1.

Informative title

Physical therapy for freezing of gait and gait impairments in Parkinson‘s disease: a systematic
review.

2. Running title

Freezing of gait and physical therapy.

3. Full names of the authors and highest academic degree

Dionys G. Rutz (Bachelor) & Dr David H. Benninger (Privat-Docent)

4. The author's institutional affiliation

Dionys G. Rutz PD Dr. David H. Benninger

Physical Therapy, Department of Neurology Department of Neurology
Centre Hospitalier Universitaire Vaudois (CHUV) Centre Hospitalier Universitaire
Vaudois (CHUV)Rue du Bugnon 46 Rue du Bugnon 46
1011 Lausanne, Switzerland 1011 Lausanne, Switzerland
Tel +41 79 556 58 56 Tel +41 79 556 38 93 and +41 21 314 95 83
Fax +41 21 314 12 56
Email: Dionys.Rutz@chuv.ch Email: David.Benninger@chuv.ch
Correspondence to: Dionys.Rutz@chuv.ch & David.Benninger@chuv.ch

5-6. Funding source or acknowledgments

We thank Dr. Victor Candia for help and comments in the revision of the final version of this
manuscript.

Disclosure: none

Physical therapy for freezing of gait and gait impairments in Parkinson disease: a systematic
review.

Abstract
Introduction: Freezing of gait (FOG) is a major cause of falls and disability in Parkinson disease (PD).
As FOG only partially improves in response to dopaminergic medication, physical therapy is an

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through the copyediting, typesetting, pagination and proofreading process which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
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important element of its management. The aim of this systematic review is to assess the evidence
for the physical interventions for FOG and gait impairments and to establish recommendations for
clinical practice.

Method: This review follows the guidelines for systematic reviews: the Preferred Reporting Items for
Systematic Reviews and Meta-Analyses (PRISMA). Systematic search in PubMed, Embase,
Physiotherapy Evidence Databases and Cinahl for randomized controlled trials of PT interventions
for FOG in PD patients until April 2018.

Results: Twenty randomized controlled trials were reviewed. In 12 RCTs, PT for FOG was assessed,
which was the primary outcome measure in nine of these RCTs. In eight RCTs, PT for gait impairment
(not targeting specifically FOG) in PD was assessed. The following PT interventions reduce FOG with
a good category A recommendation: cueing strategies (p<0.05) (visual and auditory); treadmill
walking (p<0.05); aquatic obstacle training (p<O.01); supervised slackline training (p<0.05). These
interventions can be combined and maintain their efficacy when being applied concurrently: though
there is a lack of long-term follow-up studies. The following PT interventions show possible benefit
and need further investigations: balance and coordination training; aquatic gait training; sensory
(tactile) cues. The treadmill training, auditory and visual cues are effective also for other gait
disturbances in PD and improve gait kinematics.

Conclusion: Visual and auditory cueing and the treadmill training are effective interventions for
FOG and gait impairments in PD patients (evidence level A- according to the EFNS). Tactile cues and
other specific therapies targeting FOG are probably effective but need further studies.

Keywords: Parkinson disease, freezing of gait, physical therapy, cues, treadmill, coordination and
balance

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Introduction

Parkinson disease (PD) is defined by the cardinal features bradykinesia, rigidity and tremor. As the
disease progresses, postural instability and gait difficulties appear, which are often refractory to
conventional medical therapy and become the principal cause of disability [1].

Freezing of gait (FOG) is prevalent and a disabling phenomenon in PD. FOG occurs in up to 63% of
the patient with PD [2]. FOG is defined as brief episodes of inability to do steps or by sudden, short
stepping that typically occur when initiating gait, walking and turning [3]. The environment and
cognitive tasks may trigger FOG. The patients freeze typically when initiating gait, walking, turning,
while dual tasking, and in changing environment and circumstances such as when crossing a
doorway or a narrow space, a change of luminosity, or in unusual situations. Moments of stress or
anxiety can provoke FOG especially when one needs to move fast [4, 5]. A “trembling” of the legs,
which may result from the effort to overcome freezing, and a failure of stepping forward, characterize
FOG [3, 6]. There are three phenotypes of FOG: shuffling forward with small steps, “trembling” on the
spot and a complete blocking [4]. FOG is usually brief, and normal walking may resume within a short
delay: most FOG episodes last less than 10 seconds and only a few last more than 30 seconds [4, 7,
8]. Freezing becomes more severe with disease progression [9, 10]. The mechanisms triggering FOG
(dual task, turning, etc.) are strongly related to those causing other gait disorders and often start in
parallel or after other gait disorders [11].

FOG frequently results in falls, and a fear of falling, both resulting in a decrease of functional
independence and reduced quality of life. Social consequences go along with embarrassment and
frustration provoked by freezing in society and contributes to social stigmatism [12-14].

FOG is often refractory to dopaminergic medication, especially when the disease progresses, and
complementary non-pharmacological interventions, including physical therapy, are therefore a
cornerstone of its management [6, 9].This systematic review aims to assess the evidence for the
various physical interventions for FOG and gait disturbances in PD patients in order to establish
recommendations for clinical practice.

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Methods

This review follows the guidelines for systematic reviews: the Preferred Reporting Items for
Systematic Reviews and Meta-Analyses (PRISMA) [15].

The search equation followed the clinical question based on the PICO framework (Population /
Intervention / Comparison / Outcome) [16] and included the keywords Parkinson disease, freezing
of gait, physical therapy, cues, treadmill, coordination and balance therapy in the databases Embase,
PEDro, Cinhal and PubMed for the time period from 1996 to April 2018.

Two reviewers read the abstracts and the full-texts. We selected the studies based on a consensus
according to the following eligibility criteria: 1) randomized controlled clinical trials with
participants with Parkinson disease and freezing of gait (FOG) or other gait disturbances; 2)
including physical therapy interventions such as cueing, mental strategies, treadmill, gait and balance
exercises; 3) optional gait / FOG analysis; 4) written in English or French. We excluded studies of
participants with PD and dementia or cognitive impairment (loss of memory and executive
functions), loss of independence (dependent on help for daily activities) and gait incapacity, or
studies of concurrent advanced therapies including pumps, stereotactic interventions, and robotic
devices.

The selection process and the flow chart are on the Appendix (Figure 1 and 2).

We assessed and scored the methodological quality of the RCTs using the the Physiotherapy Evidence
Database Scale (PEDro) [17, 18]. This scale scores the validity of 10 items and ranges from 0 to a
maximum of 10 points. An additional item scores the external validity.

We classified the studies (I to IV) according to the quality criteria of the European Federation of
Neurological Societies (EFNS) [19] as adapted in a paper summarizing the opinion of over 32 experts
on the use of rTMS in the treatment of neurological disorders [19]. We determined the level of clinical
recommendation according to the criteria of the EFNS [19]. (See Appendix).

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The Tables 1 and 2 (see Appendix) summarize the details of these studies including EFNS-criteria
based weighting of the scientific value and recommendation for clinical practice. Due to
heterogeneity of the interventions and limited number of studies, meta-analysis was not performed.

We assessed the quality of evidence for each intervention by down-grading or upgrading

recommendations in accordance with the GRADE criteria [20-22]. In the GRADE system, the evidence
of the outcome of a study is categorized as high, moderate, low, or very low, based on experts'
confidence in the estimate of the effect. This assessment takes into account five factors that can
downgrade the quality level of a set of evidence: (1) limitations in the design and execution of the
studies (risk of bias in patients' selection, group allocation, blinding, selective reporting...), (2)
inconsistency (unexplained heterogeneity of results across studies), (3) indirectness (according to
differences in population definition, interventions, outcome measures or comparisons), (4)
imprecision (small sample size, wide confidence intervals), and (5) publication bias (overestimation
of the effect because positive results are most likely to be reported than negative or null findings)
[20-22]. The assessment of the evidence is in Tables 3 and 4 in Appendix.

The Tables 1 and 2 (see Appendix) summarize the details of these studies including EFNS-criteria
based weighting of the scientific value and recommendation for clinical practice. Due to
heterogeneity of the interventions and limited number of studies, meta-analysis was not performed.

Results

Out of three thousand nine hundred and eighty-eight studies found, twenty randomized controlled
trials (RCT) met the inclusion criteria for this systematic review, which have been published since
1996 (see Figure 1 in Appendix).

Quality of trials

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According to the PEDro scale [17], the methodological quality of the selected studies was moderate
(median 6.5 points, range 4 to 8; see Figure 2 in Appendix). Eighteen of the twenty trials investigated
parallel groups and two had a cross-over design.

According to the EFNS –criteria [19], one of the selected RCTs was scored as Class I, 17 as class II, and
2 as class III .

Participants

In total, 762 patients with PD participated in the 20 selected RCTs. Twelve trials investigated PD
patients with FOG and eight trials PD patients with gait disturbances other than FOG without
specifying the presence of FOG whether they also experience FOG. Related to the EFNS criteria [19],
the majority of trials (n=17) were small with 10 to 25 participants, two trials had less than 10
participants and a single trial investigated more than 25 participants. The participant allocation was
balanced with the equivalence of groups in most trials (n=13), but groups differed in seven trials.

The outcome measures

The Freezing of Gait Questionnaire (FOG-Q) [23] and the modified version, the New Freezing of Gait
Questionnaire (NFOG-Q) are the primary outcome measure in nine of the 12 therapeutic trials for
FOG.

The FOG questionnaire assesses the severity and the impact of FOG in the following six items: gait
independence in daily living, worst walking capacity, FOG frequency and duration, duration of the
start hesitation and of the turning hesitation [24, 25]. The FOG-Q correlates with the UPDRS motor
(part III) as well as ADL (UPDRS-ADL part II) scores (p < 0.01), and the Hoehn-and-Yahr PD Stage
Scale (p < 0.01) [24]. The new FOG-Q (NFOG-Q) adds 3 more items to the FOG-Q “Distinction Freezers
or no-Freezers, over the past month”; “Freezing Severity” (frequency and duration); and “Freezing
impact on daily life” (fear of falling and FOG impact on daily life) [26]. The NFOG-Q offers a more
thorough evaluation of FOG with focus on the impact of FOG on daily life which allows adjust therapy

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on the patient’s need, and has been validated by Nieuwboer and colleagues in 2009 have validated
the NFOG-Q [26].

The kinematic gait analysis in a laboratory provides objective measures for assessing gait
disturbances in PD patients and has been done in all studies, which did not specifically target FOG
(8/8 trials).

Secondary outcome measures in these RCT include the Unified Parkinson’s Disease Rating Scale, part
III (UPDRS-III); the Timed Up and Go Test (TUG); the static posturography; functional scales and
tests: Functional Independence Measure, Notttingham Extended Activities of Daily Living Index,
Functional Gait Assessment, Short Physical Performance Battery, tests of balance: Tinetti Test,
Activities-specific Balance Confidence Scale, Fall Efficacy Scale International-Questionnaire,
assessment of cognition (Mini-Mental State Examination) and psychological assessments (Beck
Depression Inventory II).

Twenty trials evaluated the immediate effects of the PT and thirteen trials also included a longer-
term follow-up evaluation for up to 6 months’ post-intervention.

Tables 1 and 2 (Appendix) provide a summary of the RCT, which we have reviewed and their level of
evidence (A-C) for the therapeutic recommendations as described in the Methods. For the summary
of the intervention effects, please see Tables 3 and 4 (Appendix).

Auditory Cues
The auditory cues were effective in overcoming self-reported freezing of gait (FOG-Q)[27-31] in 3
studies, though not in all studies. Auditory cues were effectively provided with a metronome (p<0.05)
[27, 31] and by rhythmic beats and music (p<0.05) [28-30].
[32][32][30][31][31][31][31][30][29]For one study, a home education program with rhythmic
auditory cues added to a functional walking exercises had not significant improvement on NFOG-Q
[32].The results of the last study probably can be explained by a lower monitoring of the

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physiotherapist when performing cueing at home. For one study, auditory cues also increased gait
speed considered comfortable (p=0.01) [30]. Rhythmic beats of music was effective in speeding up
gait (p<0.05) by increasing the step and stride lengths (p<0.05), and their cadence (p<0.05) [33, 34].
Based on these studies, there is a level A evidence to recommend auditory cues for treating both
freezing of gait and other gait disturbances in PD.

Visual Cues

The visual cueing improved FOG according to self-reporting freezing (FOG-Q) [29, 31]. Visual cues
consisted of stationary stripes, light and laser flashes, and lines on the floor. Lines / stripes were the
most visual cues for FOG [29, 31] and gait impairments and provided effective strategies to increase
the FOG-Q and the step length [35, 36] and velocity [35, 36] . The efficacy of visual cues could not be
confirmed in all controlled studies. Schlick and colleagues [37] did not observe gait improvement
with the projection of virtual footprints on the floor, but they found the increase of stride length to
correlate with the severity of self-reported freezing of gait (FOG-Q) suggesting that the more severely
affected benefit more. In conclusion, there is a recommendation level A evidence supporting visual
cues for treating both the freezing and other gait disturbances in PD.

Tactile cues

Tactile cues could be provided by pulsed vibratory stimulation on the wrist (applied by a wrist-band)
and improved freezing according to self-reporting freezing (FOG-Q) [31]. The vibratory cues which
were applied to the plantar surfaces of both feet increased stride length, cadence, walking speed and
distance[38]. Given these results, tactile cueing appeared effective for overcoming freezing, but these
effects cannot be distinguished from the effects of the concurrent visual or auditory cues nor of the
treadmill training and the proprioceptive stimulation (Proprioceptive Neuromuscular Facilitation,
PNF) in these trials, which precludes a clinical recommendation.

Treadmill training

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The walking on a standard treadmill improved self-reported freezing of gait (FOG-Q) [29] and
increased the comfortable gait speed [CGS]), which is defined as not requiring an effort [30]. The
walking on a treadmill also increased the stride length, cadence, walking speed, step length and
walking distance [35, 38]. The effects of training on a curved treadmill was comparable as shown by
a reduction of self-reported freezing (FOG-Q) and by an improvement of the gait parameters [39].
The speed of treadmill walking and the session duration may determine the therapeutic success. PD
patients became faster and increased their step cadence when walking at their preferred speed for a
longer time and distance rather than at their maximal speed on a short distance [40]. Fast walking
itself did not increase the stride [40], but the step cadence along with greater speed and inclination
of the treadmill [41]. A single study show that standard treadmill training with rhythmic (auditory)
cues had an impact on step and stride length and these results persist in the follow-up investigations
(p <0.05) but the standard treadmill training without cues improved the walking distance (p=0.05)
[33]. The improvement in walking on the treadmill reduced freezing in daily life and resulted in a
better functional capacity. Based on these studies, there is Level A evidence for recommending
physiotherapy on a treadmill for freezing and other gait disturbances in PD.

Other therapeutic trials for FOG

There are a number of controlled trials of various other therapies for freezing. Allen et al. [42]
combined the cueing with balance training and muscle strengthening, which improved self-reported
freezing of gait (FOG-Q). El-Tamawy et al. [38] applied a rehabilitation technique known as PNF
(Proprioceptive Neuromuscular Facilitation) which consisted of practicing (3 dimensional) large
movements. The PNF technique intended to reinforce daily life movements, which could be
transferred to walking and any other activity of daily life and may reduce freezing. They combined
the PNF with physical therapy on a treadmill and tactile cueing by vibratory stimuli. They reported
improvement of gait with a significant increase in stride length, cadence, walking speed and distance.
In a similar approach, Sage and colleagues [43] applied body coordination exercises and use elastic
bands. They found significant clinical improvement in the “Posture and Gait” Test and in the motor
UPDRS- score, but no changes in the gait kinematics. They also applied exercises for better
coordination of the lower limbs, which lengthen the steps [43].

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Aquatic therapy, which refers generally to physiotherapy in a pool and includes various
interventional protocols may offer another promising approach [44, 45]. In a recent study, a
conventional physiotherapy protocol with exercises of trunk mobility, postural stability, climbing
stairs, stretching and flexibility exercises in a pool, was compared with a therapy targeting
specifically at FOG which include walking an obstacle course, a slalom line and through a narrow
passage. Both protocols appear effective in reducing FOG (FOG-Q), there is Level B of evidence for
recommending this intervention [44]. Another aquatic training protocol [45], which includes walking
at different speeds and in different directions, improved the motor UPDRS score, but had no impact
on self-reported freezing (FOG-Q) or on gait kinematics.

Another innovative approach [46] is balance and coordination training on a slackline, which is a
polyester band tensioned between two anchor points. Simply standing and walking on the slackline
alone requires good balance even in healthy young subjects, which was the aim in this trial for
patients experiencing FOG in an early stage. This training resulted in a significant reduction of
freezing according to their self-reporting freezing (FOG-Q), and improved their balance as shown by
the stabilization of the center of pressure on a baropodometry platform. There is Level B of evidence
for recommending this intervention.

Discussion

This present review of RCTs critically evaluates the evidence for physical therapy (PT) in treating the
freezing of gait (FOG) in patients with Parkinson’s disease (PD). We extended this review to
therapeutic trials for disorders of gait beyond FOG in PD, which may share a common
pathophysiology and therapeutic approaches.

We reviewed twelve RCTs of PT for freezing and eight RCTs for continuous gait impairments in PD.
In summary, the following interventions reduce FOG and improve gait in PD: treadmill walking;
cueing strategies: visual, auditory and tactile cues; balance and coordination training; and aquatic
therapy. These studies all suggest therapeutic efficacy for FOG and other gait difficulties both in their
own evaluation and measurable in gait kinematics. These results also suggest a complementary
efficacy in combining the various interventions.

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The evidence supports cueing in the different modalities to be effective also in increasing speed, step
cadence and step length. The auditory cues such as rhythmic beats of music or given by a metronome
regularize gait, increase cadence, speed and improve other gait parameters, and reduce the freezing
according to self-reporting (N- FOG-Q/FOG-Q). Also as expected, visual cues have proven their
efficacy in reducing FOG and in improving the gait kinematics mostly the stride length. There is a
large variety of visual cues, the most common being lines on the floor. Though long-term follow-up
studies lack, in our experience, auditory and visual cues remain effective for as long as being applied.
The current studies suggest an efficacy of tactile cues in improving FOG, but more controlled
investigations need to validate this treatment approach.

Wearable devices that provide auditory, tactile and visual cues offer another approach. A laser-light
source on a cane or a walker reduces FOG in daily life (FOG-Q) [47]. In a recent study, Ferraye and
colleagues (2016) [48] introduce self-developed laser-shoes, which effectively reduces freezing in
daily life. So far, there is not yet a RCT of laser-light cues for the treatment of freezing of gait.

The efficacy of attentional strategies can be experienced in daily life. This is the case when climbing
stairs, which requires attention on each single step and could well explain why patients tend not to
freeze on stairs. Thus, patients can reduce the risk of FOG when they focus the attention on walking
and while turning their head in the same direction [49] . This strategy of focusing the attention on
each single step improves the gait by increasing the step length and the speed [50]. These mental
strategies appear effective in clinical practice for FOG, though for lack of controlled studies, the
scientific evidence remains formally limited.

Specific therapies such as coordination and balance exercises appear also effective for reducing FOG.
The reason could be that by improving postural stability and balance, patients may better focus their
attention on gait. Again, the lack of controlled studies precludes evidence-based recommendations
for coordination and balance exercises to prevent FOG. Compared to PD patients without freezing,
freezers appear impaired in their gait coordination especially when challenged with a dual task such
as talking while walking or in situations, which demand a certain degree of gait coordination such as
when passing a doorway [51, 52]. Freezers often loose the fluidity in the bipedal coordination of

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walking and, thereby, become slower and walking shorter distances. The freezing tends to appear
when steps become shorter [53] and when turning, which is a good way of testing FOG in clinical
practice. The disease progression of PD comes along with an increase in postural instability and more
so in freezers [54]. Thus, exercises of coordination and balance can be helpful and may increase the
clinical efficacy of PT and facilitate cueing.

There is, thus, good evidence to support the efficacy of physiotherapy on a treadmill for reducing
freezing and improving gait in PD patients. The treadmill provides a rhythmical cue by its proper
steady movement, which could be the mechanism underlying its efficacy. This could be mediated by
the central pattern generators (CPG) [55], neuronal networks in the spinal cord, which generate the
rhythmical activation of extensor and flexor muscles during the swing and stance phases of gait and,
thereby, contribute to the locomotion. The rhythmicity of walking on the treadmill provides a
constant proprioceptive feedback from the Golgi organs in the tendons, the muscles spindles and the
cutaneous afferents on the feet, which presumably activates and maintains a normal functioning of
the CPGs [56], and this may improve the gait pattern. This could provide the rationale for physical
therapy on the treadmill. Regarding the question of the optimal speed of treadmill walking, most
studies suggest the best efficacy in improving speed, cadence and stride length when the patients
walk their comfortable pace, which corresponds also to our experience. Along with the clinical
improvement, PD patients may increase the speed considered comfortable.

The pathophysiology of freezing in PD remains largely unknown as does the mechanism how cues
contribute to overcoming freezing of gait. The current knowledge from lesional, neurophysiological
and imaging studies suggests a dysfunction within a wider network of cortical and subcortical nuclei
and their circuits on multiple levels, which encompass the frontal cortex, the basal ganglia, the
mesencephalic locomotor region and the ponto-medullary reticular formation [3]. This network
defines a presumed “top-down” control in locomotion, which is active in all stages of the gait cycle,
during gait initiation, turning, stopping, when avoiding obstacles, and also when adapting locomotion
to a changing environment. The freezing may arise from a dysfunction of both the basal ganglia which
mediate automated movements and of the cortical control of the supra-spinal locomotor generators

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in the brainstem [3]. Support comes from functional imaging, which shows an increase of cortical
activity presumably to compensate for basal ganglia dysfunction while walking [57, 58].

There is no simple explanation of the mechanism how cueing works. External cues could enhance the
cortical control of gait by focusing the attention on each single step. External cues helps walkers filter
out conflicting information and prioritize stimuli that make walking easier. [59] This shift from
automated movements to voluntary control would “bypass” the motor cortex-basal ganglia circuit
supposed to mediate the automaticity in walking and other movements. This could be the case when
transitioning from walking to climbing the stairs. The modality of the cues could have a different
effect on the motor control of gait. The visual cues could facilitate the gait initiation and enhance the
step size, which improves the gait pattern [60-62]. The auditory cues provide an external rhythm to
compensate for a presumed dysfunctional internal pace-setter and could, thereby, facilitate gait
timing and coordination. [62-64].

The emergence of freezing is closely associated with the cognitive decline in particular of the
executive functions [65-68]. Structural neuroimaging points to brain volume loss in the frontal,
dorsolateral prefrontal and parietal cortex in patients with FOG correlating with impairment in
executive functions [69]. In comparison to non-freezers, freezers appear more susceptible to
interference by cognitive tasks during walking, which may indicate an involvement of the same
neuronal networks during dual tasking [70]. This greater interference could also result from the
additional cognitive challenge freezers face as they presumably attempt to compensate for basal
ganglia dysfunction during gait. The difficulty of this review is to exclude RCTs with patients with
cognitive disorders because of this association between FOG and loss of cognitive functions. Indeed,
adherence to physical interventions aimed at reducing FOG requires a minimum integration and
memorization of instructions for motor learning. For this reason, we decided to exclude studies of
patients with a cognitive ability not allowing the learning of motor and compensatory strategies of a
FOG.

However, the kinematic analysis of FOG remains a challenge and a focus of ongoing research. This
may be a reason why four out of the eight trials, which targeted FOG did not include a kinematic

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analysis. A reduction of stride and step length [3, 71], a decreased range of the hip, knee and ankle
joints and the occurrence of high-frequency, alternating, trembling-like leg movements (3-8 Hertz)
[72, 73] and postural instability [74] have all been recorded immediately preceding and during FOG
and could be potential markers of FOG. Compared to non-freezers, the freezers experience more
postural instability in both medio-lateral and antero-posterior direction and the velocity of the
postural adjustment is reduced [74].There are yet no objective kinematic measures or validated
algorithm to detect FOG episodes in real life with wearable sensors outside of the gait laboratory.

Clinical assessment of normal and impaired gait includes besides the clinical exam, timed testing and
scores, and the gait kinematics can be assessed in the laboratory (as in 9 of the 16 reviewed RCT) and
with wearable sensors in daily life. The challenge is the episodic nature of freezing and to simulate
situations in the gait laboratory, which trigger freezing while the laboratory set-up may have patients
focus on their gait. The timed tests including the “Timed Up and Go test”, the “Dynamic Gait Index”,
the “10-Meters Walk”, the “Functional Gait Assessment” or the “Tinetti test” provide an objective
measure of speed and performance, but do not differentiate or qualify the particular gait and postural
difficulties. These tests may trigger FOG, but provide no qualitative kinematic assessment of the
freezing episodes. Wearable sensors offer a long-term monitoring during activities of daily life,
thereby, this could offer better chances to record episodes of freezing [75]. There are a number of
trials with wearable sensors, but an objective assessment to detect freezing in real life needs yet to
be validated in larger studies.

Clinical recommendations and Conclusion

Based on EFNS criteria of level of evidence, we conclude that visual and auditory cueing and treadmill
training are effective with an evidence level A for freezing and other gait disturbances and aquatic
therapy probably effective (level B) for reducing freezing. We recommend therefore the visual and
auditory cueing (auditory and visual) and treadmill therapy for FOG and other gait disturbances in
PD patients. Tactile cues and other specific therapies appear probably effective. They need further
studies to conclude for a level of evidence.

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Nevertheless, the assertion that the studies being reviewed meet EFNS level A designation should be
interpreted cautiously. We acknowledge that simply evaluating the quality of evidence in the
manuscripts might not suffice. More solid conclusions and clinical recommendations would require
a meta-analysis and subsequent analysis of effect size, confidence interval and p-values of the
selected studies. Meta-analyses are indeed considered to be at the highest hierarchical level of
statistical procedures to meaningfully summarize evidence presented in, for instance, systematic
reviews [76]: without meta-analysis, the significance of treatment effect size, comparison of p-values
in all studies and confidence intervals cannot be accurately ascertained. Nevertheless, meta-analyses
are not free of problems, and these problems become evident when, for instance, different designs
are mixed or samples are heterogeneous, just to name a few. Performing meta-analyses under these
conditions does not allow to meaningful summaries [77]. Consequently, and as pointed by others,
sometimes it is not possible to include metanalyses in a systematic review [78]. As we have
mentioned 1) the number of published evidences is still low 2) the interventions are heterogeneous
3) the number of subjects was both variable and low (10-25 subjects). Thus, running metanalyses on
these data would entail the unavoidable danger of unsustainable conclusions. On the other hand, only
20 randomized controlled studies were found to meet the inclusion criteria for a systematic review
within a time frame of 22 years. We strongly believe that this fact alone justifies performing such a
review: 3968 publications corresponding to 99.5% of the data scrutinized did not achieve the
selection criteria. Therefore, even a rough estimate, as the one we present here, would appear to be
of great value to compel researchers to largely and speedily increment the number of studies with
the quality needed to perform state of the art analyses to arrive at solid conclusions and to make
possible better clinical recommendations.

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Appendix : Classification according to the quality criteria of the European Federation of

Neurological Societies (EFNS) [19]

Study is an adequately data-supported, prospective, randomized, placebo-

controlled clinical trial with masked outcome assessment in a representative
population (n>25 patients receiving active treatment). It should include (a)
randomization concealment; (b) clearly defined primary outcomes; (c) clearly
Class I
defined exclusion/inclusion; (d) adequate accounting for dropouts and
crossovers with numbers substantially low to have minimal potential for bias;
and (e) relevant baseline characteristics equivalent among treatment groups
or appropriate statistical adjustment for differences.

Study is a randomized, placebo controlled trial performed with a smaller

Class II sample size (n≥ 10, but <25) or that lacks at least one of the above-listed
criteria (a-e).

Study includes all other controlled trials, with less than 10 patients, or more
than 10 patients, but having methodological limitation in experimental design,
Class III
control procedures or objectives.

Class IV Study is uncontrolled, cases series and cases reports.

The level of clinical recommendation according to the criteria of the EFNS [19]

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 Rating (established as effective, ineffective, or harmful) requires at least one
Level A
convincing class I study or at least two consistent, convincing class II studies.

Rating (probably effective, ineffective, or harmful) requires at least one

Level B
convincing class II study or overwhelming class III evidence

Rating (possibly effective, ineffective, or harmful) requires at least two

Level C
convincing class III studies.

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Figure 1 : Selection process

Search process in Mean keywords :

Embase, PEDro, Parkinson’s disease,
Cinhal and PubMed freezing of gait,
physical therapy, cues,
(1996 to April treadmill, coordination
2018) and balance therapy

Inclusion Criteria :
Authors consensus 1) RCT with Parkinson’s disease and (FOG) or other
gait disturbances
2) physical therapy interventions
Title-abstract 3) gait / FOG analysis
selection 4) Language : English or French
(2 reviewers)
Exclusion Criteria :
1) PD with dementia or cognitive impairment
2) loss of independence and gait incapacity
Authors consensus 3) concurrent advanced therapies including pumps,
stereotactic interventions, and robotic devices.

Full-Text
selection
(2 reviewers)

Authors consensus

PEDro Quality
evaluation
(2 reviewers)

20 Studies
reviewed
(2 reviewers)

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Figure 2: Flow chart selection adapted from Moher D. et al. (2009)

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 Table 1: Randomized controlled trials with Freezing of Gait

EFNS VALUE
AUTHORS STUDY POPULATION TYPE OF THERAPY THERAPY INTENSITY OUTCOME MAIN FINDINGS
OF EVIDENCE

NFOGQ
A (n =12) Number of falls
A : Home education program with RAC 30-60 minutes
Martin et al. B (n=9)
and functional walking exercises 6x within the first 4 weeks The home education program including auditory cues (metronome) does not
(2015) H&Y II –III T0 II
1 weekly reminders for 6 reduce the frequency and severity of the FOG (ns) and the falls (ns).
[32] Freezers: 21/21 T1 (6months)
B : 6 months wait list control group months
(100%) T2 (T1 + 6
months)
A (n =11) The visual cueing during gait training combined with a standard therapy improves
B (=n11) A : combined standard therapy (ST)+ gait 40 minutes Kinematic gait gait kinematics (0.05), the FIM (0.05) and the UPDRS III (0.05).
C (n=24) training (GT)with auditory cues 5 weekly sessions for 4 analysis
weeks (ST) UPDRS III There is no difference between auditory or visual cues except for the stance and
De Icco et al.
H&Y II- IV B : standard therapy (ST)+ gait training FIM the swing of the stride that improve with visual cues only (0.05). II
(2015)
(GT)with visual cues +
[27]
Freezers : 20 minutes T0 Cueing (auditory and visual) increases the efficacy of both interventions
A : 21.2 % C : standard therapy (ST)+ gait training 5 weekly sessions for 4 T1 (4 weeks) significantly better than without cues (0.05).
B : 20.6 % (GT) without cues weeks (GT) T2 (T1 +3 months)
C : 22.1 % There is no effect on T2.
Dynamic gait
index
UPDRS III
A (n=8)
A : Rhythmic Auditory Stimulation (RAS) Tinetti RAS improves the quality of the walk for two months better than only walking
B (n=8)
used for combination of stepping and TUG (0.05).
Kadivar et al. 45-60 minutes
direction stepping FOGQ
(2011) H&Y II-IV 3 times a week III
RAS improves balance more than without RAS (0.05).
[28] 6 weeks
B : Same but without RAS, comfortable T0
Freezers: 7/16
speed T1(6 weeks) RAS decrease the FOGQ and the TUG with a follow-up effect (0.05).
(43.75%)
T2 (T1+1 week)
T3 (T1 +4 weeks)
T4 (T1 +8 weeks)
A (n=20) B FOGQ
A : treadmill training + auditory and
(n=20) UPDRS III
visual cues synchronized
Frazzitta et al. 20 minutes Kinematic gait There is a significant improvement of the FOG (0.01) and the gait parameters
(2009) H&Y III every days analysis (6MWT) (0.05) to mixed treadmill with cues compared with traditional gait rehabilitation II
B : traditional gait rehabilitation protocol
[29] 4 weeks with cues.
with visual cues and auditory cues
Frezzers : 40/40 T0
synchronized
(100%) T1 (4weeks)
H&Y : Hoehn and Yahr stage; (N)FOGQ : (new) Freezing of Gait Questionnaire; NS : No significant; n : sample; (E)TUG : (Expanded) Timed Up and Go Test ; 6MWT : 6-minutes’ walk Test; UPDRS-III : Unified Parkinson’s Disease Rating Scale Motor
Section; T : measurements time; vs : versus; CGS : Comfortable Gait speed; FGS : Fast Gait Speed; FGA : Functional Gait Assessment; PG : Posture and Gait; PD : Parkinson Disease; SPPB : Short Physical Performance Battery; FES-I : Falls Efficacy Scale-

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International-questionnaire; FIM : Functional Independence Measure; PDQ : Parkinson’s Diseases Questionnaire; NEADLI : Nottingham Extended Activities of Daily Living Index; FAS : Fall Efficacy Scale; CSI : Carer Strain Index; MMSE : Mini-Mental
State Examination; BDI-II : Beck Depression Inventory II; ABC scale : Activities-specific Balance Confidence scale; PT : physical therapy; PNF : Proprioceptive Neuromuscular Facilitation; ST : standard therapy; GT : gait training; RAC: rhythmic
auditory cue; EFNS : European Federation of Neurological Societies; FRT : Functional Reach Test.

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 PD Falls risk score
Swaymeter
The alternate step
A (n=24)
test
B (n=24) A : progressive lower limb strengthening The therapy with strengthening and balance exercises, cueing strategy and fall
Allen et al. FOGQ
and balance exercises, instruction in 40-60 minutes prevention decreases the FOG significantly (0.05).
(2010) Physical ability
H&Y NP cueing strategies, fall prevention 3 times a week II
[42] SPPB
6 months There is no specific effect of the therapy for the other outcomes expect for Sit to
FES-I
Freezers : 27/48 B : Usual care, fall prevention stand time (0.05) that is better for the group A.
PDQ-39
(56.25%)
T0
T1 (6months)
PG score
A: Gait and balance
30 minutes measures (10MWT)
The cueing training program improve for the average of both groups for PG
A (n=76) 3 times a week FOGQ
A : Home training with various gait (0.005), gait speed (0.05), step length (0.0 5), NEADLI (0.05) and FAS (0.05).
B (n=77) 3 weeks TUG
modalities program with 1 cues
Nieuwboer et then 3 weeks with no NEADLI
preferred between 3 cues proposed : The FOGQ has a significant improvement only if we take the freezers analysis for
al. H&Y II – IV training FAS
auditory (beep), visual (light flash) and the intervention effect (0.007). I
(2007) PDQ-39
somatosensory (pulsed vibration).
[31] Freezers : B: CSI
The cueing training program has a significant immediate effect (T1) for PG (0.05),
63/153 3 weeks with no training
B : 3 weeks wait list control group gait speed (0.05) and TUG (0.01) but does not show a significant effect on time at
(41.17%) then 30 minutes T0
follow-up for the average of both groups on the main outcomes.
3 times a week T1 (T0 +3 weeks)
3 weeks T2 (T0 + 6 weeks)
T 3 (T0 +12 weeks)
Physiotherapy on the treadmill improves in stride length, gait speed for both
Kinematic gait
groups (0.05).
A (n=12) analysis
A : Treadmill training (with 20% body
B (n=11) (treadmill)
support if required) in combination with The pure treadmill group improves more the stride length and gait speed (0.05)
TUG
Schlick et al. visual cues, the step length cues is 20-40 minutes than the treadmill group with cues combination.
H&Y II-IV FOGQ
(2016) enlarged continuously according to 12 training sessions 5 II
UPDRS III
[37] progress weeks There is no effect on the cadence for both groups.
Freezers :
B : Pure treadmill training (with 20% The TUG improves for the treadmill with cues (0.05).
23/23 T0
body support if required)
(100%) T1 (5 weeks)
The increases of stride length in group with treadmill with cues was positively
T2 (two months)
correlated with the FOGQ. No such correlation in group with pure treadmill.
A (n=11) CGS
B (n=11) FGS RAS improve the Comfortable Gait Speed (0.01), the 6-Minute Walk Test (0.05) and
Harro et al. 30 minutes 6MWT the Functional Gait Assessment (0.01).
A : RAS on overground walking training
(2014) H&Y I – III 3x per week FGA II
B : Speed dependent treadmill training
[30] 6 weeks There is no significant difference between both interventions even if the RAC give
Freezers : T0 better results.
7/20 T1 (3 weeks)

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 (35%) T2 (T1 +3 months)

H&Y : Hoehn and Yahr stage; (N)FOGQ : (new) Freezing of Gait Questionnaire; NS : No significant; n : sample; (E)TUG : (Expanded) Timed Up and Go Test ; 6MWT : 6-minutes’ walk Test; UPDRS-III : Unified Parkinson’s Disease Rating Scale Motor
Section; T : measurements time; vs : versus; CGS : Comfortable Gait speed; FGS : Fast Gait Speed; FGA : Functional Gait Assessment; PG : Posture and Gait; PD : Parkinson Disease; SPPB : Short Physical Performance Battery; FES-I : Falls Efficacy Scale-
International-questionnaire; FIM : Functional Independence Measure; PDQ : Parkinson’s Diseases Questionnaire; NEADLI : Nottingham Extended Activities of Daily Living Index; FAS : Fall Efficacy Scale; CSI : Carer Strain Index; MMSE : Mini-Mental
State Examination; BDI-II : Beck Depression Inventory II; ABC scale : Activities-specific Balance Confidence scale; PT : physical therapy; PNF : Proprioceptive Neuromuscular Facilitation; ST : standard therapy; GT : gait training; RAC: rhythmic
auditory cue; EFNS : European Federation of Neurological Societies; FRT : Functional Reach Test.

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 Kinematic Gait Curved treadmill training group improves the speed, the cadence and the step
A : Curved-walking training (CWT) Analysis length on curved and straight walking (<0.05).
group : walking on a circular treadmill (curved)
A (n=12)
in both directions (15minutes each) FOGQ Curved walking training group improves significantly better the cadence and the
B (n= 12)
with a increasing speed (0.05 Kinematic gait step length than the trunk exercises group (0.05).
meters/second every 5 min) as tolered analysis (straight)
Cheng et al. H&Y I-III 40 minutes
+ 10 minutes walking program in over- TUG Intervention effect are maintained in the curved walking training group for
(2017) 12 training sessions II
ground FGA kinematic analysis in follow-up (0.05).
[39] Freezers : 4-6 weeks
B : trunk exercise that UPDRS-III
17/24
incorporated upper extremity PDQ-39 Curved walking treadmill group improves in the FOGQ. No significant effect with
(71%)
movements while in a sitting position+ the trunk exercises group.
10 minutes walking program in over- T0
ground T1 (6 weeks) Other secondary outcomes improve with the curved walking treadmill group
T2 (T1+ 30 days) (TUG<0.05 / FGA<0.01 / <UPDRS <0.01 / PDQ-39 < 0.05).
A : Obstacle aquatic therapy : slalom
walking trial, obstacle circling, crossing FOGQ
A (n=23) over steps, walking back and forth in TUG
B (n=23) narrow passage + warm up and cool UPDRS- II & III
down training (stretching and flexibility FRT The obstacle aquatic therapy improves better the FOGQ (0.001) and the TUG
Zhu et al. 40 minutes
H&Y II-III exercises) BBS (0.001) than traditional aquatic therapy.
(2017) 5 sessions per week II
B: Traditional aquatic Protocol
[44] 6 weeks
Freezers : NP (Halliwick Concept) : trunk mobility T0 Both interventions have equivalent effects on gait and balance (FRT and BBS)
exercises, postural stability and going T1 (6 weeks) (0.05).
up and down stairs + warm up and cool T2 (T1 +6
down training (stretching and flexibility months)
exercises)
Center of
A (n=11) A : Supervised slackline training The supervised slackline training program doesn’t’ improve the center of pressure
Pressure
B (n=11) program : postural stability on Slackline parameters after 6 weeks.
Santos et al. FOGQ
(unstable polyester band placed 23 minutes
(2017) FAS
H&Y I-III between two anchor points) + warm up 12 sessions The supervised slackline training program improve the FOGQ (0.05) and the FAS II
[46]
and cool-down (passive stretching of 6 weeks (0.01).
T0
Freezers : NP the main muscle groups)
T1 ( T0 + 6 weeks)
B : Usually activities routine No long effect with both interventions.
T2 (T1 + 4 weeks)
Kinematic Gait
Analysis
A : 25 minutes aquatic specific gait
FOGQ
A (n=11) training (walking with different speed,
PDQ-39
Carroll et al. B (n=10) stepping over steps, changing direction) 45 minutes Aquatic therapy does not improve better the gait than usual care.
UPDRS-III
(2017) + 10minutes warm-up (cardio-vascular 2 sessions per week III
[45] H&Y I-III and stretching trainings) + 10 minutes 6 weeks Aquatic therapy improves better the UPDRS-II than usual care (0.01).
T0 – 1week
Freezers : NP cool down.
T1 + 1 week
B : usual care
(T1=T0+ 6
weeks)

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H&Y : Hoehn and Yahr stage; (N)FOGQ : (new) Freezing of Gait Questionnaire; NS : No significant; n : sample; (E)TUG : (Expanded) Timed Up and Go Test ; 6MWT : 6-minutes’ walk Test; UPDRS-III : Unified Parkinson’s Disease Rating Scale Motor Section;
T : measurements time; vs : versus; CGS : Comfortable Gait speed; FGS : Fast Gait Speed; FGA : Functional Gait Assessment; PG : Posture and Gait; PD : Parkinson Disease; SPPB : Short Physical Performance Battery; FES-I : Falls Efficacy Scale-International-
questionnaire; FIM : Functional Independence Measure; PDQ : Parkinson’s Diseases Questionnaire; NEADLI : Nottingham Extended Activities of Daily Living Index; FAS : Fall Efficacy Scale; CSI : Carer Strain Index; MMSE : Mini-Mental State Examination;
BDI-II : Beck Depression Inventory II; ABC scale : Activities-specific Balance Confidence scale; PT : physical therapy; PNF : Proprioceptive Neuromuscular Facilitation; ST : standard therapy; GT : gait training; RAC: rhythmic auditory cue; EFNS : European
Federation of Neurological Societies; FRT : Functional Reach Test.

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Table 2: Randomized controlled trials in PD patients with gait disturbances (no Freezing of Gait)

EFNS VALUE
AUTHORS STUDY POPULATION TYPE OF THERAPY THERAPY INTENSITY OUTCOME MAIN FINDINGS
OF EVIDENCE

A: walking on a flat surface, stair stepping,

A (n=15) and stop-and-go exercises to RAC with Kinematic gait
Thaut et al. B (n=11) C three different tempos 30 minutes Analysis
(n=11) Specific exercises add with rhythm improve velocity (0.05), cadence (0.05) and
(1996) B : walking on a flat surface, stair stepping, Each days II
stride length (0.05).
[34] and stop-and-go exercises without music, 3 weeks T0
H&Y II-III walking at 3 different cadences
T1 (3 weeks)
C: Daily activities

A:
51-70 minutes Kinematic gait
El-Tamawy analysis Both interventions improve the kinematic gait topics and angular excursions
A (n=15) A : PNF, vibratory stimuli during treadmill, 3 times a week
et al. Measured angular (cadence <0.001 / stride length, walking speed, distance and measured angular
B (n=15) routine PT program 8 weeks
(2012)[38] excursion excursion <0.01.) II
B : routine PT program (stretch, balance B: The somatosensory intervention shows better results than the routine
H&Y II-III training and functional exercise) 45 minutes intervention (0.01).
T0
3 times a week T1 (8 weeks)
8 weeks

Kinematic gait
analysis
ETUG
Almeida et A (n=14) B
30 seconds chair
al. (n=14) A : Treadmill walking + visual cues 30 minutes All groups improve their step length (0.05).
stands
(2012) C (n=14) B : Over ground walking + visual cues 3 times a week The group over ground and visual cues maintain their benefit on the follow-up II
UPDRS-III
[35] C : Control group 6 weeks (0.05).
H&Y NP
T0
T1 (6 weeks)
T2 (T1 + 6 weeks)

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H&Y : Hoehn and Yahr stage; (N)FOGQ : (new) Freezing of Gait Questionnaire; NS : No significant; n : sample; (E)TUG : (Expanded) Timed Up and Go Test ; 6MWT : 6-minutes’ walk Test; UPDRS-III : Unified Parkinson’s Disease Rating Scale Motor Section; T :
measurements time ; vs : versus ; CGS : Comfortable Gait speed ; FGS : Fast Gait Speed ; FGA : Functional Gait Assessment; PG : Posture and Gait; PD : Parkinson Disease; SPPB : Short Physical Performance Battery; FES-I : Falls Efficacy Scale-International-
questionnaire; PDQ: Parkinson’s Diseases Questionnaire; NEADLI : Nottingham Extended Activities of Daily Living Index; FAS : Fall Efficacy Scale; CSI : Career Strain Index; MMSE : Mini-Mental State Examination; BDI-II : Beck Depression Inventory II; ABC scale
: Activities-specific Balance Confidence scale, PT : physical therapy; PNF : Proprioceptive Neuromuscular Facilitation; ST : standard therapy; GT : gait training; RAS : rhythmic auditory cue; EFNS : European Federation of Neurological Societies.

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 The treadmill with music cue group improves for step and stride length in the
kinematic analysis (0.05) and the results are maintained in follow up (0.05).
treadmill (+/-music) or Kinematic gait
A : treadmill with music cue and Both treadmill groups have an effect on the time in the 6- MWT (0.05) but no
walking program : analysis
stretching then home walking program difference in speed.
Chaiwanichsiri A (n=10) 3 times a week 6-MWT
et al. B (n=10)
4 weeks ETUG The treadmill group without cue improves their walking distance on 6-MWT
(2011) C (n=10) B: treadmill training without music then II
(0.05).
home walking program
[33]
then walking program : T0 The treadmill group without cue improve the TUG (0.05) but in follow up all
H&Y II- III
C: home walking program six 3 times a week T1 (4 weeks) groups improves (0.05).
days/week for 8 weeks.
4 week T2 (T1 + 4 Weeks)
The intervention group with cue improve for step and stride length in follow-up
and for TUG.

Kinematic Gait The treadmill groups improve for the kinematic gait analyze at preferred gait
analysis speed, significantly better than the over ground walking group for stride length
speed (0.05).
TUG The treadmill group maintains the effect at follow-up for speed, cadence and stride
Static length (0.05).
A (n=11) posturography The treadmill group improves only for stride length for the kinematic gait analysis
Bello et al. A : Treadmill walking treatment at maximal gait speed (0.01), with the same result in follow-up (0.05).
B (n=11) 3 session per week 5 Knee extensors
(2013) strength testing II
weeks The treadmill group improves for TUG. (0.05)
[40] B : Over ground walking treatment UPDRS-III
H&Y I-III
The treadmill group increases the displacement of the center of pressure with the
cognitive task with eyes close (static posturography) (0.05).
T0
T1 (5 weeks) Both group have no improvement for The knee extensors strength testing and the
T2 (T1+ 1 month) UPDRS-III.

A:
A : 20–30 minutes of non-aerobic gait
3 times a week UPDRS–III
exercises focused on body coordination
followed by 20–30 minutes of sensory 30-34 sessions PG
A (n=18) The group with body coordination improves the UPDRS-III and the Posture and
attention exercises utilizing latex Thera- TUG gait (0.01).
Sage et al. B (n=13) bands
B: Kinematic gait
(2009) C (n=15) analysis No significant effect on the TUG test. II
3 times a week
[79] B : 30 minutes of aerobic with lower
36 sessions
H&Y NP limb dissociation The lower limb dissociation(B) improves on the step length (0.05).
T0

C: T1 (12weeks)
C normal daily life activity
12 weeks period

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H&Y : Hoehn and Yahr stage; (N)FOGQ : (new) Freezing of Gait Questionnaire; NS : No significant; n : sample; (E)TUG : (Expanded) Timed Up and Go Test ; 6MWT : 6-minutes’ walk Test; UPDRS-III : Unified Parkinson’s Disease Rating Scale Motor Section; T :
measurements time ; vs : versus ; CGS : Comfortable Gait speed ; FGS : Fast Gait Speed ; FGA : Functional Gait Assessment; PG : Posture and Gait; PD : Parkinson Disease; SPPB : Short Physical Performance Battery; FES-I : Falls Efficacy Scale-International-
questionnaire; PDQ: Parkinson’s Diseases Questionnaire; NEADLI : Nottingham Extended Activities of Daily Living Index; FAS : Fall Efficacy Scale; CSI : Career Strain Index; MMSE : Mini-Mental State Examination; BDI-II : Beck Depression Inventory II; ABC scale
: Activities-specific Balance Confidence scale, PT : physical therapy; PNF : Proprioceptive Neuromuscular Facilitation; ST : standard therapy; GT : gait training; RAS : rhythmic auditory cue; EFNS : European Federation of Neurological Societies.

A: Control groups : Routine exercises Kinematic gait

include tai chi, dance, resistance band analysis
exercises and coordination movements
A: 6-MWT
A (=14) 2x 1 supervised hour and UPDRS
B : Speed treadmill treatment :
B (=17) treadmill speed increased (+0.2km/h) 1 hour home sessions MMSE Both treadmill groups improve in walking speed (0.01) and distance (0.05).
Nadeau et al. Mixed treadmill improves better the cadence in than other groups (0.05).
C (n=14) each session as they can tolerate (when 24 weeks BDI-II
(2014) Borg < 4 and 75% of the maximum All groups have no significant results for UPDR MMSE; PDQ-20-39 and ABC scale.
PDQ-20-39 II
[41] heart rate)
H&Y I-II B and C : ABC scale Both treadmill groups show significant results only for walking speed (0.01),
3x 1 supervised hour cadence (0.05) and stride length for follow-up (0.05).
C : Mixed treadmill treatment :
sessions T0
treadmill speed (+0.2km/h) and
inclination (+1%) increased each 24 weeks T1 (3months)
session as they can tolerate (when Borg
< 4 and 75% of the maximum heart T2 (T1 + 3 months
rate) )

A : Walk each day 10 meters distance on TUG

A (n=14) a walkway stepping over the visual Kinematic gait
B (n=14) (strips) cues, usual walk for 40 minutes analysis
and stretching and positioning Joints amplitude
Sayed et al. program for 30 minutes 3 times a week during sit-to-walk The group with cues improves the TUG (0.005), the step length and step velocity
(2013) H&Y II-III II
6 weeks (0.001) and the join amplitude during sit-to-walk (0.01).
[36]
B : Walk each day 10 meters distance on T0
Freezers : a walkway without cues, usual walk for
NP 40 minutes and stretching and T1 (6 weeks)
positioning program for 30 minutes

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H&Y : Hoehn and Yahr stage; (N)FOGQ : (new) Freezing of Gait Questionnaire; NS : No significant; n : sample; (E)TUG : (Expanded) Timed Up and Go Test ; 6MWT : 6-minutes’ walk Test; UPDRS-III : Unified Parkinson’s Disease Rating Scale Motor
Section; T : measurements time ; vs : versus ; CGS : Comfortable Gait speed ; FGS : Fast Gait Speed ; FGA : Functional Gait Assessment; PG : Posture and Gait; PD : Parkinson Disease; SPPB : Short Physical Performance Battery; FES-I : Falls Efficacy Scale-
International-questionnaire; PDQ: Parkinson’s Diseases Questionnaire; NEADLI : Nottingham Extended Activities of Daily Living Index; FAS : Fall Efficacy Scale; CSI : Career Strain Index; MMSE : Mini-Mental State Examination; BDI-II : Beck Depression
Inventory II; ABC scale : Activities-specific Balance Confidence scale, PT : physical therapy; PNF : Proprioceptive Neuromuscular Facilitation; ST : standard therapy; GT : gait training; RAS : rhythmic auditory cue; EFNS : European Federation of
Neurological Societies.

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Table 3: Intervention effects and recommendations for primary outcomes PD patients with FOG - part I

Primary Authors and Recommendation

Intervention Therapy Follow-up
outcomes classification (GRADE)
Martin et al.
NFOGQ –
Metronome N/A (2015)
Falls –
II
KGA
Number of strides*
De Icco et al.
Stride length*
(2015)
Metronome Speed* All items -
Stride duration –
II
Stance –
Swing –
Kadivar et al.
DGI* T2*, T3*, T4* A
Auditory cues Beats (2011)
FOGQ* T2*, T3*, T4 – ⊕⊕⊕○
II
Frazzitta et al.
FOGQ*
Musical beats N/A (2009)
UPDRS III*
II
CGS* T2*
Harro et al.
FGS – T2*
Musical Beats (2014)
6MWT – T2*
II
FGA* T2*
Nieuwboer et al.
PG score* T2↘*, T3↘*,
Metronome (2007)
FOGQ * T2↘*, T3↘*,
I
KGA
Number of strides*
De Icco et al.
Stride length –
(2015)
Stripes Speed* All items -
Stride duration –
II
Stance *
Swing *
Frazzitta et al.
FOGQ*
Lines N/A (2009) A
Visual Cues UPDRS III *
II ⊕⊕⊕○
Nieuwboer et al.
PG score* T2↘*, T3↘*,
Light flashes (2007)
FOGQ * T2↘*, T3↘*,
I
KGA
Stride length* T2* Schlick et al.
Virtual footprints
Gait speed* T2* (2016)
projection
Cadence – T2 – II
FOGQ – T2 –
Nieuwboer et al.
PG score * T2↘*, T3↘*,
Sensory cues Vibratory (2007) N/A
FOGQ * T2↘*, T3↘*,
I
* : significant results; - : no significant effect; N/A : not available; FOGQ: Freezing of Gait Questionnaire; KGA : kinematic gait analysis;
DGI : Dynamic Gait Index; PG: Posture and Gait score; CGS : Comfortable Gait Speed; FGS : Fast Gait Speed; 6MWT : 6-minutes’ Walk
Test; FGS : Functional Gait Assessment; PD : Parkinson’s disease; CoP : Center of Pressure; FAS : Fear of Falling Scale.

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Table 3: Intervention effects and recommendations for primary outcomes PD patients with FOG
- part II

Frazzitta et al.
FOGQ*
Standard treadmill N/A (2009)
UPDRS III*
II
KGA
Stride length* T2* Schlick et al.
body weight
Gait speed* T2* (2016) A
support
Cadence – T2 – II ⊕⊕⊕○
FOG – T2 –
Treadmill CGS* T2*
Harro et al.
FGS – T2*
Standard treadmill (2014)
6MWT – T2*
II
FGA* T2*
KGA
Speed* T2* Cheng et al.
Curved-walking B
Cadence* T2* (2017)
training ⊕⊕○○
Step Length* T2* II
FOGQ* T2*
PD falls risk score Allen et al.
Cues, balance and
- N/A (2010) N/A
strengthening
FOGQ * II
Zhu et al.
Aquatic obstacle FOGQ* T2* B
(2017)
training TUG* T2* ⊕⊕○○
Other Therapies II
Carroll et al.
Aquatic gait KGA-
N/A (2017) N/A
training FOGQ-
III
Supervised CoP- T2- Santos et al.
B
slackline training FOGQ* T2- (2017)
⊕⊕○○
program FAS* T2- II

* : significant results; - : no significant effect; N/A : not available; FOGQ: Freezing of Gait Questionnaire; KGA : kinematic gait analysis; DGI :
Dynamic Gait Index; PG: Posture and Gait score; CGS : Comfortable Gait Speed; FGS : Fast Gait Speed; 6MWT : 6-minutes’ Walk Test; FGS :
Functional Gait Assessment; PD : Parkinson’s disease; CoP : Center of Pressure; FAS : Fear of Falling Scale.

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Table 4: Intervention effects and recommendations for primary outcomes PD patients with gait
disturbances (no FOG) - part I

Authors and Recommendation

Intervention Therapy Primary outcomes Follow-up
classification (GRADE)
KGA
Thaut et al.
Rhythmic music Velocity*
N/A (1996)
and beats Cadence *
II
Stride length* A
Auditory cues
KGA Chaiwanichsiri et ⊕⊕○○
Rhythmically Step length* T2 * al.
music Stride length* T2* (2011)
Cadence – T2 – II
KGA Almeida et al.
Lines Step length* T2* (2012)
Vitesse – T2 – II
TUG *
A
Visual Cues KGA
Sayed et al. ⊕○○○
Step length*
Lines N/A (2013)
Step velocity*
II
Time between seat off and
heel off –
KGA
Stride length* El-Tamawy et al.
Sensory cues Vibratory Cadence* N/A (2012) N/A
Walking speed* II
Distance *
KGA
Stride length* El-Tamawy et al.
Standard
Cadence* N/A (2012)
treadmill
Walking speed* II
Distance *
KGA Almeida et al.
Standard
Step length* T2* (2012)
treadmill
Vitesse – T2 – II
KGA Chaiwanichsiri et
Standard Step length – T2 – al.
treadmill Stride length – T2 – (2011)
Cadence – T2 – II
KGA (preferred speed)
Speed* T2*
Bello et al.
Cadence* T2*
(2013)
Standard Stride length* T2* A
Treadmill
treadmill KGA (maximal speed) ⊕⊕⊕⊕
II
Speed – T2 –
Cadence – T2 –
Stride length* T2*
KGA
Speed* T2*
Nadeau et al.
Increased speed Cadence – T2*
(2014)
treadmill Stride length* T2*
II
Single support time – T2 –
Double support time – T2 –
KGA
Increased speed Speed* T2*
Nadeau et al.
treadmill and Cadence * T2*
(2014)
increased Stride length – T2*
II
inclination Single support time – T2 –
Double support time – T2*

* : significant; - : no Significant; N/A : not available KGA : Kinematic Gait Analysis, PNF: Proprioceptive Neuromuscular Facilitation;
PG : Posture and Gait score; UPDRS : Unified Parkinson’s Disease Raking Scale.

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Table 4: Intervention effects and recommendations for primary outcomes PD patients with
gait disturbances (no FOG) - part II
Authors and Recommendation
Intervention Therapy Primary outcomes Follow-up
classification (GRADE)
KGA
Stride length* El-Tamawy et al.
PNF Cadence* N/A (2012)
Walking speed* II
Distance *
UPDRS III*
PG*
TUG –
KGA Sage et al.
Body
Step length –
coordination, N/A (2009)
Velocity –
sensory attention II
Cadence –
Other
Double support time – N/A
Therapies
Base of support –
Step length variability –
UPDRS III –
PG –
TUG –
KGA Sage et al.
Lower limb Step length *
N/A (2009)
dissociation Velocity –
Cadence – II
Double support time –
Base of support –
Step length variability –
* : significant; - : no Significant, N/A : not available; KGA : Kinematic Gait Analysis; PNF: Proprioceptive Neuromuscular Facilitation;
PG : Posture and Gait score; UPDRS : Unified Parkinson’s Disease Raking Scale.

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