Comparing Backward Walking Performance in Parkinson’s Disease with and...

[Full title: Comparing Backward Walking Performance in Parkinson’s Disease with and without Freezing of Gait—A Systematic Review]

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Citation: Milane, T.; Hansen, C.; Chardon, M.; Bianchini, E.; Vuillerme, N. Comparing Backward Walking Performance in Parkinson’s Disease with and without Freezing of Gait—A Systematic Review Int. J Environ. Res. Public Health 2023 , 20 , 953. https://doi.org/10.3390/ ijerph 20020953 Academic Editor: Fabiola Spolaor Received: 30 November 2022 Revised: 22 December 2022 Accepted: 26 December 2022 Published: 4 January 2023 Copyright: © 2023 by the authors Licensee MDPI, Basel, Switzerland This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/) International Journal of Environmental Research and Public Health Review Comparing Backward Walking Performance in Parkinson’s Disease with and without Freezing of Gait—A Systematic Review Tracy Milane 1,2 , Clint Hansen 2, * , Matthias Chardon 1 , Edoardo Bianchini 1,2,3 and Nicolas Vuillerme 1,4,5 1 AGEIS, Universit é Grenoble Alpes, 38000 Grenoble, France 2 Department of Neurology, UKSH Campus Kiel, Kiel University, Arnold-Heller-Str. 3, Haus D, 24105 Kiel, Germany 3 Department of Neuroscience, Mental Health and Sensory Organs (NESMOS), Sapienza University of Rome, 00189 Rome, Italy 4 LabCom Telecom 4 Health, Orange Labs & Universit é Grenoble Alpes, CNRS, Inria, Grenoble INP-UGA, 38000 Grenoble, France 5 Institut Universitaire de France, 75005 Paris, France * Correspondence: c.hansen@neurologie.uni-kiel.de Abstract: Introduction: Parkinson’s disease (PD) is a neurodegenerative disease characterized by motor symptoms and gait impairments. Among them, freezing of gait (FOG) is one of the most disabling manifestations. Backward walking (BW) is an activity of daily life that individuals with PD might find difficult and could cause falls. Recent studies have reported that gait impairments in PD were more pronounced in BW, particularly in people presenting FOG. However, to the best of our knowledge, no systematic review has synthetized the literature which compared BW performance in PD patients with and without FOG. Objective: The aim of this study was to evaluate the differences in BW performance between PD patients with FOG and PD patients without FOG. Methods: Two databases, PubMed and Web of Science, were systematically searched to identify studies comparing BW performance in PD patients with and without FOG. The National Institutes of Health (NIH) tool was used to assess the quality of the studies included. Results: Seven studies with 431 PD patients (179 PD with FOG and 252 PD without FOG) met the inclusion criteria and were included in this review. Among them, 5 studies reported walking speed, 3 studies step length, stride length and lower limb range of motion, 2 studies functional ambulation profile, toe clearance height, swing, and stance percent and 1 study reported the decomposition index and stepping coordination. Compared to PD patients without FOG, PD patients with FOG showed slower walking speed and reduced step length in 3 studies, shorter stride length, lower functional ambulation profile and decreased ankle range of motion in 2 studies, and smaller swing percent, higher stance percent, worse stepping coordination, greater decomposition between movements, and lower toe clearance height in one study. Conclusion: Despite the small number of included studies, the findings of this review suggested that PD patients with FOG have worse gait performance during the BW task than PD without FOG Keywords: Parkinson’s disease; freezing of gait; backward walking; gait 1. Introduction Parkinson’s disease (PD) is a progressive neurodegenerative disorder [ 1 ] characterized by motor symptoms such as slow movement, muscle stiffness, and tremor affecting the performance of motor tasks, including walking [ 2 ]. Gait impairments are rather common in PD, particularly with disease progression [ 3 ] and are associated with an altered quality of life and an increased risk of falls [ 4 ]. These include continuous alterations such as reduced step length, low gait speed, increased cadence and variability, and episodic disturbances such as freezing of gait (FOG) [ 3 ]. FOG is a debilitating symptom of PD [ 5 ], defined as a “brief, episodic absence or marked reduction of forward progression of the feet despite the intention to walk” [ 6 ]. It impairs mobility, alters quality of life, leads to falls and is Int. J. Environ. Res. Public Health 2023 , 20 , 953. https://doi.org/10.3390/ijerph 20020953 https://www.mdpi.com/journal/ijerph

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 2 of 23 most likely to occur when initiating gait, turning, walking through narrow spaces, or approaching a destination [ 6 ]. Mobility in PD could be assessed using different tasks such as forward walking, backward walking (BW), sit-to-walk, and turning [ 7 ]. Forward walking is a basic component in human locomotion and BW is a variation of it [ 8 ]. BW is also a common activity of daily living, performed, for instance, when stepping back from a sink or when a fast-moving bus passes [ 9 ]. However, BW is more difficult and demanding because of increased postural instability and absence of visual cues [ 10 ] and elderly people demonstrated reduced cadence, shorter stride length and swing phase, and increased double support time during BW [ 11 ]. Since BW is an essential element of mobility, deficits might lead to higher risk of falls. To this end, the evaluation of BW performance could be clinically useful [ 12 ] and BW has been reported to be more accurate than forward walking in identifying the risk of falls in elderly people [ 13 ]. Concerning individuals with PD, these patients demonstrated more pronounced gait impairments in BW than in forward walking such as reductions in stride length and velocity [ 14 , 15 ]. In addition, in PD, BW impairment, differently from forward walking, has been reported to be non-responsive to levodopa, suggesting that this paradigm may provide further information about mobility [ 13 ]. Finally, BW alterations in PD have been reported to be more closely related to motor symptoms and fear of falling than forward walking, thus suggesting that BW analysis could be a potential progression biomarker [ 16 ]. Recent studies have also reported that patients with PD, particularly those with FOG, had greater impairments in BW than in forward walking [ 7 , 9 , 17 – 21 ]. This subgroup of patients demonstrated to be more prone to multiple falls and injuries [ 22 ] and backward walking has been linked to FOG occurrence [ 18 ]. Therefore, the implementation of BW evaluation in PD patients reporting FOG could be particularly relevant and could add valuable information to clinical assessment. However, to the best of our knowledge, no systematic review to date has compared BW performance reported in PD patients with and without FOG. Thus, the aim of this review was to evaluate the differences in BW performance between PD patients with FOG and PD patients without FOG 2. Methods 2.1. Protocol and Registration This systematic review’s protocol has been registered with the International Prospective Register of Systematic Reviews (PROSPERO) (CRD 42022354994). The review follows the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PRISMA) statement [ 23 ] and the Cochrane Handbook for Systematic Reviews guidelines [ 24 ]. 2.2. Eligibility Criteria This review included original articles published in peer-reviewed scientific journals Only articles published in English, French, Italian or German were included. Participants had to be diagnosed with PD. Studies reporting any measure quantifying BW performance (spatiotemporal parameters, kinematic parameters, etc.) and comparing PD patients with and without FOG were included. Case reports, abstracts, editorials, letters to the editor, case studies, reviews, and meta-analyses were excluded 2.3. Data Sources and Search Strategy The following two databases, PubMed and Web of Science, were systematically searched on 4 July 2022, and the search was repeated on 6 November 2022 Keywords related to (1) Parkinson’s disease, (2) backward walking, and (3) freezing of gait have been used. The search strategy consisted of a combination of keywords using the Boolean operator “AND” and “OR”. The first category included terms related to PD such as “idiopathic Parkinson’s Disease” OR “Lewy Body Parkinson Disease” OR “Primary Parkinsonism” OR “Idiopathic Parkinson Disease” OR “Parkinson Disease”. The second

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 3 of 23 category focused on terms related to backward walking such as “backwards walking” OR “backward walking” OR “backward gait” OR “backward locomotion” OR “backwards locomotion” OR “retrowalking” OR “retro-walking”. The third category specified FOG and comprised the following terms: “freezing of gait” OR “fog” OR “frozen gait”. For the final search, these 3 keyword’s categories were combined as follows: (1) AND (2) AND (3). Search fields were restricted to the abstract, title, and keywords 2.4. Study Selection Two independent reviewers (TM and MC) screened the titles and abstracts of all studies to identify potentially relevant articles. After the removal of duplicates, selected full-text articles were then reviewed and independently screened for eligibility according to the inclusion criteria mentioned above. If disagreements occurred between the two independent reviewers, consensus will then be achieved through discussions or contact with a third reviewer (NV) to arbitrate the disagreement 2.5. Data Extraction After the end of the selection process, two independent reviewers (TM and MC) extracted data from all included studies. Information was extracted on (1) the study’s characteristics, (2) the sample characteristics, (3) the measure of FOG, (4) the measure of BW, and (5) the main results of the comparison of BW performance in PD patients with and without FOG. Reviewers were not blinded to the authors or journals when extracting data. Any discrepancies between these independent reviewers were resolved at a consensus meeting. If disagreement persisted, a third reviewer (NV) was consulted for a final decision 2.6. Methodological Quality Two independent reviewers (TM and MC) assessed the quality of the included studies The National Institutes of Health (NIH) Quality Assessment Tool for Observational Cohort and Cross-sectional Studies (NIH, 2014) was applied to assess the methodological quality of the included studies. It consists of answering yes, no, or other to each of the 14 items Then, the overall quality of a study was evaluated by assigning a good, fair, or poor rating to each study. Any disagreements between the two independent reviewers were resolved by discussion, with the involvement of a third reviewer (NV) when necessary, who was contacted to arbitrate the disagreement to reach the final rating 3. Results 3.1. Study Selection The database search yielded 18 potentially relevant studies. One additional study was identified through hand searching. After removing duplicates ( n = 8), 11 studies remained. After the screening of titles and abstracts, 2 studies were excluded, and 9 studies were reviewed for eligibility. After full-text screening, 2 studies were excluded. The remaining 7 studies fulfilled the eligibility criteria and were included in this systematic review [ 7 , 9 , 17 – 21 ]. The study selection process is illustrated in Figure 1 . 3.2. Methodological Quality The overall quality assigned to the 7 studies was “fair” according to the NIH tool (Table 1 ). 3.3. Study Characteristics Table 2 shows general information about the studies included in this systematic review, including authors, year of publication, country, title, journal, and funding sources.

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 4 of 23 Int. J. Environ. Res. Public Health 2023 , 20 , 953 4 of 25 Figure 1. Flowchart of the study selection process 3.2. Methodological Quality The overall quality assigned to the 7 studies was “fair” according to the NIH tool (Table 1) 3.3. Study Characteristics Table 2 shows general information about the studies included in this systematic review, including authors, year of publication, country, title, journal, and funding sources Figure 1. Flowchart of the study selection process Publication year. Publication year of the 7 included studies ranged from 2009 [ 9 ] to 2022 [ 7 ]. One study (14%) was published in each of the following years: 2009 [ 9 ], 2010 [ 17 ], 2012 [ 18 ], 2017 [ 19 ], 2018 [ 20 ], 2020 [ 21 ], and 2022 [ 7 ]. Country of the first author’s affiliation. Five studies (71%) were conducted in the USA [ 7 , 9 , 17 – 20 , 20 ]. Journal. The 7 included studies have been published in 6 different journals: 2 (29%) in Gait & Posture [ 7 , 20 ], and 1 (14%) in each of the following journals: Movement Disorders [ 9 ], Neurorehabilitation and Neural Repair [ 17 ], Journal of Applied Biomechanics [ 21 ], Parkinsonism and Related Disorders [ 18 ] and Journal of Rehabilitation Medicine [ 19 ].

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 5 of 23 Table 1. The National Institutes of Health Quality Assessment Tool for Observational Cohort and Cross-sectional Studies Question/ Objective Clearly Stated Population Clearly Defined Participation Rate of Eligible Persons at Least 50% Subjects Recruited from the Same Populations Sample Size Justification, Power Description, or Variance and Effect Estimates Provided Exposure(s) of Interest Measured Prior to the Outcome(s) Timeframe Sufficient for an Association between Exposure and Outcome Study Examines Different Levels of Exposure Exposure Measures Clearly Defined Exposure(s) Assessed More Than Once over Time Outcome Measures Clearly Defined Outcome Assessors Blinded Loss to Follow-up after Baseline 20% or Less Key Potential Confounding Variables Measured and Adjusted Statistically Overall Rate Hackney & Earhart 2009 [ 9 ] Yes Fair No Other NR NA NA Hackney & Earhart 2010 [ 17 ] Yes Fair No Other NR NA NA Myers et al., 2020 [ 21 ] Yes Fair No Other NR NA Peterson et al., 2012 [ 18 ] Yes Poor No Other NR NR Son et al., 2018 [ 20 ] Yes Fair No Other NR NR NR Son et al., 2022 [ 7 ] Yes Fair No Other NR NA Sutter et al., 2017 [ 19 ] Yes Fair No Other NR NA NA NA: not applicable; NR: not reported.

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 6 of 23 Table 2. General information about the selected studies, including authors, year of publication, country, title, journal, and funding sources Author Publication Year Country Title Journal Funding Sources Study Design Hackney and Earhart [ 9 ] 2009 USA Backward Walking in Parkinson Disease Movement Disorders The American Parkinson Disease Association funded this work Cross-sectional Hackney and Earhart [ 17 ] 2010 USA The Effects of a Secondary Task on Forward and Backward Walking in Parkinson’s Disease Neurorehabilitation and Neural Repair The American Parkinson Disease Association and NIH grant K 01-HD 048437 Cross-sectional Myers et al. [ 21 ] 2020 USA Cross-sectional Analysis of Backward, Forward, and Dual Task Gait Kinematics in People With Parkinson Disease With and Without Freezing of Gait Journal of Applied Biomechanics National Institutes of Health (T 32 HD 007434), the Greater St Louis Chapter of the American Parkinson Disease Association, and the American Parkinson Disease Association Center for Advanced PD Research at Washington University School of Medicine Cross-sectional Peterson et al. [ 18 ] 2012 USA Evidence for a Relationship between Bilateral Coordination during Complex Gait Tasks and Freezing of Gait in Parkinson’s Disease Parkinsonism and Related Disorders NIH TL 1 RR 024995; NIH RO 1 HD 056051-01; NIH 2 T 32 HD 007434-18 A; Parkinson’s Disease Foundation; American Parkinson Disease Association Center for Advanced PD Research at Washington University Cross-sectional Son et al. [ 20 ] 2018 Republic of Korea Impacts of Freezing of Gait on Forward and Backward Gait in Parkinson’s Disease Gait & Posture The Dong-A University research fund Cross-sectional Son et al. [ 7 ] 2022 Republic of Korea Turning Reveals the Characteristics of Gait Freezing Better than Walking Forward and Backward in Parkinson’s Disease Gait & Posture The Dong-A University Research Fund Explorative Sutter et al. [ 19 ] 2017 USA Low to Moderate Relationships between Gait and Postural Responses in Parkinson’s Disease Journal of Rehabilitation Medicine NIH R 01 NS 077959. K.S. is supported by the Clinical and Translational Science Award (CTSA) program of the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH) at Washington University School of Medicine in St Louis (TL 1 TR 000449). R.D. is supported by NIH K 12 HD 055931 Cross-sectional

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 7 of 23 Funding. Funding information was reported in all studies ( n = 7). Four studies (57%) were supported by the American Parkinson Disease Association in the USA [ 9 , 17 , 18 , 21 ]. Four studies (57%) received grants from the National Institutes of Health [ 17 – 19 , 21 ]. One study (14%) was supported by the Parkinson’s Disease Foundation in USA [ 18 ]. Two studies (29%) were supported by the Dong-A University research fund in the Republic of Korea [ 7 , 20 ]. Design. Six studies (86%) [ 9 , 17 – 21 ] were cross-sectional analyses and one (14%) was explorative [ 7 ]. 3.4. Sample Characteristics Table 3 shows basic demographic and anthropometric information of the participants included in each study The 7 studies included covered a total of 431 patients with PD, among whom 248 (57%) were male. All studies included both men and women participants In 2 studies (29%) [ 7 , 20 ], patients were diagnosed with idiopathic PD according to the United Kingdom Brain Bank criteria [ 25 , 26 ], while in 3 studies (43%) [ 9 , 17 , 19 ], PD was determined using criteria for clinically defined “definite PD” [ 27 , 28 ]. Two studies (29%) did not mention how PD was diagnosed [ 18 , 21 ]. The mean PD sample size was n = 31 ± 16, ranging from 10 [ 20 ] to 65 [ 19 ] patients with PD. The mean PD age was 68.6 ± 1.7 years, ranging from 64.2 ± 6.6 [ 21 ] to 72 ± 9 years [ 18 ]. The average total score of the Movement Disorder Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) was reported in 4 studies [ 7 , 9 , 17 , 20 ] and ranged from 26.2 ± 8.7 [ 17 ] to 51.80 ± 14.47 [ 20 ]. The average MDS-UPDRS part III score (motor examination) was reported in 5 studies [ 7 , 9 , 17 , 18 , 20 ] and ranged from 27.5 ± 9.2 [ 17 ] to 45.5 ± 15.2 [ 18 ]. The mean Hoehn and Yahr (H&Y) score was reported in 3 studies [ 7 , 18 , 20 ] and ranged from 2.23 ± 0.59 [ 20 ] to 2.63 ± 0.83 [ 18 ]. Mean disease duration was reported in 3 studies [ 9 , 17 , 18 ] ranging from 6.4 ± 3.7 [ 17 ] to 10.5 ± 5.9 years [ 17 ]. Symptom duration was reported in 2 studies [ 7 , 20 ] ranging from 4.5 ± 4.0 [ 7 ] to 8.1 ± 5.1 years [ 7 ]. All 7 of the included studies [ 7 , 9 , 17 – 21 ] classified the PD population into 2 categories according to the absence (PD − FOG) ( n = 252 participants, 58%) or presence (PD + FOG) of FOG ( n = 179 participants, 42%). In 3 studies, PD patients were considered in PD + FOG group with a score > 1 [ 9 , 17 ] or a score > 2 [ 18 ] on item 3 of the Freezing of Gait Questionnaire (FOGQ) (“Do you feel that your feet get glued to the floor while walking, making a turn or when trying to initiate walking (freezing)?”). In 4 studies [ 7 , 19 – 21 ], PD patients were considered in PD + FOG group according to their responses to the new Freezing of Gait Questionnaire (NFOG-Q). Patients watched a video representing diverse types of FOG and then were grouped in PD + FOG group if they answered positively to item 1 of the NFOG-Q (“Did you experience ‘freezing episodes’ over the past month?”) Studies Population The 7 studies included covered a total of 179 PD patients (42%) with FOG (PD + FOG) and 252 PD patients (58%) without FOG (PD − FOG). Details about included studies, sample size, demographic, and anthropometric and clinical characteristics are shown in Table 3 . 3.5. Assessments of Freezing of Gait Two methods were used to assess the presence and severity of FOG in patients with PD: Freezing of Gait Questionnaire (FOG-Q) [ 29 ] and the new Freezing of Gait Questionnaire (NFOG-Q) [ 30 ].

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 8 of 23 Table 3. Demographic and anthropometric information of the participants included in each study Author, Year Country Sample Size ( n ) Sex (M, F) ( n ) Age, Mean (SD), Years Disease Duration (SD), Years Height, Mean (SD), m Weight, Mean (SD), kg BMI, Mean (SD), kg/m 2 MDS-UPDRS III Score H&Y Score Hackney and Earhart 2009 [ 9 ] USA PD + FOG: 35 PD − FOG: 43 NM NM 10.5 ± 1.00 6.4 ± 0.57 NM NM NM NM NM Hackney and Earhart 2010 [ 17 ] USA PD + FOG: 35 PD − FOG: 43 NM NM 10.5 ± 5.9 6.4 ± 3.7 NM NM NM NM NM Myers et al., 2020 [ 21 ] USA PD + FOG: 13 PD − FOG: 31 M: 5, F: 8 M: 12, F: 19 64.2 ± 6.6 67.3 ± 9.2 NM NM NM 24.6 ± 3.0 23.8 ± 2.7 26 (13–48) 26 (3–49) 2 (2–3) 2 (1–2) Peterson et al., 2012 [ 18 ] USA PD + FOG: 12 PD − FOG: 19 NM 72 ± 9 71 ± 9 8.0 ± 4.5 6.6 ± 5.1 NM NM NM 45.5 ± 15.2 41.6 ± 6.4 2.63 ± 0.83 2.37 ± 0.40 Son et al., 2018 [ 20 ] Republic of Korea PD + FOG: 10 PD − FOG: 16 M: 7, F: 3 M: 11, F: 5 70.24 ± 6.21 71.52 ± 6.34 symptom duration 4.60 ± 1.07 4.52 ± 1.23 1.63 ± 0.08 1.58 ± 0.01 60.99 ± 6.03 60.28 ± 10.24 23.0 ± 0.1 24.2 ± 0.1 35.95 ± 9.97 35.69 ± 7.60 2.60 ± 0.51 2.23 ± 0.59 Son et al., 2022 [ 7 ] Republic of Korea PD + FOG: 28 PD − FOG: 35 M: 18, F: 10 M: 14, F: 21 68.6 ± 5.5 70.5 ± 5.2 symptom duration 8.1 ± 5.1 4.5 ± 4.0 1.60 ± 0.01 1.55 ± 0.07 61.7 ± 9.5 57.8 ± 7.2 24.2 ± 0.1 24.1 ± 0.1 32.8 ± 8.9 33.6 ± 7.1 2.6 ± 0.4 2.4 ± 0.4 Sutter et al., 2017 [ 19 ] USA PD + FOG: 46 PD − FOG: 65 M: 28, F: 18 M: 37, F: 28 mean (95% CI): 67.9 (65.2, 70.5) 65.6 (63.2, 67.9) median (IQR): 5.0 (3.0–9.5) 4.0 (1.3–7.5) NM NM NM 41.5 (32.8–46.3) 34.0 (29.0–39.0) I: 1, II: 33, III: 10, IV: 2 I: 3, II: 55, III: 6, IV: 1 M: male; F: female; n : number; NM: not mentioned; SD: standard deviation; BMI: body mass index; CI: confidence interval; IQR: interquartile range; MDS-UPDRS III: the Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale Part III; H&Y: Hoehn and Yahr scale.

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 9 of 23 Method 1. FOG-Q [ 29 ] was used in 3 studies (43%) [ 9 , 17 , 18 ], including a total of 187 participants, namely 105 PD without FOG (56%) and 82 PD with FOG (44%). The FOG- Q is a self-administrative scale which consists of 6 items, each item scored from 0 to 4 with a maximum score of 24 points. A higher score represents more severe freezing. Four items question the duration and frequency of FOG, and two items question general gait impairment. Participants were considered in the PD + FOG group, if they had a score > 1 on item 3 (“Do you feel that your feet get glued to the floor while walking, making a turn or when trying to initiate walking (freezing)?”), suggesting a frequency of FOG at least once a week [ 29 ]. Method 2. NFOG-Q [ 30 ] was used in 4 studies (57%) [ 7 , 19 – 21 ], including a total of 244 participants, namely 147 PD without FOG (60%) and 97 PD with FOG (40%). The NFOG- Q was based on the FOG-Q version. An initial part was added to enable the detection of FOG, and the exclusion of subjects without symptoms, from the actual score of FOG severity and impact. A short video was also added to help in clarifying diverse types and durations of FOG. Participants were considered in the PD + FOG group if they answered “yes” on item 1 (“Did you experience freezing episodes over the past month?”) [ 30 ]. 3.6. Backward Walking Protocol Table 4 reports description of the BW tasks 3.6.1. Experimental Procedure Instructions. In one study (14%) [ 9 ], participants were instructed to walk at their normal pace, 3 times in each direction: forward then backward. In one study (14%) [ 17 ], participants performed single-task conditions at their normal or comfortable pace 3 times in each direction: forward then backward. Secondly, they performed one trial of a mental arithmetic task with forward then backward. In 2 studies (29%) [ 18 , 21 ] participants were asked to walk backward at a comfortable pace. In 3 studies (43%) [ 7 , 19 , 20 ], the instructions for the tasks were not reported Walking speed. Participants’ walking speed was reported in 6 studies (86%): normal speed in 3 studies (43%) [ 9 , 17 , 20 ], comfortable speed in 2 studies (29%) [ 18 , 21 ] or preferred speed in one study (14%) [ 18 ]. Walking distance. Walking distance was reported in all studies. Participants walked a length of 10 m [ 18 ], 8 m [ 7 , 20 ], 7 m [ 21 ], 5 m [ 9 , 17 ] and 4.8 m [ 19 ]. Number of trials. In 5 studies (71%), participants performed 3 trials per condition [ 7 , 9 , 17 , 19 , 20 ]. In one study (14%), they performed 5 trials [ 21 ] and in one study (14%) they performed 5 to 8 trials [ 18 ]. Only Hackney and Earhart (2010) reported that no practice trials were given to participants. In 3 studies (43%), participants were given enough time to rest and were allowed to sit between trials [ 9 , 17 , 19 ]. Results from trials were averaged in 5 studies (71%) [ 7 , 9 , 17 , 19 , 20 ], and it was not mentioned whether results were averaged or not in 2 studies (29%) [ 18 , 21 ]. Medication state during task. BW was assessed in people with PD in OFF-medication state, with assessments being carried out after not taking antiparkinsonian medication at least 12 h before the tests in 4 studies (57%) [ 7 , 18 – 20 ] ( n = 231 participants) and in the ON-medication state in 3 studies (43%) [ 9 , 17 , 21 ] ( n = 200 participants) There were no included studies in which participants were asked to perform BW only. In two studies (29%) [ 9 , 20 ] participants were asked to perform two walking tasks: backward and forward walking. In Hackney and Earhart’s (2009) study, participants walked forward then backward. The order of presentation of the conditions was not reported by Son et al. (2018) In one study (14%) [ 21 ], participants were asked to perform three walking tasks: BW, forward walking, and forward walking with a dual task (listing as many words as they could think of that start with a certain letter). By condition, trials were grouped into blocks, five trials per block, and the blocks were randomized.

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 10 of 23 Table 4. Description of the backward walking tasks Author, Year Task Length of Walkway Number of Conditions Walking Speed Hackney and Earhart 2009 [ 9 ] Instructions: Participants walked FW to accustom themselves to the mat, and then BW Number of trials per condition: 3 trials (trials were averaged) 5 m instrumented computerized GAITRite walkway 2: FW BW Normal pace Hackney and Earhart 2010 [ 17 ] Instructions: Participants performed simple conditions by FW and then BW. Next, participants performed dual conditions by FW while performing a mental arithmetic task aloud. This procedure was repeated while BW Number of trials per condition: Simple conditions: 3 trials (trials were averaged) Dual conditions: 1 trial 5 m instrumented computerized GAITRite walkway 4: Single-task conditions: 2: FW BW Dual task conditions: 2: FW + mental arithmetic task aloud (counting backward from 100 by threes, from 50 by fours and from 75 by sixes) BW+ mental arithmetic task aloud (counting backward from 100 by threes, from 50 by fours and from 75 by sixes) Normal or comfortable pace Myers et al., 2020 [ 21 ] Instructions: Participants walked a length of 7 m stretched diagonally across the capture volume in 3 conditions: FW, BW, and dual task Number of trials per condition: Trials were grouped in blocks by condition (5 trials per block), and blocks were randomized (NM if trials were averaged) 7 m 3: FW BW Dual task (FW + list as many different words as they could that begin with a specified letter. The letter changed for every dual task trial) Comfortable pace Peterson et al., 2012 [ 18 ] Instructions: Subjects completed the following 6 gait tasks in random order: FW, BW, turning to the left and right in a small radius circle and turning to the left and right in a large radius circle Number of trials per condition: 5 to 8 trials for both FW and BW (NM if trials were averaged) 10 m 6: FW BW Turning to the left in a small radius circle Turning to the right in a small radius circle Turning to the left in a large radius circle Turning to the right in a large radius circle Comfortable, preferred pace Son et al., 2018 [ 20 ] Instructions: During the FW and BW task, all patients wore Lycra shorts and a T-shirt, and completed the test with bare feet Number of trials per condition: 3 trials (trials were averaged) 8 m 2: FW BW

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 11 of 23 Table 4. Cont Author, Year Task Length of Walkway Number of Conditions Walking Speed Son et al., 2022 [ 7 ] Instructions: During FW and BW tests, participants were asked to walk at their preferred speed. During 360-degree turning test, participants were asked to turn at their preferred speed in both directions Number of trials per condition: 3 trials (trials were averaged) 8 m 3: FW BW 360-degree turning test Preferred pace Sutter et al., 2017 [ 19 ] Instructions: Participants wore shoes during evaluations and were allowed to rest as often as needed Number of trials per condition: 3 trials (trials were averaged) 4.8 m GAITRite computerized walkway 2: FW BW Preferred pace

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 12 of 23 In one study (14%) [ 17 ] participants were asked to perform four walking tasks: backward and forward walking in singleand dual-task conditions (performing a mental arithmetic task aloud that consisted of counting backward from 100 by threes, from 50 by fours, and from 75 by sixes). Participants walked forward then backward In one study (14%) [ 18 ], participants were asked to perform 6 walking tasks: BW, forward walking, turning right and left in a small radius circle and turning right and left in a large radius circle. These 6 walking tasks were performed in random order In one study (14%) [ 7 ], participants were asked to perform 4 walking tasks: BW, forward walking, and 360-degree turning in both directions. The order of presentation of the conditions was not reported In one study (14%) [ 19 ], participants were asked to perform 4 walking tasks: BW, forward walking, MDS-UPDRS-III item 12 (for postural responses), and the Mini Balance Evaluation Systems Test items 4 and 5 (for postural responses). The order of presentation of the conditions was not reported 3.6.2. Data Acquisition System Table 5 describes the data acquisition method and measured parameters during BW BW was captured using cameras in three studies (43%): in two studies (29%) (Son et al., 2018; Son et al., 2022) six infrared cameras (Vicon, MX-T 10, Bilston, UK) were used; in one study (14%) (Myers et al., 2020) a Hawk Digital RealTime 8-camera system (Motion Analysis Corp, Santa Rosa, CA, USA) with a 3.048 m × 3.048 m × 3.048 m capture volume and 100-Hz capture rate were used In one study (14%) (Peterson et al., 2012), to track the moment of heel strike and toe off, each shoe’s sole had six round footswitches (20 mm (about 0.79 in) in diameter and 1 mm (about 0.04 in) thick; Motion Lab Systems, Baton Rouge, LA, USA) attached to it 3.7. Comparison of BW Performance in PD Patients with and without FOG Spatiotemporal parameters were measured in all studies ( n = 7) [ 7 , 9 , 17 – 21 ]. Three studies (43%) [ 7 , 20 , 21 ] measured both spatiotemporal and kinematic parameters Five studies (71%) [ 7 , 9 , 17 , 19 , 20 ] reported walking speed (m/s) Three studies (43%) [ 7 , 19 , 20 ] reported step length (m). Three studies (43%) [ 7 , 9 , 17 ] reported stride length (m). Three studies (43%) [ 7 , 9 , 17 ] reported cadence (step/min) Two studies (29%) [ 7 , 20 ] reported step time (s) and asymmetry index of step time and length. Two studies (29%) [ 9 , 17 ] reported swing and stance percent, base of support (m), and functional ambulation profile which quantify gait variability. One study (14%) [ 7 ] reported stride time (s). One study (14%) [ 17 ] reported gait asymmetry. The other study (14%) of Hackney and Earhart reported double support percentage [ 9 ]. One study (14%) [ 18 ] reported stepping coordination measured as phase coordination index, a temporal gait variable that quantifies the accuracy and consistency of left to right stepping phases by assessing bilateral coordination of gait. It was calculated as the summation of 2 components: consistency of phase generation and temporal accuracy in producing anti-phased stepping through all steps [ 18 ]. One last study (14%) [ 21 ] reported cycle timing, % gait cycle of the hip, and knee and ankle joints measuring the timing of maximum and minimum angles Kinematic outcomes computed during BW in individuals with PD with and without FOG are presented in Table 6 . Kinematic parameters were measured in 3 studies (43%) [ 7 , 20 , 21 ], which reported the range of motion (ROM) of the hip, knee, and ankle joints Two studies (29%) [ 7 , 20 ] reported the maximum anti-phase ( ◦ ) and toe clearance height (cm) One study (14%) [ 21 ] measured the decomposition index which was calculated to determine percentage of the gait cycle in which a joint remained fixed while another one is moving.

[Find the meaning and references behind the names: Angle]

Int. J. Environ. Res. Public Health 2023 , 20 , 953 13 of 23 Table 5. Outcomes of gait parameters computed in individuals with Parkinson’s disease with and without freezing of gait during backward walking Author, Year Acquisition System Gait Parameters PD + FOG PD − FOG Differences between PD + FOG and PD − FOG (Absolute Difference; Percentage of Difference) Hackney and Earhart 2009 [ 9 ] 5-m instrumented, computerized GAITRite walkway (CIR Systems, Inc., Havertown, PA, USA) Spatiotemporal parameters: Walking speed (m/s) 0.61 ± 0.05 0.73 ± 0.05 NSD ( p = 0.091) Stride length (m) 0.7 ± 0.04 0.8 ± 0.05 ↓ (0.1; − 12.5%) ( p = 0.032 *) Cadence (step/min) 114 ± 4.7 110 ± 3.5 NSD ( p = 0.422) Base of support (m) 0.2 ± 0.01 0.2 ± 0.01 NSD ( p = 0.321) Functional ambulation profile 55.8 ± 2.2 64.1 ± 2.5 ↓ (8.3; − 13%) ( p = 0.027 *) Swing (%) 30.3 ± 0.8 32.4 ± 0.6 ↓ (2.1; − 6%) ( p = 0.040 *) Stance (%) 70.0 ± 0.9 67.7 ± 0.6 ↑ (2.3; 3%) ( p = 0.031 *) Double support (%) 41.2 ± 2.3 37.8 ± 11.6 NSD ( p = 0.065) Variability of swing (%) 8.6 ± 3.2 6.4 ± 2.8 ↑ (1.8; 34%) ( p = 0.013 *) Variability of stance (%) 10.8 ± 3.0 5.7 ± 0.5 ↑ (5.1; 89%) ( p = 0.010 *) Variability of stride length (m) 0.1 ± 0.01 0.1 ± 0.01 NSD ( p = 0.325) Hackney and Earhart 2010 [ 17 ] 5-m instrumented, computerized GAITRite walkway (CIR Systems, Inc, Havertown, PA) Spatiotemporal parameters: NM NM Walking speed (m/s) ↓ PD + FOG vs. PD − FOG ( p ≤ 0.00625 *) Stride length (m) ↓ PD + FOG vs. PD − FOG ( p = 0.004 *) Cadence (step/min) NSD ( p > 0.05) Base of support (m) NSD ( p > 0.05) Functional ambulation profile ↓ PD + FOG vs. PD − FOG ( p < 0.001 *) Swing (%) NSD ( p > 0.05) Stance (%) NSD ( p > 0.05) Gait asymmetry NSD ( p > 0.05) Myers et al., 2020 [ 21 ] A Hawk Digital RealTime 8-camera system (Motion Analysis Corp, Santa Rosa, CA) Spatiotemporal parameters: Timing of minimum ankle angle (% gait cycle) 95.2 ± 5.2 88.3 ± 8.4 ↑ (6.9; 8%) ( p < 0.05 *) Timing of maximum ankle angle (% gait cycle) 87.7 ± 6.2 87.4 ± 5.0 NSD ( p > 0.05) Timing of minimum knee angle (% gait cycle) 54.7 ± 8.4 51.4 ± 4.6 NSD ( p > 0.05) Timing of maximum knee angle (% gait cycle) 39.7 ± 20.8 51.1 ± 18.7 NSD ( p > 0.05) Timing of minimum hip angle (% gait cycle) 69.0 ± 3.7 69.6 ± 4.5 NSD ( p > 0.05) Timing of maximum hip angle (% gait cycle) 52.8 ± 6.8 53.5 ± 5.0 NSD ( p > 0.05) Kinematic parameters: Decomposition index hip–ankle 12.9 ± 8.2 8.8 ± 4.1 ↑ (4.1; 47%) ( p = 0.03 *) Decomposition index hip–knee 16.0 ± 8.3 10.2 ± 6.5 ↑ (5.8; 57%) ( p = 0.03 *) Decomposition index Knee-ankle 12.5 ± 4.8 10.8 ± 7.5 NSD ( p > 0.05)

[Find the meaning and references behind the names: Nexus, Plug]

Int. J. Environ. Res. Public Health 2023 , 20 , 953 14 of 23 Table 5. Cont Author, Year Acquisition System Gait Parameters PD + FOG PD − FOG Differences between PD + FOG and PD − FOG (Absolute Difference; Percentage of Difference) Hip ROM ( ◦ ) 23.2 ± 6.8 25.0 ± 5.5 NSD ( p > 0.05) Knee ROM ( ◦ ) 42.0 ± 9.6 44.9 ± 9.7 NSD ( p > 0.05) Ankle ROM ( ◦ ) 22.9 ± 5.7 23.8 ± 4.7 NSD ( p > 0.05) Peterson et al., 2012 [ 18 ] Six round footswitches (20 mm diameter, 1 mm thick; Motion Lab Systems; Baton Rouge, LA, USA) Spatiotemporal parameters: Stepping coordination: Phase coordination index 13.9 ± 3.9 10.9 ± 3.8 ↑ (3; 27%) ( p = 0.01 *) Temporal accuracy of steps 7.4 ± 3.2 5.3 ± 2.1 ↑ (2.1; 40%) ( p < 0.001 *) Consistency of steps 6.4 ± 1.4 5.6 ± 1.9 ↑ (0.8; 14%) ( p < 0.001 *) Son et al., 2018 [ 20 ] The Plug-ingait model + 39 reflective markers Six infrared cameras (Vicon, MX-T 10, UK) Nexus software (version 1.83, VICON, UK) Spatiotemporal parameters: Walking speed MAS, LAS (m/s) 0.46 ± 0.13 0.60 ± 0.14 ↓ (0.14; − 23%) ( p = 0.031 *) Step length MAS (m) 0.22 ± 0.08 0.32 ± 0.09 ↓ (0.1; − 31%) ( p = 0.014 *) Step length LAS (m) 0.27 ± 0.05 0.32 ± 0.08 NSD ( p = 0.123) Step length AI 24.03 ± 19.20 11.03 ± 7.62 ↑ (13; 118%) ( p = 0.030 *) Step time MAS (s) 0.49 ± 0.05 0.50 ± 0.07 NSD ( p = 0.902) Step time LAS (s) 0.51 ± 0.04 0.51 ± 0.07 NSD ( p = 0.946) Step time AI 5.06 ± 3.95 4.66 ± 2.18 NSD ( p = 0.755) Kinematic parameters: Hip ROM MAS ( ◦ ) 26.64 ± 7.75 32.92 ± 8.53 NSD ( p = 0.098) Hip ROM LAS ( ◦ ) 25.77 ± 7.39 33.76 ± 9.25 ↓ (7.99; − 24%) ( p = 0.048 *) Knee ROM MAS ( ◦ ) 32.16 ± 8.84 36.55 ± 13.00 NSD ( p = 0.404) Knee ROM LAS ( ◦ ) 32.58 ± 10.62 41.34 ± 11.47 NSD ( p = 0.088) Ankle ROM MAS ( ◦ ) 21.84 ± 5.60 30.43 ± 6.75 ↓ (8.59; − 28%) ( p = 0.006 *) Ankle ROM LAS ( ◦ ) 21.18 ± 3.31 27.67 ± 4.84 ↓ (6.49; − 23%) ( p = 0.003 *) Toe clearance height MAS (cm) 2.10 ± 0.65 2.96 ± 0.94 ↓ (0.86; − 29%) ( p = 0.031) Toe clearance height LAS (cm) 2.75 ± 1.26 3.05 ± 1.01 NSD ( p = 0.536) Maximum anti-phase ( ◦ ) 8.35 ± 2.42 6.74 ± 2.50 NSD ( p = 0.153)

[Find the meaning and references behind the names: Franklin, Bold]

Int. J. Environ. Res. Public Health 2023 , 20 , 953 15 of 23 Table 5. Cont Author, Year Acquisition System Gait Parameters PD + FOG PD − FOG Differences between PD + FOG and PD − FOG (Absolute Difference; Percentage of Difference) Son et al., 2022 [ 7 ] The Plug-ingait model + 39 reflective markers Six infrared cameras (Vicon, MX-T 10, UK) Nexus software (version 1.83, VICON, UK) Spatiotemporal parameters: Walking speed MAS, LAS (m/s) 0.44 ± 0.18 0.55 ± 0.17 NSD ( p > 0.05) Stride length MAS, LAS (m) 0.47 ± 0.20 0.56 ± 0.15 NSD ( p > 0.05) Stride time MAS (s) 1.03 ± 0.17 1.06 ± 0.13 NSD ( p = 0.328) Stride time LAS (s) 1.03 ± 0.16 1.06 ± 0.14 NSD ( p = 0.295) Cadence MAS (step/min) 119.78 ± 18.65 116.99 ± 17.45 NSD ( p = 0.293) Cadence LAS (step/min) 118.84 ± 19.19 114.13 ± 15.05 NSD ( p = 0.337) Step length MAS (m) 0.25 ± 0.11 0.30 ± 0.07 ↓ (0.05; − 17%) ( p = 0.000 *) Step length LAS (m) 0.26 ± 0.09 0.30 ± 0.09 NSD ( p > 0.05) Normalization of step length MAS (m) 0.15 ± 0.07 0.20 ± 0.04 ↓ (0.05; − 25%) ( p = 0.000 *) Normalization of step length LAS (m) 0.16 ± 0.05 0.19 ± 0.05 NSD ( p > 0.05) Step time MAS (s) 0.52 ± 0.09 0.52 ± 0.07 NSD ( p = 0.381) Step time LAS (s) 0.51 ± 0.08 0.54 ± 0.07 NSD ( p = 0.205) Kinematic parameters: Hip ROM MAS ( ◦ ) 27.67 ± 9.17 30.14 ± 9.80 NSD ( p > 0.05) Hip ROM LAS ( ◦ ) 27.61 ± 8.89 31.93 ± 9.24 NSD ( p > 0.05) Knee ROM MAS ( ◦ ) 33.28 ± 10.70 35.33 ± 12.32 NSD ( p > 0.05) Knee ROM LAS ( ◦ ) 34.87 ± 10.87 38.47 ± 10.68 NSD ( p > 0.05) Ankle ROM MAS ( ◦ ) 21.70 ± 6.60 28.00 ± 7.40 ↓ (6.3; − 22.5%) ( p = 0.000 *) Ankle ROM LAS ( ◦ ) 22.43 ± 6.05 27.74 ± 8.91 NSD ( p > 0.05) Toe clearance height MAS (cm) 5.84 ± 1.23 6.20 ± 0.95 NSD ( p > 0.05) Toe clearance height LAS (cm) 6.12 ± 1.39 6.29 ± 1.04 NSD ( p > 0.05) Maximum anti-phase ( ◦ ) 7.15 ± 3.38 6.94 ± 2.52 NSD ( p = 0.329) Sutter et al., 2017 [ 19 ] 4.8 m GAITRite computerized walkway (CIR Systems, Franklin, NJ, USA) Spatiotemporal parameters: Walking speed (m/s) 0.64 (0.46–0.83) 0.87 (0.67–1.02) ↓ (0.13; − 28%) ( p < 0.001 *) Step length (m) 0.33 (0.24–0.44) 0.46 (0.39–0.55) ↓ (0.23; − 26%) ( p < 0.001 *) PD + FOG: PD with FOG; PD − FOG: PD without FOG; MAS: more affected side; LAS: less affected side; AI: asymmetry index; ROM: range of motion; NM: not mentioned; NSD: Non significant difference; *: significance. Significant results are highlighted in bold ↓ : decrease of values in PD + FOG compared with PD − FOG, ↑ : increase of values in PD + FOG compared with PD − FOG.

Int. J. Environ. Res. Public Health 2023 , 20 , 953 16 of 23 Table 6. Distribution of spatiotemporal and kinematics backward walking parameters in included studies Hackney and Earhart 2009 [ 9 ] (nPD + FOG = 35 nPD − FOG = 43) Hackney and Earhart 2010 [ 17 ] (nPD + FOG = 35 nPD − FOG = 43) Myers et al., 2020 [ 21 ] (nPD + FOG = 13 nPD − FOG = 31) Peterson et al., 2012 [ 18 ] (nPD + FOG = 12 nPD − FOG = 19) Son et al., 2018 [ 20 ] (nPD + FOG = 10 nPD − FOG = 16) Son et al., 2022 [ 7 ] (nPD + FOG = 28 nPD − FOG = 35) Sutter et al., 2017 [ 19 ] (nPD + FOG = 46 nPD − FOG = 65) N (% of Articles) Walking speed (m/s) 5 (71%) Stride length (m) 3 (43%) Step length (m) 3 (43%) Cadence (step/min) 3 (43%) Functional ambulation profile 2 (29%) Base of support (m) 2 (29%) Swing (%) 2 (29%) Stance (%) 2 (29%) Step time (s) 2 (29%) Double support (%) 1 (14%) Variability of stride length (m) 1 (14%) Variability of swing (%) 1 (14%) Variability of stance (%) 1 (14%) Gait asymmetry 1 (14%) Asymmetry of step length 1 (14%) Normalization of step length 1 (14%) Stride time (s) 1 (14%) Timing of minimum hip angle (% gait cycle) 1 (14%) Timing of maximum hip angle (% gait cycle) 1 (14%) Timing of minimum knee angle (% gait cycle) 1 (14%) Timing of maximum knee angle (% gait cycle) 1 (14%) Timing of minimum ankle angle (% gait cycle) 1 (14%) Timing of maximum ankle angle (% gait cycle) 1 (14%)

Int. J. Environ. Res. Public Health 2023 , 20 , 953 17 of 23 Table 6. Cont Phase coordination index 1 (14%) Temporal accuracy of steps 1 (14%) Consistency of steps 1 (14%) Hip range of motion ( ◦ ) 3 (43%) Knee range of motion ( ◦ ) 3 (43%) Ankle range of motion ( ◦ ) 3 (43%) Maximum anti-phase ( ◦ ) 2 (29%) Toe clearance height (cm) 2 (29%) Decomposition index (hip-ankle) 1 (14%) Decomposition index (hip-knee) 1 (14%) Decomposition index (knee-ankle) 1 (14%)

[Find the meaning and references behind the names: White, Black, Bars]

Int. J. Environ. Res. Public Health 2023 , 20 , 953 18 of 23 3.7.1. Spatiotemporal BW Parameters The distribution of the kinematics and spatiotemporal parameters in included studies was reported in Table 6 . Spatiotemporal outcomes during BW in individuals with PD with and without FOG were summarized in Table 5 . Walking speed. In three studies (43%) [ 17 , 19 , 20 ], walking speed was significantly slower in PD + FOG compared with PD − FOG In one study (14%) [ 20 ], walking speed in PD + FOG was significantly slower by 23% in both the more affected side (MAS) and the less affected side (LAS) compared with PD − FOG (MAS and LAS: 0.46 ± 0.13 and 0.46 ± 0.13, respectively, in PD + FOG; 0.60 ± 0.14 and 0.60 ± 0.14, respectively, in PD − FOG; p < 0.05) [ 20 ]. The median walking speed was also lower by 26% in PD + FOG compared with PD − FOG ( p < 0.05) in another study [ 19 ]. In addition, PD + FOG walked slower than PD − FOG ( p < 0.00625) in both singleand dual-task conditions [ 17 ]. Figure 2 illustrates the average walking speed measured in PD patients with and without FOG Int. J. Environ. Res. Public Health 2023 , 20 , 953 20 of 25 Kinematic parameters were measured in 3 studies (43%) [7,20,21], which reported the range of motion (ROM) of the hip, knee, and ankle joints Two studies (29%) [7,20] reported the maximum anti ‐ phase (°) and toe clearance height (cm) One study (14%) [21] measured the decomposition index which was calculated to determine percentage of the gait cycle in which a joint remained fixed while another one is moving 3.7.1 Spatiotemporal BW Parameters The distribution of the kinematics and spatiotemporal parameters in included stud ‐ ies was reported in Table 6 Spatiotemporal outcomes during BW in individuals with PD with and without FOG were summarized in Table 5 Walking speed In three studies (43%) [17,19,20], walking speed was significantly slower in PD + FOG compared with PD − FOG In one study (14%) [20], walking speed in PD + FOG was significantly slower by 23% in both the more affected side (MAS) and the less affected side (LAS) compared with PD − FOG (MAS and LAS: 0.46 ± 0.13 and 0.46 ± 0.13, respectively, in PD + FOG; 0.60 ± 0.14 and 0.60 ± 0.14, respectively, in PD − FOG; p < 0.05) [20] The median walking speed was also lower by 26% in PD + FOG compared with PD − FOG ( p < 0.05) in another study [19] In addition, PD + FOG walked slower than PD − FOG ( p < 0.00625) in both single ‐ and dual ‐ task conditions [17] Figure 2 illustrates the average walking speed measured in PD patients with and without FOG Figure 2. Mean and standard deviation of the mean walking speed obtained in Parkinson’s disease patients with and without freezing of gait during backward walking The 2 groups are presented as: Parkinson’s disease patients without freezing of gait (black bars) and Parkinson’s disease pa ‐ tients with freezing of gait (white bars) The significant p values for comparison between the two groups are reported: (*: p < 0.05, **: p < 0.01) [7,9,17,20]. Step length In 3 studies (43%) [7,19,20] step length was significantly lower in PD + FOG than PD − FOG PD + FOG group had significantly narrower step length in the most affected side than PD − FOG group ([20]: 0.22 ± 0.08 vs 0.32 ± 0.09, p = 0.014; [7]: 0.25 ± 0.11 vs 0.30 ± 0.07, p < 0.05) [7,20] Also, the median step length was smaller by 28% in PD + FOG compared ** * * 0 0.2 0.4 0.6 0.8 1 Hackney & Earhart 2009 Hackney & Earhart 2010 Son et al 2018 (MAS) Son et al 2018 (LAS) Son et al 2022 (MAS) Son et al 2022 (LAS) Mean walking speed (m/s) Included studies PD ‐ FOG PD+FOG Figure 2. Mean and standard deviation of the mean walking speed obtained in Parkinson’s disease patients with and without freezing of gait during backward walking. The 2 groups are presented as: Parkinson’s disease patients without freezing of gait (black bars) and Parkinson’s disease patients with freezing of gait (white bars). The significant p values for comparison between the two groups are reported: (*: p < 0.05, **: p < 0.01) [ 7 , 9 , 17 , 20 ]. Step length. In 3 studies (43%) [ 7 , 19 , 20 ] step length was significantly lower in PD + FOG than PD − FOG PD + FOG group had significantly narrower step length in the most affected side than PD − FOG group ([ 20 ]: 0.22 ± 0.08 vs. 0.32 ± 0.09, p = 0.014; [ 7 ]: 0.25 ± 0.11 vs. 0.30 ± 0.07, p < 0.05) [ 7 , 20 ]. Also, the median step length was smaller by 28% in PD + FOG compared with PD − FOG ( p < 0.05) [ 19 ]. PD + FOG had an increased asymmetry of step length (24.03 ± 19.20 vs. 11.03 ± 7.62, p = 0.030) [ 20 ]. Stride length. In two studies (29%) [ 9 , 17 ], PD + FOG had shorter stride length by 12.5% than PD − FOG ([ 9 ]: 0.7 ± 0.04 vs. 0.8 ± 0.05, p = 0.032). In both simpleand dual-task BW, PD + FOG walked with shorter strides [ 17 ].

[Find the meaning and references behind the names: Resources, Lack, Due, Factor]

Int. J. Environ. Res. Public Health 2023 , 20 , 953 19 of 23 Cadence. In 3 articles (43%) [ 9 , 17 , 20 ], there was no significant difference in cadence between PD + FOG and PD − FOG groups Functional ambulation profile. PD + FOG had significantly lower functional ambulation profile by 13% than PD − FOG ([ 9 ]: 55.8 ± 2.2 vs. 64.1 ± 2.5, p = 0.027). In both simpleand dual-task BW, PD + FOG had lower functional ambulation profile values compared with PD − FOG [ 17 ]. In two studies (29%) [ 9 , 17 ], PD + FOG had a lower functional ambulation profile than PD − FOG, by 13% in Hackney and Earhart 2009: 55.8 ± 2.2 vs. 64.1 ± 2.5, p = 0.027) Swing and stance percent. PD + FOG had significantly smaller swing percent by 6% and greater stance percent by 3% than PD − FOG (30.3 ± 0.8 vs. 32.4 ± 0.6, p = 0.040 and 70.0 ± 0.9 vs. 67.7 ± 0.6, p = 0.031, respectively) [ 9 ]. PD + FOG were more variable in BW swing and stance percent than PD − FOG (swing %: 8.6 ± 3.2 vs. 6.4 ± 2.8, p = 0.013; stance %: 10.8 ± 3.0 vs. 5.7 ± 0.5, p = 0.010) [ 9 ]. Phase coordination index. PD + FOG had significantly higher phase coordination index values than PD − FOG, suggesting worse stepping coordination in PD + FOG (13.9 ± 3.9 vs. 10.9 ± 3.8) [ 18 ]. Cycle timing, % gait cycle. For the PD + FOG, the minimum ankle angle happened late in the gait cycle compared with the PD − FOG (95.2 ± 5.2 vs. 88.3 ± 8.4) [ 21 ]. 3.7.2. Kinematic BW Parameters Range of motion. PD + FOG group had significantly decreased ROM in the ankle joint in the most affected side [ 7 , 20 ] ([ 20 ]: 21.84 ± 5.60 vs. 30.43 ± 6.75; [ 7 ]: 21.70 ± 6.60 vs 28.00 ± 7.40) and the less affected side, (21.18 ± 3.31 vs. 27.67 ± 4.84) [ 20 ] and hip joint in the less affected side (25.77 ± 7.39 vs. 33.76 ± 9.25) [ 20 ] than PD − FOG group Toe clearance height. PD + FOG had a lower toe clearance height in the most affected side than PD − FOG group (2.10 ± 0.65 vs. 2.96 ± 0.94) [ 20 ]. Decomposition indices. Greater decomposition indices between hip–ankle and hip– knee movements were observed in the PD + FOG group (12.9 ± 8.2 vs. 8.8 ± 4.1 and 16.0 ± 8.3 vs. 10.2 ± 6.5, respectively) [ 21 ]. 4. Discussion To the best of our knowledge, this is the first systematic review summarizing published studies that compared BW performance in PD patients with and without FOG. The main findings of our review suggest that PD + FOG exhibited marked differences in BW compared to PD − FOG. PD + FOG had a slower walk with shorter strides and steps and a lower functional ambulation profile compared with PD − FOG. Furthermore, PD + FOG had worse stepping coordination, reduced swing percent, and greater stance percent. They also had a decreased ROM in the ankle and hip joints, greater movement decomposition and lower toe clearance height than PD − FOG. These findings could be explained by a reduction in proprioception, an impairment in attention and cognitive functions, or an alteration in visuospatial and cerebellar network in PD + FOG patients BW requires greater proprioception than forward walking due to the lack of visual control. In PD patients, an alteration of proprioception has been described [ 31 ] and, consequently, individuals with PD are more dependent on visual information [ 32 ] which is more pronounced in those with FOG [ 33 ]. This could explain why PD patients have greater impairments while walking backward [ 17 ] and the marked differences between PD with and without FOG [ 20 ]. Another factor that could explain our findings is the increased cognitive demand for BW. BW is a complex task, demanding more investment in attention and cognitive resources. As reported previously, individuals with PD might experience cognitive impairment, mainly related to attention and executive functions [ 34 ] and these have been closely related to walking and mobility performance [ 35 ]. To this end, studies examining the cognitive differences between PD + FOG and PD − FOG have suggested that PD + FOG had worse executive, attentional, and visuospatial performance [ 36 – 43 ]. Furthermore,

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 20 of 23 FOG severity was negatively correlated with performance on cognitive tests assessing executive functions, suggesting that FOG progression is associated with frontal lobe dysfunction [ 36 , 43 ]. This is also supported by neuroimaging studies suggesting a common pattern of grey matter atrophy between executive functions and FOG [ 44 ]. Additionally, PD + FOG performed worse than PD − FOG in dual task [ 40 ], that is the performance of two tasks simultaneously. Dual task is a common paradigm to test motor-cognitive interaction and a worse performance during dual task has been linked to reduced cognitive resources and lower attention and executive [ 45 ]. In PD, the coordination of bilateral stepping during gait quantified by the phase coordination index is reduced, especially in PD + FOG [ 18 , 46 ]. This result, however, is particularly marked during BW [ 18 ]. Gait coordination, rhythmicity, and asymmetry have been related to cognitive functions and proprioception; therefore, a more markedly increased gait asymmetry during BW could also be associated to the increase in attentional demands [ 20 ]. This is further supported by the finding that PD + FOG demonstrated more gait asymmetry than PD − FOG in BW under dual task conditions (Hackney and Earhart 2010) This review has reported that during the gait cycle, PD + FOG decompose movement between joints more than PD − FOG [ 21 ]. This difference in decomposition indices between PD + FOG and PD − FOG could be related to the cerebellar involvement in FOG [ 47 ]. PD + FOG, indeed, have been reported to have an abnormal functional connectivity network of pedunculopontine nucleus affecting the corticopontine-cerebellar pathways and visual temporal circuits [ 47 ]. These alterations, in the context of a demanding walking task and increased gait variability (i.e., BW), might lead PD + FOG to decompose their movement patterns to improve their stability [ 21 ]. Plotnik et al. (2008) suggested that in patients with PD, when alterations in gait surpass a certain limit, this might trigger FOG. This limit could be regulated by the attention used by PD patients in gait tasks, environmental stressors, and postural stability During BW, compared to forward walking, individuals tend to decrease their speed, most likely due to the inability to see the gait direction [ 10 ]. Moreover, during BW in healthy participants, range of motion of the hip, knee, and ankle have been reported to be reduced compared to forward walking [ 10 ]. The same study considered the ankle joint as the main joint responsible for propulsion and shock absorption during BW [ 10 ]. The findings from our review are in line with these results. PD patients, indeed, markedly reduced their hip, knee, and ankle ROM during BW, most likely due to the reduced proprioception, and this is significantly higher in PD + FOG [ 7 , 20 ], supporting the idea that this subgroup of patients have a more marked alteration of proprioceptive inputs Finally, the worse performance and higher variability of PD + FOG compared to PD − FOG, mainly evident in stance and swing percent, could be explained, at least partly, by their longer disease duration (10.5 ± 1.00 years vs. 6.4 ± 0.57 years) and greater balance impairment (Berg Balance Scale score: 46.8 ± 0.85 vs. 50.0 ± 0.61) [ 9 ]. Taken together, the present findings support the use of BW in PD patients and particularly in the subgroup of patients with FOG. These patients, indeed, have already been reported to be more prone to falls and subsequent injuries [ 22 ]. Moreover, PD + FOG have been reported to have more severe disease progression and non-motor symptoms [ 48 ] and a higher disability with a lower quality of life [ 49 ]. The findings that, in this group of patients, several walking parameters linked to all walking domains (pace, rhythm, variability, asymmetry, and postural control [ 50 ] are altered during BW and that these alterations are more pronounced than in forward walking, support the implementation of BW during clinical and instrumented evaluation, as well as considering including this paradigm in mobility research and clinical trials evaluating walking and mobility in patients reporting FOG. In addition, the alterations observed during BW could be less responsive to dopaminergic therapy, thus making this assessment more stable and less influenced by pharmacological state [ 13 ].

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Int. J. Environ. Res. Public Health 2023 , 20 , 953 21 of 23 Limitations and Future Directions The present study has some limitations. It was difficult to reproduce FOG in the laboratory [ 7 , 20 ]. Thus, the actual number of FOG episodes was unknown because FOG was rarely observed during the intervention [ 7 ]. Future studies that can detect FOG episodes in an actual daily environment are needed to understand the effect of FOG under different gait conditions [ 7 ]. The results are not generalizable due to the limited number of included studies and the small sample size therein [ 7 , 20 , 21 ]. Assessments were done during either the OFF-medication state [ 7 , 18 – 20 ] or the ON-medication state [ 9 , 17 , 21 ]. Thus, assessments in both states could be useful as FOG episodes mainly occur in the OFF-state and some in the ON-state [ 51 ]. There was a high number and heterogeneity of spatiotemporal and kinematic parameters in each article, thus, a strict comparison of results is challenging 5. Conclusions This systematic review summarized the literature about BW performance of PD patients with and without FOG. PD with FOG had worse BW performance than PD without FOG. PD with FOG walked slower with shorter stride and step than PD without FOG. Also, during the gait cycle, PD + FOG decompose joint movement more than PD − FOG. As well, PD + FOG demonstrated greater variability in gait, swing, and stance percent and showed worse stepping coordination. PD with FOG had greater reduction in ROM, mainly at the ankle joint than PD − FOG. This could be due to reduced proprioception and limited attention and cognitive resources from PD patients during a challenging mobility task, or due to altered cerebellar network and visuospatial processing. These results suggest that BW assessment could be relevant to better characterize PD patients and that this paradigm could add valuable information to clinical and instrumented evaluation as well as research and clinical trial Author Contributions: Conceptualization, T.M., C.H. and N.V.; methodology, C.H. and N.V.; formal analysis, T.M., M.C. and N.V.; investigation, T.M., C.H., M.C., E.B. and N.V.; resources, C.H. and N.V.; writing—original draft preparation, T.M., C.H., M.C., E.B. and N.V.; supervision, C.H. and N.V. All authors have read and agreed to the published version of the manuscript Funding: This research was partly funded by the French National Research Agency, within the framework of the “Investissements d’avenir” program (ANR-10-AIRT-05 and ANR-15-IDEX-02). The sponsors had no involvement in study design, the collection, analysis, and interpretation of data, or in writing the manuscript. This work also forms part of a broader translational and interdisciplinary GaitAlps research program (N.V.) Institutional Review Board Statement: Review articles do not require Institutional Review Board (IRB) approval if the data reviewed are public (including private and government databases) and if the articles reviewed have received IRB approval previously Informed Consent Statement: Not applicable Data Availability Statement: Not applicable Conflicts of Interest: The authors declare no conflict of interest References 1 Simon, D.K.; Tanner, C.M.; Brundin, P. Parkinson Disease Epidemiology, Pathology, Genetics, and Pathophysiology Clin. Geriatr Med 2020 , 36 , 1–12. [ CrossRef ] [ PubMed ] 2 Morris, M.E.; Huxham, F.; McGinley, J.; Dodd, K.; Iansek, R. The biomechanics and motor control of gait in Parkinson disease Clin. Biomech 2001 , 16 , 459–470. [ CrossRef ] [ PubMed ] 3 Mirelman, A.; Bonato, P.; Camicioli, R.; Ellis, T.D.; Giladi, N.; Hamilton, J.L.; Hass, C.J.; Hausdorff, J.M.; Pelosin, E.; Almeida, Q.J. Gait impairments in Parkinson’s disease Lancet Neurol 2019 , 18 , 697–708. [ CrossRef ] [ PubMed ] 4 Peterson, D.S.; Horak, F.B. Neural Control of Walking in People with Parkinsonism Physiology 2016 , 31 , 95–107. [ CrossRef ] [ PubMed ] 5 Giladi, N.; Nieuwboer, A. Understanding and treating freezing of gait in parkinsonism, proposed working definition, and setting the stage Mov. Disord 2008 , 23 (Suppl. S 2), 423–425. [ CrossRef ] [ PubMed ]

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Gait, Walking, Fear of falling, Quality of life, Clinical diagnosis, Significant difference, Inclusion criteria, Parkinson's disease, Cognitive impairment, Parkinsonism, Systematic Review, Knee joint, PubMed, Cognitive deficit, Range of Motion, Neurodegenerative disease, Gait impairment, Hip joint, Ankle joint, Base of support, Non-significant difference, International Journal, Biomechanics, Backward Walking, Executive function, Executive dysfunction, Disease duration, Parkinson disease, Motor Examination, Motor control, Heel strike, Open access article, Creative Commons Attribution, Freezing of gait, Parkinson's disease patients, Walking speed, Data acquisition system, Web of Science, Cadence, Gait parameters, Symptom duration, Stride length, Dual task, Gait cycle, Cross-sectional, Gait kinematics, Gait Posture, Motor task, Funding information, Cognitive correlates, Step length, Motor symptom, Stride time, Clinical phenomenon, Ankle rom, Spatiotemporal parameters, Knee rom, Postural responses, Risk of fall, Comfortable speed, Gait Asymmetry, Neural control, Academic Editor, Bilateral coordination, Kinematic parameters, Step time, Measured parameter, Capture rate, Neural Correlate, Infrared Camera, Walking tasks, Decomposition index, Data acquisition method, Turning.