Introduction

Gait initiation is a transitory phase between standing posture and steady-state locomotion [1]. Although gait initiation has been investigated in populations with disabilities, such as in individuals with Parkinson’s disease and stroke, there are only a few studies describing some components of gait initiation after an incomplete spinal cord injury (iSCI) [2,3,4]. Postural stability during gait initiation has shown to be compromised in individuals with iSCI [4], deserving further investigation especially to inform application of therapeutic interventions.

The aquatic environment is often used to assist the first steps after a neurological injury, and has been shown to positively influence balance and walking functions in the early stages [5] and chronic stages [6] of locomotor recovery in individuals with neurological disorders other than iSCI. In the iSCI population, the evidence is scarce, although promising, suggesting that walking training in water could improve walking speed, distance and daily step activity [7]. The direct effects of immersion on steady-state walking have shown that walking in water is slower than walking on land [8, 9]. We expected that the mechanical and thermal properties of water may also influence gait initiation performance compared to gait initiation on land, during anticipatory postural adjustment (APA) and execution phases of gait initiation. Therefore, we used a similar paradigm as in our previous studies [10, 11] with parameters of the center of pressure (COP) excursion, impulse forces, trunk acceleration, and reported perceptions during land and in-water performances to assist us in the understanding of different components of postural control when individuals with iSCI initiate gait in water in contrast to land.

Our previous paper, which is the first part of our study investigating the effects of water immersion on postural control in individuals with iSCI, suggested that the aquatic environment evokes postural disturbances during quasi-static standing without inducing the fear of falling [10]. In this second part of our study, we aim to explore for the first time the effects of water immersion during the transient phase to bipedal locomotion, gait initiation, across a series of case studies with individuals with iSCI with different motor and sensory functions.

Methods

Participants and location

Adult participants with iSCI were recruited through poster advertisement at a tertiary rehabilitation hospital during a 10-month period. Participants with a traumatic or non-traumatic etiology of iSCI who were able to initiate gait and walk at least three unassisted steps were included. Participants were excluded if they presented the following conditions: (i) history of mental, respiratory, cardiac or skin conditions that precluded immersion in warm water; (ii) participants who were unable to stand unsupported on land and in water; and (iii) individuals allergic to chlorine.

Based on these criteria, five adults with iSCI were eligible for participation (Table 1). Informed written consent was obtained from each participant. This study received approval from the research ethics board of the Toronto Rehabilitation Institute—University Health Network, Toronto, Canada (REB-10.029) in accordance with the declaration of Helsinki on the use of human participants in experiments.

Table 1 Participants’ characteristics
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Clinical examination

The clinical assessment prior to tests in the aquatic and land environments included the assessment of participants’ neurological impairment through the International Standards for Neurological Classification of Spinal Cord injury (ISNCSCI) [12, 13], and the clinical balance function assessed through the Berg Balance Scale (BBS) [14] and the Mini-Balance Evaluation System Test (Mini-BESTest) [15] (Table 2). Details of the clinical examination are reported in our previous study [10].

Table 2 Classification of participants’ clinical balance
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Instrumentation

A therapeutic pool measuring 9.8 × 4.9 × 1.1 m with temperature set at 34–35 degrees Celsius, was used for the assessment of gait initiation in the water. The area outside the therapy pool was used for the assessment of gait initiation on land. In both settings (i.e., land and water), we used the same instrumentation as described in our prior study with able-bodied subjects [11] and with individuals with iSCI [10], which included a waterproof force plate (AMTI, ORP-WP-1000, USA) and three wireless body-worn inertial sensors (Physilog, BioAGM, Switzerland) sealed in waterproof bags (aLoksak, Inc., Naples, USA). The inertial sensors were attached to the upper trunk region (head of sternum), and to the lower trunk region overlying L5/S1 landmarks. Data from the force plate (sampled at 1000 Hz) and from the inertial sensors (sampled at 500 Hz) were synchronized and analyzed using custom-developed routines on MATLAB (Mathworks Inc., Natick, USA).

Experimental procedures

Participants performed gait initiation on land and in water in 2 consecutive days. Exception was Participant 3 who performed one experiment on day 1 and the other one on day 3 due to conflict in his schedule.

Prior to starting to walk, participants stood in the same comfortable standing position. Participants were instructed to initiate gait using their preferred leg, immediately after a visual command. The locations of feet were marked on the force plate with water-resistant chalk to maintain the exact same feet locations between the conditions and among trials. A light was positioned at eye level and 3.5-m distance and was activated following 5 to 10 s of quiet standing. Participants walked ~4 steps with their upper limbs positioned above the water surface to avoid additional water resistance beyond what was delivered to the lower body. Ten trials of gait initiation were performed on land and ten trials were performed in water.

After completion of tests on land and in water, all participants responded to an interview consisting of five questions investigating their perceptions of walking in water and on land (Supplementary information).

Data analysis

We calculated the percentage of body weight (BW) offloading in water using the equation below:

$$\% \;{\mathrm{offloading}} = 100\;\times\;\left( {{\rm BW}_{\rm land} - \;{\rm BW}_{\rm water}} \right)/{\rm BW}_{\rm land}$$

where: BW on dry land (BWland) and apparent BW in water (BWwater) were computed from the vertical component of ground reaction force (data acquired with the force plate) during the last 2 s of quiet standing prior to initiating walking.

Butterworth low-pass filters were used for the force plate signals (second order with a cut-off frequency of 10 Hz) and inertial sensors signals (fourth-order with a cut-off frequency of 30 Hz) [11].

As in our previous study [11], gait initiation phase was defined from the first dynamic event on the force plate (APAONSET) to heel-strike of the first swing limb, determined through the free vertical moment on the force plate (Fig. 1) [11, 16]. We used the APAEND point to mark the beginning of the execution phase on the ground reaction force (GRF) and acceleration signals.

Fig. 1
figure 1

Center of pressure (COP) horizontal trajectory during gait initiation with the right leg on land. (1) Onset of Anticipatory Postural Adjustment (APA) phase. (2) Peak of APA phase. (3) End of APA phase (beginning of Execution phase). (4) Most lateral and posterior landmark towards the first stance limb. (5) End of gait initiation phase detected on the negative peak of the free vertical moment (FVM). APA phase was defined from the event 1 to the event 3. Execution phase 1 (EXE1) was defined from the event 3 to the event 4, and Execution phase 2 (EXE2) was defined from the event 4 to the event 5

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We summarized the dependent variables of all trials in each condition in mean ± SD. We used a thematic analysis to identify the themes from the participants narrative as per Braun and Clarke [17]. One researcher (AMB) searched, identified, and developed initial themes. A second member of the research team (MCV) reviewed the themes to ensure they were representative of the data and to ensure theme saturation.

Dependent variables

We calculated the duration (s), length (cm), and velocity (cm/s) of the COP within the APA, EXE1, and EXE2 trajectories. The impulse generated during the execution period of gait initiation was calculated by integrating the area under the curves of anteroposterior (AP) and vertical forces. Duration (s) of impulse, impulse forces normalized by body weight (BW) (%BW.s) and non-normalized by BW (N.s), and forces (N) in AP and vertical directions were calculated during the execution period of gait initiation (i.e., from APAEND to heel-strike).

We calculated the root mean square (RMS) acceleration (in m/s2) of the upper and lower trunk in the AP and mediolateral (ML) directions during Execution. The Execution was from the end of APA (APAEND) to the end of gait initiation phase. In order to analyze how upper and lower trunk accelerations changed in relation to each other, we calculated the upper trunk to lower trunk acceleration ratio in AP and ML directions during Execution phase.

Results

Clinical balance

The entire classification of clinical balance is presented in Table 2. The BBS score varied from 42 to 56 among participants. Participants 4 and 5 presented the highest balance performance for the BBS and Mini-BESTest. Participant 2 presented the lowest balance score both on the BBS and the Mini-BESTest and was the one using a power wheelchair to assist his mobility.

Gait initiation biomechanical parameters

COP parameters

Figure 2 illustrates the COP trajectory during gait initiation on land and in water from two participants, one with a moderate light touch and pin prick deficits and relatively low-balance function on the Mini-BESTest (P1), and the other with a high-balance function (P4) (Table 3). Overall, Participant 1 presented more inflection points in the COP trajectory in water and on land during the execution of gait initiation in contrast to the COP trajectory with less inflection points of the Participant 4. In addition, Participant 4 presented a larger APA in water (AP-water: 6.02 ± 1.42 cm) compared to dry land (AP-land: 2.22 ± 1.09 cm), while Participant 1 did not respond with a larger APA in water.

Fig. 2
figure 2

Center of pressure (COP) horizontal trajectories during gait initiation with the right leg, on land (black trace) and in water (gray trace). Left: COP trajectory of a participant with low-functioning balance performance (Participant 1). Right: COP trajectory of a participant with high-functioning balance performance (Participant 4). The COP trajectory is representative of a single trial. APA: from COP onset (1) to the end of APA (3). COP EXE1 from the end of APA (3) to the approximate toe-off of swing limb (4). COP EXE2 from toe-off (4) to the end of COP trajectory (5). (2) APA peak in mediolateral direction

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Table 3 Center of pressure (COP) trajectories during anticipatory postural adjustment (APA) and execution phases on land and in water
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Table 3 describes the COP parameters during APA, EXE1 and EXE2, separately. During APA, the length and velocity in AP and ML directions increased in water in contrast to land, more accentuated in the participants who presented higher balance function. For example, APA length and duration increased in Participants 4 and 5, only.

During the weight transfer phase, i.e., the COP EXE1, the responses were more inconsistent across participants. The ML COP length was decreased more accentuated in Participant 2 (land: 13.69 ± 2.10, water: 7.14 ± 1.50), who had the lowest balance score. Participant 4, with the shortest height (157.5 cm) and higher body offloading (62.3%), presented a much slower velocity in AP (land: 10.39 ± 2.16, water: 5.86 ± 2.78) and ML direction (land: 23.25 ± 2.17, water: 16.45 ± 5.31) in water during EXE1 (Table 3).

The pronounced changes in COP trajectory occurred in EXE2 phase, i.e., the COP trajectory occurring while individuals were stepping forward, from approximate toe-off to the heel-strike of the swing limb (Fig. 2). The duration and length of EXE2 in AP and ML directions were longer in water than on land across all participants. A decrease in COP velocity in AP direction was observed in water in contrast to land, more evident in Participant 4.

Impulses

All participants presented larger impulse durations during the execution phase of gait initiation while stepping in water compared to on land (Table 4). The vertical and AP impulses, normalized by body weight in each environment, increased in water compared to on land. The impulse not normalized by the body weight slightly reduced in vertical direction in most participants and increased in AP direction in water when contrasted to land.

Table 4 Impulses in vertical and anteroposterior directions generated during execution phase of gait initiation of participants on land and in water
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Trunk acceleration parameters

Table 5 shows the results of RMS acceleration of upper and lower trunk in AP and ML directions during execution of the first step. The acceleration of upper trunk in the ML direction, along with the lower trunk in the AP and ML directions presented a more accentuated decrease in water, in contrast to the acceleration on land, across all participants, except for Participant 4 who increased upper trunk acceleration in the AP direction. When examining the upper trunk to lower trunk acceleration ratios, most participants had a noticeable increased ratio in the AP direction, where Participant 4 had the most accentuated upper/lower trunk ratio increase in water in contrast to land and in contrast to other participants (Fig. 3).

Table 5 Trunk acceleration parameters during gait initiation on land and in water: root mean square acceleration (RMSACC) in anteroposterior (AP) and mediolateral (ML) directions
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Fig. 3
figure 3

Upper to lower trunk acceleration (ACC) ratio in anteroposterior (AP) direction of all five participants during ten trials of gait initiation in water (gray line) and on land (black line)

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Participants perceptions while walking in water and on land

Table 6 displays the supporting quotes from participants on the following three main themes analyzed across the dataset: (1) The aquatic environment as a facilitator for walking function, (2) Challenges while walking in water and on land, and (3) Safety.

Table 6 Themes and supporting quotes from participants
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Discussion

This study is the first to describe gait initiation in water after iSCI, measured by parameters of COP trajectory, impulse forces, trunk acceleration, and individual perceptions. The different neurological and balance control attributes of participants helped to explore whether the aquatic environment could influence both the quantitative parameters and qualitative perceptions of walking in water depending on each participant’s ability and interactions with the aquatic and land environments. The aquatic environment influenced the performance of gait initiation in all five participants during anticipatory and execution phases, providing both challenges and support while participants initiated gait in water.

Through the COP trajectory, we explored how the aquatic environment influenced the anticipatory and execution phases of gait initiation of individuals with different neurological deficits. For example, Participant 1, who presented with a substantial sensory deficit aligned with a moderate deficit in anticipatory and reactive balance control, was the only individual who demonstrated decreases in APA length in water in comparison to land. In contrast, the participants with higher balance function (P4 and P5) were those with the most moderate increase in APA length and AP velocity in the aquatic environment. In four participants, the length of COP trajectory in AP direction increased substantially during EXE2 while the velocity of the COP trajectory in AP direction decreased. Our previous studies with able-bodied participants showed similar results, i.e., longer COP trajectory with decreased COP velocity when starting to walk in water compared to dry land, potentially due to the effect of the water resistance on the lower body [11, 18].

All participants had greater AP impulses while executing the first step in water than on land. In previous studies examining impulses during the steady-state gait cycle in young [19] and elderly [20] participants, the horizontal impulses were higher in water than on land for both the groups. In the present study, the analysis of the non-normalized impulse and the mean impulse force showed a decrease in the vertical impulse in water versus the land, suggesting the impact of buoyancy of the water while initiating gait.

The RMS acceleration of upper and lower trunk detected different trunk acceleration patterns to maintain balance while initiating gait in water compared to land. There was an increase in RMS acceleration ratio (upper trunk/lower trunk) in the AP direction in water compared to land in most participants. As the participants walked forward in water when immersed to the umbilicus level, the water resistance applied to the lower body decreased acceleration in the lower trunk, while the upper trunk moved forward freely. The resistance on the lower body, aligned with the buoyancy of the water, appears to be an incentive for a new trunk strategy to maintain stability in water and seems to evoke a different pattern of trunk control to maintain balance while initiating gait. A change in the trunk strategy in water could be incorporated into training programs for enhancing balance control that could be beneficial for dynamic activities of daily living during standing.

The participants’ perceptions supported our interpretation of quantitative parameters of gait initiation in water and on land. For example, most participants reported the slowing down of walking, suggesting that the water resistance was a force opposing gait initiation. In fact, both the COP and GRF parameters showed more clearly the influence of resistance on decreasing velocity of COP and increasing the AP mean force while participants walked forward. While the resistance caused by water challenged the participants, the buoyancy and hydrostatic pressure may have supported the participants’ during the step in the execution phase. Most patients reported that they felt secure and safe to step forward surrounded by water. Four of five participants reported that they did not have to worry about falling because of the perceived support from the water pressure.

Other relevant clinical characteristics, such as trunk control, somatotype, and the proportion of lean and fat mass of participants, could potentially add to the interpretation of the quantitative and qualitative measures of gait initiation performance, both in water and on land. Particularly, if a more representative sample of participants with iSCI with stratification based on differing degrees of trunk control could be studied.

The present study complements our previous study investigating the effects of the aquatic environment on quasi-static standing posture [10]. Our findings indicate that the aquatic medium also influences the dynamic postural control during gait initiation and suggests that immersion in water prolonged the execution of gait initiation and may facilitate longer step execution during training in the early stages of SCI. We suggest that the increasing resistance to the lower limbs and the challenges of the trunk movement patterns during step initiation in the aquatic environment may be a coordinated training strategy worth pursuing to augment therapeutic outcomes. Altering the velocity of movement performed and the level of immersion in water provides an approach to change the water resistance and buoyancy levels incrementally. The versatility of the aquatic environment could be a venue for training specificity for individuals with different sensorimotor and balance dysfunctions.

Future studies should explore further paradigms of postural control incorporating both quiet standing posture and gait initiation, as well as patients’ perceptions when investigating how the application of customized therapeutic interventions, such as aquatic therapy, might contribute to improvement of postural control in individuals with varying sensorimotor deficits in both traumatic and non-traumatic iSCI.