Responsiveness of Objective vs. Clinical Balance Domain Outcomes for Exercise Intervention in Parkinson's Disease

Naoya Hasegawa, Vrutangkumar V Shah, Graham Harker, Patricia Carlson-Kuhta, John G Nutt, Jodi A Lapidus, Se Hee Jung, Nancy Barlow, Laurie A King, Fay B Horak, Martina Mancini, Naoya Hasegawa, Vrutangkumar V Shah, Graham Harker, Patricia Carlson-Kuhta, John G Nutt, Jodi A Lapidus, Se Hee Jung, Nancy Barlow, Laurie A King, Fay B Horak, Martina Mancini

Abstract

Background: Balance deficits in people with Parkinson's disease (PD) are often not helped by pharmacological or surgical treatment. Although balance exercise intervention has been shown to improve clinical measures of balance, the efficacy of exercise on different, objective balance domains is still unknown. Objective: To compare the sensitivity to change in objective and clinical measures of several different domains of balance and gait following an Agility Boot Camp with Cognitive Challenges (ABC-C) intervention. Methods: In this cross-over, randomized design, 86 individuals with PD participated in 6-week (3×/week) ABC-C exercise classes and 6-week education classes, consisting of 3-6 individuals. Blinded examiners tested people in their practical off state. Objective outcome measures from wearable sensors quantified four domains of balance: sway in standing balance, anticipatory postural adjustments (APAs) during step initiation, postural responses to the push-and-release test, and a 2-min natural speed walk with and without a cognitive task. Clinical outcome measures included the Unified Parkinson's Disease Rating Scale (MDS-UPDRS) Part III, the Mini Balance Evaluation Systems Test (Mini-BESTest), the Activities of Balance Confidence (ABC), and the Parkinson's Disease Questionnaire (PDQ-39). The standardized response means (SRM) of the differences between before and after each intervention compared responsiveness of outcomes to intervention. A linear mixed model compared effects of exercise with the active control-education intervention. Results: The most responsive outcome measures to exercise intervention with an SRM > 0.5 were objective measures of gait and APAs, specifically arm range of motion, gait speed during a dual-task walk, trunk coronal range of motion, foot strike angle, and first-step length at step initiation. The most responsive clinical outcome measure was the patient-reported PDQ-39 activities daily living subscore, but all clinical measures had SRMs <0.5. Conclusions: The objective measures were more sensitive to change after exercise intervention compared to the clinical measures. Spatiotemporal parameters of gait, including gait speed with a dual task, and APAs were the most sensitive objective measures, and perceived functional independence was the most sensitive clinical measure to change after the ABC-C exercise intervention. Future exercise intervention to improve gait and balance in PD should include objective outcome measures.

Keywords: Parkinson's disease; anticipatory postural adjustments; automatic postural responses; clinical measures; exercise; gait; objective measures; wearable technology.

Copyright © 2020 Hasegawa, Shah, Harker, Carlson-Kuhta, Nutt, Lapidus, Jung, Barlow, King, Horak and Mancini.

Figures

Figure 1
Figure 1
Total objective measures 24. Twenty-four sensitive objective measures have been selected to discriminate between people with Parkinson's disease (PD) and healthy elderly in four postural control domains (20). APAs, anticipatory postural adjustments; APRs, automatic postural responses; ML, mediolateral; AP, anteroposterior; ROM, range of motion; SD, standard deviation.
Figure 2
Figure 2
Significant effects of the Exercise but not Education intervention on objective measures of gait and anticipatory postural adjustments (APAs), but not sway. Mean and standard error of mean (SEM) plots of (A–D) four gait measures and (E,F) two balance measures. (A) Foot strike angle, (B) Arm range of motion (ROM), and (C) trunk coronal ROM, (D) gait speed during a dual-task walk (DT), (E) anticipatory postural adjustments (APAs) involving first-step ROM at step initiation during a single-task walk (ST), and (F) root mean square (RMS) of medio-lateral (ML) sway while standing on a foam surface with eyes open (EOFoam). Plots divide results into the randomized Exercise First and Education First groups with Exercise intervention in red and Education intervention in blue. Histograms summarize the change in each measure before vs. after the Education and Exercise intervention. Error bar shows SEM, and p-value was calculated by a linear mixed model.
Figure 3
Figure 3
Effect size of the (A) objective measure and (B) clinical measure after the ABC-C Intervention (square) and Education intervention (star). All of the plots are displayed in descending order of the difference of standardized response means (SRM) between for the education and Agility Boot Camp with Cognitive Challenges (ABC-C) intervention.

References

    1. Park JH, Kang YJ, Horak FB. What is wrong with balance in Parkinson's disease? J Mov Disord. (2015) 8:109–14. 10.14802/jmd.15018
    1. Schoneburg B, Mancini M, Horak F, Nutt JG. Framework for understanding balance dysfunction in Parkinson's disease. Mov Disord. (2013) 28:1474–82. 10.1002/mds.25613
    1. Tomlinson CL, Patel S, Meek C, Herd CP, Clarke CE, Stowe R, et al. . Physiotherapy intervention in Parkinson's disease: systematic review and meta-analysis. BMJ. (2012) 345:e5004. 10.1136/bmj.e5004
    1. Shen X, Wong-Yu IS, Mak MK. Effects of exercise on falls, balance, and gait ability in Parkinson's disease: a meta-analysis. Neurorehabil Neural Repair. (2016) 30:512–27. 10.1177/1545968315613447
    1. Berg KO, Maki BE, Williams JI, Holliday PJ, Wood-Dauphinee SL. Clinical and laboratory measures of postural balance in an elderly population. Arch Phys Med Rehabil. (1992) 73:1073–80.
    1. Mancini M, Horak FB. The relevance of clinical balance assessment tools to differentiate balance deficits. Eur J Phys Rehabil Med. (2010) 46:239–48.
    1. Franchignoni F, Horak F, Godi M, Nardone A, Giordano A. Using psychometric techniques to improve the Balance Evaluation Systems Test: the mini-BESTest. J Rehabil Med. (2010) 42:323–31. 10.2340/16501977-0537
    1. Ortiz-Rubio A, Cabrera-Martos I, Torres-Sánchez I, Casilda-López J, López-López L, Valenza MC. Effects of a resistance training program on balance and fatigue perception in patients with Parkinson's disease: a randomized controlled trial. Med Clin (Barc). (2018) 150:460–4. 10.1016/j.medcli.2017.10.022
    1. Jaeschke R, Singer J, Guyatt GH. Measurement of health status. Ascertaining the minimal clinically important difference. Control Clin Trials. (1989) 10:407–15. 10.1016/0197-2456(89)90005-6
    1. King LA, Salarian A, Mancini M, Priest KC, Nutt J, Serdar A, et al. . Exploring outcome measures for exercise intervention in people with Parkinson's disease. Parkinsons Dis. (2013) 2013:572134. 10.1155/2013/572134
    1. Zampieri C, Salarian A, Carlson-Kuhta P, Aminian K, Nutt JG, Horak FB. The instrumented timed up and go test: potential outcome measure for disease modifying therapies in Parkinson's disease. J Neurol Neurosurg Psychiatry. (2010) 81:171–6. 10.1136/jnnp.2009.173740
    1. Sprager S, Juric MB. Inertial sensor-based gait recognition: a review. Sensors (Basel). (2015) 15:22089–127. 10.3390/s150922089
    1. Horak FB, Mancini M. Objective biomarkers of balance and gait for Parkinson's disease using body-worn sensors. Mov Disord. (2013) 28:1544–51. 10.1002/mds.25684
    1. El-Gohary M, Peterson D, Gera G, Horak FB, Huisinga JM. Validity of the instrumented push and release test to quantify postural responses in persons with multiple sclerosis. Arch Phys Med Rehabil. (2017) 98:1325–31. 10.1016/j.apmr.2017.01.030
    1. Mancini M, Salarian A, Carlson-Kuhta P, Zampieri C, King L, Chiari L, et al. . ISway: a sensitive, valid and reliable measure of postural control. J Neuroeng Rehabil. (2012) 9:59. 10.1186/1743-0003-9-59
    1. Mancini M, King L, Salarian A, Holmstrom L, McNames J, Horak FB. Mobility lab to assess balance and gait with synchronized body-worn sensors. J Bioeng Biomed Sci. (2011) Suppl 1:7. 10.4172/2155-9538.S1-007
    1. Curtze C, Nutt JG, Carlson-Kuhta P, Mancini M, Horak FB. Levodopa is a double-edged sword for balance and gait in people with Parkinson's disease. Mov Disord. (2015) 30:1361–70. 10.1002/mds.26269
    1. Rawson KS, McNeely ME, Duncan RP, Pickett KA, Perlmutter JS, Earhart GM. Exercise and Parkinson disease: comparing tango, treadmill, and stretching. J Neurol Phys Ther. (2019) 43:26–32. 10.1097/NPT.0000000000000245
    1. Capato TTC, de Vries NM, IntHout J, Barbosa ER, Nonnekes J, Bloem BR. Multimodal balance training supported by rhythmical auditory stimuli in Parkinson's disease: a randomized clinical trial. J Parkinsons Dis. (2020) 10:333–46. 10.3233/JPD-191752
    1. Jung SH, Hasegawa N, King L, Carlson-Kuhta P, Smulders K, Peterson D, et al. Effects of the agility boot camp with cognitive challenge (ABC-C) exercise program for Parkinson's disease. NPJ Parkinsons Dis. (2020).
    1. King LA, Peterson DS, Mancini M, Carlson-Kuhta P, Fling BW, Smulders K, et al. . Do cognitive measures and brain circuitry predict outcomes of exercise in Parkinson Disease: a randomized clinical trial. BMC Neurol. (2015) 15:218. 10.1186/s12883-015-0474-2
    1. King LA, Mancini M, Smulders K, Harker G, Lapidus JA, Ramsey K, et al. . Cognitively challenging agility boot camp program for freezing of gait in Parkinson disease. Neurorehabil Neural Repair. (2020) 34:417–7. 10.1177/1545968320909331
    1. Peterson DS, King LA, Cohen RG, Horak FB. Cognitive contributions to freezing of gait in parkinson disease: implications for physical rehabilitation. Phys Ther. (2016) 96:659–70. 10.2522/ptj.20140603
    1. Hasegawa N, Shah VV, Carlson-Kuhta P, Nutt JG, Horak FB, Mancini M. How to select balance measures sensitive to Parkinson's disease from body-worn inertial sensors-separating the trees from the forest. Sensors (Basel). (2019) 19:E3320. 10.3390/s19153320
    1. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. (1992) 55:181–4. 10.1136/jnnp.55.3.181
    1. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, 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) 23:2129–70. 10.1002/mds.22340
    1. Powell LE, Myers AM. The activities- specific balance confidence (ABC) scale. J Gerontol A Biol Sci Med Sci. (1995) 50:M28–M34. 10.1093/gerona/50A.1.M28
    1. Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, et al. . The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. (2005) 53:695–9. 10.1111/j.1532-5415.2005.53221.x
    1. Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, et al. . Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson's disease and their carers. Gait Posture. (2009) 30:459–63. 10.1016/j.gaitpost.2009.07.108
    1. Jenkinson C, Fitzpatrick R, Peto V, Greenhall R, Hyman N. The Parkinson's disease questionnaire (PDQ-39): development and validation of a Parkinson's disease summary index score. Age Ageing. (1997) 26:353–7. 10.1093/ageing/26.5.353
    1. Farley BG, Koshland GF. Training BIG to move faster: the application of the speed-amplitude relation as a rehabilitation strategy for people with Parkinson's disease. Exp Brain Res. (2005) 167:462–7. 10.1007/s00221-005-0179-7
    1. Li F, Harmer P, Fitzgerald K. Implementing an evidence-based fall prevention intervention in community senior centers. Am J Public Health. (2016) 106:2026–31. 10.2105/AJPH.2016.303386
    1. Cohen J. Statistical Power Analysis for the Behavioural Sciences. 2nd ed Hillsdales, NJ: Lawrence Erlbaum; (1988).
    1. Revicki D, Hays RD, Cella D, Sloan J. Recommended methods for determining responsiveness and minimally important differences for patient-reported outcomes. J Clin Epidemiol. (2008) 61:102–9. 10.1016/j.jclinepi.2007.03.012
    1. Hauser RA, Auinger P; Parkinson Study Group. Determination of minimal clinically important change in early and advanced Parkinson's disease. Mov Disord. (2011) 26:813–8. 10.1002/mds.23638
    1. Rice ME, Harris GT. Comparing effect sizes in follow-up studies: ROC Area, Cohen's d, and r. Law Hum Behav. (2005) 29:615–20. 10.1007/s10979-005-6832-7
    1. King LA, Wilhelm J, Chen Y, Blehm R, Nutt J, Chen Z, et al. . Effects of group, individual, and home exercise in persons with Parkinson disease: a randomized clinical trial. J Neurol Phys Ther. (2015) 39:204–12. 10.1097/NPT.0000000000000101
    1. Mellone S, Mancini M, King LA, Horak FB, Chiari L. The quality of turning in Parkinson's disease: a compensatory strategy to prevent postural instability? J Neuroeng Rehabil. (2016) 13:39. 10.1186/s12984-016-0147-4
    1. Jöbges M, Heuschkel G, Pretzel C, Illhardt C, Renner C, Hummelsheim H. Repetitive training of compensatory steps: a therapeutic approach for postural instability in Parkinson's disease. J Neurol Neurosurg Psychiatry. (2004) 75:1682–7. 10.1136/jnnp.2003.016550
    1. Peterson DS, Horak FB. The effect of levodopa on improvements in protective stepping in People With Parkinson's disease. Neurorehabil Neural Repair. (2016) 30:931–40. 10.1177/1545968316648669
    1. Gaßner H, Steib S, Klamroth S, Pasluosta CF, Adler W, Eskofier BM, et al. . Perturbation treadmill training improves clinical characteristics of gait and balance in Parkinson's disease. J Parkinsons Dis. (2019) 9:413–26. 10.3233/JPD-181534
    1. Handelzalts S, Kenner-Furman M, Gray G, Soroker N, Shani G, Melzer I. Effects of perturbation-based balance training in subacute persons with stroke: a randomized controlled trial. Neurorehabil Neural Repair. (2019) 33:213–24. 10.1177/1545968319829453
    1. Fitzpatrick R, Norquist JM, Jenkinson C. Distribution-based criteria for change in health-related quality of life in Parkinson's disease. J Clin Epidemiol. (2004) 57:40–4. 10.1016/j.jclinepi.2003.07.003
    1. Martínez-Martín P, Serrano-Dueñas M, Vaca-Baquero V. Psychometric characteristics of the Parkinson's disease questionnaire (PDQ-39)-Ecuadorian version. Parkinsonism Relat Disord. (2005) 11:297–304. 10.1016/j.parkreldis.2005.02.003
    1. Corcos DM, Robichaud JA, David FJ, Leurgans SE, Vaillancourt DE, Poon C, et al. . A two-year randomized controlled trial of progressive resistance exercise for Parkinson's disease. Mov Disord. (2013) 28:1230–40. 10.1002/mds.25380
    1. Conradsson D, Löfgren N, Nero H, Hagströmer M, Ståhle A, Lökk J, et al. . The effects of highly challenging balance training in elderly with Parkinson's disease: a randomized controlled trial. Neurorehabil Neural Repair. (2015) 29:827–36. 10.1177/1545968314567150
    1. Sparrow D, DeAngelis TR, Hendron K, Thomas CA, Saint-Hilaire M, Ellis T. Highly challenging balance program reduces fall rate in Parkinson disease. J Neurol Phys Ther. (2016) 40:24–30. 10.1097/NPT.0000000000000111
    1. Wallén MB, Hagströmer M, Conradsson D, Sorjonen K, Franzén E. Long-term effects of highly challenging balance training in Parkinson's disease-a randomized controlled trial. Clin Rehabil. (2018) 32:1520–9. 10.1177/0269215518784338
    1. Frazzitta G, Maestri R, Bertotti G, Riboldazzi G, Boveri N, Perini M, et al. . Intensive rehabilitation treatment in early Parkinson's disease: a randomized pilot study with a 2-year follow-up. Neurorehabil Neural Repair. (2015) 29:123–31. 10.1177/1545968314542981

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться