Quantitative Evaluation of Muscle Function, Gait, and Postural Control in People Experiencing Critical Illness After Discharge From the Intensive Care Unit

Quantitative Evaluation of Muscle Function, Gait, and Postural Control in People Experiencing... Abstract Background The path to recovery of muscle strength and mobility following discharge from the intensive care unit (ICU) has not been well described. Objective The study objective was to quantify muscle function, gait, and postural control at 3 and 6 months after discharge in people who were recovering from critical illness and who were ventilated for 7 days or more. Design This was a nested longitudinal study with continuous inclusion of individuals over a 2-year period and with age- and sex-matched controls. Methods Twenty-four people were tested at 3 months after ICU discharge; 16 of them (67%) were reevaluated at 6 months (post-ICU group). Healthy controls (n = 12) were tested at a single time point. Muscle function of the knee extensors (KEs), plantar flexors (PFs), and dorsiflexors (DFs) was assessed on a dynamometer. Gait was measured using an electronic walkway, and postural control was measured with 2 portable force plates. Results Muscle weakness was observed across all muscle groups at 3 months, with the greatest strength reductions in the ankle PFs (45%) and DFs (30%). Muscle power was reduced in the PFs and DFs but was not reduced in the KEs. Gait in the post-ICU group was characterized by a narrower step, longer stride, and longer double-support time than in the controls. Improvements were found in KE strength and in stride time and double-support time during gait at 6 months. Leg muscle strength and power had moderate associations with gait velocity, step width, and stride length (r = .44–.65). Limitations The small heterogeneous sample of people with a high level of function was a limitation of this study. Conclusions Muscle strength and power were impaired at 6 months after ICU discharge and were associated with gait parameters. Future studies are needed to examine the role of muscle strength and power training in post-ICU rehabilitation programs to improve mobility. Intensive care unit (ICU)–acquired weakness (ICUAW) is an important consequence of critical illness. ICUAW affects about 25% of people on mechanical ventilation, particularly in those with prolonged mechanical ventilation,1 and is associated with greater morbidity and mortality.2–4 ICUAW develops within hours of admission, and is persistent5 during critical illness, as evidenced by an early reduction in quadriceps muscle size,6,7 abnormal muscle contractility,8 and muscle weakness.2–4 Development of ICUAW is the result of interacting factors such as length of ICU stay, sepsis, myotoxic medications (eg, corticosteroids, neuromuscular blockers), multi-organ dysfunction, aging, and comorbidities.9,10 Muscle weakness and functional deficits may persist for years after ICU discharge.11,12 Yet, few studies have quantified any long-term functional muscle deficits. In a study by van der Schaaf et al,13 handgrip strength was reduced to 50% of the predicted values 1 week after ICU discharge. However, Medical Research Council scores of the same participants were normal or near normal (grades 4 or 5).13 Poulsen et al14 used dynamometry to evaluate knee extensor muscle strength, power, and endurance in individuals 1 year after ICU discharge. Although all aspects of muscle performance were reduced compared to the controls, the rate of force development (an indicator of muscle power) was the most impaired.14 To date, the distal muscles of the lower extremity, such as the plantar flexors (PFs) and dorsiflexors (DFs) of the ankle, have not been evaluated. These muscle groups have important functional implications in gait and balance control.15,16 Loss of lower extremity muscle mass and strength is associated with mobility limitations,17,18 gait alterations,19 and impaired postural control and balance.20 Spatiotemporal gait parameters are commonly evaluated using instrumented walkways that measure gait velocity, step length and width, and time spent in single- and double-limb support.21 This information can be used to study changes in walking pattern that may reflect altered dynamic balance or neuromotor control.21,22 Quantitative posturography is an additional tool that uses force plates to estimate the center of pressure (COP), in order to determine postural control and static stability during quiet standing and functional tasks. However, these measures have not been applied in individuals following a critical illness. This unique biomechanical information may provide novel understanding into the impact of any potential postural control changes resulting from critical illness. The relationship between muscle function and mobility in people who have experienced a period of critical illness may provide important information about how to optimize physical rehabilitation to restore functional independence. To date, no studies have examined biomechanical properties of gait and postural control, together with muscle function, in this population. The objectives of this study were to quantify lower-limb muscle function and mobility outcomes at 3 and 6 months after ICU discharge; to compare with age- and sex-matched controls; and to identify associations between muscle strength and power with measures of gait and postural control in the post-ICU period. We hypothesized that deficits in muscle function, gait, and postural control would be observed at 3 months after ICU discharge compared to healthy controls, with improvement at 6 months post discharge. We also hypothesized that lower-limb muscle dysfunction would be associated with altered patterns of gait and postural control. Methods The study design was a nested, longitudinal study with continuous inclusion of people recruited between June 2011 to June 2013 from an ongoing study of long-term outcomes following critical illness11 (phase 1: toward RECOVER; trial registration: NCT00896220). Informed consent was obtained from all participants. Inclusion and exclusion criteria are detailed in the primary study.11 In brief, people in the ICU were included if they were 16 years or older and were mechanically ventilated for at least 7 days. People in the ICU were excluded if they had a preexisting or current neurological injury, had a diagnosis of neuromuscular disease, or were nonambulatory prior to their ICU admission. Specifically, for this substudy participants were excluded if they reported any functional limitations affecting their ability to perform the required muscle function and mobility tests. Control participants were recruited from the local community, and were matched for age and sex to the post-ICU group. Control participants were excluded if they reported musculoskeletal problems (eg, arthritis, previous orthopedic surgery); a history of neurological conditions (eg, stroke, Parkinson disease); or cardiovascular, respiratory, or metabolic conditions (eg, heart attack, asthma, diabetes) that could affect muscle strength, balance, or gait performance. Participants in the post-ICU group were from a sample of convenience from those attending follow-up appointments at 3 and 6 months for the primary study.11 Participants were approached at the end of their appointment by the study coordinator to determine their interest in participating in the muscle and gait substudy. Follow-up appointments at 6 months were booked through telephone reminders by the study coordinators. Controls were tested at a single time point and were recruited between March 2012 and July 2013. Muscle Function Assessment Muscle strength (torque-generating capacity of the muscle) and power (rate of torque generation determined from a torque-time curve) were measured using Biodex System 4 isokinetic dynamometer (Biodex Medical Systems, Shirley, New York). Participants were asked to perform maximum isometric voluntary contractions of the knee extensors (KEs), PFs, and DFs. Participants were seated on the Biodex with straps placed across the shoulders, hips, and thigh for stability. Hip angle was kept at 90° for all assessments. Joint angles selected for isometric tests were based on the angle of peak torque generation: KEs at 60° of knee flexion;23 and PFs and DFs with the ankle joint at 15° of plantar flexion with the knee stabilized at 35° to 40° degrees of flexion. We selected a single for both PF and DF torque that optimized the torque generation for both muscle groups.24 For each muscle group tested, a warm-up contraction was followed by 5 maximal efforts to obtain peak torque. A 1-minute rest period was given between trials to minimize muscular fatigue. The raw signals from the Biodex dynamometer (torque, position, velocity) were sampled at a frequency of 100 Hz. Peak torque (N·m) was calculated at the highest torque reached among the trials, within 10% coefficient of variation. The rate of torque development (N·m/s), a measure of muscle power, was calculated from the time taken between 40% to 80% of the peak torque25 and taken from the highest of the 5 trials. Gait and Postural Control Assessment Gait was assessed during a 6-minute walk test conducted in a quiet and leveled 30-m corridor using standardized procedures.26 Spatiotemporal gait parameters were assessed using a portable, 6-m-long instrumented carpet (GAITRite; CIR Systems Inc, Franklin, New Jersey), which was placed midway along the corridor. GAITRite signals were sampled at 50 Hz, with the following variables extracted for analysis: gait velocity, stride time, stride length, step width, single support time, and double-support time. In addition, the coefficient of variation for stride time was calculated as a measure of gait stability, with lower variation indicating greater stability and reduced fall risk.27 Postural control was assessed during quiet standing using two 6-degrees-of-freedom force plates (AMTI, Watertown, Massachusetts). All standing trials were on level ground and force plates. These plates were placed adjacent to each other, such that participants stood with 1 foot on each plate. The location of each foot was marked for repeated trials. The duration of each trial was 120 seconds, and analysis was completed on the middle 60 seconds. Participants engaged in four 2-minute trials of quiet standing; 2 eyes open and 2 eyes closed. Ground reaction forces were collected and sampled at 100 Hz and digitally filtered using a Butterworth filter with a 4-Hz cutoff frequency. Mean power frequency content for both the anteroposterior (AP) and mediolateral (ML) directions was determined using a Discrete Fast Fourier Transformation to calculate the average power of the signal content. The mean power frequency defines the average frequency of the COP signal during a quiet standing session. The root mean square (RMS) of the COP signal represents the magnitude of variability. Both measures were used to characterize balance control, and have been employed to assess postural control strategies with clinical populations.28 Data Analysis All statistical analyses were completed using JMP v. 9.0 software (SAS Campus, Cary, North Carolina). Normality was assessed using the Shapiro-Wilk test. Data that did not satisfy the assumption of normality was transformed with a logarithmic for negatively skewed data or square transformation for positively skewed data. Measures requiring transformation included physical therapy (KEs and PFs), rates of torque development (KEs and PFs), gait velocity, stride length, step width, stride-time coefficient of variation, single-support time, double-support time, AP RMS, ML RMS, and AP mean power frequency. To test our first hypothesis (between-group comparisons) and second hypothesis (change over time), a mixed-effects analysis of variance {group [control/post-ICU (3 months or 6 months)]} was used to compare each group on muscle strength, power, and gait outcomes. A mixed-effects analysis of variance {group [control (3 months or 6 months)] × vision (eyes open or eyes closed)} was used to test postural control–dependent measures (RMS and mean power frequency of COP). Tukey-Kramer post hoc comparisons were made on any significant interactions effects. Significance was set a priori at an alpha value of .05. The 95% confidence intervals of the mean difference were calculated for each variable. To test our third hypothesis, the Pearson r was used to determine correlations between mobility and muscle function measures in each group, and was interpreted as follows: very low = .15–.24, low = .25–.49, moderate = .50–.69, high = .70–.89, and very high = .90–1.00.29 Role of the Funding Source Funding support was provided by a Canadian Institutes of Health Research Operating Grant (M.H., J.I.C.), a New Investigator Award (J.I.C.), and Ontario Ministry of Health Innovation Funding (M.H., J.I.C.). The funders had no role in the study's design, conduct, and reporting. Results Sample Characteristics Twenty-four individuals were tested 3 months after ICU discharge (6 women; age = 47.5 ± 16.1 years; weight = 74.2 ± 19.6 kg; height = 1.68 ± 0.12 m); 16 of them (67.0%) repeated the testing at 6 months after discharge (Fig. 1). Participants lost to follow-up at 6 months were primarily due to being too busy or unavailable for a follow-up appointment (ie, lack of time) (n = 7) and missed appointment (n = 1). Age- and sex-matched healthy controls (n = 13) were tested at a single time point (4 women; age = 44.2 ± 16.2 years; weight = 72.9 ± 14.5 kg; height = 1.12 ± 0.42 m). Detailed characteristics of the post-ICU group are shown in Table 1. The subgroup of 16 individuals who were tested at 6 months after ICU discharge did not differ from the group who was tested at 3 months in demographic or clinical characteristics (Tab. 1). Figure 1. View largeDownload slide Diagram of participant inclusion. ICU = intensive care unit. Figure 1. View largeDownload slide Diagram of participant inclusion. ICU = intensive care unit. Table 1. Characteristics of Participants at 3 and 6 Months After ICU Discharge.a Characteristic  Participants at 3 mo (n = 24)  Participants at 6 mo (n = 16)  Age (y)  47.5 ± 16.1  46.4 ± 19.5  Weight (kg)  74.2 ± 19.6  72.9 ± 22.5  Height (m)  1.68 ± 0.12  1.68 ± 0.13  BMI (kg/m2)  25.9 ± 5.2  25.7 ± 5.0  APACHE II (24 h after ICU admission)  19.5 ± 7.2  18.6 ± 6.7  Duration of mechanical ventilation (d)  16 ± 11  15 ± 10  ICU length of stay (d)  43 ± 24  43 ± 28  Hospital length of stay (d)  44 ± 26  44 ± 28  6MWT (m)  441 ± 124 (63.0 ± 17.0)b  494 ± 118 (71.0 ± 17.0)b  FVC (% predicted)  79.0 ± 18.0  80.0 ± 21.0  FEV (% predicted)  74.0 ± 17.0  77.0 ± 20.0  Corticosteroid treatment (% of participants)  40.0 (n = 9)  31.0 (n = 5)  FIM scorec  117 ± 9  118 ± 8  Characteristic  Participants at 3 mo (n = 24)  Participants at 6 mo (n = 16)  Age (y)  47.5 ± 16.1  46.4 ± 19.5  Weight (kg)  74.2 ± 19.6  72.9 ± 22.5  Height (m)  1.68 ± 0.12  1.68 ± 0.13  BMI (kg/m2)  25.9 ± 5.2  25.7 ± 5.0  APACHE II (24 h after ICU admission)  19.5 ± 7.2  18.6 ± 6.7  Duration of mechanical ventilation (d)  16 ± 11  15 ± 10  ICU length of stay (d)  43 ± 24  43 ± 28  Hospital length of stay (d)  44 ± 26  44 ± 28  6MWT (m)  441 ± 124 (63.0 ± 17.0)b  494 ± 118 (71.0 ± 17.0)b  FVC (% predicted)  79.0 ± 18.0  80.0 ± 21.0  FEV (% predicted)  74.0 ± 17.0  77.0 ± 20.0  Corticosteroid treatment (% of participants)  40.0 (n = 9)  31.0 (n = 5)  FIM scorec  117 ± 9  118 ± 8  a 6MWT = 6-minute walk test, APACHE = Acute Physiology and Chronic Health Evaluation, BMI = body mass index, FEV = forced expiratory volume, FIM = Functional Independence Measure, FVC = forced vital capacity, ICU = intensive care unit. b Values in parentheses are percent predicted. c Obtained 7 days after ICU discharge; scores ranged from 18 (lowest) to 126 (highest). View Large Muscle Strength and Power Muscle strength and power measures are shown in Figure 2. A significant group effect in muscle strength was found for KE peak torque (P = .01) and DF peak torque (P = .002). Tukey-Kramer post hoc analysis revealed significant differences between controls and post-ICU at 3 months (95% CIs = 25.08 to 88.60 for KEs and 7.06 to 18.96 for DFs) as well as controls and post-ICU at 6 months (95% CIs = 0.55 to 80.50 for KEs and 6.37 to 19.29 for DFs). No significant differences were observed in muscle strength measures between the 3- and 6-month post-ICU groups. Only minor, nonsignificant improvements in the strength of the KEs (15.2%) and DFs (8.3%), with a slight decrement in PFs (−3.7%), were observed between 3 months and 6 months in the post-ICU group. Figure 2. View largeDownload slide Comparison of mean absolute values of strength (top) and power (bottom) of lower-limb muscle groups between participants at 3 and 6 months after discharge and age- and sex-matched controls. Values are means and standard deviations. Asterisks indicate significant differences, with significance accepted at a P value of <.05. DF = dorsiflexors, KE = knee extensors, PF = plantar flexors, RTD = rate of torque development. Figure 2. View largeDownload slide Comparison of mean absolute values of strength (top) and power (bottom) of lower-limb muscle groups between participants at 3 and 6 months after discharge and age- and sex-matched controls. Values are means and standard deviations. Asterisks indicate significant differences, with significance accepted at a P value of <.05. DF = dorsiflexors, KE = knee extensors, PF = plantar flexors, RTD = rate of torque development. For muscle power measures, between-group differences were found for the DF rate of torque development (P = .03) and post hoc comparisons revealed that controls differed from the 3-month post-ICU (95% CI for DFs = 10.85 to 55.09) and 6-month post-ICU (95% CI for DFs = 9.16 to 56.20) groups. No significant differences were observed between the 3- and 6-month post-ICU groups. Minimal improvement in power was found between 3 and 6 months in KEs (6.2%) and DFs (1%), whereas a decrement in power in PFs (−10.7%) was observed. Spatiotemporal Parameters of Gait and Postural Control The gait parameters are summarized in Table 2. Significant group effects were observed for step width (P = .01), step length (P = .01), and double-support time (P = .01). Tukey-Kramer post hoc comparisons revealed that the 3-month post-ICU group had a significantly shorter step length (95% CI = 0.09 to 0.35), narrower step width (95% CI = 0.05 to 0.19), and spent more time in double-support time (95% CI = −0.09 to −0.01) than controls. No differences in gait parameters were found between the post-ICU group at 6 months and the control group or between the post-ICU group at 3 months and the post-ICU group at 6 months. Table 2. Spatiotemporal Gait Parameters in Participants After ICU Discharge and Healthy Controls.a Gait Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  P  Post Hoc Significant Comparisons  Gait velocity (m/s)  1.50 ± 0.23  1.31 ± 0.35  1.56 ± 0.17  .06    Stride length (m)  1.61 ± 0.15  1.39 ± 0.26  1.46 ± 0.26  .01c  CON vs 3MO  Step-width (cm)  0.81 ± 0.08  0.69 ± 0.15  0.79 ± 0.07  .01c  CON vs 3MO  Stride time (s)  1.05 ± 0.12  1.09 ± 0.14  1.05 ± 0.10  .07    Single-support time (s)  0.42 ± 0.04  0.41 ± 0.03  0.40 ± 0.02  .13    Double-support time (s)  0.23 ± 0.04  0.28 ± 0.08  0.25 ± 0.09  .01c  CON vs 3MO  Stride time CV (%)  1.62 ± 0.79  2.42 ± 1.66  2.26 ± 1.19  .21    Gait Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  P  Post Hoc Significant Comparisons  Gait velocity (m/s)  1.50 ± 0.23  1.31 ± 0.35  1.56 ± 0.17  .06    Stride length (m)  1.61 ± 0.15  1.39 ± 0.26  1.46 ± 0.26  .01c  CON vs 3MO  Step-width (cm)  0.81 ± 0.08  0.69 ± 0.15  0.79 ± 0.07  .01c  CON vs 3MO  Stride time (s)  1.05 ± 0.12  1.09 ± 0.14  1.05 ± 0.10  .07    Single-support time (s)  0.42 ± 0.04  0.41 ± 0.03  0.40 ± 0.02  .13    Double-support time (s)  0.23 ± 0.04  0.28 ± 0.08  0.25 ± 0.09  .01c  CON vs 3MO  Stride time CV (%)  1.62 ± 0.79  2.42 ± 1.66  2.26 ± 1.19  .21    a CON vs 3MO = healthy controls versus participants at 3 months after intensive care unit (ICU) discharge, CV = coefficient of variation. b Values are reported as mean±standard deviation. c Significant at an α value of .05. View Large Table 3 displays mean postural control data for each compared group and condition. A main effect of vision (eyes open vs eyes closed) was observed for several of the postural control measures across all groups. Specifically, differences in the ML RMS (P = .049; 95% CI = –0.02 to 0.08), AP RMS (P = .001; 95% CI = −0.25 to −0.05), and ML mean power frequency (P = .04; 95% CI = −0.09 to 0.01) were observed with eyes open vs eyes closed, indicating that postural control was affected with the inclusion of visual input in both the control and the post-ICU groups alike. Comparisons of postural control measures between the 3- and 6-month post-ICU and control groups did not reveal any significant main or interaction effects. Table 3. Postural Control Measures in Participants After ICU Discharge and Healthy Controls.a Eye Condition  Postural Control Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  Open  RMS (AP) (mm)  0.38 ± 0.06  0.55 ± 0.17  0.46 ± 0.13  RMS (ML) (mm)  0.23 ± 0.06  0.34 ± 0.21  0.47 ± 0.20  MPF (AP) (Hz)  0.22 ± 0.10  0.24 ± 0.11  0.27 ± 0.13  MPF (ML) (Hz)  0.26 ± 0.06  0.24 ± 0.10  0.21 ± 0.09  Closed  RMS (AP) (mm)  0.52 ± 0.23  0.68 ± 0.23  0.63 ± 0.13  RMS (ML) (mm)  0.26 ± 0.12  0.34 ± 0.26  0.30 ± 0.19  MPF (AP) (Hz)  0.30 ± 0.10  0.24 ± 0.11  0.21 ± 0.11  MPF (ML) (Hz)  0.28 ± 0.08  0.27 ± 0.14  0.26 ± 0.10  Eye Condition  Postural Control Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  Open  RMS (AP) (mm)  0.38 ± 0.06  0.55 ± 0.17  0.46 ± 0.13  RMS (ML) (mm)  0.23 ± 0.06  0.34 ± 0.21  0.47 ± 0.20  MPF (AP) (Hz)  0.22 ± 0.10  0.24 ± 0.11  0.27 ± 0.13  MPF (ML) (Hz)  0.26 ± 0.06  0.24 ± 0.10  0.21 ± 0.09  Closed  RMS (AP) (mm)  0.52 ± 0.23  0.68 ± 0.23  0.63 ± 0.13  RMS (ML) (mm)  0.26 ± 0.12  0.34 ± 0.26  0.30 ± 0.19  MPF (AP) (Hz)  0.30 ± 0.10  0.24 ± 0.11  0.21 ± 0.11  MPF (ML) (Hz)  0.28 ± 0.08  0.27 ± 0.14  0.26 ± 0.10  a AP = anteroposterior, ICU = intensive care unit, ML = mediolateral, MPF = mean power frequency, RMS = root mean square. b Values are reported as mean±standard deviation. View Large Relationships of Muscle Function With Gait and Posture Significant correlations between muscle function and gait measures were observed in the post-ICU and control groups (eTab. 1; available at https://academic.oup.com/ptj). Leg muscle strength and power showed low to moderate positive correlations with gait velocity, stride length, and step width in the post-ICU group at 3 months (r = .44 to .65; P = .003–.02) (eTab. 1). PF strength and power were negatively associated with double-support time (r = −.42; P = .035) and single-support time (r = −.50; P = .011). KE power also showed a negative association with double-support time (r = −.039; P = .049). In the control group, KE strength, KE power, and PF strength showed moderate correlations with stride length and step width. However, muscle function was not associated with gait velocity or temporal parameters (eTab. 1). Postural control measures were not associated with muscle function measures in either the post-ICU or the control group (eTab. 2). Discussion To our knowledge, this is the first study to quantify muscle function, gait, and postural control in the early, post-discharge recovery period in individuals who were mechanically ventilated for at least 7 days in the ICU. Our results demonstrate impaired lower limb muscle strength and power, particularly of the distal leg muscles, with only minimal changes in muscle function from 3 to 6 months after ICU discharge. Indications of a “cautious gait” strategy were observed in the 3-month post-ICU group compared to the control group, but this was no longer present in the 6-month post-ICU group. Alterations in gait parameters were associated with impairments in leg muscle strength and power with the 3-month post-ICU group. Finally, static postural control was not impaired in individuals after ICU discharge, and did not show a relationship with muscle function. Our findings suggest that a “cautious gait” strategy observed in the early phase after ICU discharge is consistent with deficits in lower extremity muscle strength and power. Our data revealed a deficit in knee extensor strength in people recovering from critical illness 3 months after ICU discharge, with minimal (15.2%) improvement by 6 months. Knee extensor power was also compromised in our cohort at 3 and 6 months post discharge. This is similar to the findings of Poulsen et al14 in men who were 12 months after ICU discharge and who had lower peak torque and rate of torque development of the knee extensors compared to controls. In our study, we also measured the strength and power of distal muscles; the ankle PFs and DFs. Our results revealed significant reductions in DF muscle strength and power between the post-ICU group at 3 and 6 months compared to the control group. The deficits observed in PF strength and power in the post-ICU group did not reach statistical significance, which may have been due to large within-group variability in the measures. Weakness of proximal muscle groups, such as the hip extensors and hip abductors, is common in ICUAW; however, due to limitations in positioning participants comfortably to test these muscles using computerized dynamometry (supine or side lying), we were unable to test these muscle groups in the current study. We found that at 3 months after ICU discharge, there were greater deficits in muscle power than muscle strength compared to controls, particularly in the distal leg muscles. At 3 months, the post-ICU group demonstrated 43.5% lower rate of torque development for KEs, 42.3% lower for DFs, and 69.3% lower for PFs compared to the control group. Similarly, decrements in muscle power with aging are more substantial than loss of muscle strength,30 and muscle power is reported to be a better predictor of physical function (walking speed and sit-to-stand) than muscle strength in older adults.31–33 The age-related decrements in muscle power have been attributed to a preferential atrophy and loss of fast twitch (type II) muscle fibers, loss of motor units, impaired neuromuscular recruitment, and muscle fat infiltration.34 In individuals at 12 months after ICU discharge, Poulsen et al14 found that muscle decrements were due to intrinsic muscle properties rather than deficits in neural activation. A study from our group in individuals at 6 months after ICU discharge also showed that the recovery of muscle size may not translate into improved muscle functional outcomes, lending further support for the importance of deficits in the intrinsic muscle contractile capacity.35 Therefore, further studies are needed to understand the mechanisms of muscle power deficits particularly in DFs, which appear to persist for a longer period after ICU discharge. Our participant group exhibited signs of “cautious” gait at 3 months post discharge. This result suggests that during gait, participants had an altered walking strategy, as demonstrated by significantly shorter strides and longer time spent in double support as well as slower gait velocity and longer stride time. Improvements in gait parameters were observed at 6 months and did not demonstrate any statistical difference between our 6-month group and control group. Step length and step width were associated with KE, DF, and PF strength and power outcomes. Similar relationship of gait parameters and muscle function has been reported in older adults,36,37 knee osteoarthritis,38,39 and neuromuscular diseases.40–45 Impairments in muscle strength and power may also have implications for daily functional tasks such as sit-to-stand, higher-level balance activities, and physical activity levels, and should be examined in the post-ICU population. Our data did not reveal any differences in static postural control in the early post-ICU discharge period using quantitative posturography between groups tested in the current study. However, the use of visual input (eyes open vs eyes closed, quiet standing) affected postural control and indicates a normal dependence on vision to maintain balance for participants, considering no interaction was found between visual input and group. This study included a small, heterogeneous sample of individuals who were tested at 2 discrete time points after ICU discharge. We only tested individuals who volunteered to undergo additional tests of physical function, apart from the main study. These individuals were younger and had better function, based on 7-day post-ICU Functional Independence Measure scores, than the overall cohort in the toward RECOVER study. This placed them in the disability risk group with the best recovery trajectory.11 These participants were likely to have better functional recovery, and may also have better caregiver support than the larger group of patients in the toward RECOVER study. This limits the generalizability of our findings. In this small sample, we were not able to investigate several confounding factors affecting muscle function, such as age, length of ICU stay, or comorbidities. We did not systematically collect the use of myotoxic and/or neurotoxic medications during the period of critical illness. The study participants may have been exposed to high-dose corticosteroids affecting muscle, or ototoxic and neurotoxic medications affecting their vestibular system (eg, high-dose Lasix, aminoglycosides, and vancomycin), which could have led to long-term deficits in muscle function or postural control. However, medication use was not carefully tracked in our study participants. The study was also underpowered for within-group comparisons of participants from 3 to 6 months; post hoc power analysis revealed that we achieved 20.0% power for difference in KE strength from 3 to 6 months. Although all participants received physical therapy, including early mobilization in the ICU, we did not specifically examine activity during hospitalization, or current level of physical activity or functional status prior to ICU admission. Furthermore, our study recruited participants who did not feel restricted in their mobility and could perform the tests—all of which may have impacted the data reported. Finally, our postural control data reflected the COP trajectory and did not directly reflect center-of-mass displacements, which would require full body kinematics. Therefore, direct conclusions on control of center of mass cannot be made but would provide further insight into how postural control was affected in our study participants. The findings from the current study provide a longitudinal description of mobility and muscle function in a group of individuals recovering from critical illness. Our findings indicate that lower-limb muscle functions remain in deficit up to 6 months after ICU discharge, and that muscle dysfunction is more prominent in the distal muscles of the ankle compared to the knee extensors. Muscle strength and power are associated with the parameters of gait, whereas static postural control is not affected in these individuals or associated with muscle function. The findings of this study provide direction for prospective observational and rehabilitation intervention studies in the early post-ICU discharge period. Future studies are needed to examine the role of proximal muscle groups (eg, hip abductors and extensors) on gait and mobility in this population and the impact of muscle weakness on other functional outcomes, such as physical activity level and higher-level balance tasks in the post-ICU period. Funding Funding support was provided by a Canadian Institutes of Health Research Operating Grant (M.H., J.I.C.), a New Investigator Award (J.I.C.), and Ontario Ministry of Health Innovation Funding (M.H., J.I.C.). Author Contributions and Acknowledgments Concept/idea/research design: M. Vergara, J.I. Cameron, M. Herridge, W.H. Gage, S. Mathur Writing: J.B. Kiriella, J.I. Cameron, W.H. Gage, S. Mathur Data collection: J.B. Kiriella, T. Araujo, M. Vergara, L. Lopez-Hernandez, M. Herridge, S. Mathur Data analysis: J.B. Kiriella, L. Lopez-Hernandez, M. Herridge, S. Mathur Project management: J.B. Kiriella, T. Araujo, M. Vergara, S. Mathur Fund procurement: J.I. Cameron Providing participants: M. Herridge Providing facilities/equipment: S. Mathur Providing institutional liaisons: M. Herridge, S. Mathur Consultation (including review of manuscript before submitting): J.I. Cameron, M. Herridge, S. Mathur The authors thank the administrative staffs at Toronto General Hospital and St Michael's Hospital for their continual assistance with recruiting and organizing testing sessions. Ethics Approval All procedures were carried out in accordance with the ethical standards of the University of Toronto Human Research Ethics Board (REB #24421) and the University Health Network Research Ethics Board (REB #08-080). Disclosure and Presentations The authors completed the ICJME Form for Disclosure of Potential Conflicts of Interest and reported no conflicts of interest. The authors declare that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest with regard to the study's design, conduct, and subject matter or materials reported in this manuscript. References 1. De Jonghe B Sharshar T , Lefaucheur JPet al.   Paresis acquired in the intensive care unit: a prospective multicenter study. JAMA . 2002; 288: 2859– 2867. Google Scholar CrossRef Search ADS PubMed  2. Hermans G , Van Mechelen H, Clerckx B. et al.   Acute outcomes and 1-year mortality of intensive care unit–acquired weakness: a cohort study and propensity-matched analysis. Am J Respir Crit Care Med . 2014; 190: 410– 420. Google Scholar CrossRef Search ADS PubMed  3. 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Herridge MS , Tansey CM, Matte A. Canadian Critical Care Trials Group: functional disability 5 years after acute respiratory distress syndrome. N Engl J Med . 2011; 364: 1293– 1304. Google Scholar CrossRef Search ADS PubMed  13. Van der Schaaf M , Dettling DS, Beelen Aet al.   Poor functional status immediately after discharge from an intensive care unit. Disabil Rehabil . 2008; 30: 1812– 1818. Google Scholar CrossRef Search ADS PubMed  14. Poulsen J , Martin R, Jensen BRet al.   Biomechanical and nonfunctional assessment of physical capacity in male ICU survivors. Crit Care Med . 2013; 41: 93– 101. Google Scholar CrossRef Search ADS PubMed  15. Neptune RR , Kautz SA, Zajac FE. Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. J Biomech . 2001; 34: 1387– 1398. Google Scholar CrossRef Search ADS PubMed  16. Hasson CJ , van Emmerik RE, Caldwell GE. Balance decrements are associated with age-related muscle property changes. J Appl Biomech . 2014; 30: 555– 562. Google Scholar CrossRef Search ADS PubMed  17. Cress ME , Meyer M. Maximal voluntary and functional performance levels needed for independence in adults aged 65 to 97 years. Phys Ther . 2003; 83: 37– 48. Google Scholar PubMed  18. LaRoche DP , Millett ED, Kralian RJ. Low strength is related to diminished ground reaction forces and walking performance in older women. Gait Posture . 2011; 33: 668– 672. Google Scholar CrossRef Search ADS PubMed  19. Van der Krogt MM , Delp SL, Schwartz MH. How robust is human gait to muscle activation? Gait Posture . 2012; 36: 113– 119. Google Scholar CrossRef Search ADS PubMed  20. Muehlbauer T , Gollhofer A, Granacher U. Is there an association between variables of postural control and strength in adolescents? J Strength Cond Res . 2011; 25: 1718– 1725. Google Scholar CrossRef Search ADS PubMed  21. Oh-Park M , Holtzer R, Xue X, Verghese J. Conventional and robust quantitative gait norms in community dwelling older adults. J Am Geriatr Soc . 2010; 58: 1512– 1518. Google Scholar CrossRef Search ADS PubMed  22. Hollman JH , McDade EM, Petersen RC. Normative spatiotemporal gait parameters in older adults. Gait Posture . 2011; 34: 111– 118. Google Scholar CrossRef Search ADS PubMed  23. Samuel D , Rowe PJ. Effect of ageing on isometric strength through joint range at knee and hip joints in three age groups of older adults. Gerontology . 2009; 55: 621– 629. Google Scholar CrossRef Search ADS PubMed  24. Hussain SJ , Frey-Law L. 3D strength surfaces for ankle plantar- and dorsi-flexion in healthy adults: an isometric and isokinetic dynamometry study. J Foot Ankle Res . 2016; 9: 1– 10. Google Scholar CrossRef Search ADS PubMed  25. Webber SC , Porter MM. Reliability of ankle isometric, isotonic and isokinetic strength and power testing in older women. Phys Ther . 2010; 90: 1165– 1175. Google Scholar CrossRef Search ADS PubMed  26. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories . ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med . 2002; 166: 111– 117. CrossRef Search ADS PubMed  27. Hausdorff JM. Gait variability: methods, modeling and meaning. J Neuroeng Rehabil . 2005; 2: 1– 19. Google Scholar CrossRef Search ADS PubMed  28. Vergara ME , O’Shea FD, Inman RDet al.   Postural control is altered in patients with ankylosing spondylitis. Clin Biomech . 2012; 27: 334– 340. Google Scholar CrossRef Search ADS   29. Munro B , Page E, Visintainer M. Statistical methods for health care research . Philadelphia, PA: Lippincott Williams & Wilkins; 1986. 30. Mendes P , Wickerson L, Helm D. et al.   Skeletal muscle atrophy in advanced interstitial lung disease. Respirology . 2015; 20: 953– 959. Google Scholar CrossRef Search ADS PubMed  31. Lauretani F , Russo CR, Bandinelli Set al.   Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol . 2003; 95: 1851– 1860. Google Scholar CrossRef Search ADS PubMed  32. Bean JF , Kiely DK, Herman Set al.   The relationship between leg power and physical performance in mobility-limited older people. J Am Geriatr Soc . 2002; 50: 461– 467. Google Scholar CrossRef Search ADS PubMed  33. Reid KF , Fielding RA. Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev . 2012; 40: 4– 12. Google Scholar CrossRef Search ADS PubMed  34. Reid KF , Pasha E, Doros G. Longitudinal decline of lower extremity muscle power in healthy and mobility-limited older adults: influence of muscle mass, strength, composition, neuromuscular activation and single fiber contractile properties. Eur J Appl Physiol . 2014: 114: 29– 39. Google Scholar CrossRef Search ADS PubMed  35. Dos Santos C , Hussain SN, Mathur Set al.   Mechanisms of chronic muscle wasting and dysfunction after an intensive care unit stay: a pilot study. Am J Respir Crit Care Med . 2016; 194: 821– 830. Google Scholar CrossRef Search ADS PubMed  36. Marsh AP , Miller ME, Saikin AMet al.   Lower extremity strength and power are associated with 400-meter walk time in older adults: the InCHIANTI study. J Gerontol A Biol Sci Med Sci . 2006; 61: 1186– 1193. Google Scholar CrossRef Search ADS PubMed  37. Puthoff ML , Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations and disability in older adults. Phys Ther . 2007; 87: 1334– 1347. Google Scholar CrossRef Search ADS PubMed  38. Winters JD , Rudolph KS. Quadriceps rate of force development affects gait and function in people with knee osteoarthritis. Eur J Appl Physiol . 2014; 114: 273– 284. Google Scholar CrossRef Search ADS PubMed  39. Baert IAC , Jonkers I, Staes Fet al.   Gait characteristics and lower limb muscle strength in women with early and established knee osteoarthritis. Clin Biomech . 2013; 28: 40– 47. Google Scholar CrossRef Search ADS   40. Dallmeijer AJ , Baker R, Dodd KJ, Taylor NF. Association between isometric muscle strength and gait joint kinetics in adolescents and young adults with cerebral palsy. Gait Posture . 2011; 33: 326– 332. Google Scholar CrossRef Search ADS PubMed  41. Thompson N , Stebbins J, Seniorou M, Newham D. Muscle strength and walking ability in diplegic cerebral palsy: implications for assessment and management. Gait Posture . 2011; 33: 321– 325. Google Scholar CrossRef Search ADS PubMed  42. Steele KM , van der Krogt MM, Schwartz MH, Delp SL. How much muscle strength is required to walk in a crouch gait? J Biomech . 2012; 45: 2564– 2569. Google Scholar CrossRef Search ADS PubMed  43. D’Angelo MG , Berti M, Piccinini Let al.   Gait pattern in Duchenne muscular dystrophy. Gait Posture . 2009; 29: 36– 41. Google Scholar CrossRef Search ADS PubMed  44. Gaudreault N , Gravel D, Nadeau S, Houde S, Gagnon D. Gait patterns comparison of children with Duchenne muscular dystrophy to those of control subjects considering the effect of gait velocity. Gait Posture . 2010; 32: 342– 347. Google Scholar CrossRef Search ADS PubMed  45. Doglio L , Pavan E, Pernigotti Iet al.   Early signs of gait deviation in Duchenne muscular dystrophy. Eur J Phys Rehabil Med . 2011; 47: 587– 594. Google Scholar PubMed  © 2017 American Physical Therapy Association http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Physical Therapy Oxford University Press

Quantitative Evaluation of Muscle Function, Gait, and Postural Control in People Experiencing Critical Illness After Discharge From the Intensive Care Unit

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American Physical Therapy Association
Copyright
© 2017 American Physical Therapy Association
ISSN
0031-9023
eISSN
1538-6724
D.O.I.
10.1093/ptj/pzx102
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Abstract

Abstract Background The path to recovery of muscle strength and mobility following discharge from the intensive care unit (ICU) has not been well described. Objective The study objective was to quantify muscle function, gait, and postural control at 3 and 6 months after discharge in people who were recovering from critical illness and who were ventilated for 7 days or more. Design This was a nested longitudinal study with continuous inclusion of individuals over a 2-year period and with age- and sex-matched controls. Methods Twenty-four people were tested at 3 months after ICU discharge; 16 of them (67%) were reevaluated at 6 months (post-ICU group). Healthy controls (n = 12) were tested at a single time point. Muscle function of the knee extensors (KEs), plantar flexors (PFs), and dorsiflexors (DFs) was assessed on a dynamometer. Gait was measured using an electronic walkway, and postural control was measured with 2 portable force plates. Results Muscle weakness was observed across all muscle groups at 3 months, with the greatest strength reductions in the ankle PFs (45%) and DFs (30%). Muscle power was reduced in the PFs and DFs but was not reduced in the KEs. Gait in the post-ICU group was characterized by a narrower step, longer stride, and longer double-support time than in the controls. Improvements were found in KE strength and in stride time and double-support time during gait at 6 months. Leg muscle strength and power had moderate associations with gait velocity, step width, and stride length (r = .44–.65). Limitations The small heterogeneous sample of people with a high level of function was a limitation of this study. Conclusions Muscle strength and power were impaired at 6 months after ICU discharge and were associated with gait parameters. Future studies are needed to examine the role of muscle strength and power training in post-ICU rehabilitation programs to improve mobility. Intensive care unit (ICU)–acquired weakness (ICUAW) is an important consequence of critical illness. ICUAW affects about 25% of people on mechanical ventilation, particularly in those with prolonged mechanical ventilation,1 and is associated with greater morbidity and mortality.2–4 ICUAW develops within hours of admission, and is persistent5 during critical illness, as evidenced by an early reduction in quadriceps muscle size,6,7 abnormal muscle contractility,8 and muscle weakness.2–4 Development of ICUAW is the result of interacting factors such as length of ICU stay, sepsis, myotoxic medications (eg, corticosteroids, neuromuscular blockers), multi-organ dysfunction, aging, and comorbidities.9,10 Muscle weakness and functional deficits may persist for years after ICU discharge.11,12 Yet, few studies have quantified any long-term functional muscle deficits. In a study by van der Schaaf et al,13 handgrip strength was reduced to 50% of the predicted values 1 week after ICU discharge. However, Medical Research Council scores of the same participants were normal or near normal (grades 4 or 5).13 Poulsen et al14 used dynamometry to evaluate knee extensor muscle strength, power, and endurance in individuals 1 year after ICU discharge. Although all aspects of muscle performance were reduced compared to the controls, the rate of force development (an indicator of muscle power) was the most impaired.14 To date, the distal muscles of the lower extremity, such as the plantar flexors (PFs) and dorsiflexors (DFs) of the ankle, have not been evaluated. These muscle groups have important functional implications in gait and balance control.15,16 Loss of lower extremity muscle mass and strength is associated with mobility limitations,17,18 gait alterations,19 and impaired postural control and balance.20 Spatiotemporal gait parameters are commonly evaluated using instrumented walkways that measure gait velocity, step length and width, and time spent in single- and double-limb support.21 This information can be used to study changes in walking pattern that may reflect altered dynamic balance or neuromotor control.21,22 Quantitative posturography is an additional tool that uses force plates to estimate the center of pressure (COP), in order to determine postural control and static stability during quiet standing and functional tasks. However, these measures have not been applied in individuals following a critical illness. This unique biomechanical information may provide novel understanding into the impact of any potential postural control changes resulting from critical illness. The relationship between muscle function and mobility in people who have experienced a period of critical illness may provide important information about how to optimize physical rehabilitation to restore functional independence. To date, no studies have examined biomechanical properties of gait and postural control, together with muscle function, in this population. The objectives of this study were to quantify lower-limb muscle function and mobility outcomes at 3 and 6 months after ICU discharge; to compare with age- and sex-matched controls; and to identify associations between muscle strength and power with measures of gait and postural control in the post-ICU period. We hypothesized that deficits in muscle function, gait, and postural control would be observed at 3 months after ICU discharge compared to healthy controls, with improvement at 6 months post discharge. We also hypothesized that lower-limb muscle dysfunction would be associated with altered patterns of gait and postural control. Methods The study design was a nested, longitudinal study with continuous inclusion of people recruited between June 2011 to June 2013 from an ongoing study of long-term outcomes following critical illness11 (phase 1: toward RECOVER; trial registration: NCT00896220). Informed consent was obtained from all participants. Inclusion and exclusion criteria are detailed in the primary study.11 In brief, people in the ICU were included if they were 16 years or older and were mechanically ventilated for at least 7 days. People in the ICU were excluded if they had a preexisting or current neurological injury, had a diagnosis of neuromuscular disease, or were nonambulatory prior to their ICU admission. Specifically, for this substudy participants were excluded if they reported any functional limitations affecting their ability to perform the required muscle function and mobility tests. Control participants were recruited from the local community, and were matched for age and sex to the post-ICU group. Control participants were excluded if they reported musculoskeletal problems (eg, arthritis, previous orthopedic surgery); a history of neurological conditions (eg, stroke, Parkinson disease); or cardiovascular, respiratory, or metabolic conditions (eg, heart attack, asthma, diabetes) that could affect muscle strength, balance, or gait performance. Participants in the post-ICU group were from a sample of convenience from those attending follow-up appointments at 3 and 6 months for the primary study.11 Participants were approached at the end of their appointment by the study coordinator to determine their interest in participating in the muscle and gait substudy. Follow-up appointments at 6 months were booked through telephone reminders by the study coordinators. Controls were tested at a single time point and were recruited between March 2012 and July 2013. Muscle Function Assessment Muscle strength (torque-generating capacity of the muscle) and power (rate of torque generation determined from a torque-time curve) were measured using Biodex System 4 isokinetic dynamometer (Biodex Medical Systems, Shirley, New York). Participants were asked to perform maximum isometric voluntary contractions of the knee extensors (KEs), PFs, and DFs. Participants were seated on the Biodex with straps placed across the shoulders, hips, and thigh for stability. Hip angle was kept at 90° for all assessments. Joint angles selected for isometric tests were based on the angle of peak torque generation: KEs at 60° of knee flexion;23 and PFs and DFs with the ankle joint at 15° of plantar flexion with the knee stabilized at 35° to 40° degrees of flexion. We selected a single for both PF and DF torque that optimized the torque generation for both muscle groups.24 For each muscle group tested, a warm-up contraction was followed by 5 maximal efforts to obtain peak torque. A 1-minute rest period was given between trials to minimize muscular fatigue. The raw signals from the Biodex dynamometer (torque, position, velocity) were sampled at a frequency of 100 Hz. Peak torque (N·m) was calculated at the highest torque reached among the trials, within 10% coefficient of variation. The rate of torque development (N·m/s), a measure of muscle power, was calculated from the time taken between 40% to 80% of the peak torque25 and taken from the highest of the 5 trials. Gait and Postural Control Assessment Gait was assessed during a 6-minute walk test conducted in a quiet and leveled 30-m corridor using standardized procedures.26 Spatiotemporal gait parameters were assessed using a portable, 6-m-long instrumented carpet (GAITRite; CIR Systems Inc, Franklin, New Jersey), which was placed midway along the corridor. GAITRite signals were sampled at 50 Hz, with the following variables extracted for analysis: gait velocity, stride time, stride length, step width, single support time, and double-support time. In addition, the coefficient of variation for stride time was calculated as a measure of gait stability, with lower variation indicating greater stability and reduced fall risk.27 Postural control was assessed during quiet standing using two 6-degrees-of-freedom force plates (AMTI, Watertown, Massachusetts). All standing trials were on level ground and force plates. These plates were placed adjacent to each other, such that participants stood with 1 foot on each plate. The location of each foot was marked for repeated trials. The duration of each trial was 120 seconds, and analysis was completed on the middle 60 seconds. Participants engaged in four 2-minute trials of quiet standing; 2 eyes open and 2 eyes closed. Ground reaction forces were collected and sampled at 100 Hz and digitally filtered using a Butterworth filter with a 4-Hz cutoff frequency. Mean power frequency content for both the anteroposterior (AP) and mediolateral (ML) directions was determined using a Discrete Fast Fourier Transformation to calculate the average power of the signal content. The mean power frequency defines the average frequency of the COP signal during a quiet standing session. The root mean square (RMS) of the COP signal represents the magnitude of variability. Both measures were used to characterize balance control, and have been employed to assess postural control strategies with clinical populations.28 Data Analysis All statistical analyses were completed using JMP v. 9.0 software (SAS Campus, Cary, North Carolina). Normality was assessed using the Shapiro-Wilk test. Data that did not satisfy the assumption of normality was transformed with a logarithmic for negatively skewed data or square transformation for positively skewed data. Measures requiring transformation included physical therapy (KEs and PFs), rates of torque development (KEs and PFs), gait velocity, stride length, step width, stride-time coefficient of variation, single-support time, double-support time, AP RMS, ML RMS, and AP mean power frequency. To test our first hypothesis (between-group comparisons) and second hypothesis (change over time), a mixed-effects analysis of variance {group [control/post-ICU (3 months or 6 months)]} was used to compare each group on muscle strength, power, and gait outcomes. A mixed-effects analysis of variance {group [control (3 months or 6 months)] × vision (eyes open or eyes closed)} was used to test postural control–dependent measures (RMS and mean power frequency of COP). Tukey-Kramer post hoc comparisons were made on any significant interactions effects. Significance was set a priori at an alpha value of .05. The 95% confidence intervals of the mean difference were calculated for each variable. To test our third hypothesis, the Pearson r was used to determine correlations between mobility and muscle function measures in each group, and was interpreted as follows: very low = .15–.24, low = .25–.49, moderate = .50–.69, high = .70–.89, and very high = .90–1.00.29 Role of the Funding Source Funding support was provided by a Canadian Institutes of Health Research Operating Grant (M.H., J.I.C.), a New Investigator Award (J.I.C.), and Ontario Ministry of Health Innovation Funding (M.H., J.I.C.). The funders had no role in the study's design, conduct, and reporting. Results Sample Characteristics Twenty-four individuals were tested 3 months after ICU discharge (6 women; age = 47.5 ± 16.1 years; weight = 74.2 ± 19.6 kg; height = 1.68 ± 0.12 m); 16 of them (67.0%) repeated the testing at 6 months after discharge (Fig. 1). Participants lost to follow-up at 6 months were primarily due to being too busy or unavailable for a follow-up appointment (ie, lack of time) (n = 7) and missed appointment (n = 1). Age- and sex-matched healthy controls (n = 13) were tested at a single time point (4 women; age = 44.2 ± 16.2 years; weight = 72.9 ± 14.5 kg; height = 1.12 ± 0.42 m). Detailed characteristics of the post-ICU group are shown in Table 1. The subgroup of 16 individuals who were tested at 6 months after ICU discharge did not differ from the group who was tested at 3 months in demographic or clinical characteristics (Tab. 1). Figure 1. View largeDownload slide Diagram of participant inclusion. ICU = intensive care unit. Figure 1. View largeDownload slide Diagram of participant inclusion. ICU = intensive care unit. Table 1. Characteristics of Participants at 3 and 6 Months After ICU Discharge.a Characteristic  Participants at 3 mo (n = 24)  Participants at 6 mo (n = 16)  Age (y)  47.5 ± 16.1  46.4 ± 19.5  Weight (kg)  74.2 ± 19.6  72.9 ± 22.5  Height (m)  1.68 ± 0.12  1.68 ± 0.13  BMI (kg/m2)  25.9 ± 5.2  25.7 ± 5.0  APACHE II (24 h after ICU admission)  19.5 ± 7.2  18.6 ± 6.7  Duration of mechanical ventilation (d)  16 ± 11  15 ± 10  ICU length of stay (d)  43 ± 24  43 ± 28  Hospital length of stay (d)  44 ± 26  44 ± 28  6MWT (m)  441 ± 124 (63.0 ± 17.0)b  494 ± 118 (71.0 ± 17.0)b  FVC (% predicted)  79.0 ± 18.0  80.0 ± 21.0  FEV (% predicted)  74.0 ± 17.0  77.0 ± 20.0  Corticosteroid treatment (% of participants)  40.0 (n = 9)  31.0 (n = 5)  FIM scorec  117 ± 9  118 ± 8  Characteristic  Participants at 3 mo (n = 24)  Participants at 6 mo (n = 16)  Age (y)  47.5 ± 16.1  46.4 ± 19.5  Weight (kg)  74.2 ± 19.6  72.9 ± 22.5  Height (m)  1.68 ± 0.12  1.68 ± 0.13  BMI (kg/m2)  25.9 ± 5.2  25.7 ± 5.0  APACHE II (24 h after ICU admission)  19.5 ± 7.2  18.6 ± 6.7  Duration of mechanical ventilation (d)  16 ± 11  15 ± 10  ICU length of stay (d)  43 ± 24  43 ± 28  Hospital length of stay (d)  44 ± 26  44 ± 28  6MWT (m)  441 ± 124 (63.0 ± 17.0)b  494 ± 118 (71.0 ± 17.0)b  FVC (% predicted)  79.0 ± 18.0  80.0 ± 21.0  FEV (% predicted)  74.0 ± 17.0  77.0 ± 20.0  Corticosteroid treatment (% of participants)  40.0 (n = 9)  31.0 (n = 5)  FIM scorec  117 ± 9  118 ± 8  a 6MWT = 6-minute walk test, APACHE = Acute Physiology and Chronic Health Evaluation, BMI = body mass index, FEV = forced expiratory volume, FIM = Functional Independence Measure, FVC = forced vital capacity, ICU = intensive care unit. b Values in parentheses are percent predicted. c Obtained 7 days after ICU discharge; scores ranged from 18 (lowest) to 126 (highest). View Large Muscle Strength and Power Muscle strength and power measures are shown in Figure 2. A significant group effect in muscle strength was found for KE peak torque (P = .01) and DF peak torque (P = .002). Tukey-Kramer post hoc analysis revealed significant differences between controls and post-ICU at 3 months (95% CIs = 25.08 to 88.60 for KEs and 7.06 to 18.96 for DFs) as well as controls and post-ICU at 6 months (95% CIs = 0.55 to 80.50 for KEs and 6.37 to 19.29 for DFs). No significant differences were observed in muscle strength measures between the 3- and 6-month post-ICU groups. Only minor, nonsignificant improvements in the strength of the KEs (15.2%) and DFs (8.3%), with a slight decrement in PFs (−3.7%), were observed between 3 months and 6 months in the post-ICU group. Figure 2. View largeDownload slide Comparison of mean absolute values of strength (top) and power (bottom) of lower-limb muscle groups between participants at 3 and 6 months after discharge and age- and sex-matched controls. Values are means and standard deviations. Asterisks indicate significant differences, with significance accepted at a P value of <.05. DF = dorsiflexors, KE = knee extensors, PF = plantar flexors, RTD = rate of torque development. Figure 2. View largeDownload slide Comparison of mean absolute values of strength (top) and power (bottom) of lower-limb muscle groups between participants at 3 and 6 months after discharge and age- and sex-matched controls. Values are means and standard deviations. Asterisks indicate significant differences, with significance accepted at a P value of <.05. DF = dorsiflexors, KE = knee extensors, PF = plantar flexors, RTD = rate of torque development. For muscle power measures, between-group differences were found for the DF rate of torque development (P = .03) and post hoc comparisons revealed that controls differed from the 3-month post-ICU (95% CI for DFs = 10.85 to 55.09) and 6-month post-ICU (95% CI for DFs = 9.16 to 56.20) groups. No significant differences were observed between the 3- and 6-month post-ICU groups. Minimal improvement in power was found between 3 and 6 months in KEs (6.2%) and DFs (1%), whereas a decrement in power in PFs (−10.7%) was observed. Spatiotemporal Parameters of Gait and Postural Control The gait parameters are summarized in Table 2. Significant group effects were observed for step width (P = .01), step length (P = .01), and double-support time (P = .01). Tukey-Kramer post hoc comparisons revealed that the 3-month post-ICU group had a significantly shorter step length (95% CI = 0.09 to 0.35), narrower step width (95% CI = 0.05 to 0.19), and spent more time in double-support time (95% CI = −0.09 to −0.01) than controls. No differences in gait parameters were found between the post-ICU group at 6 months and the control group or between the post-ICU group at 3 months and the post-ICU group at 6 months. Table 2. Spatiotemporal Gait Parameters in Participants After ICU Discharge and Healthy Controls.a Gait Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  P  Post Hoc Significant Comparisons  Gait velocity (m/s)  1.50 ± 0.23  1.31 ± 0.35  1.56 ± 0.17  .06    Stride length (m)  1.61 ± 0.15  1.39 ± 0.26  1.46 ± 0.26  .01c  CON vs 3MO  Step-width (cm)  0.81 ± 0.08  0.69 ± 0.15  0.79 ± 0.07  .01c  CON vs 3MO  Stride time (s)  1.05 ± 0.12  1.09 ± 0.14  1.05 ± 0.10  .07    Single-support time (s)  0.42 ± 0.04  0.41 ± 0.03  0.40 ± 0.02  .13    Double-support time (s)  0.23 ± 0.04  0.28 ± 0.08  0.25 ± 0.09  .01c  CON vs 3MO  Stride time CV (%)  1.62 ± 0.79  2.42 ± 1.66  2.26 ± 1.19  .21    Gait Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  P  Post Hoc Significant Comparisons  Gait velocity (m/s)  1.50 ± 0.23  1.31 ± 0.35  1.56 ± 0.17  .06    Stride length (m)  1.61 ± 0.15  1.39 ± 0.26  1.46 ± 0.26  .01c  CON vs 3MO  Step-width (cm)  0.81 ± 0.08  0.69 ± 0.15  0.79 ± 0.07  .01c  CON vs 3MO  Stride time (s)  1.05 ± 0.12  1.09 ± 0.14  1.05 ± 0.10  .07    Single-support time (s)  0.42 ± 0.04  0.41 ± 0.03  0.40 ± 0.02  .13    Double-support time (s)  0.23 ± 0.04  0.28 ± 0.08  0.25 ± 0.09  .01c  CON vs 3MO  Stride time CV (%)  1.62 ± 0.79  2.42 ± 1.66  2.26 ± 1.19  .21    a CON vs 3MO = healthy controls versus participants at 3 months after intensive care unit (ICU) discharge, CV = coefficient of variation. b Values are reported as mean±standard deviation. c Significant at an α value of .05. View Large Table 3 displays mean postural control data for each compared group and condition. A main effect of vision (eyes open vs eyes closed) was observed for several of the postural control measures across all groups. Specifically, differences in the ML RMS (P = .049; 95% CI = –0.02 to 0.08), AP RMS (P = .001; 95% CI = −0.25 to −0.05), and ML mean power frequency (P = .04; 95% CI = −0.09 to 0.01) were observed with eyes open vs eyes closed, indicating that postural control was affected with the inclusion of visual input in both the control and the post-ICU groups alike. Comparisons of postural control measures between the 3- and 6-month post-ICU and control groups did not reveal any significant main or interaction effects. Table 3. Postural Control Measures in Participants After ICU Discharge and Healthy Controls.a Eye Condition  Postural Control Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  Open  RMS (AP) (mm)  0.38 ± 0.06  0.55 ± 0.17  0.46 ± 0.13  RMS (ML) (mm)  0.23 ± 0.06  0.34 ± 0.21  0.47 ± 0.20  MPF (AP) (Hz)  0.22 ± 0.10  0.24 ± 0.11  0.27 ± 0.13  MPF (ML) (Hz)  0.26 ± 0.06  0.24 ± 0.10  0.21 ± 0.09  Closed  RMS (AP) (mm)  0.52 ± 0.23  0.68 ± 0.23  0.63 ± 0.13  RMS (ML) (mm)  0.26 ± 0.12  0.34 ± 0.26  0.30 ± 0.19  MPF (AP) (Hz)  0.30 ± 0.10  0.24 ± 0.11  0.21 ± 0.11  MPF (ML) (Hz)  0.28 ± 0.08  0.27 ± 0.14  0.26 ± 0.10  Eye Condition  Postural Control Measure  Healthy Controls (n = 13)b  Participants at 3 mo After ICU Discharge (n = 24)b  Participants at 6 mo After ICU Discharge (n = 16)b  Open  RMS (AP) (mm)  0.38 ± 0.06  0.55 ± 0.17  0.46 ± 0.13  RMS (ML) (mm)  0.23 ± 0.06  0.34 ± 0.21  0.47 ± 0.20  MPF (AP) (Hz)  0.22 ± 0.10  0.24 ± 0.11  0.27 ± 0.13  MPF (ML) (Hz)  0.26 ± 0.06  0.24 ± 0.10  0.21 ± 0.09  Closed  RMS (AP) (mm)  0.52 ± 0.23  0.68 ± 0.23  0.63 ± 0.13  RMS (ML) (mm)  0.26 ± 0.12  0.34 ± 0.26  0.30 ± 0.19  MPF (AP) (Hz)  0.30 ± 0.10  0.24 ± 0.11  0.21 ± 0.11  MPF (ML) (Hz)  0.28 ± 0.08  0.27 ± 0.14  0.26 ± 0.10  a AP = anteroposterior, ICU = intensive care unit, ML = mediolateral, MPF = mean power frequency, RMS = root mean square. b Values are reported as mean±standard deviation. View Large Relationships of Muscle Function With Gait and Posture Significant correlations between muscle function and gait measures were observed in the post-ICU and control groups (eTab. 1; available at https://academic.oup.com/ptj). Leg muscle strength and power showed low to moderate positive correlations with gait velocity, stride length, and step width in the post-ICU group at 3 months (r = .44 to .65; P = .003–.02) (eTab. 1). PF strength and power were negatively associated with double-support time (r = −.42; P = .035) and single-support time (r = −.50; P = .011). KE power also showed a negative association with double-support time (r = −.039; P = .049). In the control group, KE strength, KE power, and PF strength showed moderate correlations with stride length and step width. However, muscle function was not associated with gait velocity or temporal parameters (eTab. 1). Postural control measures were not associated with muscle function measures in either the post-ICU or the control group (eTab. 2). Discussion To our knowledge, this is the first study to quantify muscle function, gait, and postural control in the early, post-discharge recovery period in individuals who were mechanically ventilated for at least 7 days in the ICU. Our results demonstrate impaired lower limb muscle strength and power, particularly of the distal leg muscles, with only minimal changes in muscle function from 3 to 6 months after ICU discharge. Indications of a “cautious gait” strategy were observed in the 3-month post-ICU group compared to the control group, but this was no longer present in the 6-month post-ICU group. Alterations in gait parameters were associated with impairments in leg muscle strength and power with the 3-month post-ICU group. Finally, static postural control was not impaired in individuals after ICU discharge, and did not show a relationship with muscle function. Our findings suggest that a “cautious gait” strategy observed in the early phase after ICU discharge is consistent with deficits in lower extremity muscle strength and power. Our data revealed a deficit in knee extensor strength in people recovering from critical illness 3 months after ICU discharge, with minimal (15.2%) improvement by 6 months. Knee extensor power was also compromised in our cohort at 3 and 6 months post discharge. This is similar to the findings of Poulsen et al14 in men who were 12 months after ICU discharge and who had lower peak torque and rate of torque development of the knee extensors compared to controls. In our study, we also measured the strength and power of distal muscles; the ankle PFs and DFs. Our results revealed significant reductions in DF muscle strength and power between the post-ICU group at 3 and 6 months compared to the control group. The deficits observed in PF strength and power in the post-ICU group did not reach statistical significance, which may have been due to large within-group variability in the measures. Weakness of proximal muscle groups, such as the hip extensors and hip abductors, is common in ICUAW; however, due to limitations in positioning participants comfortably to test these muscles using computerized dynamometry (supine or side lying), we were unable to test these muscle groups in the current study. We found that at 3 months after ICU discharge, there were greater deficits in muscle power than muscle strength compared to controls, particularly in the distal leg muscles. At 3 months, the post-ICU group demonstrated 43.5% lower rate of torque development for KEs, 42.3% lower for DFs, and 69.3% lower for PFs compared to the control group. Similarly, decrements in muscle power with aging are more substantial than loss of muscle strength,30 and muscle power is reported to be a better predictor of physical function (walking speed and sit-to-stand) than muscle strength in older adults.31–33 The age-related decrements in muscle power have been attributed to a preferential atrophy and loss of fast twitch (type II) muscle fibers, loss of motor units, impaired neuromuscular recruitment, and muscle fat infiltration.34 In individuals at 12 months after ICU discharge, Poulsen et al14 found that muscle decrements were due to intrinsic muscle properties rather than deficits in neural activation. A study from our group in individuals at 6 months after ICU discharge also showed that the recovery of muscle size may not translate into improved muscle functional outcomes, lending further support for the importance of deficits in the intrinsic muscle contractile capacity.35 Therefore, further studies are needed to understand the mechanisms of muscle power deficits particularly in DFs, which appear to persist for a longer period after ICU discharge. Our participant group exhibited signs of “cautious” gait at 3 months post discharge. This result suggests that during gait, participants had an altered walking strategy, as demonstrated by significantly shorter strides and longer time spent in double support as well as slower gait velocity and longer stride time. Improvements in gait parameters were observed at 6 months and did not demonstrate any statistical difference between our 6-month group and control group. Step length and step width were associated with KE, DF, and PF strength and power outcomes. Similar relationship of gait parameters and muscle function has been reported in older adults,36,37 knee osteoarthritis,38,39 and neuromuscular diseases.40–45 Impairments in muscle strength and power may also have implications for daily functional tasks such as sit-to-stand, higher-level balance activities, and physical activity levels, and should be examined in the post-ICU population. Our data did not reveal any differences in static postural control in the early post-ICU discharge period using quantitative posturography between groups tested in the current study. However, the use of visual input (eyes open vs eyes closed, quiet standing) affected postural control and indicates a normal dependence on vision to maintain balance for participants, considering no interaction was found between visual input and group. This study included a small, heterogeneous sample of individuals who were tested at 2 discrete time points after ICU discharge. We only tested individuals who volunteered to undergo additional tests of physical function, apart from the main study. These individuals were younger and had better function, based on 7-day post-ICU Functional Independence Measure scores, than the overall cohort in the toward RECOVER study. This placed them in the disability risk group with the best recovery trajectory.11 These participants were likely to have better functional recovery, and may also have better caregiver support than the larger group of patients in the toward RECOVER study. This limits the generalizability of our findings. In this small sample, we were not able to investigate several confounding factors affecting muscle function, such as age, length of ICU stay, or comorbidities. We did not systematically collect the use of myotoxic and/or neurotoxic medications during the period of critical illness. The study participants may have been exposed to high-dose corticosteroids affecting muscle, or ototoxic and neurotoxic medications affecting their vestibular system (eg, high-dose Lasix, aminoglycosides, and vancomycin), which could have led to long-term deficits in muscle function or postural control. However, medication use was not carefully tracked in our study participants. The study was also underpowered for within-group comparisons of participants from 3 to 6 months; post hoc power analysis revealed that we achieved 20.0% power for difference in KE strength from 3 to 6 months. Although all participants received physical therapy, including early mobilization in the ICU, we did not specifically examine activity during hospitalization, or current level of physical activity or functional status prior to ICU admission. Furthermore, our study recruited participants who did not feel restricted in their mobility and could perform the tests—all of which may have impacted the data reported. Finally, our postural control data reflected the COP trajectory and did not directly reflect center-of-mass displacements, which would require full body kinematics. Therefore, direct conclusions on control of center of mass cannot be made but would provide further insight into how postural control was affected in our study participants. The findings from the current study provide a longitudinal description of mobility and muscle function in a group of individuals recovering from critical illness. Our findings indicate that lower-limb muscle functions remain in deficit up to 6 months after ICU discharge, and that muscle dysfunction is more prominent in the distal muscles of the ankle compared to the knee extensors. Muscle strength and power are associated with the parameters of gait, whereas static postural control is not affected in these individuals or associated with muscle function. The findings of this study provide direction for prospective observational and rehabilitation intervention studies in the early post-ICU discharge period. Future studies are needed to examine the role of proximal muscle groups (eg, hip abductors and extensors) on gait and mobility in this population and the impact of muscle weakness on other functional outcomes, such as physical activity level and higher-level balance tasks in the post-ICU period. Funding Funding support was provided by a Canadian Institutes of Health Research Operating Grant (M.H., J.I.C.), a New Investigator Award (J.I.C.), and Ontario Ministry of Health Innovation Funding (M.H., J.I.C.). Author Contributions and Acknowledgments Concept/idea/research design: M. Vergara, J.I. Cameron, M. Herridge, W.H. Gage, S. Mathur Writing: J.B. Kiriella, J.I. Cameron, W.H. Gage, S. Mathur Data collection: J.B. Kiriella, T. Araujo, M. Vergara, L. Lopez-Hernandez, M. Herridge, S. Mathur Data analysis: J.B. Kiriella, L. Lopez-Hernandez, M. Herridge, S. Mathur Project management: J.B. Kiriella, T. Araujo, M. Vergara, S. Mathur Fund procurement: J.I. Cameron Providing participants: M. Herridge Providing facilities/equipment: S. Mathur Providing institutional liaisons: M. Herridge, S. Mathur Consultation (including review of manuscript before submitting): J.I. Cameron, M. Herridge, S. Mathur The authors thank the administrative staffs at Toronto General Hospital and St Michael's Hospital for their continual assistance with recruiting and organizing testing sessions. Ethics Approval All procedures were carried out in accordance with the ethical standards of the University of Toronto Human Research Ethics Board (REB #24421) and the University Health Network Research Ethics Board (REB #08-080). 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Physical TherapyOxford University Press

Published: Jan 1, 2018

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