Stay in a GeneralGlobal Muscle Strength But Not Grip Strength

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