Neuromechanical Assessment of Activated vs. Resting Leg Rigidity Using the Pendulum Test Is Associated With a Fall History in People With Parkinson's Disease

Abstract

Leg rigidity is associated with frequent falls in people with Parkinson's disease (PD), suggesting a potential role in functional balance and gait impairments. Changes in the neural state due to secondary tasks, e.g., activation maneuvers, can exacerbate (or "activate") rigidity, possibly increasing the risk of falls. However, the subjective interpretation and coarse classification of the standard clinical rigidity scale has prohibited the systematic, objective assessment of resting and activated leg rigidity. The pendulum test is an objective diagnostic method that we hypothesized would be sensitive enough to characterize resting and activated leg rigidity. We recorded kinematic data and electromyographic signals from rectus femoris and biceps femoris during the pendulum test in 15 individuals with PD, spanning a range of leg rigidity severity. From the recorded data of leg swing kinematics, we measured biomechanical outcomes including first swing excursion, first extension peak, number and duration of the oscillations, resting angle, relaxation index, maximum and minimum angular velocity. We examined associations between biomechanical outcomes and clinical leg rigidity score. We evaluated the effect of increasing rigidity through activation maneuvers on biomechanical outcomes. Finally, we assessed whether either biomechanical outcomes or changes in outcomes with activation were associated with a fall history. Our results suggest that the biomechanical assessment of the pendulum test can objectively quantify parkinsonian leg rigidity. We found that the presence of high rigidity during clinical exam significantly impacted biomechanical outcomes, i.e., first extension peak, number of oscillations, relaxation index, and maximum angular velocity. No differences in the effect of activation maneuvers between groups with clinically assessed low rigidity were observed, suggesting that activated rigidity may be independent of resting rigidity and should be scored as independent variables. Moreover, we found that fall history was more common among people whose rigidity was increased with a secondary task, as measured by biomechanical outcomes. We conclude that different mechanisms contributing to resting and activated rigidity may play an important yet unexplored functional role in balance impairments. The pendulum test may contribute to a better understanding of fundamental mechanisms underlying motor symptoms in PD, evaluating the efficacy of treatments, and predicting the risk of falls.

Keywords: EMG; activation maneuver; biomechanics; dual-task; hyper-resistance; hyperreflexia; kinematics; neural control.

Figure 1

Experimental setup and outcomes of the pendulum test. The example refers to the activated condition in which the participant performs finger tapping. The pendulum test was performed with the subject sitting on a treatment table with the trunk inclined approximated 60° from the horizontal to provide a comfortable starting position (A). The swinging leg behaves as a damped pendulum, oscillating several times before coming to rest. First swing excursion (FSE), number (N) and duration (d) of the oscillations, first extension peak (FEP), resting angle (θ_rest), maximum (V_max), and minimum (V_min) angular velocity were assessed from kinematic data. The middle panels show the typical “whirlpool” pattern of angular velocity against angle data. EMG activity of rectus femoris (RF) and biceps femoris (BF) were also recorded in a subset of participants (bottom panel; B).

Figure 2

Example of successful and excluded trials. The pattern of the knee angle during the pendulum test follows an exponential decrease of the peaks, while the phase plot of angular velocity against angular displacement follows a uniform “whirlpool” shape (A). The voluntary input of the participant disrupts the uniform shape of the whirlpool and causes increased variations in limb excursion peak (B). We excluded the trials in which the decrement from the i-th peak to i-th+1 is not greater than the following one.

Figure 3

Example of pendulum test kinematic traces and EMGs in four PD individuals with increasing levels of lower leg rigidity (as measured by following the UPDRS guidelines). Slight rigidity (A). Mild to moderate rigidity (B). Marked rigidity (C). Severe rigidity (D). No EMG was recorded in PD01 and PD04.

Figure 4

Kinematic outcomes of the pendulum test in the baseline condition. First swing excursion (FSE; A), first extension peak (FPE; B), number (N; C) and duration (d; D) of the oscillations, resting angle (θ_rest; E), relaxation index (RI; F), maximum (V_max; G) and minimum (V_max; H) angular velocity. Subjects were grouped based on the rigidity score of the recorded leg: subjects with leg rigidity score from 1 to 2 (low rigidity, n = 8) and subjects with leg rigidity score from 3 to 4 (high rigidity, n = 5). Gray areas correspond to mean ± SD of biomechanical outcomes for healthy subjects estimated from Stillman and McMeeken (1995). Asterisks denote significant values (p < 0.05).

Figure 5

Individual specific changes in the pattern of leg movement and EMG activity among PD subjects while performing an activation maneuver (AM). In subject PD06 we found no kinematic changes with an activation maneuver (A). In subject PD14 we found a decrease in the first extension peak and of the number and duration of the oscillations during AM (B). In subject PD15 we found a decrease in the first swing excursion and of the number and duration of the oscillations during AM (C). In the subject with severe rigidity (PD04), we found a decrease in the angular velocity of the leg during AM. No EMG recorded in PD04 (D).

Figure 6

Variation of kinematic outcomes of the pendulum test during an activation maneuver. First swing excursion (FSE; A), first extension peak (FPE; B), number (N; C) and duration (d; D) of the oscillations, resting angle (θ_rest; E), relaxation index (RI; F), maximum (V_max; G) and minimum (V_min; H) angular velocity. Each point represents the difference between the mean values of each outcome for one participant while performing an activation maneuver vs. the resting condition. Subjects were grouped based on the rigidity score of the recorded leg: subjects with leg rigidity score from 0 to 2 (low rigidity, n = 7) and subjects with leg rigidity score from 3 to 4 (high rigidity, n = 5). Asterisks denote significant values (p < 0.05).

Figure 7

Variation of kinematic outcomes of the pendulum test during an activation maneuver in non-fallers (n = 7) and fallers (n = 5). First swing excursion (FSE; A), first extension peak (FPE; B), number (N; C) and duration (d; D) of the oscillations, resting angle (θ_rest; E), relaxation index (RI; F), maximum (V_max; G) and minimum (V_min; H) angular velocity. Each point represents the difference between the mean values of each outcome for a participant while performing an activation maneuver vs. during the baseline condition. Asterisks denote significant values (p < 0.05).