Does positive pressure body weight-support alter spatiotemporal gait parameters in healthy and parkinsonian individuals?

Abstract

BACKGROUND: Evidence suggests treadmill training (TT) and body weight-supported treadmill training (BWSTT) are effective strategies to improve gait in Parkinson’s disease (PD) patients. However, few researchers have investigated the spatiotemporal parameters during TT or BWSTT.

OBJECTIVE: The goal of this study is to determine gait adaptations in PD and healthy subjects during positive pressure BWSTT and post-intervention overground walking.

METHODS: Ten PD and ten healthy individuals participated in this study. Baseline spatiotemporal parameters were assessed using a six meter instrumented mat. A 10-min progressive BWSTT trial from 10% to 40% body weight support (BWS) was then completed. Video capture and analysis of 10-min BWSTT trials were performed to determine spatiotemporal gait parameters. Three (5-min, 10-min, and 15-min) post-intervention overground assessments were obtained.

RESULTS: During positive pressure BWSTT there was a significant effect of BW support on step length(SL) increase (p < 0.01) and cadence decrease (p < 0.001) in the healthy group but not in the PD group (p = 0.45 SL, p = 0.21 cadence). In post-intervention assessments there was a significant effect of time on velocity (p < 0.002 non-PD, p < 0.001 PD) and cadence (p < 0.05 non-PD, p < 0.01 PD) in both groups.

CONCLUSIONS: There appears to be a generalized effect of TT on overground gait mechanics after a single session of positive pressure BWSTT regardless of PD impairment.

Keywords

Parkinson’s disease treadmill training central pattern generator proprioception

1 Introduction

Parkinson’s disease is a progressive neurodegenerative movement disorder with worldwide prevalence (Muangpaisan, Mathews, Hori, & Seidel, 2011). The classic signs and symptoms of PD are rigidity, bradykinesia, and resting tremor. Other signs and symptoms include postural ataxia, gait and balance disturbances, abnormal proprioception, and diminished motor skill learning. The locus of neural dysfunction is the substantia nigra pars compacta of the mesencephalon (Hutchinson & Raff, 2000).

The standard treatment for PD is dopaminergic medication (Hauser et al., 2009; Hauser, Silver, Choudry, Eyal, & Isaacson, 2014); however, dopamine agonists and/or precursors have relatively short therapeutic duration (2–4 hours) most notably for tremor, bradykinesia, and motor skills (Kang & Auinger, 2012). Other functional symptoms of PD such as postural and gait ataxia, poor balance, and abnormal proprioception are less improved with medication (Vu, Nutt, & Holford, 2012; Jacobs & Horak, 2006). Recently, extended-release dopaminergic medications have been introduced to prolong therapeutic effects (Pahwa et al., 2014). Any therapeutic intervention that slows the progression of PD, or improves motor function, is considered highly successful and should be considered for co-management along with medication. As such, various forms of exercise have been proposed as therapeutic strategies for PD (Schenkman et al., 2012; King & Horak, 2009).

Treadmill training (TT) is a well-studied mode of exercise for PD patients (Merholzet et al., 2010). A subset of TT is body weight-supported treadmill training (BWSTT) using a harness or a positive pressure air chamber. Utilization of TT and BWSTT results in improved walking economy (Fernandez-Del-Olmo et al., 2014), endurance (Nadeau, Pourcher, & Corbeil, 2014), gait mechanics (Bello, Sanchez, Vasquez-Santos, & Fernandez-Del-Olmo, 2014), and functional capacity (Rose, Lokkegaard, Sonne-Holm, & Jensen, 2013). Relevant to the present study, Protas et al. (2005) and Fisher et al. (2008) both report gait improvements in PD subjects after TT interventions. Protas et al. (2005) observed increases in gait velocity, increased stride length and self-reported reduced incidence of falls after an eight week trial of TT. Fisher et al. (2008) also report dose responsive increases in gait velocity and stride length in an eight week trial of graded intensity TT. Additionally, PD patients have improved function during daily activities after trials of TT and BWSTT as measured by the Unified Parkinsons Disease Rating Scale (UPDRS) (Rose et al., 2013; Miyai et al., 2002). Still, few researchers have studied the neuromechanical factors underpinning these positive findings. Bello et al. (2008) report a decreased cadence and increased step length in PD individuals during treadmill walking. In a follow-up study, Bello, Marquez, Camblor, and Fernandez-Del-Olmo (2010) observed decreased cadence and increased step length in PD subjects walking over a treadmill but, notably, not over a beltless treadmill simulator. Rose, Lokkegaard, Sonne-Holm, and Jensen (2013) measured lower extremity muscle activity in PD subjects and a healthy group using surface electromyography during positive pressure BWSTT. Rose et al. (2013) observed increased knee flexor activity with a higher percentage of body weight-support (BWS). Reciprocally, knee extensor activity had an inverse relationship with percentage of BWS. The findings from Bello et al. (2008; 2010) and Rose et al. (2013) suggest that TT and BWSTT have neuromechanical effects on gait in parkinsonian individuals. However, the causal mechanisms of the spatiotemporal and kinematic changes observed remain theoretical.

The goals of the present study are to 1) quantify gait changes in PD and healthy individuals during positive pressure BWSTT and 2) assess the influence of a single session positive pressure BWSTT on spatiotemporal parameters during post-trial overground walking. Gait mechanics are load and sensory dependent (Harkema et al., 1997; Dietz & Duysens, 2000) and therefore expected to be altered during BWSTT.

2 Methods

The investigation was implemented using a non-randomized, quasi-experimental controlled trial. The Institutional Review Board of Sacred Heart University approved the study. Purposive referral sampling was used to recruit the study participants from local PD support groups. Ten individuals previously diagnosed with PD (60.6 ± 14.9 y, 7 M/3 F) and ten healthy, age matched individuals (64.1 ± 7.9 y, 5 M/5 F) participated (Table 1). All participants granted informed consent and completed a health history questionnaire. All PD participants were evaluated with the UPDRS and had a functional level of Hoehn & Yahr stage 3 or lower (1.6 ± 0.6). Additionally, all participants met the following criteria: (1) no history of orthopedic or cardiovascular conditions that preclude or interfere with walking and (2) maintenance of current medication schedule.

Baseline spatiotemporal gait parameters were assessed with an instrumented 6-m mat (GAITRite, CIR systems Inc.; Sparta, NJ). The GAITRite mat has been validated for spatiotemporal analysis in the PD population(Pahwa et al., 2014). All participants were allowed one practice repetition walking over the mat. Participants were then asked to walk over the instrumented mat at their self-selected pace. Participants then completed a 10-min trial of positive pressure BWSTT (AlterG Inc.; Fremont, CA). Walking pace was determined for each participant based on the self-selected velocity from baseline trials. A 1-min warm-up period was permitted on the AlterG treadmill. Progressive BWS was increased every 2 minutes during the 10-min trial as follows: (0–2 min 100% BW, 2–4 min 90% BW, 4–6 min 80% BW, 6–8 min 70% BW, 8–10 min 60% BW). The AlterG treadmill provides BWS through a positive air pressure chamber that surrounds the user at waist level. Users of the treadmill wear specially designed shorts that zip along the top of the chamber but still allow freedom of lower extremity and trunk mobility. During the BWSTT trial participants were instructed to walk normally and were not given any cues or feedback. Sagittal plane video capture of each phase was obtained at 210fps (Casio Exilim; Tokyo, Japan). At the completion of the 10-min trial participants exited the treadmill and sat comfortably for five minute intervals. Three additional self-selected walking trials across the GaitRite mat were collected at 5-min, 10-min, and 15-min post BWSTT.

Spatiotemporal video gait analysis of each BWS phase of the 10-min BWSTT trial was performed via MyoVideo software (Noraxon USA; Scottsdale, AZ). Treadmill velocity was constant during BWSTT thus step frequency and step length were determined during the last 30 sec of each BWS phase. Significance was set at p < 0.05 for overground differences in velocity, step length, and cadence using a repeated measures analysis of variance (ANOVA) (group by time). Differences in BWSTT step length and cadence were assessed for significance (p < 0.05) using a repeated measures ANOVA (group by BWS). Pairwise comparisons with Bonferroni adjustments were utilized for post-hoc analysis. All data analysis was performed with PASW SPSS version 18.

3 Results

A Shapiro-Wilk test confirmed that all results for spatiotemporal analysis were distributed normally (p > 0.05). Generally, there was a lower cadence and longer step length between overground walking and TT in both groups (Tables 2, 3). There was a significant main effect of percentage BWS on step length in the healthy group [F(1.8, 15.9) = 6.6; p < 0.01; partial η² = 0.42] but not in the PD group [F(4,36) = 0.946; p = 0.45]. BWS also had a significant effect on cadence in the healthy group [F(1.8, 15.9) = 6.3; p < 0.001; partial η² = 0.41] but did not change in the PD group [F(4,36) = 1.5; p = 0.21] (Table 2). Post-BWSTT spatiotemporal analysis revealed a significant main effect of time on velocity for both groups (Table 3). The PD group increased velocity [F(3,54) = 8.0; p < 0.001; partial η² = 0.31] and cadence [F(3,54) = 6.6; p < 0.01; partial η² = 0.27]. Increased step length approached significance [F(1.7,26.9) = 2.0; p = 0.06]. The non-PD group also increased velocity [F(3,27) = 6.8; p < 0.002; partial η² = 0.43] and cadence [F(3,27) = 3.0; p < 0.05; partial η² = 0.25]. There was also an increase in right foot step length in the non-PD group [F(3,27) = 6.3; p < 0.002; partial η² = 0.41]. There were no significant differences between groups and spatio-temporal parameters during the three post-BWSTT trials indicating the response to BWSTT was the same regardless of PD impairment.

4 Discussion

Walking is an important factor of functional health and freedom among older adults and especially individuals with PD. The current literature supports the use of TT as a therapeutic modality to improve gait in PD patients (Nadeau et al., 2014; Rose et al., 2013). The present study examined the influence of a 10-min session of positive pressure BWSTT on spatiotemporal gait parameters in a PD group and a healthy, non-PD group. During the BWSTT trial only the healthy group displayed altered gait as an effect of BWS, specifically decreased cadence and an increased step length. Our findings support, yet, partially contrast previous reports of decreased cadence and increased step length for PD patients during TT (Bello et al., 2013, 2014). To our knowledge, no other researchers have reported on spatiotemporal parameters for PD during positive pressure BWSTT using the AlterG. Most investigations have focused on spatiotemporal effects after TT or BWSTT interventions, as opposed to during intervention (Fernandez-Del-Olmo et al., 2014; Nadeau et al., 2014; Protas et al., 2005). The current findings of increased velocity and increased cadence post-BWSTT are consistent with previous reports. Conversely, spatiotemporal parameters were not altered the same in each group during BWSTT. Yet, post-BWSTT overgound gait was similarly improved in both healthy and PD individuals.

The gait changes observed in the healthy, non-PD group suggest a neuro-mechanical BWSTT effect on gait. Specifically, the findings support the existing evidence of human central pattern generators (CPG) on gait control (Dietz, 2003; Duysens & Van de Crommert, 1998). CPG are sensory and load dependent (Harkema et al., 1997) and BWSTT may alter the spinal and supraspinal influences on CPG neuromotor activity. The results of the BWSTT trial showed the PD individuals did not alter their gait patterns as BWS increased. One explanation may be that parkinsonian individuals have abnormal proprioception and dysfunctional sensorimotor integration (Jacobs & Horak, 2006). Lower extremity loading is an important stimulus for gait control in PD, specifically for extensor activation (Harkema et al., 1997; Dietz & Colombo, 1998). Decreased lower extremity afferent input results in decreased extensor activation and an increased flexor pattern. In their study of PD subjects using positive pressure BWSTT, Rose et al. (2013) found increased lower extremity flexor muscle activation and decreased extensor muscle activity. This finding may support the theory of a primitive flexor dominant gait (Duysens De Groote, & Jonkers, 2013) and the half-center asymmetrical model (Zhong, Shevtsova, Rybak, & Harris-Warrick, 2012) of CPG neural activation. A decrease in extensor activation during the stance phase of gait may result in a flexor burst pattern and lengthened stride. Walking in the AlterG reduces lower extremity extensor activation and mechanoreceptive afferent input and thus, positive pressure BWSTT with the AlterG should, in theory, lengthen the stride of users. However, reduced extensor activation in the AlterG may affect PD individuals differently due to an already compromised proprioceptive sensorimotor system and failing feedforward control.

The AlterG treadmill used in this study for BWSTT blocks the user’s feet from view. This may have resulted in further sensory compromise in PD individuals as they require increased visual feedback to maintain gait (Suteerawattananon, Morris, Etnyre, Jankovic, & Protas, 2004). The loss of visual perception of their feet may have caused some PD subjects to involuntarily shorten their stride (Jacobs & Horak, 2006), thus negating the expected lengthening as observed in the healthy group.

Interestingly, both groups in this study improved gait parameters after the BWSTT session as a function of time (5-min, 10-min, 15-min post). This suggests a potential neuromechanical training effect that transferred to overground walking as reported in previous studies. This also could have been the result of a “learning” response during repeated trials. Although PD individuals did not display the same gait alterations as the healthy group during BWSTT there appears to have been a training stimulus as demonstrated by post-BWSTT overground gait analysis. Altogether, the data presented in this study support a “generalized treadmill effect” as originally discussed by Bello et al. (2008).

5 Limitations

This study used progressive unloading by increasing BWS 10% every 2 minutes. Spatiotemporal pattern changes in healthy adults were directly correlated to the amount of BWS. However, in PD individuals the frequent change in BWS may have disrupted their gait pattern and rhythm. Bello et al. (2008) suggest that treadmills act as gait pacemakers for PD patients. Maintaining a constant 40% BWS for the entire session may result in further adaptation and neuromotor learning in PD individuals. The loss of visual perception has been discussed. Allowing the participants to view their feet during AlterG TT may reveal alternative results to the current findings.

6 Conclusion

In this study of one session of BWSTT, spatiotemporal gait parameters changes were observed in a healthy group but not in a PD group. The results provide evidence of differences in sensory-driven neuromotor control of gait in PD compared to non-PD individuals. The findings further support the current literature regarding CPG theories of locomotor control. Treadmill training is a practical option to improve gait mechanics in

The results in this study suggest overground gait may improve after TT regardless of PD impairment. Furthermore, due to inherent proprioceptive and sensory deficiencies of PD, neuromechanical control of gait in PD may be better influenced under normal body weight load compared to BWS or hypogravitational conditions.

Conflict of interest

The authors confirm that they have no conflicts of interest or financial incentive related to the content of this manuscript.

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