Festination-like steps during forward and backward gait while playing tennis

Introduction

Freezing of gait (FOG) is a common phenomenon in persons with Parkinson's disease (PD), which typically occurs during attempts to produce forward stepping. Festination is a related episodic gait disorder during which the patient takes progressively shorter steps at an increasing frequency, ¹ and which is often a precursor of FOG episodes. The emergence of FOG signifies an important milestone in the disease course, with an enormous impact on quality of life. However, the very first appearances of festination and FOG often remain elusive during history taking, as recognition of these gait blocks by patients themselves is unreliable.^2,3

Case report

We report a now 64-year old man with PD, diagnosed at the age of 53, who had to quit tennis at the age of 59 due to falls when he was moving backwards while playing. To illustrate his problem, he produced a self-made video (Supplemental Video 1). Unexpectedly, the video demonstrated not merely retropulsion as a sign of imbalance, but two episodes of backward festination-like steps. The patient described that these backward festination-like steps led to falling when his feet were unable to follow his body movements. Detailed tests of forward and backward walking in the gait laboratory showed no abnormalities other than typical PD signs, i.e., a reduced arm swing and slower walking velocity (1.17 m/s) in relation to age-corrected norm values (1.36 ± 0.18 m/s) (Supplemental Video 2). Furthermore, no FOG was clinically observed during forward and backward normal walking by the patient. We expected based on the patient's symptoms description a festinating response to the pull test but none was observed. A common test to elicit FOG, rapid 360-degree-turning-in-place to both directions, ⁴ provoked a very brief FOG episode at the moment of directional change. The FOG-ratio (i.e., amount of FOG-related high-frequency movement divided by the amount of normal movement) during this turning task was 2.22, which is slightly raised but within the confidence limits of people without FOG (1.75 ± 1.45). ⁴ Consistently, however, the patient's backward festination-like steps was provoked when playing tennis, especially when the ball bounce was near the feet, forcing him to produce fast steps backward while preparing for a forehand or backhand return. During a tennis game, this situation occurred more typically after the service as it is more difficult for the opponent to play the ball near the feet during a rally, but festination-like steps also occurred during other circumstances requiring adaptive stepping (Supplemental Video 3). We hypothesize that the combination of having to produce adaptive steps, high spatial and temporal stress and the distraction of the tennis game elicited the festination-like steps. Amantadine 2 × 100 mg/day led to a temporary improvement, so he could resume playing tennis. Two years later, at the age of 61, troublesome festination-like steps reoccurred.

Discussion

This case illustrates five messages. First, patient videos can sometimes be invaluable in the diagnostic process when a movement disorder occurs under rare circumstances. This is particularly helpful when history taking is unreliable, as is the case for FOG and festination.

Second, festination-like steps may also present during backward gait, and this can be as troublesome and fall-provoking (if not more) as classical forward freezing-related phenomena. Backward festination-like steps are underreported, except for occasional FOG episodes in response to the pull test. ¹ Because forward progression is the most common direction of walking and included in the definitions of festination, ¹ it is possible that freezing-related abnormal stepping in the backward direction was not identified earlier. In this patient, it was striking how debilitating this abnormal backward stepping was. It is also remarkable that the video also demonstrated unambiguous festination during forward gait, without the patient realizing it, potentially because it was not causing fall events. Importantly, backward stepping occurs frequently in daily life activities, e.g., when navigating in a small kitchen or bathroom. We therefore suspect that abnormal backward stepping and freezing, with concurrent falls, may be more common than previously assumed. Our findings also illustrate that the abnormal stepping patterns, often indicated as shuffling or festination, need to be better defined and their relationship with freezing clarified.

There are similarities between our video and another short freezing on turning video. ⁵ That video reveals that there is an attempt by the patient to generate a step, as shown by the knee trembling and lifting up the heel of the right foot. However, the patient is unable to lift the forefoot from the ground to make it a step. It is true that there is forward movement because the right foot is sliding on the tile surface. Furthermore, the weight is on the left (inner turning) leg and the patient appears unable to shift the center of mass to produce ‘normal’ stepping behavior. Probably, if the patient would have been able to shift his center of mass it may have resulted either in festination-like stepping or a fall incident. This is different from the festination-like steps that we show in the current case since the patient is able to lift off the full feet from the ground and also shift the center of mass as a driver for stepping movement. However, the difference is very subtle and the phenomena of festination and FOG are closely related and may even be the same along a continuum of freezing severity. This is currently also a matter of debate among FOG experts in an international research consortium.

Third, a combination of clinically rated videos and a quantitative analysis with sensors in a gait laboratory can provide valuable details in reaching the correct diagnosis when the initial manifestations of festination, shuffling steps and FOG are still relatively mild and largely undetected by patients themselves. Yet, laboratory testing is neither infallible because many patients perform paradoxically well when under close clinical scrutiny. Indeed, no difficulties were observed in our patient during regular assessments. Thus, this case illustrates that even in quantitative analysis, testing conditions are best tuned towards the patient's reported difficulties.

Fourth, although exercise is important and should be recommended to all PD patients, sports can also be dangerous. For patients experiencing backward falls due to FOG or festination, it is important to recommend alternative forms of exercise that do not produce such hazardous situations, e.g., cycling on a regular or stationary bicycle. ³ Also, treadmill training offers a controlled mode of exercise that ameliorates both forward and backward walking. ⁶ Our patient took up a less physically demanding activity, namely petanque, and has had no falling incidents since. Badminton could have been an alternative and safer suggestion for this patient as it is very similar to tennis, but without the festination inducing circumstances of the ball bounce near the feet. The difference is that the shuttlecock by default moves in a more arc type of trajectory through the air, offering the player more time to position himself and as such taking away the time-pressure component. It was explicitly mentioned by the patient that it was in these circumstances that the festination-like steps were elicited and also during the tennis assessment it was observed, yet not visible on video, that when the tennis ball made a higher curved trajectory, the patient could prepare himself better with less of a time component. It may be that due to the disease progression, the patient experienced more difficulties to see and predict the ball trajectory, decreasing the available time to move and putting stress to the system and causing the festination-like steps. Speculatively, the same festination-like phenomenon would be expected in badminton if the shuttlecock was played in a more competitive and straight-lined trajectory towards his body. Thus, exercise prescription requires expertise about the activities, the challenges a patient faces and their preferences.

Fifth, amantadine can bring temporary relief in patients with festination and/or freezing-associated manifestations of gait. This beneficial effect may well have resulted from enhanced dopaminergic stimulation, and it is quite possible that higher doses of levodopa would have achieved the same effect. Combining both drugs can be considered in patients with debilitating freezing.

In conclusion, rather than a first sign of impaired balance, falling backwards during tennis, appeared to be ‘a red flag’ for gait impairment, heralding conversion to FOG.

No festination-like steps were observed during the pull test. Earlier studies suggest the pull test can be normal in less severe FOG Questionnaire scores. ⁷ As such these subtle signs whereby a patient develops freezing-related abnormal stepping only under spatial and/or temporal stress provide us with a window into the early progression of PD into a full-blown FOG phenotype.