Is freezing of gait in Parkinson's disease a result of multiple gait impairments? Implications for treatment

Abstract

Several gait impairments have been associated with freezing of gait (FOG) in patients with Parkinson's disease (PD). These include deteriorations in rhythm control, gait symmetry, bilateral coordination of gait, dynamic postural control and step scaling. We suggest that these seemingly independent gait features may have mutual interactions which, during certain circumstances, jointly drive the predisposed locomotion system into a FOG episode. This new theoretical framework is illustrated by the evaluation of the potential relationships between the so-called "sequence effect", that is, impairments in step scaling, and gait asymmetry just prior to FOG. We further discuss what factors influence gait control to maintain functional gait. "Triggers", for example, such as attention shifts or trajectory transitions, may precede FOG. We propose distinct categories of interventions and describe examples of existing work that support this idea: (a) interventions which aim to maintain a good level of locomotion control especially with respect to aspects related to FOG; (b) those that aim at avoiding FOG "triggers"; and (c) those that merely aim to escape from FOG once it occurs. The proposed theoretical framework sets the stage for testable hypotheses regarding the mechanisms that lead to FOG and may also lead to new treatment ideas.

Figure 1

Freezing of gait and gait features deterioration. (a) Quality of performance of gait features associated with FOG (thin lines in top 5 traces) may vary over time (hypothetical data). Similarly the level of interaction between these gait features may vary with time and in response to different circumstances or provocations (see text). BCG—Bilateral coordination of gait. (b) The combination of the performances of the individual gait features dictates whether FOG will occur or whether functional walking will be maintained. If the overall performance deteriorates below a certain threshold (horizontal line), then gait freezes (FOG zone). Deterioration in the overall gait performance can be an expression of malfunction of single gait feature associated with FOG (see text). In some cases, the deterioration of one gait feature can cause the deterioration of one or more gait features as portrayed in (a). FOG—Freezing of gait, a.u.—arbitrary units

Figure 2

Relationship between reduced step length and asymmetry in gait. (a) Reconstruction of data presented in Figure 2 of Chee et al. [7]. The data is taken from reduced step length condition from one PD + FOG patient. (b) Similar reconstruction was performed to all 6 traces presented in Chee et al. In this panel, the mean step length value of one leg (white bar) is plotted on top of the mean step length value of the other leg (grey bar), for one reduced step length trial of PD + FOG (based on the data from (a)), a PD patient who did not experience FOG, and a control subject (based on similar reconstruction of the original traces denoted in the original figure by “b 25%01” and “c25%01,” resp.). The asymmetry coefficient for these single gait trials is depicted above. GA values indicated in the text are the means obtained from two traces from each subject. GA—Gait asymmetry as expressed by step length differences between the left and right legs. (c) Average Step Length in the (i+1)th stride as a function of step length asymmetry calculated for the preceding stride (ith). Based on data from (a).

Figure 3

Intervening to improve overall gait performance and to reduce the FOG burden. (a) Improving gait performance in general, for example, by maintaining a sustained effective therapeutic effect on multiple gait features associated with FOG (recall Figure 1(a)) is a target for therapy that will likely reduce the FOG burden (see text). The black arrows reflect two instances where FOG might normally occur when the patient is OFF anti-parkinsonian medications. This might represent some diversion or divided attention that increase the likelihood of FOG. In the ON medication condition, when the overall performance is further away from the FOG threshold (horizontal line), attention still has a negative effect, but it is no longer sufficient to cause FOG. In general, one way of reducing the likelihood of FOG is to move the overall gait performance further away from this threshold. (b) Online intervention may reduce the duration of FOG episodes (see text). Key: Gait performance OFF—gait during the “off” medication periods. Gait performance ON—gait during the “on” medication periods.