Freezing of gait in Parkinson’s disease – a literature review on clinical aspects and physiotherapy management
Manzur Kader,Reg. Physiotherapist, MSc, MPH, PhD researcher, Lund University, Sweden
Kristina Rosqvist,Reg.Physiotherapist, MSc, PhD researcher, Lund University, Sweden
Parkinson’s disease (PD) is a chronic progressive neurodegenerative disease that results in a gradual progression of functional loss and disability due to motor symptoms (i.e. tremor, rigidity, bradykinesia and postural instability) as well as non-motor symptoms (such as fatigue, cognitive dysfunction) (1, 2).
A disturbed gait is common in PD, and about 75% of people with a PD duration of more than five years have gait and balance problems (3). People with PD often walk with reduced gait speed, decreased stride length, stooped posture, reduced arm swing (4, 5). They are particularly unstable when perturbed backwards due to impaired postural reflexes (6), which is recommended to be assessed clinically by using an unexpected shoulder pull test (7). The average step rate or cadence is generally intact, but the stepping frequency may be increase to compensate for a reduced stride length (8). Gait and balance problems are also associated with non-motor symptoms (e.g. cognitive impairments) of PD and are aggravated by dual-task activities (9). Over half of patients in the advanced stages of PD experience freezing of gait (FOG), is often described by the patients as if their feet are “glued to the floor” (10, 11). FOG is a unique and disabling clinical problem, defined as “brief, episodic absence or marked reduction of forward progression of the feet despite the intention to walk” (12, 13). It typically occurs when initiating gait (start hesitation), on turning or just before reaching a target (destination hesitation or “target freezing”) (10, 11). Pathophysiological mechanisms underlying symptom of FOG is not understood and reliable and effective treatment options are limited (4). There is limited evidence of contributing factors for and the impact of FOG on function and disability as well as physiotherapy management in people with PD. Accordingly, the aim of the assignment is to perform a literature review on different aspects of FOG phenomena in people with PD, including the physiotherapy management.
- What are the different clinical features of FOG?
- What are the factors associated with or predictors of FOG?
- What are the consequences/impacts of FOG?
- What are the physiotherapy treatments available to manage FOG?
References for this Review were identified through searches of PubMed, Cinahl, Cochrane library, and Google scholar. Additionally, information was collected from other sources (such as homepages) on the internet. Specific search strategies included combinations of the following key words: ‘gait difficulty’, ‘freezing of gait’, “freezing” ‘Parkinson’s disease’, ‘treatment’ and ‘physiotherapy’. Additional studies were retrieved from manually searching the reference lists of previous reviews in this area. The inclusion criteria were the studies describing FOG in patients/persons with Parkinson disease. The section of articles to be included in this literature review was based on the quality of each study, the relevance to the topics studied and only articles published in peer-reviewed English-language journals. Excluding criteria were being reports published only in abstract form, editorials, unpublished reports, dissertations and study protocols. Studies describing freezing like phenomena for example “festinating gait” (rapid, small steps, in order to keep the center of gravity in between the feet) and studies of freezing of gait in patients with other parkinsonisms and parkinson’s plus syndromes such as multiple system atrophy and progressive supranuclear palsy were also excluded. Moreover, freezing phenomenon appeared not in locomotion or in gait but other parts of the body such as in hand movements were excluded.
Clinical features FOG
On the basis of clinical findings, three different subtypes of FOG have been suggested (14):
- Trembling in place: alternating tremor of the legs (knees)- at a frequency of 3–8 Hz; the best-known clinical feature with PD when a patient suddenly, for no apparent reason, becomes unable to start walking.
- Shuffling forward: very short, shuffling steps that are millimeters to a couple of centimeters in length.
- Complete akinesia: no movement of the limbs or trunk, but a complete absence of movement is uncommon.
The patient has a subjective feeling of the feet are “glued to the floor” or the foot or toe does not leave the ground. This description is suggested to use when asking people about the phenomenon. FOG phenomena usually last for a couple of seconds, but can occasionally exceed 30 seconds, rarely, FOG might be continuous (14). FOG can be asymmetrical, affecting mainly one foot or being most commonly elicited by turning in one direction. The likelihood that FOG will occur depends on the situation. It is more easily elicited when initiating the first step (start hesitation), turning, passing through narrow passages, just before reaching destination, by stress, in crowded and confined spaces as well as in time limiting circumstances, e.g., when crossing a street. Conditions or circumstances that improve FOG episode include excitement, auditory cueing at the proper pace, conditions that distract the patient from walking or focus attention on stepping and climbing stairs (10, 11, 15).
FOG is commonly assessed by either by asking or by using a single item assessment
such as item 14 of the Unified PD Rating Scale (UPDRS) (16-18). Therefore, several measurement tools have been developed so far to asses FOG (19-24), whereas clinician/interview administered the Freezing of Gait Questionnaire (FOG-Q) (19), the New Freezing of Gait Questionnaire (NFOG-Q) (20), and the self-administered version of the FOG-Q (FOG-Qsa) (22) assess FOG from a patient’s perspective.
Factors associated with or predictors of FOG
In a variety of research studies following factors have been found to be significantly associated/correlate with or predictors of FOG:
# Increased disease severity (11, 16, 25-27)
# Long duration of levodopa treatment or a high daily dose of levodopa (16, 25, 26)
# Increased PD duration (11, 16, 26-29)
# Dual tasks or performing a secondary task while walking that require more attention and problem solving (30-32)
# Untreated patients or not treated by levodopa (L-dopa) (11, 25, 26, 29) or patients with levodopa-resistant (33)
# The use of a dopamine receptor agonist (16, 27, 34)
# The severity of urinary symptoms (27)
# Mobility device (MD)- Standard walker (35)
Consequences of FOG
FOG episodes have been demonstrated negatively impacts on following factors:
# Increased risk of falls (13, 18, 36-38)
# Cognitive decline, particularly executive dysfunction (39-41)
# ADL and activity limitations (19, 42)
# Altered gait and balance for example, festination (27, 43, 44), increased cadence, decreased stride length or step length (14, 25, 30, 45, 46)
# Depression (27, 41, 47, 48)
# Anxiety (41, 48, 49)
# Sleep disturbance (48, 50)
# Health-related quality of life HRQoL(51-55)
FoG does not correlate with the cardinal features of parkinsonism: tremor, bradykinesia, or rigidity (25, 56).
Physiotherapy treatments available to manage FOG
Rehabilitation is a possible treatment for gait disorders in PD patients (57); general physical exercise training and specific training in the treatment of FOG. Effective rehabilitation in the management of FOG commonly consists of auditory and visual cues (58).
There is a recent Cochrane systematic review on the subject of physiotherapy interventions generally and PD (59). They looked at randomized controlled trials (RCTs) of physiotherapy intervention compared to no physiotherapy intervention in patients with PD. Generally, improvement was found in most tests of gait with physiotherapy intervention. These improvements were significant for walking speed, walking endurance and freezing of gait. In the review it is concluded there is a wide range of physiotherapy interventions in treatment of PD, but no evidence was found in difference of treatment effect and there is a need for further research on this subject.
Cues can be either external (such as visual or auditory) or internal (cognitive prompting or instructions), the first category being the most commonly used approach in physiotherapy treatment of FOG (60). External cueing means that external stimuli are presented in the form of visual, auditory or tactile information aimed at triggering movements or providing some kind of support to improve movements, such as for example a using a metronome to help patients follow the rhythm. This technique can improve the quality of walking and help overcoming and preventing episodes of FOG (61). Auditory cueing is commonly used in walking treatment (62).
Auditory cues can also be the physiotherapist guiding the patient by counting out loud “1-2, 1-2” or for the patient to hear the rhythm of (marching) music, in order to facilitate walking pace and initiation of walking (60). There are even applications for smart phones that provide sounds like a metronome that the patient can use (63). Other practical tips on gait management may include emphasizing putting down the heel first, and then toe when walking. When it comes to proprioception, emphasis could be turned to feeling the “heel down” or rocking backwards/forwards or taking a step back (64).
Visual cues aim to through the patient’s vision provide help on where to put his or her foot when walking. Visual cues could consist of lines made from tape, placed on the floor, suitable for example in tight spaces. There are also technical solutions that include visual cues, such as laser beam canes (63).
It seems that auditory cues have a greater influence on improving cadence/gait speed than on stride length, while visual cues improve stride length more than cadence/gait speed. A combination of both methods did not improve gait more than one of the cues at a time in a study that investigated the different cueing techniques while the patients performed a 7 m gait test (65).
Specific cognitive training may also be an option in the treatment of FOG, with the aim to improve cognitive function where deficits are present, this method not yet being fully explored. This is further explained through suggesting that the pathophysiology behind FOG includes more than motor dysfunction, as it appears it could also involve executive dysfunction (60).
Typical occasions when FOG may occur, many of them often experienced for example in a hospital ward, are when turning corners, crossing thresholds, tight enclosed spaces (such as bathrooms), turning around in a circle (for example when coming into the patient’s room and going to sit down on a chair after having walked in the corridor for example), changes in flooring and also divided attention or distractions (63). Therefore it may be useful performing part of the physiotherapy practice in such functional environments.
Treadmill training associated with auditory and visual cues is yet another way of trying to improve gait pattern, like an external rhythmic pace-setter. This has been investigated in some studies, though more research is needed before it can be considered an evidence based method (66). In one study (57) the authors compared treadmill training to the same type of training without treadmill, where the results suggested that treadmill training might give better results than conventional training.
A European project on rehabilitation in PD, the RESCUE project (2003-05), investigated strategies for cueing with new technological device (61, 62).
PD patients from three European centers were involved in the study, where the effects of physiotherapy program on rhythmical cueing when walking was investigated. The authors concluded that cuing training has effect on gait, freezing and balance but that the effectiveness of the intervention declines after the intervention and a need for permanent cueing devices and follow-up treatment is needed (61, 62). It is therefore important that the patient integrates these different cueing techniques into his or her movement patterns and daily activities (67).
One study where cueing training combined with general physical therapy, including sessions of strength and balance training, showed good results. There was statistically significant results for the training group compared to the non-training group for the outcome measure Freezing of Gait Questionnaire (FOG-Q) (68), which is an assessment instrument for measuring FOG where the patient is asked to rate his or her current problems relating to FOG (69).
In another recent study a two-week program of exercising cueing and movement strategies was shown to be effective in reducing the severity of FOG (70).
Yet another recent (quite small) study where a six-week progressive motor-learning program through intensive cueing was performed, the effects were retained also after four weeks. In this study participants were trained in FOG-provoking situations (for example turns) and with the help of rhythmic auditory stimulation the participants were trained to walk rhythmically (71).
In conclusion, in this report we searched the literature on different aspects of FOG, including; clinical features, associated factors, consequences and finally physiotherapy treatments available to manage FOG.
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Manzur Kader, PhD researcher in Physiotherapy
Faculty of Medicine, Lund University, Sweden