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The interobserver agreement of handheld dynamometry for muscle strength assessment in critically ill patients

Goele Vanpee, MSc, PT; Johan Segers, MSc, PT; Helena Van Mechelen, MSc, PT; Pieter Wouters, MSc, RN; Greet Van den Berghe, PhD, MD; Greet Hermans, PhD, MD; Rik Gosselink, PhD, PT
Objective: Muscle weakness often complicates critical illness and is associated with increased risk of morbidity, mortality, and limiting functional outcome even years later. To assess the presence of muscle weakness and to examine the effects of interventions, objective and reliable muscle strength measurements are required. The rst objective of this study is to determine interobserver reliability of handheld dynamometry. Secondary objectives are to quantify muscle weakness, to evaluate distribution of muscle weakness, and to evaluate gender-related differences in muscle strength. Design: Cross-sectional observational study. Setting: The surgical and medical intensive care units of a large, tertiary referral, university hospital. Patients: A cross-sectional, randomly selected sample of awake and cooperative critically ill patients. Interventions: None. Measurements and Main Results: Handheld dynamometry was performed in critically ill patients who had at least a score of 3 (movement against gravity) on the Medical Research Council scale. Three upper limb and three lower limb muscle groups were tested at the right-hand side. Patients were tested twice daily by two independent raters. Fifty-one testretests were performed in 39 critically ill patients. Handheld dynamometry demonstrated good interobserver agreement with intraclass correlation coefcients >0.90 in four of the muscle groups tested (range, 0.91 0.96) and somewhat less for hip exion (intraclass correlation coefcient, 0.80) and ankle dorsiexion (intraclass correlation coefcient, 0.76). Limb muscle strength was considerably reduced in all muscle groups as shown by the median z-score (range, 1.08 to 3.48 SD units). Elbow exors, knee extensors, and ankle dorsiexors were the most affected muscle groups. Loss of muscle strength was comparable between men and women. Conclusions: Handheld dynamometry is a tool with a very good interobserver reliability to assess limb muscle strength in awake and cooperative critically ill patients. Future studies should focus on the sensitivity of handheld dynamometry in longitudinal studies to evaluate predictive values toward patients functional outcome. (Crit Care Med 2011; 39:1929 1934) KEY WORDS: critical illness; muscle weakness; muscle strength dynamometer; reproducibility of results; intensive care; isometric contraction

ritically ill patients treated in an intensive care unit (ICU) often develop muscle weakness (1), which is associated with an increased duration of mechanical ventilation and ICU stay (2), mortality (3), and might impair functional status even years later (4). Early mobilization and exercise training have been shown to attenuate limb muscle atrophy (5), decrease ICU and hospital stay (6), and im-

From the Departments of Rehabilitation Sciences (GV, JS, HVM, RG), Intensive Care Medicine (PW, GVdB), and Medical Intensive Care Unit of the Department of General Internal Medicine (GH), University Hospitals Leuven, Katholieke Universiteit Leuven, Leuven, Belgium. The authors have not disclosed any potential conicts of interest. For information regarding this article, E-mail: rik.gosselink@faber.kuleuven.be Copyright 2011 by the Society of Critical Care Medicine and Lippincott Williams & Wilkins DOI: 10.1097/CCM.0b013e31821f050b

prove functional outcome at hospital discharge (7, 8). A study by Morris et al (6) suggests regular strength measurements to guide the clinical process of early exercise training and mobilization. Therefore, reliable and objective strength measurements are required. The Medical Research Council (MRC) scale is a categorized scale to assess the entire range of muscle strength, from 0 (no visible or palpable muscle contraction) through 5 (movement through the complete range of motion against gravity and maximal resistance) (9, 10). The MRC scale is a reliable and valid method to detect clinical signicant muscle weakness in patients treated in the ICU and is related to outcome (2, 3, 11, 12). However, when MRC scores exceed grade 3 (movement against gravity), the MRC loses much of its ability to discriminate between gradations of strength (13, 14). Therefore, additional assessment tools are necessary to measure muscle

strength of upper and lower limb muscle groups that are powerful enough to overcome gravity (MRC 3). Handheld dynamometry (HHD) has been designed to assess maximal isometric limb muscle strength objectively (15). Interobserver reliability has been studied in healthy subjects (intraclass correlation coefcient [ICC], 0.77 0.88) (16), elderly (ICC, 0.48 0.94) (17), football players (ICC, 0.66 0.87) (18), and neurologic patients (ICC, 0.69 0.99) (19 21). To our knowledge, interobserver reliability of HHD has not yet been studied in critically ill patients who are being treated in the ICU. The rst objective of this study is to examine the interobserver reliability of the handheld electronic dynamometer between two physiotherapists in patients treated in the surgical and medical ICUs of a university hospital. Secondary objectives are to quantify muscle weakness by comparing the obtained muscle strength
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Table 1. Test positions Muscle Action Shoulder abduction Elbow exion Wrist extension Hip exion Knee extension Ankle dorsiexion Extremity/Joint Positions Shoulder abducted 45, elbow fully extended Shoulder neutral, elbow 90, forearm supinated Shoulder neutral, elbow 90, wrist neutral Hip exed 90, knee exed 90, contralateral hip neutral Hip exed 90, knee exed 90, contralateral hip neutral Hip and knee fully extended, ankle neutral Location of Dynamometer Application Just Just Just Just Just Just proximal proximal proximal proximal proximal proximal to to to to to to later epicondyle of humerus styloid processes metacarpophalangeal joints femoral condyles malleoli metatarsophalangeal joints

values of critically ill patients with reference values obtained by Bohannon (15), evaluate the distribution of muscle weakness across muscle groups, and compare loss of muscle strength between men and women.

MATERIALS AND METHODS


Patient Selection. Critically ill patients, being treated in the medical or surgical ICU for at least 7 days, were recruited for the purpose of reliability testing of HHD. All patients were included in an ongoing randomized controlled trial examining two feeding strategies (ClinicalTrials.gov:NCT00512122) and constituted a cross-sectional, randomly selected sample. Analgetics and sedatives were administered according to the local clinical guidelines. Isometric muscle strength of three upper and three lower limb muscle groups was measured at the right-hand side. Before testing, each patient was screened for adequacy by the response to ve questions (open and close your eyes, look at me, nod your head, stick out your tongue, raise your eyebrows when I have counted up to ve) (12). A score of 5 on the ve questions was required to participate in the study. A score of 3 on the MRC scale was required in at least four of six muscle groups being tested. If patients were limited to generate an isometric contraction on the right side as a result of an orthopedic or focal neurologic problem, isometric muscle strength of the affected joints was measured at the lefthand side. Furthermore, patients with preexisting neuromuscular diseases, musculoskeletal conditions, cardiovascular instability (mean arterial pressure 60 mm Hg or FIO2 60% or PaO2/FIO2 200), anxiety, extreme shortness of breath, or hypoxemia (SaO2 90%), were excluded from testing. Diagnosis, age, gender, height, weight, dominant side, ventilator mode or spontaneous breathing, and type of ICU were recorded for each patient. Patients could participate maximally twice in the testretest session when at least 1 week separated the measurements to ensure independence of the measurements. Written informed consent was required. The study protocol was approved by the Leuven institutional review board (ML4190). Assessment Procedure. Patients were tested in a supine position for all measurements (except for knee extension) with the

head end at 10 upright. Test positions were similar as described in the study by Bohannon (15) except for knee extension (Table 1). Isometric strength of three upper limb muscle groups (shoulder abductors, elbow exors, wrist extensors) and three lower limb muscle groups (hip exors, knee extensors, ankle dorsiexors) were tested at the right-hand side using the make method (15). In the make method, patients are asked to perform a maximal voluntary isometric contraction and maintain the contraction for 35 secs. To familiarize the patient, the assessor passively demonstrated the direction of the movement required and then asked the patient to perform the movement actively. Three consecutive isometric contractions of each muscle group were recorded. If the highest value differed 10% of the second value or the measurement was technically not satisfactory, a fourth measurement was performed. Quality of the performance of the test was evaluated by the assessor using visual feedback on the monitor. An ideal curve consisted of a steep increase in force followed by a plateau phase and ended by a sudden decrease of force. Approximately 30 60 secs of rest were allowed between repeated tests of the same muscle group. Verbal encouragement was given during each contraction. Patients were tested twice on the same day by two independent assessors with at least 2 hrs in between. The assessors were blinded to each others HHD testing by being not present during the other testers measurements. The assessors were also blinded to the results of each other because each assessor electronically stored their data separately during the entire study period. The selection of the assessor who performed the rst test session of the day was based on the working schedule of both assessors and therefore can be considered as randomly selected. Observer 1 is a male physiotherapist (height: 185 cm, weight: 85 kg) with 3 yrs of clinical experience and observer 2 is a female physiotherapist (height: 165 cm, weight: 59 kg) with 1 year of clinical experience. Both of them gained experience with HHD in critically ill patients during 6 months preceding the study. Materials. Isometric muscle force was measured using a HHD (CompuFet 2; Biometrics, Almere, The Netherlands) that was connected to a laptop. The dynamometer was set to read the force in Newtons. The upper limit

of the dynamometer is 660 N. It measures forces to the nearest 0.1 N. The accuracy of the device was veried with standard weights (range, 150 kg) every month by the same assessor. The margin of error was within 5%. Statistical Analysis. All statistical analysis was conducted using SPSS software (SPSS Inc, Chicago, IL). Baseline and outcome variables were depicted as means SDs when normally distributed or medians with interquartile ranges (IQRs) when skewed. To determine the interobserver reliability of the strength measurements, ICCs using the method of absolute agreement and with single measurement as unit of analysis were calculated. The highest score of the three contractions was used for analysis. To compare median values between observers, the Wilcoxon signed-ranks test for related samples was used. The effect of the order of measurement was calculated with repeated-measures two-way analysis of variance. A Bonferroni test was used for post hoc analysis. The highest score of three contractions from the rst test session was used to compare muscle strength values of our population with reference values obtained by Bohannon (15). Data were expressed as z-score. The z-score is a standard score indicating the amount of SD the observation is above or below the mean of the normative values. A z-score of 2 SD units above or below the mean can be considered as clinically relevant (22). Between-muscle group comparison was performed with the Friedman test and a Dunns multiple comparison test was used for the post hoc analysis. Gender-related differences in muscle strength among muscle groups were estimated with a two-way analysis of variance for independent samples and a Bonferroni test was used for post hoc analysis.

RESULTS
Data were obtained during a 5-month period from April until August 2010. Sixty critically ill patients were eligible for the study, but 21 patients refused to participate. Consequently, 39 critically ill patients were tested by two independent assessors, whereas 12 of them participated in the testretest twice. Therefore,
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a convenience sample of 51 testretests was obtained. Each tester assessed 286 muscle groups because 20 muscle groups could not be evaluated because of an MRC level 3 (n 10), bilateral burn (n 2), bilateral articular problem (n 1), abdominal surgery (n 4), muscle spasm (n 1), friction lesion (n 1), and one patient did not understand the required movement (n 1). Characteristics of these patients at the time of measurement are shown in Table 2. Interobserver Reliability. Interobserver reliability was very good for four of the six muscle groups tested with ICCs between 0.91 and 0.96. Somewhat lower values were obtained for hip exion (ICC,

Table 2. Characteristics at the time of measurement (n 51) Diagnosis Abdominal/pelvic surgery Cardiac surgery Gastrointestinal/hepatic surgery Respiratory failure Transplant surgery Thoracic surgery Trauma/burns Vascular surgery Others Age, years Height, cm Weight, kg Body mass index, kg/m2 Sex, male, no. (%) Surgical intensive care unit, no. (%) Respiratory status, no. with mechanical ventilation (%) Pressure support ventilation, no. (%) Neurally adjusted ventilator assist, no. (%) Continuous positive airway pressure, no. (%) Hand dominance, left no. (%) No. (%) 11 (21) 11 (21) 3 (6) 6 (12) 4 (8) 7 (14) 7 (14) 1 (2) 1 (2) 64 (5372) 169 (162180) 75 (6080) 25 (2228) 32 (62) 42 (82) 17 (33) 14 (82) 2 (12) 1 (6) 5 (10)

Data are expressed as absolute number, percentage or median, and interquartile range.

0.80) and ankle dorsiexion (ICC, 0.76). For ankle dorsiexion, observer 2 obtained statistically signicant higher values than observer 1 (p .0001) (Table 3; Fig. 1). TestRetest Evaluation. Because patients were tested twice on the same day by two assessors and only a short time interval separated the testretest sessions, the potential interference of a learning effect or fatigue after the rst measurement was examined. Therefore, we compared data from the test and retest sessions obtained on the same day. This was also relevant because the rst examiner was randomly selected. No overall signicant differences were observed (p .4). Comparison of Muscle Groups in Upper and Lower Limbs. Muscle strength of upper and lower limbs is summarized in Figure 2AB. Moderate to severe reductions in muscle force were present for all muscle groups as shown by the median z-score: shoulder: 2.8 (IQR, 3.2 to 2.3); elbow: 3.5 (IQR, 4.5 to 2.7); wrist: 2.6 (IQR, 3.2 to 1.8); hip: 1.08 (IQR, 1.9 to 0.2); knee: 3.4 (IQR, 4.0 to 2.9); and ankle: 3.0 (IQR, 3.9 to 2.5) SD units. Friedmans test revealed signicant differences in muscle strength among all muscle groups (p .0001). In the upper limbs (Fig. 2A), post hoc analysis revealed that the elbow muscles decreased signicantly more SD units than the shoulder (p .01) and the wrist muscles (p .001). No signicant differences were found between the shoulder and the wrist muscle groups. In the lower limbs (Fig. 2B), muscle strength of the knee and ankle decreased signicantly more SD units than the hip (p .001). There were no signicant differences between knee and ankle muscle groups. Comparison of Muscle Groups Between Upper and Lower Limbs. Proximal

muscle strength decreased signicantly more SD units (p .001) in the upper limb compared with the lower limb. No signicant difference was found between the middle muscle groups of the upper and lower limbs. In contrast, muscle strength of the distal muscle groups decreased signicantly more SD units (p .05) in the lower than in the upper limb (Fig. 3). No signicant differences were found in loss of muscle strength among muscle groups between men and women (p .6).

DISCUSSION
This study showed that HHD is a reliable method to assess maximal voluntary isometric muscle strength of upper and lower limbs in cooperative critically ill patients being treated in an ICU. Good to excellent agreement was shown for upper limb muscle groups and knee extension, whereas hip exion and ankle dorsiexion had moderate to good reproducibility. These results were obtained given that patients were adequate and cooperative, standardized test positions were used, and verbal encouragement was given by the assessors. This is the rst study that objectively assessed muscle strength with HHD in critically ill patients admitted to the ICU. Several interobserver studies with HHD have been performed in patient populations with similar results. Studies by Bohannon et al (20) and Merlini et al (21) tested upper and lower extremities in neurologic patients using the make method. Intertester reliability in both studies was good to excellent (20, 21). Similarly, a study by Burns et al (23) observed excellent agreement for assessment of elbow exion and extension force in 19 men with tetraplegia. All these studies were performed in patients with muscle weakness and conrm our data in critically ill patients and support that consistent measurements can be obtained in these patients. Interobserver agreement for hip exion was somewhat lower in our study. A study by Fulcher et al (18) found also a reduced reliability with increased magnitude of the generated force while testing 30 football players. Hip exors were the strongest muscle group tested and showed moderate reliability (18). Also in our population, absolute strength values of the hip exors were the highest (median, 112; IQR, 69 146 N) among all muscle groups tested. This could explain
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Table 3. Interobserver agreement of handheld dynamometry Intraclass Correlation Coefcient (95% Condence Interval) 0.91 (0.850.95) 0.96 (0.930.98) 0.94 (0.910.97) 0.80 (0.670.89) 0.94 (0.900.97) 0.76 (0.330.90)

Muscle Group Shoulder abduction Elbow exion Wrist extension Hip exion Knee extension Ankle dorsiexion

Observer 1 74 (57111) 79 (50115) 61 (3878) 112 (69138) 85 (41142) 57 (3595)

Observer 2 74 (5494) 75 (53108) 62 (3784) 119 (78149) 94 (53138) 80 (46106)a

a p .0001. Values are expressed in Newtons (median, interquartile range).

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Figure 1. Identity plots of muscle strength (expressed in N) of six muscle groups: shoulder abduction, elbow exion, wrist extension, hip exors, knee extension, and ankle dorsiexion.

Figure 2. Limb muscle strength expressed as zscore. A, Three upper limb muscle groups. Box plots represent medians, interquartile ranges, percentiles 10 and 90. *p .01; **p .001. B, Three lower limb muscle groups. Box plots represent medians, interquartile ranges, percentiles 10 and 90. **p .001.

the somewhat lower ICC. However, patients in our study were much weaker than the football players examined in the study by Fulcher et al (18). In addition, the assessors of the current study did not have any problems resisting the strength of the patient. Analysis of height of the assessor revealed no interaction with values obtained in small ( 162 cm), medium (162180 cm), and tall patients ( 180 cm). Interobserver reliability of ankle dorsiexion was somewhat lower in our study (ICC, 0.76). Similar ndings were found in the studies of Merlini et al (21) and Arnold et al (17) who reported even lower interrater reliability scores for ankle dorsiexion. Several factors may contribute to this nding such as a short lever arm of the dynamometer on the dorsal side of the foot, discomfort, difculties aligning the transducer of the dynamometer perfectly in line with the force exerted by the subject, and the presence of ankle contractures (17, 21). Ankle mobility is oftentimes impaired in critically ill patients (24) and may have resulted in somewhat lower reliability. The overrating of ankle dorsiexion force by observer 2 (Fig. 1) is probably the result of a small difference in joint position. In retrospect, observer 1 started measuring in the end range of the ankle (0 plantar exion) in contrast with observer 2 who started measuring in the midrange (10 plantar exion) of the ankle. At variance with our results, other studies reported

good interobserver agreement for ankle dorsiexion (16, 19, 20). Differences in procedures are that in the study by Visser et al (19), HHD was performed using the break method, whereas the study by Spink et al (16) examined older and younger healthy participants without ankle mobility impairment. The values obtained in this crosssectional sample showed that patients, strong enough to overcome gravity (MRC 3), have severely reduced muscle force compared with reference values obtained by Bohannon (15). Loss of muscle strength between men and women was similar. Elbow, knee, and ankle muscle groups were the most affected muscles. In our population, no statistically significant differences in strength between proximal and distal muscle groups were observed for the upper limbs. For the lower limbs, muscle strength in the proximal muscle groups was signicantly higher than in the middle and distal muscle groups. This leads to the presumption that patients might have developed critical illness polyneuropathy. Critical illness polyneuropathy is a predominantly distal axonal degeneration of motor and sensory bers. Therefore, muscle weakness will affect the distal muscle groups more than the proximal muscle groups. This is at variance with the observations of De Jonghe et al who observed signicantly more reduction in proximal muscle strength compared with distal muscle strength in both upper and lower limbs (12). Several authors (12, 25) suggest that underlying myopathic changes, affecting mainly the proximal regions of the limbs, are present in the majority of the critically ill patients who developed muscle weakness. At variance with the study by De Jonghe et al (12), all muscle groups being tested in our study had at least a score of 3 on the MRC scale, whereas De Jonghe et al reported results in patients that scored MRC 48 with a median MRC 3. Considerations for Clinical Practice. Critically ill patients admitted to the ICU may present with various levels of muscle weakness. The MRC scale is a reliable and valid method to assess muscle strength (10, 11) and is able to detect clinical signicant muscle weakness (MRC 48) (3, 12). However, when muscle strength exceeds level 3 (movement against gravity), the MRC scale loses much of its ability to discriminate between gradations of muscle strength and is less sensitive to detect changes in muscle strength over time
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Figure 3. Comparison of muscle strength in the proximal, middle, and distal muscle groups of upper and lower extremities. Expressed as z-score (**p .001; #p .05). Box plots represent medians, interquartile ranges, percentiles 10 and 90.

(13). HHD as shown in the present study is a reliable and valid tool for objective measurement of muscle strength of upper and lower limb muscle groups that are powerful enough to overcome gravity (MRC 3) (26). In critically ill patients, an important additional factor limiting clinical evaluation is the level of consciousness. Patients need to be fully adequate and cooperative to obtain reliable data. A maximal score of 5 on the ve questions for adequacy is required for volitional muscle strength assessment. In addition, it is of great importance to use standardized test positions so that results are comparable between different assessors. The standardized test positions used in the current study have previously been dened by Bohannon (15) and can be implemented, except for the measurement of knee extension muscle strength, in critically ill patients. Another essential prerequisite for valid HHD is that the assessor is strong enough to counter the force generated by the muscle group (27). Several authors have indicated that HHD underestimates strength when forces exceed 25 kg or 250 N (19, 28, 29). This can be the result of the limited strength of the rater and the inability to stabilize the dynamometer. A study by Wadsworth et al (30) reported the effects of anthropometric characteristics of the raters on the ability to stabilize the dynamometer during HHD testing in healthy subjects. Female raters lost stabilization more frequently than male raters when testing stronger muscle groups (elbow exion and knee extension) of a male subject (values ranging between 250 and 324 N) (30). In the present study, both (male and female) raters obtained the highest values for muscle strength during hip exion of a male subject (male rater: 105 N, female rater: 115
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N). These values were clearly 250 N and the muscle strength values of the healthy population (30). Because none of the raters in the present study had difculties in stabilizing the dynamometer, we conclude that the effect of anthropometric characteristics of the raters on obtaining muscle strength values in critically ill patients is negligible. Limitations of the Study. Only patients who had a MRC score of 3 in at least four of six muscle groups at the right-hand side were recruited for HHD meaning that patients with severe muscle weakness (MRC sum 36) were excluded from the study. However, we specically aimed at muscle strength of MRC score 3 because HHD has been shown to be less accurate to measure muscle strength below a MRC score of 3 (13, 26, 31). Second, critically ill patients were not capable to perform HHD of the knee in an sitting upright position on the edge of the bed as described by Bohannon (15). Knee extension was therefore measured in the supine position with the hip and knee in 90 exion. Normative values for this alternative test position might be necessary to develop. Finally, to relieve the patients from extensive muscle testing, muscle strength was measured unilaterally assuming that muscle weakness is symmetric in critically ill patients. So far, no data are available that indicate asymmetric development of muscle weakness.

ACKNOWLEDGMENTS
We thank the patients for their willingness to cooperate; Dr. D. Langer for the statistical support; and the physiotherapists, medical, and nursery staff of the intensive care units for their support to this study.

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CONCLUSION
HHD is a reliable and objective tool for the assessment of strength of skeletal muscles that are strong enough to overcome gravity in cooperative critically ill patients. Future studies should focus on the sensitivity of HHD in longitudinal studies and on the relationship of muscle strength with functional outcome.

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