This study utilized a novel perturbation-based assessment device to characterize the biomechanical control of induced weight transfer in individuals post-stroke and age-matched healthy control participants. The findings confirmed our hypothesis that individuals post-stroke demonstrated reduced ankle dorsiflexion, knee flexion, and hip abduction during the shock absorption phase of weight transfer. In addition, the onset timing of knee flexion relative to ankle dorsiflexion was delayed for participants with stroke, indicating possible abnormalities in inter-joint coordination or joint stiffness during loading. Compared to controls, individuals with stroke took more time to stabilize the COPv,M-L following ground contact. Prolonged paretic limb COPv,Max stabilization time and lower CMSA score were associated with lower scores on clinical balance and mobility tests in stroke. These findings suggested that diminished lower limb joint flexion and hip abduction, inter-joint timing delays, and prolonged COP stabilization time likely reflected deficits in weight transfer and weight bearing ability following stroke.
Significantly greater passive resistance to dorsiflexion of the paretic ankle has been documented after stroke when perturbations were applied to the ankle joint during sitting (42). Our results expanded this finding and demonstrated that when rapid weight transfer was induced, participants with stroke did not produce timely and sufficient joint flexion in the ankle and knee during the shock absorption phase. Potential factors that could contribute to reductions in joint flexion include muscle weakness and spasticity (43). In particular, the hypertonicity of ankle plantarflexors has been well-documented in individuals with chronic stroke during passive ankle dorsiflexion in seated and supine positions (44,45). Spasticity could result in higher resistance to passive muscle stretch during dorsiflexion and lead to the reduced dorsiflexion displacement and angular velocity during limb loading observed in the present study. Based on the description of the CMSA foot subscale score, spasticity is present and marked in stages 2 and 3. By stage 5, spasticity has waned and is only evident with rapid movement or at the extremes of the range (46). In our study more than half of the participants had a foot staged at 4 or less. In addition, lesion-induced alterations in intrinsic muscle properties (47–52) and/or architecture of the plantarflexors may cause an abnormal increase in passive ankle stiffness during dorsiflexion. Further research on the ankle and knee muscle properties and muscle activities during rapid weight transfer is warranted to determine the neuromuscular mechanisms underlying abnormal joint reactions during weight transfer in individuals post-stroke.
A coordinated spatio-temporal muscle synergy linking distal and proximal musculature is fundamental in providing an efficient postural response and in maintaining upright stability following external perturbations of standing. Following standing platform horizontal translations, a timing delay between the initiation of the proximal and distal muscle was 170% longer in post-stroke fallers compared to non-fallers (53). This suggests that abnormalities in initiating muscle activity or intermuscular timing likely disrupts intralimb coupling and could contribute to falls in persons with stroke (53). Our results supported the previous findings by demonstrating that knee joint flexion timing relative to the ankle was delayed in individuals post-stroke compared to controls. The inter-joint timing delays in flexion likely contributed to the disrupted weight transfer processes that may influence balance control. These findings highlight the importance of targeting problems of ankle-knee joint coordination during weight bearing activities for rehabilitation post-stroke.
Previous studies in landing have identified that trunk and lower extremity joint movements and neuromuscular activity are coordinated to effectively perform landing shock absorption (54,55). With reduced lower limb joint movements and disrupted inter-joint timing observed in participants with stroke, it is likely that more energy dissipation was required at the upper body. Thus, the increased trunk and body COM downward displacement observed in the stroke group may indicate that the upper body was destabilized partly due to the inefficient shock absorption from the lower limb. This observation may have important implications for gait performance. During the weight transfer phase of walking, the body COM is shifted forward and downward towards the leading limb following heel strike. An important function of the leading limb is to provide sufficient support and redirect the body COM forward and upward during this step-to-step transition. The mechanical work done during the step-to-step transition is a major determinant of the metabolic cost of walking (56). If stroke-related deficits in ankle and knee impact absorption increase downward displacement of COM and mechanical work, a greater energy cost of walking would likely occur. However, although postural control principles of standing and gait are similar, the task performed in the present study was different from walking and, therefore, the abnormalities identified may or may not be directly applicable to continuous gait. In this regard, studies forcing weight transfer towards the paretic limb should also be conducted during steady state gait.
Our finding that individuals post-stoke showed abnormalities in ankle dorsiflexion during induced weight transfer is in agreement with previous gait studies that identified limited ankle dorsiflexion at initial contact and during stance in persons with stroke (43,57). In other continuous gait studies, premature ankle plantarflexor muscle excitation on the paretic side was observed and may prevent the knee from flexing further in response to early stance phase loading (58,59). During the weight acceptance phase of walking, contraction of the pretibial muscles restrains ankle plantarflexion and moves the tibia forward. This coordinated knee flexion and ankle dorsiflexion facilitates the weight transfer process to the leading limb and likely aides in maintaining higher instantaneous gait speed during loading response (60). Without sufficient and timely joint flexion in the ankle and knee, greater body center of mass elevation is needed in order to advance the body over the heel fulcrum. A CMSA stage 4 and above indicates full active range of dorsiflexion and plantarflexion of the foot and full active range of knee flexion and extension. Based on the CMSA results, 7/15 and 11/15 participants had full active range of the foot and leg, respectively. Considering the importance of ankle and knee joints during weight bearing, it is likely that the reduced and slower knee and ankle joint flexion limited the ability to perform rapid weight transfer for individuals post-stroke during locomotion.
Previous studies suggest the importance of COPv,M-L and amplitude as a tool for predicting fall risk (61) and balance control assessment (62). In the present study, the perturbation imposed a rapid body COM displacement in the M-L direction challenging the individuals’ ability to control the COPv,M-L and whole-body balance. Following ground contact, the COPv,M-L was initially large and then decayed as balance became more stable. The prolonged time for COPv,M-L to achieve a final steady-state level in individuals post-stroke reflects difficulties in balance control. For able-bodied individuals, the hip loading/unloading mechanism and control of ankle joint motion are the primary mechanisms for COP movement control (29). After stroke, deficits in hip (14,63,64) and ankle (65) frontal plane movement control have been observed. This is consistent with our findings that hip abduction angular displacement and velocity were reduced and COP medial–lateral stabilization was delayed in participants with stroke. Thus, improving hip joint abduction/adduction, trunk, and ankle in/eversion control is likely important for improving COP control after a stroke. Findings from this research showed that in addition to abnormalities during vertical loading impact, difficulties in M-L balance control in individuals post-stroke also limit their weight transferability. These observations suggest that interventions aimed at improving weight transfer function in individuals post-stroke should consider both weight bearing and balance components during training.
The CMSAfoot was associated with COPv,A-P stabilization time, likely because the majority of CMSAfoot assessment involved ankle dorsiflexion/plantarflexion movements and inversion/eversion was assessed in higher stages. Thus, motor recovery of the ankle is important for COP stabilization ability. In addition, CMSAleg predicted paretic limb ST score. During paretic ST, paretic ankle and knee motion are key elements to move the paretic limb in and out of synergistic movements that were also assessed during the CMSAleg. Thus, lower extremity joint range of motion and the ability to move in and out synergistic patterns likely affected stepping performance. However, CMSA foot and leg subscales and COPv measurements did not predict non-paretic ST score. During non-paretic ST, the paretic limb served as the stance limb. Unlike the CMSA and the induced weight transfer assessment, the flexion-extension coordination of the paretic stance limb has less influence on non-paretic ST scores. Rather, participants with stroke appeared to constantly extend the paretic limb during non-paretic ST. Thus, the induced weight transfer assessment and CMSAleg better reflected the ability to coordinate flexion/extension movements rather than constant extension synergy alone. During the FSST, because multiple step directions were required, timely control of COM and COP movement in both A-P and M-L directions is essential for sustaining balance stability. Participants with stroke who required longer COPv,max stabilization time during the imposed weight transfer assessment needed more time to complete FSST. These results confirmed that lower extremity joint coordination and COPv stabilization in response to loading are key factors of functional weight transfer performance in individuals post-stroke. Given the relationship between the ST and FSST and fall risk (66), the imposed weight transfer assessment approach appeared to be useful in revealing possible mechanisms underlying deficits in balance and mobility following stroke.
Among the limitations of the present study was that the perturbation was designed to force vertical loading impact and challenge M-L balance control, however balance control in the A-P direction was not directly targeted. This may in part contribute to the COPv,A-P stabilization time not being different in participants with stroke compared to controls. A more comprehensive setup to examine A-P, as well as M-L balance control, could be to provide the perturbation during a diagonal stance configuration as opposed to parallel foot placement. The diagonal orientation may also simulate the weight acceptance phase of gait. Another limitation of the present study is that joint torque/power and muscle activation patterns were not investigated. Thus, our results are consistent with but do not provide evidence to directly support abnormalities in neuromuscular control and intralimb coordination. Information regarding the effects of stroke on joint torque production during induced weight transfer is important to reveal the mechanism underlying abnormal joint reactions during weight bearing. Moreover, direct measurements of joint range of motion and muscle tone could provide important insight in addition to CMSA scores. In addition, because this study aimed to study the limb loading responses during individual’s natural stance, foot position was not standardized. Differences in initial stance width and shoe characteristics may influence the results. Finally, a limited number of participants with right hemiparesis and female participants with stroke were recruited for this study. Thus, further testing of a broader population of individuals post-stroke may enhance the generalizability of the results to these populations.