Abstract
Introduction
Multiple sclerosis (MS) is a chronic progressive disease of the central nervous system. Signs and symptoms of MS are dependent on the location of the lesions within the central nervous system. Vision, motor, sensory and central processing deficits are common in persons with MS (PwMS) and contribute to impaired balance and gait and resultant falls. Compared to healthy individuals, PwMS have increased postural sway in quiet stance, decreased gait speed (Cameron & Lord, 2010) and increased fall incidence (Mazumder, Murchison, Bourdette, & Cameron, 2014). Recently researchers have established a relationship between postural control and gait measures (Fritz et al., 2015 a, b). Voluntary antero-posterior postural sway is highly correlated with gait speed (Fritz et al., 2015 a). Over time increases in static posturography and decreases in voluntary postural sway are associated with a decline in gait velocity in PwMS (Fritz et al., 2015 b). Also, static posturography, specifically the center of pressure path while standing feet apart with eyes open, predicted the risk for accidental falls over 3 months (Prosperini et al., 2013).
Trunk muscle performance has been implicated in postural control and gait dysfunction. Fall history in the elderly has been reported to be associated with trunk stability during walking (Toebes et al., 2012). Abdominal and back muscles contribute significantly to trunk control throughout the gait cycle and should be considered in the design of rehabilitation programs for impaired trunk control and fall prevention (Klemetti et al., 2014; Hu et al., 2011). A recent systematic review (Granacher et al., 2013) reported correlations between trunk muscle strength, balance and falls in older adults. Additionally, core strengthening exercise has improved balance and functional performance, and reduced falls in older adults (Granacher et al., 2013). However, little attention has been paid to the contribution of trunk muscle performance to balance and gait deficits in PwMS. Recently, it was reported PwMS had increased trunk range of motion during gait which may contribute to instability (Spain et al., 2012). Verheyden et al., (2006) reported impaired trunk performance in PwMS with a suggested relationship to disability. A case series provided preliminary evidence on the effectiveness of core stability training to improve balance and mobility in PwMS (Freeman et al., 2010).
Trunk stability requires low level activation of the trunk flexor and extensor muscles (Cholewicki, Panjab, & Khachatryan, 1997). Ultrasound imaging has been used to study the structure and performance of these muscles in persons with low back pain and healthy individuals (Kiesel et al., 2007; Teyhen 2012). Ultrasound imaging reference measurements have been established for trunk muscle thickness at rest and contracted to be used for comparisons to individuals with pain, altered function or pathology (Teyhen et al., 2012; Hebert, Koppenhaver, Parent, & Fritz, 2009; Koppenhaver et al., 2009).
Biomechanical theory suggests that sufficient spine stability for daily tasks is not compromised by insufficient trunk strength, but instead by insufficient endurance (McGill, 2007). Additionally, trunk muscle performance has been evaluated using isometric endurance tests. Several researchers have established the relationship between trunk endurance and static balance in young adults (McGill, Childs, & Liebenson, 1999; del Pozo Cruz et al., 2013; Barati et al., 2013), while Suri et al. (2013) reported a strong relationship between trunk extension endurance and the Short Physical Performance Battery and Berg Balance Scale in community dwelling older adults. Change in trunk extension endurance has been associated with meaningful change on the Berg Balance Scale and Unipedal Stance Test following a training program in older adults (Suri et al., 2011). However, only one known study has examined the validity and reliability of trunk endurance tests in PwMS (Fry, Huang, & Rodda, 2015). The relationship of trunk performance to postural control and gait has not been adequately studied in PwMS.
The purposes of this study were to: (1) compare trunk muscle structure and performance in PwMS to healthy age and gendered-matched controls (HC), (2) determine the effects of isometric trunk endurance testing on postural control in both populations and (3) determine the relationship of trunk performance with balance, gait and step activity in PwMS.
Methods
Participants
Fifteen ambulatory people with mild to moderate MS and 15 age and gender-matched healthy controls (HC) participated in the study. See Table 1 for participant demographics. PwMS were recruited through MS Society support groups, a local hospital rehabilitation department and a neurologist. HC were recruited from the local community. Exclusion criteria included: exacerbation of MS within past three months; current or recent history (within six months) of low back pain which resulted in either change in physical activity, need for medical care or three lost days from work; history of spinal, or abdominal surgery; lower extremity joint replacement surgery; respiratory or neurologic disorders (other than MS); structural scoliosis; body mass index (BMI) > than 30 kg/m2; cardiac pacemaker; severe arthritis resulting in joint deformities of the hips, knees or feet; and pain with weight bearing; pregnancy within the last 2 years; cognitive impairment as measured by Mini-Cognitive Test (Borson et al., 2000); inability to walk 14 meters or inability to stand 3 minutes without support. The study was approved by Elon University Institutional Review Board and all participants provided written informed consent.
Procedures
In one session lasting 2.5 hours, each participant was interviewed to obtain a medical history and then completed a battery of self-reported outcome measures, ultrasound imaging of trunk muscles, a 10 meter walk test, and isometric trunk endurance tests. A quiet standing postural sway test was performed before and after trunk endurance tests. At the end of the session participants were provided with a StepWatch Activity Monitor (Modus Health LLC., Washington DC) to be worn for 7 days to record step activity.
Self-reported outcome measures
The MS Walking Scale (MSWS-12), a 12-item questionnaire, was used to determine each PwMS’s perception of their walking ability (Hobart et al., 2003) in the prior two weeks. Raw scores were used with a possible range of 12 to 60. A higher score denotes greater perceived limitations in walking. Each participant’s concern about falling during daily activities was collected using The Short Falls Efficacy Scale-International (FES-I), a 7-item questionnaire (Kempen et al., 2008). A higher score denotes greater concern for falling. The Modified Fatigue Impact Scale – 5 (MFIS-5), a five item questionnaire, was used to determine each participant’s perception of how fatigue affected him or her over the past four weeks. A higher score indicates a greater impact of fatigue (Multiple Sclerosis Council for Clinical Practice Guidelines, Paralyzed Veterans of American, 1998). Fatigue was also assessed before and after trunk endurance testing. Each subject’s perception of current fatigue was reported on a 0 to 10 Numeric Rating Scale with 10 being maximum fatigue and 0 no fatigue. Finally, each participant in the PwMS group completed the Self-administered Expanded Disability Status Scale (EDSS-S), a self-report of the disability status of PwMS (Bowen, Gibbons, & Kraft, 2001). The EDSS-S strongly correlates with a physician-administered EDSS (Bowen, Gibbons, & Kraft, 2001 ).
Ultrasound imaging
Trunk muscle structure was examined using Terason T3200 (Burlington, MA) ultrasound imaging of the lateral abdominals (transversus abdominis, internal oblique, external oblique) and mulitifidi muscles. Prior to imaging each participant received brief instruction in the anatomy and function of the abdominal muscles and the proper performance of the abdominal drawing-in maneuver (ADIM), a maneuver to preferentially activate the transversus abdominis. Participants were positioned on a plinth in a supine hook-lying position with arms across the chest and the head in midline. The ADIM was performed by pulling the abdominal muscles up and in toward the spine during exhalation while maintaining a neutral posture of the lumbar spine. The examiners provided verbal and hands on cues to minimize substitution patterns and facilitate proper performance. After practice three ultrasound images of the lateral abdominal muscles were taken on each side at rest and during the ADIM (Teyhen et al., 2007).
Each participant then received brief instruction in the anatomy and function of the multifidi muscles. Participants were positioned prone on a plinth witha pillow positioned under the pelvis and both arms at 120 degrees of shoulder abduction and 90 degrees of elbow flexion. Three ultrasound images were taken at the level of the L4 lumbar multifidi at rest (on the left and right sides) and during contraction. Submaximal contraction of the multifidi occurred during a contralateral arm lift, approximately 2 inches off the table while holding a light hand weight based on the subject’s body mass (Koppehaver et al., 2009). Stored ultrasound images of trunk muscles at rest and during ADIM (Fig. 1a, b) and prone at rest and during contralateral arm lift (Fig. 2a, b) were used to measure thickness of muscles using Image J software, version 1.38, Oct 2006, provided by NIH. A contraction ratio of muscle thickness defined as a ratio of thickness in contracted and resting states was calculated for: transversus abdominis (TrA), external and internal oblique (EOIO) combined, total lateral abdominal muscles (TLA = TrA + EO + IO) and multifidi (MTF) for each side.
10 Meter walk test
Each participant completed two trials each at self-selected comfortable and fast pace walking 14 m with the middle 10 m timed using a standard stopwatch. Mean gait speed was calculated for each condition.
Postural sway test: Each participant stood quietly with their eyes open and feet in a comfortable position for 60 seconds on the BioSway system (Biodex Medical Systems, Shirley, NY) while center of pressure (CoP) data was collected. The comfortable foot position was marked and used for both trials. Range and mean velocity, path length in the medio-lateral (ML) and antero-posterior (AP) directions along with total path length and 95% elliptical sway area were analyzed for each trial of quiet standing using the Patient Data Collection software (Biodex Medical Systems, Shirley, NY) and custom-written Matlab script (MathWorks, Inc., Natick, MA; Evans et al., 2015).
Trunk isometric endurance tests (McGill, Childs & Liebenson, 1999) (Fig. 3)
Each test was timed using a standard stopwatch. Isometric trunk flexion endurance was tested with each participant positioned on a treatment table in a sit-up position with a trunk angle of 60 degrees and feet secured with a belt to the treatment table. Initially, the trunk was supported by a wedge which was then removed. Each participant was instructed to maintain the position as long as possible (Fig. 3a). The test was stopped when the participant could no longer maintain the position or at a maximum time of 10 minutes. After a 5 minute rest each participant was positioned prone on the treatment table for the isometric trunk extension endurance test with the participant’s anterior superior iliac spines of the pelvis at end of table and arms across the chest with legs and ankles strapped to the treatment table. Each participant was instructed to maintain the horizontal position for as long as possible (Fig. 3b). The test was stopped when the participant could no longer hold the test position. Unpublished data from our lab demonstrated good inter-rater reliability (ICC = 0.99) and good test-retest reliability (ICC range = 0.92 flexion to 0.97 extension) for the trunk isometric endurance tests in PwMS.
Step activity
Each participant was instructed to wear a step activity monitor StepWatch (Modus Health LLC., Washington DC) for seven days during all waking hours. Step activity monitors have been demonstrated to produce highly accurate measurement of steps in PwMS (Sandroff et al., 2014). Each participant kept a daily log of time wearing the monitor which was compared for accuracy to the data downloaded from the monitor. The step activity monitor collects data on the number of strides the participant takes (heel-strike to heel-strike) in consecutive one minute intervals (defined as a “bout”). This data was downloaded using the software provided by the company. The data was further processed using custom-written Matlab script to obtain: total number of steps; number of bouts; average time per bout; average number of steps per bout; total minutes of activity; and a % of inactive time (Cavanaugh, Gappmaier, Dibble, & Gappmaier, 2012). An average of seven days for each of these variables was used for statistical analysis.
Statistical analysis
Age, body mass index (BMI), FES-I score and MFIS-5 scores for both the groups were compared using independent samples t-test. An independent samples t-test was run to compare the muscle thickness values in resting state of TrA, IO, EO, EOIO, TLA and MTF muscles of PwMS and healthy controls. A Side (Right vs. Left)×Group (HC vs. PwMS) ANOVA was run separately for contraction ratio of TrA, EOIO, TLA, and MTF muscles. A paired samples-test was run to compare the contraction ratio values of TrA, IO, EO, EOIO, TLA and MTF muscles on the impaired and unimpaired sides in PwMS. Side was used as the within-subject factor, and Group was used as a between-subject factor. Time (Pre, Post)×Group (PwMS, HC) mixed ANOVA was performed to estimate the effects on postural sway due to trunk endurance testing. Trunk flexion and extension endurance times, self-selected comfortable and fast gait speed and step activity measures were compared between both the groups using either an independent samples T-test or Mann-Whitney U test depending on the distribution of the data. Correlation analysis was performed to determine the relationships of the following categories:
Contraction Ratios Contraction ratio for imaged muscles and postural sway measures Contraction ratio for imaged muscles and gait speed Contraction ratio for imaged muscles and step activity measures
Flexion endurance time and extension endurance time for each group Flexion and extension trunk endurance times and postural sway measures Flexion and extension trunk endurance times and gait speed Flexion and extension trunk endurance times and step activity measures
In PwMS, MSWS-12 and trunk structure, endurance, gait, postural sway and step activity measures.
If data was normally distributed, Pearson’s Product moment correlation coefficient was used. Else Spearman’s rank correlation coefficient was used. All statistical analysis was done using SPSS software v22 (IBM, Armonk, NY). The α– value was set at 0.05.
Results
Self-Report measures
There were no significant differences between the groups in terms of age and BMI. PwMS group had significantly greater FES-I and MFIS-5 scores compared to healthy controls (Table 1).
Trunk muscles at rest
There were no significant differences between the groups for muscle thickness values in resting state for any of the muscles. There was a trend towards significance for resting state muscle thickness value of IO that was lesser in PwMS than healthy controls (Table 2). The pattern of order of absolute muscle thickness in both groups from largest to smallest was MTF > IO > EO > TrA (Table 2).
Trunk muscles contraction ratios
No significant Side×Group interaction was found for any of the measures (Table 3). There were no significant group main effects for any of the contraction ratio measures (Table 3). There was a significant Side main effect for MTF contraction ratio (P = 0.019). The contraction ratio for MTF was significantly greater on the right side compared to the left side (Table 3). In PwMS, the contraction ratios of IO, EO, EOIO, and TLA on the impaired side were significantly lesser than the contraction ratio on the unimpaired side. There was no significant difference in the contraction ratio values of TrA and MTF between the impaired and unimpaired sides (Table 4).
Postural sway pre to post trunk endurance testing
No significant time×group interactions were found (Table 5). Significant group main effects showed that PwMS had greater CoP ML range (58%), velocity (39%) and path length (39%), AP range (32%), velocity (42%) and path length (42.5%), total path length (38%) and sway area (103%) (Table 5). Significant time effect showed that on average both groups increased their CoP range in ML (31%) and AP (19%) (Table 5).
Trunk endurance tests
PwMs could perform trunk endurance tests for a significantly less time compared to HC (Table 6).
Gait speed
Gait speed was significantly less in PwMS compared to HC for both self-selected comfortable and fast gait speed conditions (Table 6).
Step activity
PwMS had significantly lesser total step count, average time per bout, average number of steps per bout, total minutes of activity and greater percentage of inactivity compared to healthy individuals (Table 6). However, the number of bouts was similar between the two groups.
Relationship of gait, postural control, trunk endurance, trunk muscle contraction ratios and step activity
Correlation parameters for PwMS and healthy control groups are reported in Table 7 and Table 8, respectively. For PwMS group, there were no significant correlations between trunk muscle contraction ratios and the other parameters. PwMS who had lesser flexion endurance times had significantly greater CoP ML range, path length and mean velocity, total path length, elliptical sway area and MSWS-12 score. PwMS who had lesser flexion endurance times also had significantly lesser comfortable and fast gait speed, and average number of steps per bout. PwMS who had lesser extension endurance times had significantly greater AP range. PwMS who had lesser MSWS-12 score had significantly lesser CoP AP range, path length and mean velocity, total path length, ML mean velocity and FES-I score. PwMS who had lesser MSWS-12 had significantly greater comfortable and fast gait speed, total step count, average time per bout, and average number of steps per bout.
For healthy control group, participants with greater TrA contraction ratio exhibited significantly longer extension endurance times (Table 8). Similarly, those with greater EOIO contraction ratio and TLA contraction ratio showed significantly greater ML path length and mean velocity. Participants with longer flexion endurance time also showed significantly longer extension time.
Discussion
To our knowledge this study is the first to compare trunk muscle thickness at rest and in contracted state in PwMS and HC. There was minimal difference between PwMS and HC groups for trunk muscle structure and performance as demonstrated using ultrasound imaging during ADIM or prone contralateral arm lift. However, PwMS did have comparatively worse trunk performance as measured by timed isometric trunk flexion and extension endurance. Although both groups had increased sway from pre to post trunk endurance testing, there was no difference between PwMS and HC in the effect of trunk endurance testing on postural sway. Trunk flexion endurance was negatively correlated to several measures of postural control and positively correlated to gait speed and step activity while trunk extension endurance was negatively correlated to AP CoP range.
Comparison of trunk muscles’ structure and performance in PwMS and HC
Resting muscle thickness as measured from ultrasound images
The resting thickness measurements for all imaged muscles for both groups in the current study were similar to those obtained in other studies (Rankin, Stokes, & Newham, 2006; Hides et al., 1992; Kiesel et al., 2007). Also, the previously reported pattern of relative absolute muscle thickness, MTF > IO > EO > TrA, (Rankin, Stokes, & Newham, 2006; Teyhen et al., 2012) was confirmed in the current study in both groups.
Contracted muscle thickness as measured from ultrasound images
In the current study change in trunk muscle thickness during performance of the ADIM and contralateral arm lift were not significantly different in PwMS compared to HC (Table 3). As previously described in a young, healthy population (Teyhenet al., 2005), preferential activation of the TrA, contraction ratio ≥ 2.0 during the ADIM was demonstrated in the HC group. However, mean TrA contraction ratios in PwMS were similar to mean contraction ratios of older adults (Stetts, Freund, Allison, & Carpenter, 2009). No known normative values for MTF contraction ratios have been reported.
Side-to-side differences in trunk muscle contraction may potentially identify motor control deficits in PwMS who report greater impairment on one side. In the current study a between side comparison of impaired versus unimpaired contraction ratios in PwMS revealed significant differences in change of muscle thickness in the IO, EO, EOIO and TLA, but not TrA during the ADIM or MTF during contralateral arm lift (Table 4). Side to side comparisons in the current study agree with recent research using other methods which also demonstrated greater activation of the internal and external obliques on the less impaired side during gait in PwMS (Ketelhut et al., 2015). The clinical relevance of this finding needs further investigation.
Comparison of trunk isometric endurance in PwMS and HC
To our knowledge this is the first study to compare trunk isometric endurance in PwMS to HC. Prior research in this area has primarily focused on individuals with low back pain, young healthy persons and athletes (McGill, Childs, & Liebenson, 1999; Evans, Refshauge, & Adams, 2007; del Pozo-Cruz et al., 2013). Trunk isometric extension endurance using a modified test position has also been examined in older adults (Suri et al., 2009). In the current study PwMS had a comparative lesser performance on both isometric trunk flexion and extension endurance tests which may have functional consequences. One difference in this study compared to normative values (McGill, Childs, & Liebenson, 1999) was both healthy and MS groups had greater endurance in trunk flexion than extension. The different results may have been due to the populations studied or our methods. Although we provided at least 5 minutes rest between tests, we tested trunk flexion first while McGill, Childs, & Liebenson, (1999) randomized the order of testing.
Comparison of step activity in PwMS and HC
As expected, PwMS had less amount and intensity of step activity compared to HC indicating negative effects of MS on free-living walking behavior. PwMS were less active than HC with less total minutes of activity, shorter bouts and fewer steps per bout. Total step activity for PwMS was similar to prior research, although our participants had a mean of 7,041 steps per day and previous research reported approximately 6,000 steps per day in PwMS (Cavanaugh, Gappmaier, Dibble, & Gappmaier, 2011; Dlugonski et al., 2007; Motl et al., 2013). According to an activity classification the PwMS in this study were classified as low active with 5,000–7,499 steps per day while the HC participants were classified as active with 10,000–12,499 steps per day (Tudor-Locke 2011) Steps per day in PwMS can vary dependent on the clinical course of MS and disease duration (Motl et al., 2013). The average time per bout for PwMS reported in the current study, approximately five minutes, was similar to the time per bout reported in prior research for PwMS with less disability, EDSS < 4.5 (Cavanaugh, Gappmaier, Dibble, & Gappmaier, 2011).
Comparison of postural control pre and post endurance testing in PwMS and HC
As previously reported (Karst, Venema, Roehrs, & Tyler, 2005; Van Emmerik et al., 2010; McLoughlin et al., 2015), PwMS demonstrated greater postural sway in comfortable stance with eyes open than HC in the current study. Both PwMS and HC had greater postural sway from pre to post trunk endurance tests. Lack of significant interaction suggests that the effect of the trunk endurance tests was similar on both the groups, indicating a similar response to trunk fatigue. Trunk muscle fatigue was not specifically measured post endurance testing although participants rated their pre and post-test overall fatigue using the Fatigue Numeric Rating Scale. PwMS reported greater fatigue level pre trunk endurance testing than HC, however, both groups reported increased fatigue post trunk endurance testing. Perceived fatigue has been related to muscle fatigue in PwMS (Steens et al., 2012). No difference between groups in postural sway pre to post trunk endurance testing was unlike previously reported greater changes in postural sway in PwMS compared to healthy controls after a 6 minute walk test (McLoughlin et al., 2015). This difference between studies may be due to greater fatigue in healthy individuals after trunk endurance testing compared to following a 6 minute walk. Since HC may have been more fatigued by trunk endurance testing there was not as much difference between HC and PwMS as after the 6 minute walk.
Relationship of trunk performance with balance, gait and walking activity in PwMS
There were no significant correlations between trunk muscle contraction ratios identified with ultrasound imaging and balance or gait measures in PwMS, therefore, trunk muscle contraction ratios may not be an effective method of identifying trunk impairments related to gait and balance.
In PwMS trunk flexion endurance time was negatively correlated with several measures of postural control including CoP total path length which has been reported as a predictor of fall incidence in PwMS (Prosperini et al., 2013). Particularly, trunk flexion endurance time was negatively correlated with ML but not AP measures of postural control in PwMS. This may be related to role of the abdominal muscles functioning as lateral flexors of the trunk for postural control. Speed and amplitude of ML movement of CoP has been related to falls in older adults (Piirtola and Era, 2006). In PwMS trunk flexion isometric endurance time was also positively correlated with both self-selected and fast gait speed and steps per walking bout. Trunk flexion endurance may be correlated to gait speed and steps as the lateral abdominal muscles (TrA, IO, EO) are active during greater than 75% of the gait cycle in healthy adults (Hu et al.,2012). The only correlation for trunk extension endurance time was a negative one with CoP AP range in PwMS. Increased trunk extensor endurance has also been associated with better balance in older adults (Suri et al., 2009, 2011).
Core stability training has improved balance and gait in various populations including a small case series with PwMS (Freeman et al., 2010). Additional research supports that both dynamic and isometric trunk stabilization exercises improve gait velocity, left and right step length, left and right stride length, and cadence in older adults with evidence to suggest that isometric trunk exercise is more effective than dynamic trunk exercise in increasing gait velocity (Kim et al., 2015). Gait velocity and step length increases could theoretically be due to improved balance through improvement in trunk stability.
We acknowledge limitations of this study. Due to the varied clinical presentation of PwMS and potential for a recurrent history of low back pain, specific exclusion criteria were necessary to assess correlations in a more homogeneous population resulting in a relatively small group. Also, although we were primarily interested in the role of trunk endurance in balance and gait, many other variables such as lower extremity strength, sensation, vision, etc, could be contributing to these measures.
Conclusion
As trunk endurance, especially flexion, was correlated with several measures of postural sway and gait in PwMS, clinicians should consider the evaluation and implementation of interventions directed at impaired trunk endurance in this population. Additional research related to the effects of trunk endurance on gait, balance, and step activity in PwMS is warranted.
Conflict of interest
The authors have no declarations of interest. This research was funded through an Elon University faculty research and development grant.
