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Relationship between gait initiation and disability in individuals affected by multiple sclerosis
Multiple Sclerosis and Related Disorders 4 (2015) 594–597
Contents lists available at ScienceDirect
Multiple Sclerosis and Related Disorders journal homepage: www.elsevier.com/locate/msard
Relationship between gait initiation and disability in individuals affected by multiple sclerosis Manuela Galli a,d, Giancarlo Coghe b, Paola Sanna a, Eleonora Cocco b, Maria Giovanna Marrosu b, Massimiliano Pau c,n a
Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milan, Italy Multiple Sclerosis Center, Department of Public Health, Clinical and Molecular Medicine, University of Cagliari, Cagliari, Italy c Department of Mechanical, Chemical and Materials Engineering,University of Cagliari, Piazza d'Armi, 09123 Cagliari, Italy d Gait Analysis Lab, IRCCS San Raffaele Pisana, Rome, Italy b
art ic l e i nf o
a b s t r a c t
Article history: Received 26 December 2014 Received in revised form 12 September 2015 Accepted 22 September 2015
This study analyzes how multiple sclerosis (MS) does affect one of the most common voluntary activities in life: the gait initiation (GI). The main aim of the work is to characterize the execution of this task by measuring and comparing relevant parameters based on center of pressure (COP) patterns and to study the relationship between these and the level of expanded disability status scale (EDSS). To this aim, 95 MS subjects with an average EDSS score of 2.4 and 35 healthy subjects were tested using a force platform during the transition from standing posture to gait. COP time-series were acquired and processed to extract a number of parameters related to the trajectory followed by the COP. The statistical analysis revealed that only a few measurements were statistically different between the two groups and only these were subsequently correlated with EDSS score. The correlation analysis underlined that a progressive alteration of the task execution can be directly related with the increase of EDSS score. These finding suggest that most of the impairment found in people with MS comes from the first part of the COP pattern, the anticipatory postural adjustments (APAs). The central nervous system performs APAs before every voluntary movement to minimize balance perturbation due to the movement itself. Gait Initiation's APAs consist in some ankle muscles contractions that induce a backward COP shift to the swing limb. The analysis here performed highlighted that MS affected patients have a reduced posterior COP shift that reveals that the anticipatory mechanism is impaired. & 2015 Elsevier B.V. All rights reserved.
Keywords: Gait initiation Multiple sclerosis Balance Gait
1. Introduction Multiple sclerosis (MS) is a chronic disease of the central nervous system (CNS) that affects a wide range of neurological systems including, vision, brainstem, cerebellar, pyramidal, sensory, cognition, bowel, bladder and sexual. Many people with MS have abnormal balance and gait control, with consequent frequent falls (Cameron and Lord, 2010). Actually the expanded disability status scale (EDSS) is the most widely used method to estimate disability in MS. It is as a quantified neurological examination scale that considers 7 functional systems (FSs). Each FS subscale range from 0 to 5 or 0 to 6. The EDSS global score is a combination of the single FS values and the ambulatory or daily living autonomy and range from 0 (no disability) to 10 (death by MS) (Kurtzke, 1983). Imbalance has been related to the impairment of multiple CNS n
Corresponding author. Fax: þ39 070 6755717. E-mail address: [email protected] (M. Pau).
http://dx.doi.org/10.1016/j.msard.2015.09.005 2211-0348/& 2015 Elsevier B.V. All rights reserved.
areas related to balance and gait control as brainstem, spinal cord and cerebellar lesions (Cameron et al., 2012) slowed somatosensory conduction, pyramidal, vestibular and visual pathways, and finally central integration dysfunction (Cameron et al., 2008). The majority of studies on balance impairment in MS refer to the evaluation of unperturbed standing position. During quiet stance, in fact, people with MS sway more than healthy controls (HC) and a positive correlation between the amplitude of sway and the degree of disability (measured by EDSS) has been observed (Cameron et al., 2012). Conversely, subjects with MS have significantly reduced center of pressure (COP) displacements during voluntary leaning and reaching from a standing position (Karst et al., 2005) probably due to a functional strategy aimed at avoiding unstable postural states by limiting COP movements. Although the study of quiet stance is important for the analysis of balance problems, a more challenging situation, such as gait initiation (GI), may give a deeper insight into the mechanisms underlying dynamic postural control. Transition to gait, in fact,
M. Galli et al. / Multiple Sclerosis and Related Disorders 4 (2015) 594–597
puzzle postural control because consist in a transition from a relatively steady state (stance) to walk (Martin et al., 2002). During such a transition, controlled muscular effort is required to move the body center of mass (COM) away from the stable position, where COM and COP are aligned, thus producing an inherent unstable position. Stability is further affected because the wide base provided by bipedal support is replaced by a more narrow and unstable unipedal position (Martin et al., 2002, 2006). The GI gives a fundamental contribution to the forward progression (Brenière et al., 1987; Brunt et al., 1999; Couillandre et al., 2000; Gélat et al., 2006; Lepers and Brenière, 1995) and to the postural stability (Caderby et al., 2014; McIlroy and Maki, 1999). Thus, GI represents a natural but deliberately destabilizing task and can be a valid instrument in assessing the balance ability of subjects with neurological and motor impairments as in the case of MS. The postural phase of GI is typically referred to as an anticipatory postural adjustment (APA) and occurs prior to the phase of gross segmental movement (Brenière and Do, 1986) supporting changes of the first step (LOC). The dynamic COP shifts within the stability boundary during the APA exemplify synergistic behavior. In fact, the coordinated actions of the two postural mechanisms (the “ankle strategy” and the “hip strategy”) shift the COP during the APA in a systematic manner: first a translation in the lateral posterior directions toward the initial swing foot heel (APA1), then a lateral translation of the COP towards the stance limb ending in the point where the COP shifts from lateral to anterior motion (APA2). A third segment (LOC) extends from this latter point until toe-off of the initial stance limb as the COP moves in the anteroposterior direction (Remelius et al., 2008; Halliday et al., 1998). Some works evaluated GI in small MS patient's groups. Remelius et al. (2008) described the GI in twelve women with MS (the mean EDSS score was 4) and twelve women without MS by computing spatiotemporal parameters and parameters related to the subjects' center of mass (COM) and center of pressure (COP) displacements. Consistent with the fact that people with MS can lean less far when standing, the study suggests that during GI, MS group displace the center of mass less far, less quickly and less close from their stability boundaries (defined as the perimeter of the feet). In author's opinion these strategies are aimed to limit balance problems and are effective in predictable situations, but may be ineffective in the case of larger, faster or unexpected perturbations. Jacobs and Kasser (2012a, 2012b) evaluated GI in 13 MS patients showing a delayed foot-lift onset and longer APA duration respect control group. In addiction they highlighted a delayed onset latencies of APA's posterior component during a dual (cognitive plus motor) task respect a single (only motor) task. Basing on these data GI may be an ideal task to identify abnormalities in the dynamic postural control system and the changes that occur with advancing disability. Furthermore given the great variability of MS, it is important to include a large number of subjects with MS with different degree of disability to better describe GI. The aim of this study was to characterize GI kinetics in a large group of MS subjects considering a wide range of disability thus to represent the wide spectrum and degree of functional system involvement. Furthermore we correlated the patients' disability scores with quantitative parameters calculated from the COP data to find out how GI change with the disease evolution and if it can be applied as a clinical tool to detect also subtle disability progression during the MS course or as outcome of rehabilitation programs.
595
2. Materials and methods 2.1. Subjects Ninety-five individuals with MS 28 men, 67 women of mean age 38.8 years (SD 9.5, range 22–67 years) and 35 healthy controls (HC, 9 men, 26 women, mean age 35.9 years, SD 13.1, range 22–71 years) matched for anthropometric features and age were enrolled for the study. Inclusion criteria were a diagnosis of MS according to 2005 McDonald criteria (Polman et al., 2005) and been able to walk for at least 2 m without any aid. The only exclusion criterion was the presence of any concomitant condition that could affect the assessment (i.e. orthopedic problems or balance problems not related to MS). The local ethics committee approved the study and all the participants signed the informed consent. Neurological disability was evaluated for each patient by neurologists expert in MS (GC, EC, MGM). The EDSS score for the individuals with SM was between 1 and 7 (the 59% had a score between 1 and 2, the 18% between 3 and 4, the 11% between 4 and 5, the 11% between 5 and 7 and only 1% equal to 7). The average EDSS score was 2.44 with SD 1.64. 2.2. Task and instrumentation The tests were performed using a Footscans 0.5 pressure platform (RS Scan International, Belgium) of size 50 40 cm2, equipped with 4096 piezo-resistive sensors arranged on a 64 64 matrix and setting the acquisition frequency to 100 Hz. Subjects were asked to stand on the platform in bipedal stance with feet placed at a comfortable distance and then instructed to start walking, at a self-selected speed, following a verbal input. Then, participants were required to maintain a posture motionless during the initial upright stance and to make the GI movement selfselecting the swing leg. One trial was acquired for each subject. 2.3. Data processing and GI parameters The management software of the platform (Footscans Balance 7.7) allowed acquisition, collection and exporting in text files of the raw COP time series which were then analyzed using a dedicated routine developed in the Smart Analyzer environment (BTS Bioengineering S.p.A, Italy). This allows computation of quantitative parameters necessary for the analysis as follows (Fig. 1):
Medio-lateral and anterior-posterior coordinates of points A, B, C, D (Fig. 1).
Track length (m) of the segments APA1, APA2a, APA2b, LOC. Track velocity, average value considering both medio-lateral
and anterior-posterior displacement (m/s) in the segments APA1, APA2a, APA2b, LOC. Track duration (s) during the segments APA1, APA2a, APA2b, LOC.
In particular, the APAs and LOC phases were defined according to Remelius et al. (2008) and Halliday et al. (1998). The APA2 segment (which indicates the weight transition phase from the swing foot to the stance foot) was further divided in APA2a and APA2b to better characterize the pattern (Fig. 1). The position of the feet in standing position, before the movement execution, was checked by analyzing the pressure distribution of the feet during the first 2 s using the Footscan Balance software in order to verify if different positions were assumed by the participants.
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M. Galli et al. / Multiple Sclerosis and Related Disorders 4 (2015) 594–597
Table 2 Results of the correlation analysis for EDSS score and GI parameters.
EDSS EDSS EDSS EDSS EDSS EDSS
–Y coordinate of point B – Y component of APA1 velocity – Y component of APA2a velocity – Y component of LOC velocity – APA2b duration – LOC duration
N valid
ρ
p-value
93 93 84 88 84 88
0.513 0.264 0.218 0.482 0.423 0.475
o 0.001 0.008 0.039 o 0.001 o 0.001 o 0.001
score and the Y coordinate of point B (ρ ¼ 0.513, po 0.001), the Y component of APA1 velocity (ρ ¼0.264, p ¼0.008), APA2b duration (ρ ¼ 0.423, po 0.001) and LOC duration (ρ ¼0.475, po 0.001). Significant negative correlations were found with Y component of APA2a velocity (ρ ¼ 0.218, p ¼0.039) and Y component of LOC velocity (ρ ¼ 0.482, p o0.001).
4. Discussion
Fig. 1. Scheme of the COP trace division for the analysis (APA1, APA2a, APA2b, LOC). SW foot¼ swing foot (i.e. the leading foot); ST foot¼stance foot (i.e. the supporting foot during GI).
2.4. Statistical analysis After checking for normality using the Kolmogorov–Smirnov Test, median, Q1 and Q3 values were calculated for the parameters in the two groups of subjects. Differences between groups were analyzed using the Mann–Whitney U Test. Significance level was set at p-value o 0.05. The relationship between the EDSS score and the GI parameters was assessed by means of the Spearman rank correlation analysis. Even in this case, the level of significance was set at po 0.05.
3. Results No differences were found in the feet position in starting posture across the evaluated subjects. Among the whole set of parameters, 6 of them (listed in Table 1) resulted significantly different between MS and HC groups. The results of the correlation analysis are reported in Table 2. A significant positive correlation was observed between the EDSS
Transition movements are characterized by an important increase in postural stress, which can lead to a high risk of falls and injuries (Mbourou et al., 2003). GI is a very powerful task in studying these phenomena: in fact, it represents the passage from standing in wide support to action in narrow support. Furthermore it replicates a normal and frequent action during daily life. Several studies have underlined postural impairment in MS, most of them by using static evaluation (Cameron and Lord, 2010; Prosperini et al., 2011). Our aim was to categorize COP measures during GI in a large number of MS with a broad spectrum of disability. Furthermore, we evaluated the correlation between COP parameters and EDSS to find the kinetic markers of disability useful in monitoring disease progression and motor rehabilitation. According to our results the main features of GI in MS are slowing and reduction of COP posterior displacement. These findings confirm in a larger number of subjects the findings of previous studies in MS (Remelius et al., 2008; Jacobs and Kasser, 2012a) and other pathologies such as Parkinson's disease (PD – Halliday et al., 1998). It is relevant that velocity is reduced significantly in APA1 and APA2a. Those segments are the APAs initial phase and are consecutive to the most posterior excursion of COP (point B). It is indeed likely that reduction of speed in the Y direction and B point displacement are different manifestations of the same phenomenon: avoiding the approach to stability boundaries in the posterior direction during the initial APAs. During the LOC phase the reduction of COP speed is probably due to more than one reason. In agreement with the APAs, it is a functional adaptation aimed at avoiding stability perturbation. In addition, reduction of strength may play a prominent role leading to slower movements and slower COP displacement. Moreover,
Table 1 Values of mean, median, Q1 and Q3 for statistically significant parameters after the Mann–Whitney U Test for MS and HC groups. Gait Initiation Parameters Parameter
Y coordinate of point B (m) Y component of APA1 velocity (m/s) Y component of APA2a velocity (m/s) Y component of LOC velocity (m/s) APA2b duration (s) LOC duration (s)
Multiple sclerosis
Healthy controls
Mean
Median
Q1
Q3
Mean
Median
Q1
Q3
p-value
0.022 0.017 0.112 0.233 0.140 0.802
0.019 0.015 0.109 0.237 0.100 0.650
0.032 0.023 0.039 0.180 0.075 0.575
0.009 0.006 0.171 0.289 0.140 0.820
0.034 0.024 0.150 0.290 0.093 0.609
0.029 0.022 0.146 0.286 0.080 0.590
0.042 0.027 0.102 0.226 0.060 0.525
0.024 0.015 0.184 0.343 0.110 0.660
o 0.001 0.003 0.018 0.003 0.032 0.008
M. Galli et al. / Multiple Sclerosis and Related Disorders 4 (2015) 594–597
the LOC phase is prevalently oriented in the Y direction, thus changes in the antero-posterior component are more likely to be significant. Posterior displacement of point B is significantly reduced in patients with respect to HC. This data complies with the results of Remelius et al. (2008) and is a hallmark of postural damage that MS shares with other pathological conditions (Halliday et al., 1998). In PD reduction of COP, posterior displacement has been interpreted as a central impairment of muscle activation/deactivation (Frank et al., 2000). For instance, the incomplete deactivation of the tibialis anterior muscle leads to low level forces in the APA1 phase, thus explaining at the same time APA slowing and diminished Y coordinate of point B (Polcyn et al., 1998; Mickelborough et al., 2004). The backward shift of the COP during the APAs serves to propel the center of mass (COM) forwards and to reach the intended gait velocity at the end of the first step (Brenière et al., 1987; Brunt et al., 1999; Couillandre et al., 2000; Gélat et al., 2006; Lepers and Brenière, 1995). Thus, the reduction point B represent a strategy to decrease the forward propulsion of the COM and LOC speed in order to make safer the gait initiation. Based on this data, reduction of Point B posterior displacement in MS can be interpreted not only as a movement programming “bug” but also as a compensatory strategy. It represents a functional adaptation aimed at minimizing the approach towards posterior stability boundaries and limits the risk of falls. This adaptation is potentially generalized to the entire COP trajectory but results most prominent in the posterior direction because of the lack of visual control and the implication of backward shift in movement programming. Furthermore, it has to be considered that Point B the extreme excursion of the COP during the whole GI and results particularly near to stability boundaries (Remelius et al., 2008). To our knowledge this is the first study that correlates GI parameters with clinical disability in MS and our findings underline that GI kinetics parameters represent a hallmark of MS disability patterns. In particular the Y coordinate of point B showed a relevant correlation with EDSS. According to this relief COP posterior displacement in the initial APA phase is closely related to postural impairment and disability and the Y coordinate of point B is a valid surrogate of postural impairment useful as a marker of disability progression, risk of fall and an outcome measure of rehabilitation. In previous studies in PD, APA disturbances have been related to the damage in areas involved in movement programming. In particular, the connection between basal ganglia and supplementary and premotor area or with the peduncular pontine nucleus are involved (Massion, 1992; Nakano et al., 2000; Pahapil and Lozano, 2000). We cannot exclude that in the context of the widespread white and gray matter injury in MS these connections participate in determining the particular APA pattern. Furthermore, given the dissemination of CNS damage, as suggested by other authors (Cameron and Lord, 2010) the central integration of different stimuli may play a prominent role in MS postural impairment. In summary, we evaluated a large number of MS patients with a wide variety of disability level. The characteristics of the COP trajectory exhibit a pattern of alterations that in part overlaps with other neurological pathologies. COP posterior displacement during the initial APA phase may play a relevant role in measuring postural impairment. In addition, this study can lead to COP-centered rehabilitation strategies aimed at re-educating MS patients to use a correct transition from stance to movement. Conflict of interest The authors report no conflicts of interest.
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Acknowledgments We are very grateful to the people with MS who participated in the study. The help provided by Ms. Cristina Scalas during data acquisition was also greatly appreciated.
References Brenière, Y., Do, M., 1986. When and how does steady state gait movement induced from upright posture begin? J. Biomech. 19 (12), 1035–1040. Brenière, Y., Do, M., Bouisset, S., 1987. Are dynamic phenomena prior to stepping essential to walking? J. Mot. Behav. 19 (1), 62–76. Brunt, D., Liu, S.M., Trimble, M., Bauer, J., Short, M., 1999. Principles underlying the organization of movement initiation from quiet stance. Gait Posture 10 (2), 121–128. Caderby, T., Yiou, E., Peyrot, N., Begon, M., Dalleau, G., 2014. Influence of gait speed on the control of mediolateral dynamic stability during gait initiation. J. Biomech. 47 (2), 417–423. Cameron, M.H., Horak, F.B., Herndon, R.R., Bourdette, D., 2008. Imbalance in multiple sclerosis: a result of slowed spinal somatosensory conduction. Somatosens. Mot. Res. 25 (2), 113–122. Cameron, M.H., Lord, S., 2010. Postural control in Multiple Sclerosis: implications for fall prevention. Curr. Neurol. Neurosci. Rep. 10 (5), 407–412. Cameron, M., Wagner, J., Zackowski, K., Spain, R., 2012. 1st International symposium on gait and balance in Multiple Sclerosis: gait and balance measures in the evaluation of people with multiple sclerosis. Mult. Scler. Int, 720206 (accessed 27.07.15)〈http://downloads.hindawi.com/journals/msi/2012/720206. pdf〉. Couillandre, A., Brenière, Y., Maton, B., 2000. Is human gait initiation program affected by a reduction of the postural basis? Neurosci. Lett. 285 (2), 150–154. Frank, J.S., Horak, F.B., Nutt, J., 2000. Centrally initiated postural adjustments in parkinsonian patients on and off levodopa. J. Neurophysiol. 84 (5), 2440–2448. Gélat, T., Pellec, A.L., Brenière, Y., 2006. Evidence for a common process in gait initiation and stepping on to a new level to reach gait velocity. Exp. Brain Res. 170 (3), 336–344. Halliday, S.E., Winter, D.A., Frank, J.S., Patla, A.E., Prince, F., 1998. The initiation of gait in young, elderly, and Parkinson's disease subjects. Gait Posture 8 (1), 8–14. Jacobs, J.V., Kasser, S.L., 2012a. Effects of dual tasking on the postural performance of people with and without multiple sclerosis: a pilot study. J. Neurol. 259, 1166–1176. Jacobs, J.V., Kasser, S.L., 2012b. Balance impairment in people with multiple sclerosis: preliminary evidence for the Balance Evaluation Systems Test. Gait Posture 36 (3), 414–418. Karst, G.M., Venema, D.M., Roehrs, T.G., Tyler, A.E., 2005. Center of pressure measures during standing tasks in minimally impaired persons with multiple sclerosis. J Neurol. Phys. Ther. 29 (4), 170–180. Kurtzke, J.F., 1983. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33 (11), 1444–1452. Lepers, R., Brenière, Y., 1995. The role of anticipatory postural adjustments and gravity in gait initiation. Exp. Brain Res. 107 (1), 118–124. Martin, M., Shinberg, M., Kuchibhatla, M., Ray, L., Carollo, J.J., Schenkman, M.L., 2002. Gait initiation in community dwelling adults with Parkinson disease: comparison with older and younger adults without the disease. Phys. Ther. 82 (6), 566–577. Martin, C.L., Phillips, B.A., Kilpatrick, T.J., Butzkueven, H., Tubridy, N., McDonald, E., et al., 2006. Gait and balance impairment in early Multiple Sclerosis in the absence of clinical disability. Mult. Scler. 12 (5), 620–628. Massion, J., 1992. Movement, posture and equilibrium: interaction and coordination. Prog. Neurobiol. 38 (1), 35–56. Mbourou, G.A., Lajoie, Y., Teasdale, N., 2003. Step length variability at gait initiation in elderly fallers and non-fallers, and young adults. Gerontology 49 (1), 21–26. McIlroy, W.E., Maki, B.E., 1999. The control of lateral stability during rapid stepping reactions evoked by antero-posterior perturbation: does anticipatory control play a role? Gait Posture 9 (3), 190–198. Mickelborough, J., van der Linden, M.L., Tallis, R.C., Ennos, A.R., 2004. Muscle activity during gait initiation in normal elderly people. Gait Posture 19 (1), 50–57. Nakano, K., Kayahara, T., Tsutsumi, T., Ushiro, H., 2000. Neural circuits and functional organization of the striatum. J. Neurol 247 (5), V1–V15. Pahapil, P.A., Lozano, A.M., 2000. The pedunculopontine nucleus and Parkinson's disease. Brain 123 (Pt 9), 1767–1783. Polcyn, A.F., Lipsitz, L.A., Kerrigan, D.C., Collins, J.J., 1998. Age-related changes in the initiation of gait: degradation of central mechanisms for momentum generation. Arch. Phys. Med. Rehab 79 (12), 1582–1589. Polman, C.H., Reingold, S.C., Edand, G., Filippi, M., Hartung, H.P., Kappos, L., et al., 2005. Diagnostic criteria for multiple sclerosis: 2005 Revisions to the “McDonald Criteria”. Ann. Neurol. 58 (6), 840–846. Prosperini, L., Kouleridou, A., Petsas, N., Leonardi, L., Tona, F., Pantano, P., et al., 2011. The relationship between infratentorial lesions, balance deficit and accidental falls in multiple sclerosis. J. Neurol. 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Contents lists available at ScienceDirect
Multiple Sclerosis and Related Disorders journal homepage: www.elsevier.com/locate/msard
Relationship between gait initiation and disability in individuals affected by multiple sclerosis Manuela Galli a,d, Giancarlo Coghe b, Paola Sanna a, Eleonora Cocco b, Maria Giovanna Marrosu b, Massimiliano Pau c,n a
Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milan, Italy Multiple Sclerosis Center, Department of Public Health, Clinical and Molecular Medicine, University of Cagliari, Cagliari, Italy c Department of Mechanical, Chemical and Materials Engineering,University of Cagliari, Piazza d'Armi, 09123 Cagliari, Italy d Gait Analysis Lab, IRCCS San Raffaele Pisana, Rome, Italy b
art ic l e i nf o
a b s t r a c t
Article history: Received 26 December 2014 Received in revised form 12 September 2015 Accepted 22 September 2015
This study analyzes how multiple sclerosis (MS) does affect one of the most common voluntary activities in life: the gait initiation (GI). The main aim of the work is to characterize the execution of this task by measuring and comparing relevant parameters based on center of pressure (COP) patterns and to study the relationship between these and the level of expanded disability status scale (EDSS). To this aim, 95 MS subjects with an average EDSS score of 2.4 and 35 healthy subjects were tested using a force platform during the transition from standing posture to gait. COP time-series were acquired and processed to extract a number of parameters related to the trajectory followed by the COP. The statistical analysis revealed that only a few measurements were statistically different between the two groups and only these were subsequently correlated with EDSS score. The correlation analysis underlined that a progressive alteration of the task execution can be directly related with the increase of EDSS score. These finding suggest that most of the impairment found in people with MS comes from the first part of the COP pattern, the anticipatory postural adjustments (APAs). The central nervous system performs APAs before every voluntary movement to minimize balance perturbation due to the movement itself. Gait Initiation's APAs consist in some ankle muscles contractions that induce a backward COP shift to the swing limb. The analysis here performed highlighted that MS affected patients have a reduced posterior COP shift that reveals that the anticipatory mechanism is impaired. & 2015 Elsevier B.V. All rights reserved.
Keywords: Gait initiation Multiple sclerosis Balance Gait
1. Introduction Multiple sclerosis (MS) is a chronic disease of the central nervous system (CNS) that affects a wide range of neurological systems including, vision, brainstem, cerebellar, pyramidal, sensory, cognition, bowel, bladder and sexual. Many people with MS have abnormal balance and gait control, with consequent frequent falls (Cameron and Lord, 2010). Actually the expanded disability status scale (EDSS) is the most widely used method to estimate disability in MS. It is as a quantified neurological examination scale that considers 7 functional systems (FSs). Each FS subscale range from 0 to 5 or 0 to 6. The EDSS global score is a combination of the single FS values and the ambulatory or daily living autonomy and range from 0 (no disability) to 10 (death by MS) (Kurtzke, 1983). Imbalance has been related to the impairment of multiple CNS n
Corresponding author. Fax: þ39 070 6755717. E-mail address: [email protected] (M. Pau).
http://dx.doi.org/10.1016/j.msard.2015.09.005 2211-0348/& 2015 Elsevier B.V. All rights reserved.
areas related to balance and gait control as brainstem, spinal cord and cerebellar lesions (Cameron et al., 2012) slowed somatosensory conduction, pyramidal, vestibular and visual pathways, and finally central integration dysfunction (Cameron et al., 2008). The majority of studies on balance impairment in MS refer to the evaluation of unperturbed standing position. During quiet stance, in fact, people with MS sway more than healthy controls (HC) and a positive correlation between the amplitude of sway and the degree of disability (measured by EDSS) has been observed (Cameron et al., 2012). Conversely, subjects with MS have significantly reduced center of pressure (COP) displacements during voluntary leaning and reaching from a standing position (Karst et al., 2005) probably due to a functional strategy aimed at avoiding unstable postural states by limiting COP movements. Although the study of quiet stance is important for the analysis of balance problems, a more challenging situation, such as gait initiation (GI), may give a deeper insight into the mechanisms underlying dynamic postural control. Transition to gait, in fact,
M. Galli et al. / Multiple Sclerosis and Related Disorders 4 (2015) 594–597
puzzle postural control because consist in a transition from a relatively steady state (stance) to walk (Martin et al., 2002). During such a transition, controlled muscular effort is required to move the body center of mass (COM) away from the stable position, where COM and COP are aligned, thus producing an inherent unstable position. Stability is further affected because the wide base provided by bipedal support is replaced by a more narrow and unstable unipedal position (Martin et al., 2002, 2006). The GI gives a fundamental contribution to the forward progression (Brenière et al., 1987; Brunt et al., 1999; Couillandre et al., 2000; Gélat et al., 2006; Lepers and Brenière, 1995) and to the postural stability (Caderby et al., 2014; McIlroy and Maki, 1999). Thus, GI represents a natural but deliberately destabilizing task and can be a valid instrument in assessing the balance ability of subjects with neurological and motor impairments as in the case of MS. The postural phase of GI is typically referred to as an anticipatory postural adjustment (APA) and occurs prior to the phase of gross segmental movement (Brenière and Do, 1986) supporting changes of the first step (LOC). The dynamic COP shifts within the stability boundary during the APA exemplify synergistic behavior. In fact, the coordinated actions of the two postural mechanisms (the “ankle strategy” and the “hip strategy”) shift the COP during the APA in a systematic manner: first a translation in the lateral posterior directions toward the initial swing foot heel (APA1), then a lateral translation of the COP towards the stance limb ending in the point where the COP shifts from lateral to anterior motion (APA2). A third segment (LOC) extends from this latter point until toe-off of the initial stance limb as the COP moves in the anteroposterior direction (Remelius et al., 2008; Halliday et al., 1998). Some works evaluated GI in small MS patient's groups. Remelius et al. (2008) described the GI in twelve women with MS (the mean EDSS score was 4) and twelve women without MS by computing spatiotemporal parameters and parameters related to the subjects' center of mass (COM) and center of pressure (COP) displacements. Consistent with the fact that people with MS can lean less far when standing, the study suggests that during GI, MS group displace the center of mass less far, less quickly and less close from their stability boundaries (defined as the perimeter of the feet). In author's opinion these strategies are aimed to limit balance problems and are effective in predictable situations, but may be ineffective in the case of larger, faster or unexpected perturbations. Jacobs and Kasser (2012a, 2012b) evaluated GI in 13 MS patients showing a delayed foot-lift onset and longer APA duration respect control group. In addiction they highlighted a delayed onset latencies of APA's posterior component during a dual (cognitive plus motor) task respect a single (only motor) task. Basing on these data GI may be an ideal task to identify abnormalities in the dynamic postural control system and the changes that occur with advancing disability. Furthermore given the great variability of MS, it is important to include a large number of subjects with MS with different degree of disability to better describe GI. The aim of this study was to characterize GI kinetics in a large group of MS subjects considering a wide range of disability thus to represent the wide spectrum and degree of functional system involvement. Furthermore we correlated the patients' disability scores with quantitative parameters calculated from the COP data to find out how GI change with the disease evolution and if it can be applied as a clinical tool to detect also subtle disability progression during the MS course or as outcome of rehabilitation programs.
595
2. Materials and methods 2.1. Subjects Ninety-five individuals with MS 28 men, 67 women of mean age 38.8 years (SD 9.5, range 22–67 years) and 35 healthy controls (HC, 9 men, 26 women, mean age 35.9 years, SD 13.1, range 22–71 years) matched for anthropometric features and age were enrolled for the study. Inclusion criteria were a diagnosis of MS according to 2005 McDonald criteria (Polman et al., 2005) and been able to walk for at least 2 m without any aid. The only exclusion criterion was the presence of any concomitant condition that could affect the assessment (i.e. orthopedic problems or balance problems not related to MS). The local ethics committee approved the study and all the participants signed the informed consent. Neurological disability was evaluated for each patient by neurologists expert in MS (GC, EC, MGM). The EDSS score for the individuals with SM was between 1 and 7 (the 59% had a score between 1 and 2, the 18% between 3 and 4, the 11% between 4 and 5, the 11% between 5 and 7 and only 1% equal to 7). The average EDSS score was 2.44 with SD 1.64. 2.2. Task and instrumentation The tests were performed using a Footscans 0.5 pressure platform (RS Scan International, Belgium) of size 50 40 cm2, equipped with 4096 piezo-resistive sensors arranged on a 64 64 matrix and setting the acquisition frequency to 100 Hz. Subjects were asked to stand on the platform in bipedal stance with feet placed at a comfortable distance and then instructed to start walking, at a self-selected speed, following a verbal input. Then, participants were required to maintain a posture motionless during the initial upright stance and to make the GI movement selfselecting the swing leg. One trial was acquired for each subject. 2.3. Data processing and GI parameters The management software of the platform (Footscans Balance 7.7) allowed acquisition, collection and exporting in text files of the raw COP time series which were then analyzed using a dedicated routine developed in the Smart Analyzer environment (BTS Bioengineering S.p.A, Italy). This allows computation of quantitative parameters necessary for the analysis as follows (Fig. 1):
Medio-lateral and anterior-posterior coordinates of points A, B, C, D (Fig. 1).
Track length (m) of the segments APA1, APA2a, APA2b, LOC. Track velocity, average value considering both medio-lateral
and anterior-posterior displacement (m/s) in the segments APA1, APA2a, APA2b, LOC. Track duration (s) during the segments APA1, APA2a, APA2b, LOC.
In particular, the APAs and LOC phases were defined according to Remelius et al. (2008) and Halliday et al. (1998). The APA2 segment (which indicates the weight transition phase from the swing foot to the stance foot) was further divided in APA2a and APA2b to better characterize the pattern (Fig. 1). The position of the feet in standing position, before the movement execution, was checked by analyzing the pressure distribution of the feet during the first 2 s using the Footscan Balance software in order to verify if different positions were assumed by the participants.
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Table 2 Results of the correlation analysis for EDSS score and GI parameters.
EDSS EDSS EDSS EDSS EDSS EDSS
–Y coordinate of point B – Y component of APA1 velocity – Y component of APA2a velocity – Y component of LOC velocity – APA2b duration – LOC duration
N valid
ρ
p-value
93 93 84 88 84 88
0.513 0.264 0.218 0.482 0.423 0.475
o 0.001 0.008 0.039 o 0.001 o 0.001 o 0.001
score and the Y coordinate of point B (ρ ¼ 0.513, po 0.001), the Y component of APA1 velocity (ρ ¼0.264, p ¼0.008), APA2b duration (ρ ¼ 0.423, po 0.001) and LOC duration (ρ ¼0.475, po 0.001). Significant negative correlations were found with Y component of APA2a velocity (ρ ¼ 0.218, p ¼0.039) and Y component of LOC velocity (ρ ¼ 0.482, p o0.001).
4. Discussion
Fig. 1. Scheme of the COP trace division for the analysis (APA1, APA2a, APA2b, LOC). SW foot¼ swing foot (i.e. the leading foot); ST foot¼stance foot (i.e. the supporting foot during GI).
2.4. Statistical analysis After checking for normality using the Kolmogorov–Smirnov Test, median, Q1 and Q3 values were calculated for the parameters in the two groups of subjects. Differences between groups were analyzed using the Mann–Whitney U Test. Significance level was set at p-value o 0.05. The relationship between the EDSS score and the GI parameters was assessed by means of the Spearman rank correlation analysis. Even in this case, the level of significance was set at po 0.05.
3. Results No differences were found in the feet position in starting posture across the evaluated subjects. Among the whole set of parameters, 6 of them (listed in Table 1) resulted significantly different between MS and HC groups. The results of the correlation analysis are reported in Table 2. A significant positive correlation was observed between the EDSS
Transition movements are characterized by an important increase in postural stress, which can lead to a high risk of falls and injuries (Mbourou et al., 2003). GI is a very powerful task in studying these phenomena: in fact, it represents the passage from standing in wide support to action in narrow support. Furthermore it replicates a normal and frequent action during daily life. Several studies have underlined postural impairment in MS, most of them by using static evaluation (Cameron and Lord, 2010; Prosperini et al., 2011). Our aim was to categorize COP measures during GI in a large number of MS with a broad spectrum of disability. Furthermore, we evaluated the correlation between COP parameters and EDSS to find the kinetic markers of disability useful in monitoring disease progression and motor rehabilitation. According to our results the main features of GI in MS are slowing and reduction of COP posterior displacement. These findings confirm in a larger number of subjects the findings of previous studies in MS (Remelius et al., 2008; Jacobs and Kasser, 2012a) and other pathologies such as Parkinson's disease (PD – Halliday et al., 1998). It is relevant that velocity is reduced significantly in APA1 and APA2a. Those segments are the APAs initial phase and are consecutive to the most posterior excursion of COP (point B). It is indeed likely that reduction of speed in the Y direction and B point displacement are different manifestations of the same phenomenon: avoiding the approach to stability boundaries in the posterior direction during the initial APAs. During the LOC phase the reduction of COP speed is probably due to more than one reason. In agreement with the APAs, it is a functional adaptation aimed at avoiding stability perturbation. In addition, reduction of strength may play a prominent role leading to slower movements and slower COP displacement. Moreover,
Table 1 Values of mean, median, Q1 and Q3 for statistically significant parameters after the Mann–Whitney U Test for MS and HC groups. Gait Initiation Parameters Parameter
Y coordinate of point B (m) Y component of APA1 velocity (m/s) Y component of APA2a velocity (m/s) Y component of LOC velocity (m/s) APA2b duration (s) LOC duration (s)
Multiple sclerosis
Healthy controls
Mean
Median
Q1
Q3
Mean
Median
Q1
Q3
p-value
0.022 0.017 0.112 0.233 0.140 0.802
0.019 0.015 0.109 0.237 0.100 0.650
0.032 0.023 0.039 0.180 0.075 0.575
0.009 0.006 0.171 0.289 0.140 0.820
0.034 0.024 0.150 0.290 0.093 0.609
0.029 0.022 0.146 0.286 0.080 0.590
0.042 0.027 0.102 0.226 0.060 0.525
0.024 0.015 0.184 0.343 0.110 0.660
o 0.001 0.003 0.018 0.003 0.032 0.008
M. Galli et al. / Multiple Sclerosis and Related Disorders 4 (2015) 594–597
the LOC phase is prevalently oriented in the Y direction, thus changes in the antero-posterior component are more likely to be significant. Posterior displacement of point B is significantly reduced in patients with respect to HC. This data complies with the results of Remelius et al. (2008) and is a hallmark of postural damage that MS shares with other pathological conditions (Halliday et al., 1998). In PD reduction of COP, posterior displacement has been interpreted as a central impairment of muscle activation/deactivation (Frank et al., 2000). For instance, the incomplete deactivation of the tibialis anterior muscle leads to low level forces in the APA1 phase, thus explaining at the same time APA slowing and diminished Y coordinate of point B (Polcyn et al., 1998; Mickelborough et al., 2004). The backward shift of the COP during the APAs serves to propel the center of mass (COM) forwards and to reach the intended gait velocity at the end of the first step (Brenière et al., 1987; Brunt et al., 1999; Couillandre et al., 2000; Gélat et al., 2006; Lepers and Brenière, 1995). Thus, the reduction point B represent a strategy to decrease the forward propulsion of the COM and LOC speed in order to make safer the gait initiation. Based on this data, reduction of Point B posterior displacement in MS can be interpreted not only as a movement programming “bug” but also as a compensatory strategy. It represents a functional adaptation aimed at minimizing the approach towards posterior stability boundaries and limits the risk of falls. This adaptation is potentially generalized to the entire COP trajectory but results most prominent in the posterior direction because of the lack of visual control and the implication of backward shift in movement programming. Furthermore, it has to be considered that Point B the extreme excursion of the COP during the whole GI and results particularly near to stability boundaries (Remelius et al., 2008). To our knowledge this is the first study that correlates GI parameters with clinical disability in MS and our findings underline that GI kinetics parameters represent a hallmark of MS disability patterns. In particular the Y coordinate of point B showed a relevant correlation with EDSS. According to this relief COP posterior displacement in the initial APA phase is closely related to postural impairment and disability and the Y coordinate of point B is a valid surrogate of postural impairment useful as a marker of disability progression, risk of fall and an outcome measure of rehabilitation. In previous studies in PD, APA disturbances have been related to the damage in areas involved in movement programming. In particular, the connection between basal ganglia and supplementary and premotor area or with the peduncular pontine nucleus are involved (Massion, 1992; Nakano et al., 2000; Pahapil and Lozano, 2000). We cannot exclude that in the context of the widespread white and gray matter injury in MS these connections participate in determining the particular APA pattern. Furthermore, given the dissemination of CNS damage, as suggested by other authors (Cameron and Lord, 2010) the central integration of different stimuli may play a prominent role in MS postural impairment. In summary, we evaluated a large number of MS patients with a wide variety of disability level. The characteristics of the COP trajectory exhibit a pattern of alterations that in part overlaps with other neurological pathologies. COP posterior displacement during the initial APA phase may play a relevant role in measuring postural impairment. In addition, this study can lead to COP-centered rehabilitation strategies aimed at re-educating MS patients to use a correct transition from stance to movement. Conflict of interest The authors report no conflicts of interest.
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Acknowledgments We are very grateful to the people with MS who participated in the study. The help provided by Ms. Cristina Scalas during data acquisition was also greatly appreciated.
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