Parkinsonism and Related Disorders 21 (2015) 888e893

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Discriminating features of gait performance in progressive supranuclear palsy € ller a, c, Shinichi Amano a, b, Jared W. Skinner a, Hyo Keun Lee a, Elizabeth L. Stegemo Nawaz Hack d, e, Umer Akbar d, e, David Vaillancourt a, Nikolaus R. McFarland d, e, Chris J. Hass a, d, * a

Department of Applied Physiology & Kinesiology, University of Florida, Gainesville, FL, USA Ohio Musculoskeletal and Neurological Institute, Ohio University, Athens, OH, USA Department of Kinesiology, Iowa State University, Ames, IA, USA d Center for Movement Disorders and Neurorestoration, Gainesville, FL, USA e Department of Neurology, University of Florida, Gainesville, FL, USA b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 30 October 2014 Received in revised form 14 May 2015 Accepted 22 May 2015

Introduction: Progressive supranuclear palsy (PSP) is the most common form of atypical Parkinsonism; however it is underdiagnosed and often misdiagnosed as Parkinson's disease (PD). Methods: We investigated gait initiation (GI) and gait performance in a total of 36 participants (12 PSP, 12 PD and 12 healthy age- and gender-matched controls) to gain further insight into specific motor deficits that characterize dynamic postural control and gait in PSP. Anticipatory postural adjustments (APAs), quantified by center of pressure (COP) displacement and speed prior to an initial heel off, and the maximum distance (COPCOM) between COP and center of mass (COM) during all three GI phases were calculated to evaluate dynamic postural control. Steady-state gait performance was also evaluated and compared across the groups. Results: APAs in PSP were significantly altered such that the posterior COP shift is profoundly diminished when compared to PD (p < 0.05). Moreover, proper velocity control during GI in PSP was affected, particularly in the mediolateral direction, when compared to PD (p < 0.05). The diminished COPCOM distance is further indicative of more severe dynamic postural instability in PSP than in PD (p < 0.05). Significant differences in spatiotemporal parameters, inter-step variability, and asymmetry during gait in PSP, in comparison with PD were also identified (all p's < 0.05). Conclusion: The present study reveals that the compensatory GI strategy in PSP is distinct from PD and paradoxically induces lateral instability. Further, gait performance in PSP is slower and more variable which could be the consequence of lateral instability and fear of falling. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Postural control Gait initiation Gait Progressive supranuclear palsy Parkinson's disease

1. Introduction Progressive supranuclear palsy (PSP) is the most common form of atypical Parkinsonism, or Parkinson-plus syndromes [1]. Individuals with PSP experience profound gait and balance impairment that appears early in the course of the disease, supranuclear gaze palsy, rapid disease progression and shorter survival times when compared to persons with Parkinson's disease (PD) [2]. PSP is

* Corresponding author. University of Florida, Department of Applied Physiology and Kinesiology, P.O Box 118205, Rm 100 Florida Gym, Gainesville, FL 32611, USA. E-mail address: [email protected]fl.edu (C.J. Hass). http://dx.doi.org/10.1016/j.parkreldis.2015.05.017 1353-8020/© 2015 Elsevier Ltd. All rights reserved.

often underdiagnosed and misdiagnosed as PD, which may delay appropriate care [3]. The relative paucity of quantitative information regarding postural control and gait function in PSP is a limiting factor for the development of evidence-based diagnostic criteria and the design of disease-specific therapeutic options. PSP gait has been characterized as a “drunken sailor” like gait, leading to frequent falls [4]. In contrast, PD gait is often slow, narrow-based, with reduced stride and shuffling, but largely stable at least early in disease progression. However, quantitative information to understand which specific aspects of gait function are altered and how they differ from PD is lacking. Measures of gait variability and asymmetry could potentially reveal important clinical features that augment our understanding beyond conventional

S. Amano et al. / Parkinsonism and Related Disorders 21 (2015) 888e893

spatiotemporal parameters, such as average step length, gait velocity, and cadence [5,6]. Furthermore, extensive investigation of postural control, beyond measures of static balance is needed to advance our knowledge regarding underlying postural instability. Particularly, postural control during transitional states in persons with PSP remains mostly unstudied [7]. Collectively, gaining more insight into dynamic postural instability and gait dysfunction in PSP is imperative to advance the knowledge of underlying motor symptoms and the design of optimal interventions to improve gait and postural stability in PSP. Our primary aim was to investigate the underlying biomechanical characteristics of dynamic postural control during gait initiation (GI) and ambulation in PSP to gain further insight into specific deficits that characterize dynamic postural control and gait performance in PSP. A secondary aim was to better elucidate the disease-specific differences in GI and gait performance between PSP and PD. Specifically, we attempted to understand how PSP vs. PD differ in terms of movement capabilities with emphasis on the anticipatory postural adjustments (APAs) during GI, the relationship between the center of pressure (COP), which is the point of application of the ground reaction force, and center of mass (COM), which is the point at which all the body's mass seems to be concentrated, and the magnitude and variability of spatiotemporal performance of gait. Based on the clinical presentation of PSP and previous findings, we hypothesized that both PSP and PD subjects would exhibit more dynamic postural instability during GI and altered spatiotemporal gait characteristics when compared to ageand gender-matched healthy elderly individuals. Furthermore, we hypothesized that persons with PSP would exhibit more severe dynamic postural instability and more pronounced gait impairment compared to persons with PD. 2. Methods 2.1. Participants Thirty-six older adults volunteered to participate. These included 12 ambulatory individuals meeting clinical diagnostic criteria for PSP [8], 12 individuals with a clinical diagnosis of PD, and 12 healthy subjects (Control). All participants signed an informed consent approved by the University's Institutional Review Board. Each PSP participant was age (±2 years) and gendermatched to a person with mild to moderate (i.e., Hoehn and Yahr 1e3.5) idiopathic PD and a Control participant with no history of neurological or orthopedic problems which could affect gait and postural control. Diagnosis of PSP or PD for each participant was confirmed by a fellowship-trained movement disorders neurologist at the University of Florida Center for Movement Disorders & Neurorestoration, using the National Institute of Neurological Disorders and Society for Progressive Supranuclear Palsy criteria for PSP [8] and the UK Brain Bank Clinical Diagnostic criteria for PD [9]. All participants were asked to come to laboratory in the selfdefined best “on-state” while taking their usual medications. For PSP and PD participants, the Unified Parkinson's Disease Rating Scale (UPDRS) was evaluated by an experienced neurologist blinded to participants' diagnosis. 2.2. Procedures Prior to data collection, participants were fitted with retroreflective markers according to the modified Helen Hayes marker set [10]. Ground reaction forces were collected at 360 Hz using three force platforms (Bertec Corp., Columbus, OH) embedded within an 8-m walkway. Kinematic data were collected at 120 Hz by a 10-camera 3D motion capture system (VICON, Oxford, UK).

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2.2.1. Gait initiation Participants performed five GI trials at a self-selected speed along the walkway. A starting position for each trial was established on the force platform located in the center of the walkway so that subsequent foot strikes could be measured by the two other force platforms forward to the starting position. The initial stepping limb and the positioning of the feet were self-selected and maintained for all trials. Upon hearing a verbal signal and after a brief pause, participants initiated walking toward a target placed at the end of the walkway, approximately 4 m away from the starting position. 2.2.2. Gait A starting position for each trial was established so that participants could walk at their steady gait speed when entering the motion capture volume. Participants performed ten trials at a selfselected speed. To obtain and evaluate participants' steady state gait patterns (without any acceleration/deceleration phase), only two middle strides of each trial were used for further analyses. 2.3. Outcome measures 2.3.1. Gait initiation The GI cycle was divided into three distinct phases, namely S1, S2, and S3, which have previously been defined [11,12] (Fig. 1(a)). Briefly, the S1 phase encompasses from the start of GI to the time point where the COP undergoes maximum posterior and lateral displacement towards the initial swing limb. The S2 phase is marked from the end of the S1 phase to the time point of the initial swing limb toe-off. The final S3 phase is identified from the end of the S2 phase to the time-point of initial stance limb toe-off. In the present study, the following outcome variables were evaluated: 1 S1COPDisp: displacement of COP in both anteroposterior (AP) and mediolateral (ML) direction during S1 phase, 2 S1COPVel/Spd: mean COP velocity and speed in both AP and ML direction during the S1 phase (COPVel and COPSpd, respectively), 3 COPCOM: maximum distance between COP and COM (COPCOM) in AP, ML and resultant directions during each phase (S1COPCOM, S2COPCOM, and S3COPCOM respectively). The posterolateral COP displacement prior to an initial step, which corresponds to S1COPDisp, and the distance between the COP and COM have been proposed and used to evaluate dynamic postural control and stability in a series of studies [11,13]. Positive values in the AP and ML directions correspond to posterior movement and movement toward the initial swing limb, respectively. Data reduction procedures and the GI outcome measures presented here are described in greater detail elsewhere [11,13]. 2.3.2. Gait The primary outcome measures were: (1) cadence, (2) gait velocity, (3) step length, (4) step width, (5) step duration, (6) double limb support time, and (7) gait asymmetry based on swing time, calculated using the standard definitions based on the marker data [14]. The step length and width were normalized by individuals' leg length (LL), and step duration and double limb support time were normalized to the gait cycle (GC). The coefficient of variation (CV) of step length and duration were also calculated to describe inter-step variability. 2.4. Statistical analyses A one-way ANOVA was performed with Group as a betweensubject factor for each outcome variable for each task (GI and

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Fig. 1. Representative overhead view of the center of pressure (COP; solid line) and the center of mass (COM; dotted line) trajectory during gait initiation (GI), when stepping with a right foot, of each group: (a) Controls, (b) PSP, and (c) PD. The three distinct GI phases (i.e., S1, S2, and S3) are described in Figure (a). The arrow in Figure (a) represents the calculated distance between the COP-COM. The point where GI starts is marked with an open circle. Positive values in the anteroposterior and mediolateral directions correspond to posterior movement and movement toward the initial swing limb, respectively.

Gait). Additionally for the gait evaluation, a supplemental analysis of covariance (ANCOVA) with gait velocity as a covariate was performed to control for its effect. In case that any of assumptions of ANOVA are violated, KruskaleWallis test was alternatively performed for each variable. A traditional level of significance was used (p  0.05). Upon detection of a significant difference, post-hoc pairwise comparisons with Tukey's adjustment (or SteeleDwass tests for non-parametric tests) were conducted. 3. Results No significant differences among the groups in age, height, or mass were found (p > 0.05; Table 1). While disease duration did not differ between PSP and PD, PSP subjects exhibited greater total motor part of the UPDRS score, as well as the posture and gait subscore, than PD (Table 1). Since the primary purpose of this study was to determine the biomechanical characteristics of GI and gait in PSP and its difference from PD, herein we mainly report findings regarding how PSP participants differed from PD and Controls. 3.1. Gait initiation Fig. 1 shows representative COP and COM trajectories for each participant group, and the GI characteristics (i.e., COP displacement, velocity and speed, as well as COPCOM characteristics) during GI for

each group are shown on Table 2 with statistical comparisons reported. The S1COPDisp in both directions significantly differed among the groups. Specifically, S1COPdisp for the PSP group was positive on the AP and ML directions, whereas it was negative for the other two groups, indicating the PSP subjects, on average, shifted their COP anteriorly and toward the initial stance limb during the S1 phase (Fig. 1(b)), while PD subjects shifted in the opposite direction: posteriorly and toward the initial swing limb (Fig. 1(c)). Furthermore, a significant main effect of Group for S1COPSpd in the AP direction revealed that the PSP subjects shifted their COP anteriorly significantly slower than the Control group, but not the PD group. While no significant main effect of Group was observed for COP speed in the ML direction, COP velocity in that direction in PSP significantly differed from the other groups. The GI outcomes related to the COPCOM moment arm during GI phases are also shown on Table 2. COPCOM moment arm in the AP direction for all three phases, as well as in the resultant direction during S2 and S3 phases significantly differed among the groups. Specifically, the PSP group exhibited significantly reduced COPCOM moment arm in the AP direction at all phases when compared to the controls. Even compared to the PD group, the COPCOM moment arm in the AP direction at the S2 and S3 phase for the PSP group were significantly diminished. The resultant COPCOM moment arm during the S3 phase in PSP was significantly reduced when compared to both the PD and Control groups. Despite a significant Group difference, the

Table 1 Mean (±standard deviation) values of demographic information and clinical characteristics of the study participants. Group

PSP

PD

Control

N M/F Age (years) Height (cm) Mass (kg) Disease duration (years) *UPDRS total *UPDRS motor *UPDRS PIGD (item 28e30)

12 5/7 66 (8) 164.9 (11.4) 77.4 (14.9) 6.5 (4.9) a 71.3 (15.6) a 49.6 (10.4) 6.33 (2.46)

12 5/7 64 (7) 169.8 (12.7) 78.4 (15.3) 7.8 (7.1) a 33.9 (8.2) a 23.5 (8.5) 3.33 (2.42)

12 5/7 67 (7) 168.1 (11.8) 72.1 (12.5) e e e

* a significant main effect of Group was observed in both conditions (p  0.05). Abbreviations: UPDRS, unified Parkinson's disease rating scale; PIGD, postural instability and gait disturbance. a A significant difference between PSP and PD was observed (p  0.05).

p-value

0.65 0.62 0.54 0.61 0.00 0.00 0.01

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Table 2 Mean (±standard deviation) values of gait initiation characteristics in each group. Group

PSP

PD

Control

Post-hoc p-value PSP vs. PD

COP displacement * S1DispAP (cm) * S1DispML (cm) COP velocity * S1VelAP (cm/s) * S1Vel ML (cm/s) COP speed * S1SpdAP (cm/s) S1Spd ML (cm/s) S1COPCOM *AP (cm) ML (cm) *Resultant (cm) S2COPCOM *AP (cm) ML (cm) *Resultant (cm) S3COPCOM *AP (cm) ML (cm) *Resultant (cm)

PSP vs. Control

PD vs. Control

0.01 0.01

0.01

Discriminating features of gait performance in progressive supranuclear palsy.

Progressive supranuclear palsy (PSP) is the most common form of atypical Parkinsonism; however it is underdiagnosed and often misdiagnosed as Parkinso...
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