Association between Backward Walking and Cognition in Parkinson Disease: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Selection of Articles
- -
- original peer-reviewed scientific journal articles on humans published in English, French, or German;
- -
- studies reporting both backward walking and cognitive variables to assess the relationship between these variables. Only cross-sectional studies and longitudinal studies were included.
2.3. Quality Assessment
2.4. Data Extraction
3. Results
3.1. Study Selection
3.2. Study Characteristics
3.3. Participant Characteristics
3.4. Backward Walking and Study Design
3.5. Measures of Disease Severity and Cognitive Function
3.6. Main Findings of the Association between Backward Walking Performance and Cognitive Function in PD Populations
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Appendix A
Criteria | Tseng and Yuan, 2012 [21] | Christofoletti et al., 2016 [24] |
---|---|---|
1. Was the research question or objective in this paper clearly stated? | Y | Y |
2. Was the study population clearly specified and defined? | Y | Y |
3. Was the participation rate of eligible persons at least 50%? | Y | Y |
4. Were all the subjects selected or recruited from the same or similar population? Were inclusion and exclusion criteria for being in the study prespecified and applied uniformly to all participants? | Y | Y |
5. Was a sample size justification, power description, or variance and effect estimates provided? | N | Y |
6. For the analyses in this paper, were the exposure(s) of interest measured prior to the outcome(s) being measured? | Y | Y |
7. Was the timeframe sufficient so that one could reasonably expect to see an association between exposure and outcome if it existed? | NA | NA |
8. For exposures that can vary in amount or level, did the study examine different levels of the exposure as related to the outcome (e.g., categories of exposure, or exposure measured as continuous variable)? | N | Y |
9. Were the exposure measures (independent variables) clearly defined, valid, reliable, and implemented consistently across all study participants? | Y | NA |
10. Was the exposure(s) assessed more than once over time? | NA | NA |
11. Were the outcome measures (dependent variables) clearly defined, valid, reliable, and implemented consistently across all study participants? | Y | Y |
12. Were the outcome assessors blinded to the exposure status of participants? | NR | NR |
13. Was loss to follow-up after baseline 20% or less? | NA | NA |
14. Were key potential confounding variables measured and adjusted statistically for their impact on the relationship between exposure(s) and outcome(s)? | Y | Y |
Quality Rating | Good | Good |
Section and Topic | Item # | Checklist Item | Location where Item Is Reported |
---|---|---|---|
TITLE | |||
Title | 1 | Identify the report as a systematic review. | 3 |
ABSTRACT | |||
Abstract | 2 | See the PRISMA 2020 for Abstracts checklist. | 15–28 |
INTRODUCTION | |||
Rationale | 3 | Describe the rationale for the review in the context of existing knowledge. | 32–45 |
Objectives | 4 | Provide an explicit statement of the objective(s) or question(s) the review addresses. | 77–79 |
METHODS | |||
Eligibility criteria | 5 | Specify the inclusion and exclusion criteria for the review and how studies were grouped for the syntheses. | 103–111 |
Information sources | 6 | Specify all databases, registers, websites, organisations, reference lists and other sources searched or consulted to identify studies. Specify the date when each source was last searched or consulted. | 86–89 |
Search strategy | 7 | Present the full search strategies for all databases, registers and websites, including any filters and limits used. | 86–101 |
Selection process | 8 | Specify the methods used to decide whether a study met the inclusion criteria of the review, including how many reviewers screened each record and each report retrieved, whether they worked independently, and if applicable, details of automation tools used in the process. | 112–114 |
Data collection process | 9 | Specify the methods used to collect data from reports, including how many reviewers collected data from each report, whether they worked independently, any processes for obtaining or confirming data from study investigators, and if applicable, details of automation tools used in the process. | 122–133 |
Data items | 10a | List and define all outcomes for which data were sought. Specify whether all results that were compatible with each outcome domain in each study were sought (e.g., for all measures, time points, analyses), and if not, the methods used to decide which results to collect. | 127–131 |
10b | List and define all other variables for which data were sought (e.g., participant and intervention characteristics, funding sources). Describe any assumptions made about any missing or unclear information. | N/A | |
Study risk of bias assessment | 11 | Specify the methods used to assess risk of bias in the included studies, including details of the tool(s) used, how many reviewers assessed each study and whether they worked independently, and if applicable, details of automation tools used in the process. | 116–120 |
Effect measures | 12 | Specify for each outcome the effect measure(s) (e.g., risk ratio, mean difference) used in the synthesis or presentation of results. | N/A |
Synthesis methods | 13a | Describe the processes used to decide which studies were eligible for each synthesis (e.g., tabulating the study intervention characteristics and comparing against the planned groups for each synthesis (item #5)). | N/A |
13b | Describe any methods required to prepare the data for presentation or synthesis, such as handling of missing summary statistics, or data conversions. | N/A | |
13c | Describe any methods used to tabulate or visually display results of individual studies and syntheses. | N/A | |
13d | Describe any methods used to synthesize results and provide a rationale for the choice(s). If meta-analysis was performed, describe the model(s), method(s) to identify the presence and extent of statistical heterogeneity, and software package(s) used. | N/A | |
13e | Describe any methods used to explore possible causes of heterogeneity among study results (e.g., subgroup analysis, meta-regression). | N/A | |
13f | Describe any sensitivity analyses conducted to assess robustness of the synthesized results. | N/A | |
Reporting bias assessment | 14 | Describe any methods used to assess risk of bias due to missing results in a synthesis (arising from reporting biases). | N/A |
Certainty assessment | 15 | Describe any methods used to assess certainty (or confidence) in the body of evidence for an outcome. | N/A |
RESULTS | |||
Study selection | 16a | Describe the results of the search and selection process, from the number of records identified in the search to the number of studies included in the review, ideally using a flow diagram. | 136–142 |
16b | Cite studies that might appear to meet the inclusion criteria, but which were excluded, and explain why they were excluded. | N/A | |
Study characteristics | 17 | Cite each included study and present its characteristics. | 151–154 |
Risk of bias in studies | 18 | Present assessments of risk of bias for each included study. | 405 |
Results of individual studies | 19 | For all outcomes, present, for each study: (a) summary statistics for each group (where appropriate) and (b) an effect estimate and its precision (e.g., confidence/credible interval), ideally using structured tables or plots. | 143–147 |
Results of syntheses | 20a | For each synthesis, briefly summarise the characteristics and risk of bias among contributing studies. | N/A |
20b | Present results of all statistical syntheses conducted. If meta-analysis was done, present for each the summary estimate and its precision (e.g., confidence/credible interval) and measures of statistical heterogeneity. If comparing groups, describe the direction of the effect. | 212–217 | |
20c | Present results of all investigations of possible causes of heterogeneity among study results. | N/A | |
20d | Present results of all sensitivity analyses conducted to assess the robustness of the synthesized results. | N/A | |
Reporting biases | 21 | Present assessments of risk of bias due to missing results (arising from reporting biases) for each synthesis assessed. | N/A |
Certainty of evidence | 22 | Present assessments of certainty (or confidence) in the body of evidence for each outcome assessed. | N/A |
DISCUSSION | |||
Discussion | 23a | Provide a general interpretation of the results in the context of other evidence. | 223–250 |
23b | Discuss any limitations of the evidence included in the review. | N/A | |
23c | Discuss any limitations of the review processes used. | 276–282 | |
23d | Discuss implications of the results for practice, policy, and future research. | 284–290 | |
OTHER INFORMATION | |||
Registration and protocol | 24a | Provide registration information for the review, including register name and registration number, or state that the review was not registered. | 81–84 |
24b | Indicate where the review protocol can be accessed, or state that a protocol was not prepared. | 81–84 | |
24c | Describe and explain any amendments to information provided at registration or in the protocol. | 81–84 | |
Support | 25 | Describe sources of financial or non-financial support for the review, and the role of the funders or sponsors in the review. | 297–302 |
Competing interests | 26 | Declare any competing interests of review authors. | 307 |
Availability of data, code and other materials | 27 | Report which of the following are publicly available and where they can be found: template data collection forms; data extracted from included studies; data used for all analyses; analytic code; any other materials used in the review. | 291–292; 306 |
References
- Warmerdam, E.; Romijnders, R.; Hansen, C.; Elshehabi, M.; Zimmermann, M.; Metzger, F.G.; von Thaler, A.-K.; Berg, D.; Schmidt, G.; Maetzler, W. Arm swing responsiveness to dopaminergic medication in Parkinson’s disease depends on task complexity. NPJ Park. Dis. 2021, 7, 89. [Google Scholar] [CrossRef] [PubMed]
- Aarsland, D.; Batzu, L.; Halliday, G.M.; Geurtsen, G.J.; Ballard, C.; Chaudhuri, K.R.; Weintraub, D. Parkinson disease-associated cognitive impairment. Nat. Rev. Dis. Prim. 2021, 7, 47. [Google Scholar] [CrossRef] [PubMed]
- Hong, M.; Earhart, G.M. Effects of medication on turning deficits in individuals with Parkinson’s disease. J. Neurol. Phys. Ther. 2010, 34, 11–16. [Google Scholar] [CrossRef] [Green Version]
- Bernhard, F.P.; Sartor, J.; Bettecken, K.; Hobert, M.A.; Arnold, C.; Weber, Y.G.; Poli, S.; Margraf, N.G.; Schlenstedt, C.; Hansen, C.; et al. Wearables for gait and balance assessment in the neurological ward—Study design and first results of a prospective cross-sectional feasibility study with 384 inpatients. BMC Neurol. 2018, 18, 114. [Google Scholar] [CrossRef]
- Bloem, B.R.; Beckley, D.J.; van Dijk, J.G.; Zwinderman, A.H.; Remler, M.P.; Roos, R.A.C. Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov. Disord. 1996, 11, 509–521. [Google Scholar] [CrossRef] [PubMed]
- Zach, H.; Dirkx, M.; Pasman, J.W.; Bloem, B.R.; Helmich, R. The patient’s perspective: The effect of levodopa on Parkinson symptoms. Park. Relat. Disord. 2017, 35, 48–54. [Google Scholar] [CrossRef] [PubMed]
- Curtze, C.; Nutt, J.G.; Carlson-Kuhta, P.; Mancini, M.; Horak, F.B. Levodopa is a double-edged sword for balance and gait in people with Parkinson’s disease. Mov. Disord. 2015, 30, 1361–1370. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Marxreiter, F.; Gaßner, H.; Borozdina, O.; Barth, J.; Kohl, Z.; Schlachetzki, J.C.M.; Thun-Hohenstein, C.; Volc, D.; Eskofier, B.M.; Winkler, J.; et al. Sensor-based gait analysis of individualized improvement during apomorphine titration in Parkinson’s disease. J. Neurol. 2018, 265, 2656–2665. [Google Scholar] [CrossRef]
- McNeely, M.E.; Duncan, R.P.; Earhart, G.M. Medication improves balance and complex gait performance in Parkinson disease. Gait Posture 2012, 36, 144–148. [Google Scholar] [CrossRef]
- Rochester, L.; Baker, K.; Nieuwboer, A.; Burn, D. Targeting dopa-sensitive and dopa-resistant gait dysfunction in Parkinson’s disease: Selective responses to internal and external cues. Mov. Disord. 2011, 26, 430–435. [Google Scholar] [CrossRef] [PubMed]
- Hackney, M.E.; Earhart, G.M. Effects of dance on balance and gait in severe Parkinson disease: A case study. Disabil. Rehabil. 2010, 32, 679–684. [Google Scholar] [CrossRef] [PubMed]
- Fritz, N.E.; Worstell, A.M.; Kloos, A.D.; Siles, A.B.; White, S.E.; Kegelmeyer, D.A. Backward walking measures are sensitive to age-related changes in mobility and balance. Gait Posture 2013, 37, 593–597. [Google Scholar] [CrossRef] [PubMed]
- Carter, V.; Jain, T.; James, J.; Cornwall, M.; Aldrich, A.; de Heer, H.D. The 3-m Backwards Walk and Retrospective Falls: Diagnostic Accuracy of a Novel Clinical Measure. J. Geriatr. Phys. Ther. 2019, 42, 249–255. [Google Scholar] [CrossRef] [PubMed]
- Elnahhas, A.M.; Elshennawy, S.; Aly, M.G. Effects of backward gait training on balance, gross motor function, and gait in children with cerebral palsy: A systematic review. Clin. Rehabil. 2019, 33, 3–12. [Google Scholar] [CrossRef]
- Abdel-Aziem, A.A.; El-Basatiny, H.M. Effectiveness of backward walking training on walking ability in children with hemiparetic cerebral palsy: A randomized controlled trial. Clin. Rehabil. 2017, 31, 790–797. [Google Scholar] [CrossRef]
- Balasukumaran, T.; Olivier, B.; Ntsiea, M.V. The effectiveness of backward walking as a treatment for people with gait impairments: A systematic review and meta-analysis. Clin. Rehabil. 2019, 33, 171–182. [Google Scholar] [CrossRef]
- Hackney, M.E.; Earhart, G.M. Backward walking in Parkinson’s disease. Mov. Disord. 2009, 24, 218–223. [Google Scholar] [CrossRef]
- Hackney, M.E.; Earhart, G.M. The effects of a secondary task on forward and backward walking in Parkinson’s disease. Neurorehabilit. Neural Repair 2010, 24, 97–106. [Google Scholar] [CrossRef] [Green Version]
- Takakusaki, K. Functional neuroanatomy for posture and gait control. J. Mov. Disord. 2017, 10, 1–17. [Google Scholar] [CrossRef]
- Tseng, I.-J.; Jeng, C.; Yuan, R.-Y. Comparisons of forward and backward gait between poorer and better attention capabilities in early Parkinson’s disease. Gait Posture 2012, 36, 367–371. [Google Scholar] [CrossRef] [PubMed]
- Page, M.J.; Moher, D.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews. BMJ 2021, 372, n160. [Google Scholar] [CrossRef] [PubMed]
- National Institutes of Health. Quality Assessment Tools. 2014. Available online: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools (accessed on 4 September 2022).
- Christofoletti, G.; McNeely, M.E.; Campbell, M.; Duncan, R.P.; Earhart, G.M. Investigation of factors impacting mobility and gait in Parkinson disease. Hum. Mov. Sci. 2016, 49, 308–314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoehn, M.M.; Yahr, M.D. Parkinsonism: Onset, progression, and mortality. Neurology 1967, 17, 427–442. [Google Scholar] [CrossRef] [Green Version]
- Goetz, C.G.; Tilley, B.C.; Shaftman, S.R.; Stebbins, G.T.; Fahn, S.; Martinez-Martin, P.; Poewe, W.; Sampaio, C.; Stern, M.B.; Dodel, R.; et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Mov. Disord. 2008, 23, 2129–2170. [Google Scholar] [CrossRef]
- Folstein, M.F.; Folstein, S.E.; McHugh, P.R. “Mini-Mental State”. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12, 189–198. [Google Scholar] [CrossRef]
- Yogev-Seligmann, G.; Hausdorff, J.M.; Giladi, N. The role of executive function and attention in gait. Mov. Disord. 2008, 23, 329–342. [Google Scholar] [CrossRef] [Green Version]
- Dirnberger, G.; Jahanshahi, M. Executive dysfunction in Parkinson’s disease: A review. J. Neuropsychol. 2013, 7, 193–224. [Google Scholar] [CrossRef]
- Burdick, D.J.; Cholerton, B.; Watson, G.; Siderowf, A.; Trojanowski, J.Q.; Weintraub, D.; Ritz, B.; Rhodes, S.L.; Rausch, R.; Do, S.A.F.; et al. People with Parkinson’s disease and normal MMSE score have a broad range of cognitive performance. Mov. Disord. 2014, 29, 1258–1264. [Google Scholar] [CrossRef] [Green Version]
- Dujardin, K.; Dubois, B.; Tison, F.; Durif, F.; Bourdeix, I.; Pere, J.-J.; Duhamel, A.; EXECUTIVE Study Group. Parkinson’s disease dementia can be easily detected in routine clinical practice. Mov. Disord. 2010, 25, 2769–2776. [Google Scholar] [CrossRef]
- Nóbrega-Sousa, P.; Gobbi, L.T.B.; Orcioli-Silva, D.; da Conceição, N.R.; Beretta, V.S.; Vitório, R. Prefrontal cortex activity during walking: Effects of aging and associations with gait and executive function. Neurorehabilit. Neural Repair 2020, 34, 915–924. [Google Scholar] [CrossRef] [PubMed]
- Gilmore, G.; Gouelle, A.; Adamson, M.B.; Pieterman, M.; Jog, M. Forward and backward walking in Parkinson disease: A factor analysis. Gait Posture 2019, 74, 14–19. [Google Scholar] [CrossRef] [PubMed]
- Edwards, E.M.; Daugherty, A.M.; Nitta, M.; Atalla, M.; Fritz, N.E. Backward walking sensitively detects fallers in persons with multiple sclerosis. Mult. Scler. Relat. Disord. 2020, 45, 102390. [Google Scholar] [CrossRef] [PubMed]
- Toots, A.; Domellöf, M.E.; Lundin-Olsson, L.; Gustafson, Y.; Rosendahl, E. Backward relative to forward walking speed and falls in older adults with dementia. Gait Posture 2022, 96, 60–66. [Google Scholar] [CrossRef] [PubMed]
- Michaelsen, S.M.; Ovando, A.C.; Romaguera, F.; Ada, L. Effect of backward walking treadmill training on walking capacity after Stroke: A randomized clinical trial. Int. J. Stroke 2014, 9, 529–532. [Google Scholar] [CrossRef]
- Foster, H.; DeMark, L.; Spigel, P.M.; Rose, D.K.; Fox, E.J. The effects of backward walking training on balance and mobility in an individual with chronic incomplete spinal cord injury: A case report. Physiother. Theory Pract. 2016, 32, 536–545. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Zhang, Y.; Gao, X.; Wu, J.; Jiao, X.; Zhao, J.; Lv, X. Investigating the role of backward walking therapy in alleviating plantar pressure of patients with diabetic peripheral neuropathy. Arch. Phys. Med. Rehabil. 2014, 95, 832–839. [Google Scholar] [CrossRef]
Study | Tseng et al., 2012 [21] | Christofoletti et al., 2016 [24] |
---|---|---|
Number of PD patients | 22 | 114 |
Number of controls | 42 | - |
Age (ys) (mean ± SD) | 70.5 ± 8.8 | 66.6 ± 9.4 |
Gender Male/Female (n, %) | 11(50)/11(50) | - |
BMI in kg/m2 (mean ± SD) | 23.00 ± 4.31 | - |
Disease duration (ys) (mean ± SD) | 5.09 ± 4.87 | 5.4 ± 4.4 |
H&Y stage (mean ± SD) | 1.5 ± 0.5 | 2.4 ± 0.4 |
MDS-UPDRS-III (mean ± SD) | - | 34.8 ± 10.4 |
MMSE (mean ± SD) | 26.82 ± 3.11 | 28.6 ± 1.4 |
Training trials | Yes, 5 in either each condition | - |
Walking speed | Preferred pace | Preferred speed |
Experimental conditions | N = 2 Forward/backward walking | N = 4 Forward/forward walking with a cognitive task (phonemic listing task using a different letter), forward walking fast as possible, backward walking |
Number of trials per condition | One trial for each condition | 3 |
Walking distance | 5.0 m | 4.8 m |
Collection of gait parameters | 5 m Instrumented GAITRite walkway | 4.8 m GAITRite instrumented walkway |
Rest | Yes. Rest sitting between the audition trial and formal test. | - |
Order randomized | Not reported | Yes |
Other information | Barefoot | - |
Authors | Statistical Analysis | Effect of BW on Gait Parameters |
---|---|---|
Tseng et al., 2012 [21] | Post-hoc test | Speed: PD-P (1): FW: 62.98; BW: 32.69; ↓ 48.09% PD-B (2): FW: 98.78; BW: 63.63; ↓ 35.58% HC-P (3): FW: 86.67; BW: 54.86; ↓ 36.70% HC-B (4): FW: 109.06; BW: 84.65; ↓ 22.38% Interactions: -FW: 1 < 2, 1 < 3, 1 < 4, 3 < 4 -BW: 1 < 2, 1 < 3, 1 < 4, 2 < 4, 3 < 4 Swing phase: PD-P (1): FW: 33.15; BW: 30.36; ↓ 8.42% PD-B (2): FW: 36.65; BW: 34.8; ↓ 5.05% HC-P (3): FW: 36.66; BW: 33.68; ↓ 8.13% HC-B (4): FW: 37.69; BW: 36.82; ↓ 2.31% Interactions: -FW: 1 < 2, 1 < 3, 1 < 4 -BW: 1 < 2, 1 < 3, 1 < 4, 3 < 4 Stride length: PD-P (1): FW: 78.56; BW: 47.87; ↓ 39.07% PD-B (2): FW: 110.85; BW: 75.15; ↓ 32.21% HC-P (3): FW: 102.09; BW: 66.95; ↓ 34.42% HC-B (4): FW: 120.13; BW: 96.96; ↓ 19.29% Interactions: -FW: 1 < 2, 1 < 3, 1 < 4, 3 < 4 -BW: 1 < 2, 1 < 3, 1 < 4, 2 < 4, 3 < 4 |
Christofoletti et al., 2016 [24] | Pearson for parametric variables Spearman for non-parametric variables Regression coefficients | Direction: BW: −0.415 * MDS-UPDRS III: FW: −0.443 *; BW: −0.391 * MDS-UPDRS IV: FW: −0.069; BW: 0.068 Mini-BESTest: FW: 0.664 *; BW: 0.685 * CWIT: FW: −0.380 *; BW: −0.291 * VF: FW: 0.336 *; BW: 0.334 * |
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Share and Cite
Correno, M.B.; Hansen, C.; Chardon, M.; Milane, T.; Bianchini, E.; Vuillerme, N. Association between Backward Walking and Cognition in Parkinson Disease: A Systematic Review. Int. J. Environ. Res. Public Health 2022, 19, 12810. https://doi.org/10.3390/ijerph191912810
Correno MB, Hansen C, Chardon M, Milane T, Bianchini E, Vuillerme N. Association between Backward Walking and Cognition in Parkinson Disease: A Systematic Review. International Journal of Environmental Research and Public Health. 2022; 19(19):12810. https://doi.org/10.3390/ijerph191912810
Chicago/Turabian StyleCorreno, Mathias Baptiste, Clint Hansen, Matthias Chardon, Tracy Milane, Edoardo Bianchini, and Nicolas Vuillerme. 2022. "Association between Backward Walking and Cognition in Parkinson Disease: A Systematic Review" International Journal of Environmental Research and Public Health 19, no. 19: 12810. https://doi.org/10.3390/ijerph191912810