Quantitative sensory and motor measures detect change over time and correlate with walking speed in individuals with multiple sclerosis

doi:10.1016/j.msard.2014.11.001

Multiple Sclerosis and Related Disorders

Volume 4, Issue 1, January 2015, Pages 67-74

https://doi.org/10.1016/j.msard.2014.11.001 Get rights and content

Highlights

•
Dynamometry measures show significant changes in leg strength over one year.
•
The PPMS group shows the most significant loss in hip strength per year.
•
Vibratory sensation decline was detected even in subjects with “near normal” sensation.
•
Walking speed is most affected by weak hip flexor muscles.

Abstract

Background

Impairments of sensation, strength, and walking are common in multiple sclerosis (MS). The relationship among these abnormalities and how they change over time remains unclear.

Objective

To determine the extent that quantitative lower extremity sensory and motor measures detect abnormalities over time, relate to global disability, and to walking speed in individuals with MS.

Methods

This prospective, longitudinal analysis evaluated 136 MS subjects. Measures included measures of leg strength, sensation, the Expanded Disability Status Scale(EDSS) and timed 25-foot walk test (T25FW). Mixed effects regression models were used.

Results

Our cohort׳s mean age is 44.3±10.8 years (mean±SD), EDSS score range 0–7.5, 66% were females, and follow-up time was 2.1±1.2 years. Strength significantly changed over time; the RRMS group demonstrated the greatest changes in ADF (3.3 lbs/yr) while the PPMS group showed significant HF changes (−2.1 lbs/yr). Walking speed was affected most by HF, especially in the weakest individuals (HF<20 lbs); T25FW increased by 0.20 s for each 1 lb loss (p=0.001). Likewise T25FW changed by 0.19 s for each 1 lb change in ADF (p<0.01).

Conclusion

Quantitative measures detected changes in sensation and strength over time, despite a stable respective functional systems scores of the EDSS. Quantitative measurement tools may improve the sensitivity of disability measures in MS and further investigation of these tools as outcomes in future clinical trials of rehabilitative and neuroreparative interventions is warranted.

Introduction

Multiple sclerosis (MS) is a primary demyelinating disease of the central nervous system that often results in accumulation of neurological disability. Rating scales such as the Expanded Disability Status Scale Score (EDSS) are often used to evaluate global disability (Kurtzke, 1983). However, rating scales provide limited information about specific impairments and their relationship to functional disability, resulting in treatment interventions that are broad and typically tested on a “trial-by-trial” basis (Schwid et al., 1997, Schwid et al., 2000, Cohen et al., 2000). Following the natural history of changes in strength and sensation in a large group of individuals with MS is useful to determine differences in the impairment among MS subtypes and for understanding the extent that these impairments affect disability over time. Development of quantitative outcome measures could then be used to more precisely measure their effects on disability and lead to more focused rehabilitation interventions.

Quantitative devices to measure strength and sensation have been previously shown to detect impairments in MS versus healthy controls, in addition these measures correlated with the EDSS and the Timed 25-foot walk (T25FW) (Newsome et al., 2011). However, it is not known to what extent these tools can detect change over time and how they relate to global disability measures and ambulation. The purpose of this study was to determine the extent that quantitative measures of lower extremity strength and sensation detect abnormalities over two years, as well as how they relate to global disability measures and walking speed in individuals MS.

Section snippets

Participants

Participants were recruited by Johns Hopkins MS Center physicians from November 2004 to May 2011. Participants were excluded if they had an MS relapse within three months of testing or reported a history of peripheral neuropathy or any other orthopedic, neurologic, or cognitive condition that might interfere with study procedures. All participants provided signed, informed consent in accordance with Institutional Review Board regulations at Johns Hopkins University and Kennedy Krieger Institute.

Study population

MS participants were a mean age of 44.3±10.8 years (mean±SD) (range: 20–67), disease duration of 6.7±8.9 years (range: 0.5–42), and 66% were females. Disability varied from EDSS 0–7.5 (Table 1). Participants included 83 with RRMS, 31 with SPMS, and 22 with PPMS with a mean longitudinal follow up of 2.1±1.2 years. The mean age for individuals with RRMS was 38.3±10.7 years, 61 female; with SPMS, 51.9±7.4 years, 18 female; with PPMS, 50.1±9.8 years, 12 female.

Changes over time

Table 1 shows baseline and year 2 data

Discussion

Overall, our data show that quantitative measures of strength and sensation detect specific impairments in MS and these relate to global disability measures and ambulation. Quantitative measures of strength significantly changed over time; when accounting for MS subtype the RRMS group had the most significant change in ADF and the PPMS group for HF strength. Individuals starting out with the strongest HF showed the largest decline in strength. Quantitative vibration sensation showed trends for

Conclusions

In summary, the results of this 2-year natural history study demonstrate the slow but steady progression of sensory and motor impairments in MS. The quantitative devices used in this study detected changes in impairments in MS subjects that correlated with walking speed. Proximal lower extremity weakness contributed the most to slowing walking speed especially in the weakest individuals. Vibratory sensation shows the greatest trend toward detecting subtle changes early in the disease course,

Disclosures

Dr. Newsome has served as a consultant for Biogen-Idec, Novartis, and Genzyme.

Dr. Calabresi has been a consultant for Vertex, Vaccinex, Prothena, and Abbvie.. Dr. Calabresi receives research support from Biogen-Idec, Novartis, NINDS, NIH, and the National MS Society.

Mr. Wang reports no disclosures.

Dr. McGready reports no disclosures.

Dr. Zackowski reports no disclosures.

Funding acknowledgments

This study was supported by National Multiple Sclerosis Society Tissue Repair Grant (K.M.Z. and P.A.C.) and NIH NICHD K01 HD049476 (K.M.Z.), and a Sylvia Lawry Physician Fellowship from the National Multiple Sclerosis Society (S.D.N.).

Acknowledgments

The authors would like to thank Rhul Marasigan for his assistance in collecting parts of this data, and assisting with graphs for this data.

References (24)

RA Bogey et al.
Determination of ankle muscle power in normal gait using an EMG-to-force processing approach
J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol
(2010)
S Citaker et al.
Relationship between foot sensation and standing balance in patients with multiple sclerosis
Gait Posture
(2011)
SD Newsome et al.
Quantitative measures detect sensory and motor impairments in multiple sclerosis
J Neurol Sci
(2011)
BM Sandroff et al.
Physical fitness, walking performance, and gait in multiple sclerosis
J Neurol Sci
(2013)
MH Sutliff et al.
Efficacy and safety of a hip flexion assist orthosis in ambulatory multiple sclerosis patients
Arch Phys Med Rehabil
(2008)
JC. Arezzo
The vibratron: a simple device for quantitative evaluation of tactile/vibratory sense
Neurology
(1985)
RW. Bohannon
Comfortable and maximum walking speed of adults aged 20–79 years: reference values and determinants
Age Ageing
(1997)
T Broekmans et al.
The relationship between upper leg muscle strength and walking capacity in persons with multiple sclerosis
Mult Scler J
(2013)
JA Cohen et al.
Intrarater and interrater reliability of the MS functional composite outcome measure
Neurology
(2000)
S Coote et al.
Getting the balance right: a randomised controlled trial of physiotherapy and Exercise Interventions for ambulatory people with multiple sclerosis
BMC Neurol
(2009)

U Dalgas et al.

Muscle fiber size increases following resistance training in multiple sclerosis

Mult Scler

(2010)

K Dodd et al.

Progressive resistance training did not improve walking but can improve muscle performance, quality of life and fatigue in adults with multiple sclerosis: a randomized controlled trial

Mult Scler J

(2011)

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The aim of this study is to assess the factors affecting falls in people with MS and map out the most significant ones. This study also aims to determine whether fatigue has a moderation effect and balance has a mediation effect on falls in people with MS
In total, 103 people with MS with a mean age of 32.09 ± 7.17 were enrolled. All subjects were assessed for multiple variables including balance using the Berg Balance Scale (BBS), speed of gait using the Timed Up and Go (TUG) test, fear of falling using the Falls Efficacy Scale—International (FES-I), level of fatigue using the Modified Fatigue Impact Scale (MFIS), and lower limb muscle strength using a handheld digital dynamometer
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People with MS with impaired balance, slower gait speeds, higher levels of fatigue, and a fear of falling were at a high risk of falling. The relationship between gait speed and falls can be mediated by impaired balance and moderated by the level of fatigue. Our data suggest that targeting balance and fatigue while developing rehabilitation interventions could decrease the incidence of falls among people with MS.
Spatiotemporal gait changes in people with multiple sclerosis with different disease progression subtypes
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Gait impairment is common in people with multiple sclerosis (MS), but less is known about gait differences between MS disease progression subtypes. The objective here was to examine differences in spatiotemporal gait in MS and between relapsing-remitting and progressive subtypes during the timed-25-ft-walk test. Our specific aims were to investigate (1) spatiotemporal, (2) spatiotemporal variability, and (3) gait modulation differences between healthy controls and MS subtypes at preferred and fast walking speed.
This study included 27 controls, 18 relapsing-remitting MS, and 13 progressive MS participants. Participants wore six inertial sensors and walked overground without walking aids at preferred and fast-as-possible speeds.
Both MS groups had significantly lower walking speed than controls, with a trend towards lower preferred gait speed in progressive compared to relapsing-remitting MS (ES = 0.502). Although most spatiotemporal gait parameters differed between controls and MS groups, differences were not significant between MS subtypes in these parameters and their variability, with low to moderate effect sizes during preferred and fast walking. Both MS groups showed reduced modulation in gait compared to controls and no significant differences between MS subtypes.
Gait in MS is altered compared to controls. Although gait may change with progressive MS, the overall small differences in the gait parameters between the MS subtypes observed in this sample suggests that those with the progressive form of MS who are independently ambulatory and without further clinically meaningful changes in gait speed may not show gait decrements greater than the relapsing-remitting form of the disease.
Cognition and proprioception in persons with multiple sclerosis and healthy controls: Nascent findings
2022, Multiple Sclerosis and Related Disorders
Although proprioception and cognitive dysfunction are commonly associated with balance impairment and fall risk in persons with multiple sclerosis (MS), the relationship between cognitive functioning and a quantitative measure of proprioception has not been examined in MS.
The primary goals of this study were to determine differences in vibratory sensation, a proxy measure of proprioception between persons with MS and healthy controls, examine relationships between cognition and vibration sensation, and determine the contribution of cognitive function and demographics to vibratory sensation between persons with MS and healthy controls.
One hundred and twenty-two individuals with MS, aged 20–60, with Expanded Disability Status Scale (EDSS) scores ≤5.5 and 48 healthy controls completed reaction time testing, the Stroop test and lower extremity vibratory sensation.
Persons with MS performed significantly worse than controls on measures of vibratory sensation (p = 0.001), two-choice reaction time (p = 0.018), and Stroop Incongruent (p < 0.001) Relative Incongruent Score (RIS) (p = 0.047). In MS, average vibration was significantly related to age (p = 0.002), sex (p = 0.038), disease severity (EDSS; p < 0.001), years since diagnosis (p = 0.016), and Stroop Word (p = 0.041). A model with demographics; including age and disease severity, two-choice reaction time, and RIS explained 33.2% of the variance vibratory sensation in persons with MS.
These results provide early evidence for the relation between cognitive functioning and proprioception in persons with MS and add to prior work linking cognitive functioning, postural control and falls in persons with MS. This work provides a basis for future studies combining quantitative measures of proprioception and cognitive and postural control assessment to improve fall prediction.
Cerebellar Contributions to Motor and Cognitive Control in Multiple Sclerosis<sup>✰✰✰</sup>
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To evaluate relationships between specific cerebellar regions and common clinical measures of motor and cognitive function in persons with multiple sclerosis (PwMS).
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Laboratory.
Twenty-nine PwMS and 28 age- and sex-matched controls without multiple sclerosis (MS) (N=57).
Not applicable.
Both diffusion and lobule magnetic resonance imaging analyses and common clinical measures of motor and cognitive function were used to examine structure-function relationships in the cerebellum.
PwMS demonstrate significantly worse motor and cognitive function than controls, including weaker strength, slower walking, and poorer performance on the Symbol Digit Modalities Test, but demonstrate no differences in cerebellar volume. However, PwMS demonstrate significantly worse diffusivity (mean diffusivity: P=.0003; axial diffusivity: P=.0015; radial diffusivity: P=.0005; fractional anisotropy: P=.016) of the superior cerebellar peduncle, the primary output of the cerebellum. Increased volume of the motor lobules (I-V, VIII) was significantly related to better motor (P<.022) and cognitive (P=.046) performance, and increased volume of the cognitive lobules (VI-VII) was also related to better motor (P<.032) and cognitive (P=.008) performance, supporting the role of the cerebellum in both motor and cognitive functioning.
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The relationship between plantar sensation and muscle onset during automatic postural responses in people with multiple sclerosis and healthy controls
2021, Multiple Sclerosis and Related Disorders
Citation Excerpt :
We used the Vibratron II device , a valid instrument used previously in this population and clinically accessible, to measure vibration threshold as a proxy for plantar sensation. This is consistent with previous literature and study designs (Newsome et al., 2011; Zackowski et al., 2015). Ideally, it would be desirable to test plantar sensation at multiple locations on the sole (e.g., the first and fifth metatarsal and the heel).
Plantar sensation is critical for balance control in people with multiple sclerosis (PwMS). While previous research has described its impact on standing balance, the influence of plantar sensation during automatic postural responses (APRs) is not well understood in PwMS. The purpose of this study was to characterize the relationship between plantar sensation and APRs in PwMS and controls. A secondary aim was to determine whether the relationship between plantar sensation and APRs is different across PwMS and control groups.
122 PwMS and 48 age-matched controls underwent forward and backward support-surface perturbations from stance. The onset of the tibialis anterior (TA) and medial gastrocnemius (MG) were the primary reactive balance outcome measures for backward and forward losses of balance, respectively. Plantar sensation was measured as the vibration sensation threshold (VT).
As expected, PwMS had significantly higher (i.e., worse) VT (p<0.001) and an increased MG and TA onset latency (TA: p<0.001, MG: p = 0.01) compared to the control group. A higher VT was related to increased MG (p<0.001) and TA latency (p<0.001) across all participants. However, no moderating effect of group (control or PwMS) was observed for the relationship between VT and muscle onset (MG: p = 0.14; TA: p = 0.34).
PwMS demonstrated poorer plantar sensation and delayed muscle onset during APRs compared to controls. Plantar sensation was also related to muscle onset after perturbations in all participants. Although this relationship was not moderated by group, this may be related to the lack of dynamic range of VT scores in controls. These results indicate that plantar sensation may be related to reactive balance and provides insight into a potential contributing factor of delayed automatic postural responses in people with MS.
Non-ambulatory measures of lower extremity sensorimotor function are associated with walking function in Multiple Sclerosis
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Disease progression of multiple sclerosis (MS) is often monitored by ambulatory measures, but how non-ambulatory sensorimotor measures differentially associate to walking measures in MS subtypes is unknown. We determined whether there are characteristic differences between relapsing-remitting MS (RRMS), progressive MS (PMS), and non-MS controls in lower extremity sensorimotor function and clinical walking tasks and the sensorimotor associations with walking function in each group.
18 RRMS, 13 PMS and 28 non-MS control participants were evaluated in their plantar cutaneous sensitivity (vibration perception threshold, Volts), proprioception during ankle joint position-matching (|∆°| in dorsiflexion), motor coordination (rapid foot-tap count/10 s), and walking function with three tests: Timed 25-foot walk (T25FW) at preferred and fast speeds (s), and timed-up-and-go (TUG, s).
Foot-tapping (p = 0.039, Mean difference (MD)= 5.65 taps) and plantar cutaneous sensation (p = 0.026, MD= -10.30 V) differed between the MS subtypes. For the RRMS group faster walking was related to better proprioceptive function (preferred T25FW: p = 0.019, Root mean square error (RMSE)=1.94; fast T25FW: p = 0.004, RMSE=1.65; TUG: p = 0.001, RMSE=2.12) and foot-tap performance (preferred T25FW: p = 0.033, RMSE = 2.74; fast T25FW: p = 0.010, RMSE=2.02). These associations were not observed in the PMS group.
Foot-tap performance and plantar cutaneous sensitivity but not ankle proprioception differed between MS subtypes. Lower walking performance was associated with lower foot-tapping and plantar cutaneous sensitivity in the RRMS but not the PMS group. This result suggests a change in the relationship of lower extremity sensorimotor function to walking performance in the PMS subtype.

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View full text

Quantitative sensory and motor measures detect change over time and correlate with walking speed in individuals with multiple sclerosis

Highlights

Abstract

Background

Objective

Methods

Results

Conclusion

Introduction

Section snippets

Participants

Study population

Changes over time

Discussion

Conclusions

Disclosures

Funding acknowledgments

Acknowledgments

J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol

Gait Posture

J Neurol Sci

J Neurol Sci

Arch Phys Med Rehabil

The vibratron: a simple device for quantitative evaluation of tactile/vibratory sense

Neurology

Comfortable and maximum walking speed of adults aged 20–79 years: reference values and determinants

Age Ageing

The relationship between upper leg muscle strength and walking capacity in persons with multiple sclerosis

Mult Scler J

Intrarater and interrater reliability of the MS functional composite outcome measure

Neurology

Getting the balance right: a randomised controlled trial of physiotherapy and Exercise Interventions for ambulatory people with multiple sclerosis

BMC Neurol

Muscle fiber size increases following resistance training in multiple sclerosis

Mult Scler

Progressive resistance training did not improve walking but can improve muscle performance, quality of life and fatigue in adults with multiple sclerosis: a randomized controlled trial

Mult Scler J