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10.1016@j.gaitpost.2017.10.006

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  R  ESEARCH  A RTICLES Sensory-Challenge Balance Exercises ImproveMultisensory Reweighting in Fall-Prone Older Adults  Leslie K. Allison, PT, PhD, Tim Kiemel, PhD, and John J. Jeka, PhD Background and Purpose:  Multisensory reweighting (MSR)deficits in older adults contribute to fall risk. Sensory-challenge bal-ance exercises may have value for addressing the MSR deficits infall-prone older adults. The purpose of this study was to examine theeffect of sensory-challenge balance exercises on MSR and clinical balance measures in fall-prone older adults. Methods:  Weusedaquasi-experimental,repeated-measures,within-subjects design. Older adults with a history of falls underwent an8-week baseline (control) period. This was followed by an 8-week intervention period that included 16 sensory-challenge balance exer-cise sessions performed with computerized balance training equip-ment. Measurements, taken twice before and once after interven-tion, included laboratory measures of MSR (center of mass gain and  phase,position,andvelocityvariability)andclinicaltests(Activities-specific Balance Confidence Scale, Berg Balance Scale, Sensory Or-ganization Test, Limits of Stability test, and lower extremity strengthand range of motion). Results:  Twenty adults 70 years of age and older with a historyof falls completed all 16 sessions. Significant improvements wereobserved in laboratory-based MSR measures of touch gain (  P   = 0.006)andphase(  P  = 0.05),BergBalanceScale(  P  = 0.002),SensoryOrganization Test (  P  = 0.002), Limits of Stability Test (  P  = 0.001),and lower extremity strength scores (  P   =  0.005). Mean values of vision gain increased more than those for touch gain, but did notreach significance. Discussion and Conclusions:  A balance exercise program specifi-cally targeting multisensory integration mechanisms improved MSR, balance, and lower extremity strength in this mechanistic study.These valuable findings provide the scientific rationale for sensory- Department of Physical Therapy, Winston-Salem State University, Winston-Salem, North Carolina (L.K.A.); Department of Kinesiology, Universityof Maryland, College Park (T.K.); and Department of Kinesiology and Applied Physiology, University of Delaware, Newark, Delaware (J.J.J.).Preliminary findings were presented at the Combined Sections Meeting of theAmericanPhysicalTherapyAssociation inTampa,Florida,February2003.This research was supported by a grant from The Erickson Foundation.The authors declare no conflict of interest.Supplemental digital content is available for this article. Direct URL citationsappear in the printed text and are provided in the HTML and PDF versionsof this article on the journal’s Web site (www.jnpt.org). Correspondence:  Leslie K. Allison, PT, PhD, Department of Physical Ther-apy, School of Health Sciences, Winston-Salem State University, 342 FLAtkins Bldg, 601 S. Martin Luther King Jr Dr, Winston-Salem, NC 27110(allisonlk@wssu.edu).Copyright  C  2018 Academy of Neurologic Physical Therapy, APTA.ISSN: 1557-0576/18/4202-0084DOI: 10.1097/NPT.0000000000000214 challenge balance exercise to improve perception of body positionand motion in space and potential reduction in fall risk. Key words:  exercise, falls, multisensory reweighting, postural control  (  JNPT   2018;42: 84–93) INTRODUCTION F all-prone older adults have multiple risk factors, particu-larlyimbalance. 1,2 Horaketal 3,4 describedaposturalcon-trol model indicating how age- and disease-related changes in postural control system components lead to balance deficitsand falls. One critical component is multisensory reweighting(MSR),anadaptivecentralnervoussystemprocesstoestimate body position and motion in space. 5 - 7 Multisensory reweight-ing of visual, vestibular, and somatosensory inputs allows usto maintain balance as environmental conditions change. 8 - 11 Multisensory reweighting is impaired in healthy older adultsandmoresointhefall-proneelderly. 3,12,13 Healthyolderadultsrapidlyadapttochangingenvironments;fall-proneolderadultsdonot. 3,13 - 22 ImpairedMSRmay,therefore,beassociatedwithincreased fall risk.Balance exercise interventions reduce fall risk. 23 - 26 However, it isnot known which types of balance exercises bestremediate specific balance impairments, nor do we understand the mechanisms by which exercise might mediate changes inoneormorecomponentsoftheposturalcontrolsystem. 27 Thisgap in our knowledge hampers clinical decision making. 28 Sensory-challenge balance exercises contribute to im- proved balance and reduced fall risk. 29,30 Whipple 27 system-atically reviewed 25 balance training studies performed witholderadults.Hefoundthatsuccessfulexerciseinterventionsin-corporate sensorychallenge activities.However,toourknowl-edge, no previous balance exercise intervention studies haverestricted the intervention only to sensory-challenge balanceexercises, excluding dynamic balance exercises, functional balance activities, or other forms of exercise.Because prior studies used various types of balance ex-ercises and other forms of exercise (eg, strengthening, stretch-ing, aerobics) in addition to sensory-challenge exercises, itis not possible to separately assess the potential effects of the sensory challenge exercises. Furthermore, previous stud-ies did not use discriminatory measures of MSR, nor examinewhetherchangesinbalanceandfallriskoccurredconcurrentlywithchangesinMSR.Thesestudiesusedoverallposturalsway Copyright © 2018 Academy of Neurologic Physical Therapy, APTA. Unauthorized reproduction of this article is prohibited. 84  JNPT     Volume 42, April 2018   JNPT     Volume 42, April 2018  Sensory-Challenge Balance Exercises  measuresthatdonotdiscriminatechangesinsensoryreweight-ing from other postural control processes that affect sway. 31 We explored MSR as a specific adaptive balance con-trol mechanism using methods that permitted MSR changesto be explicitly determined. 31,32 Exercises challenged sensoryreweighting abilities by manipulating surface and visual con-ditions such that MSR would benefit postural stability. The purposes of this study were to (1) measure whether sensory-challenge exercises influenced MSR and (2) determinewhether MSR changes were associated with improvementsin clinical measures of balance and fall risk. Other influential postural control system components were also measured toisolate MSR contributions to changes in balance and fall risk. METHODSDesign We used a quasi-experimental, repeated-measures,within-subjects design in which participants served as their own controls. All tests were performed 3 times: pretest 1, pretest 2, and posttest. One 8-week no-training control period (between pretests 1 and 2) and one 8-week training period (between pretest 2 and posttest) were provided. Participants Adults 70 years of age and older with a history of fallsin the prior year were recruited from a congregate retirementcommunity. A fall was defined as an event resulting in a person coming to rest inadvertently on the ground, floor, or other lower level. 33 Volunteers were screened via an eligibil-ity questionnaire, telephone screening, and clinical screening byanexperiencedphysicaltherapist(forexclusioncriteriaand screeningtests,seeSupplementalDigitalContent1,Appendix1, http://links.lww.com/JNPT/A202) The participant recruit-ment, screening, testing, and attrition process is illustrated inFigure 1.This study was approved by the Institutional ReviewBoard at the University of Maryland, College Park. Writtenconsent was obtained from all participants according to theguidelines proscribed by the Institutional Review Board at theUniversity. Outcome Measures Laboratory MSR Assessment The MSR experimental paradigm (Figure 2) has been previouslydescribed. 31,34 Briefly,participantsstoodinfrontof a large rear-projection screen on a force plate (Kistler Instru-ment Corp, Amherst, New York) in a modified tandem stance.The narrowed stance induced mild instability to heighten theneed for attention to sensory inputs. They wore goggles limit-ing their peripheral vision. Participants lightly touched a fin-gertip force plate, located at hip height on the right side. Thisforce plate sounded an alarm if the touch force exceeded 1 N.Bothvisualandtouchmotionstimulioscillatedmediolaterally.Medial-lateral center of mass (COM) motion wasapproximated using an ultrasound position tracking system(Logitech, Inc, Fremont, California). A posterior trackingsensorwasattached toawaistbelt.Participantsworeaharnessattached to the ceiling with slack straps to permit postural Figure 1.  Flowchart of participant recruitment, testing, andattrition. sway but prevent a fall. An assistant stood close behind each participant. Data were sampled at 50 Hz.Postural sway measures in the time domain (Figure 3)were converted to the frequency domain (Figure 4) to allowthe discrimination of postural response adaptations to separatevisual and touch stimuli. Each sensory motion input stimuluswas provided at a different frequency. The visual display and fingertip touch plate were simultaneously oscillated mediolat-erallyat0.20and0.28Hz,respectively.Thepeakamplitudesof the 2 stimuli were varied such that across 5 conditions, touchmotion amplitude declined while visual motion amplitude in-creased (see Table 1).Participants performed 3 trials in each of the 5 con-ditions (15 total). Trial duration was 120 s, with the order of trials pseudorandomized within 5-trial blocks. Seated restswere taken between trials. Clinical Assessment To determine whether improvements in MSR were as-sociated with improvements in balance measures associated  Copyright © 2018 Academy of Neurologic Physical Therapy, APTA. Unauthorized reproduction of this article is prohibited. C  2018 Academy of Neurologic Physical Therapy, APTA  85   Allison et al   JNPT     Volume 42, April 2018 Figure 2.  Experimental setup. A participant is illustrated in amodified tandem stance facing the computer-generatedvisual display while lightly contacting the touch surface withher right fingertip. Markers on the occiput and lower lumbar region tracked the trajectories of the head and estimatedcenter of mass, respectively. with fall risk, the Berg Balance Scale (BBS) was used as aglobalbalanceandfall-riskmeasure. 35 - 39 Multipleimpairmentoutcome measures associated with fall risk were also used, in-cluding the Activities-specific Balance Confidence Scale, 38,40 compositebilaterallowerextremityrangeofmotion(goniome-try)andstrength(hand-helddynamometer;ChatillonCSD100,AMETEK, Inc, Largo, Florida), 41 - 44 the Sensory Organiza-tion Test (NeuroCom International, Inc, Clackamas, Oregon,now Natus Medical, Inc, Pleasanton, California), 10 - 13,32,45 - 47 and Limits of Stability Test (NeuroCom International, Inc,Clackamas, Oregon, now Natus Medical, Inc, Pleasanton,California). 30,48 Each of these tests has been shown to bereliable with older adults. Appendix 2 describes these tests(see Supplemental Digital Content 2, Appendix 2, http://links.lww.com/JNPT/A202). All clinical testing was performed byan experienced PT prior to laboratory testing. Intervention Sensory Challenge Balance Exercise Program Participants attended two, 45-minute exercise sessionseach week for 8 weeks. All sessions occurred in an outpatient physical therapy clinic in the congregate retirement commu-nity.One-on-onesessionswereprovidedbytrainers(1physicaltherapist and 2 physical therapist assistants) who were blinded to test results and trained in the exercise protocol by 1 author who is a physical therapist.The exercise program was designed (by author LKA)to improve (1) estimation of body position and motionin space and (2) adaptation to changing sensory envi- Figure 3.  Time series. Three exemplar time series are shown from 1 fall-prone older adult at pretest 1 (top), pretest 2(center), and posttest (bottom). A 125-s segment of data from each test session shows the time series of visual displaymotion at 0.2 Hz (upper trace), mediolateral center of massdisplacement (middle trace), and touch surface motion at0.28 Hz (lower trace). In these exemplars, visual motionamplitude is 4 mm and touch surface motion amplitude is2 mm. ronments (see Supplemental Digital Content 1, Appendix1, http://links.lww.com/JNPT/A202). All exercises were performed on a SMART Balance Master (NeuroCom Inter-national, Inc, Clackamas, Oregon; now Natus Medical, Inc,Pleasanton, California), a computerized balance testing and trainingdevice.Wechosetousethisequipmentbecauseitpro-vides operator-controlled surface and/or visual environmentmotion that can be finely graded up or down in small, quantifi-able increments that are precisely repeatable between sessionsand participants and closely matched to participant ability lev-els. If desired, the equipment also provides visual feedback  Figure 4.  A-E. Amplitude spectra. Five exemplar amplitudespectra are shown for visual display motion (A), touch surfacemotion (B), and center of mass displacements from the same fall-prone older adult in Figure 3 at pretest 1 (C), pretest 2(D), and posttest (E). In these exemplars, visual motionamplitude is 4 mm and touch surface motion amplitude is2 mm. Note the lower posttest center of mass responseamplitudes to the dynamic vision and touch stimuli. Copyright © 2018 Academy of Neurologic Physical Therapy, APTA. Unauthorized reproduction of this article is prohibited. 86  C  2018 Academy of Neurologic Physical Therapy, APTA   JNPT     Volume 42, April 2018  Sensory-Challenge Balance Exercises  Table 1. Sensory Stimulus Motion Amplitudes Across Conditions Sensory StimulusMotion Amplitudes Condition 1 Condition 2 Condition 3 Condition 4 Condition 5Touch, mm  8 4 2 2 2 Vision, mm  2 2 2 4 8 Postural stabilitybenefits from Upweight vision;Downweight touchUpweight vision;Downweight touch Neutral Upweight touch;Downweight visionUpweight touch;Downweight vision about center-of-gravity position and motion to promote earlymotor learning. Participants stood quietly, with instructions toavoid “standing too stiffly, like a soldier”, to achieve maxi-mum stability in each exercise. Stability was challenged by progressively reducing base-of-support size, reducing targetsize to increase the control demand, and making the motionof the support surface and visual surround larger and less predictable.All participants followed the same standardized balanceexercise progression, with the initial exercise difficulty leveladjusted for each participant. Balance exercises became pro-gressively more difficult over the 16 sessions. Visual center of gravity feedback was provided during and weaned over the first 8 training sessions to facilitate the development of correct spatial orientation. Supplemental Digital Content 1,Appendix 3, http://links.lww.com/JNPT/A202, describes the progression of balance exercise tasks and environmental mo-tion conditions and the reduction in visual center of gravityfeedback. Data Analysis Conversion of Data From Time Series to FrequencyDomain Asampletimeseriesofthemedial-lateralCOMposturalsway data and the visual and touch motion stimuli is shownin Figure 3. To represent the same data in the frequencydomain, the amplitude spectrum was computed from the timeseries by taking the absolute value of the Fourier transform(Figure 4A-E).For each sensory input (vision or touch) the mathemati-cal transfer function at the stimulus frequency was calculated  by dividing the transformed COM postural sway by the trans-formed sensory stimulus motion. From each transfer func-tion, we obtained 2 COM motion variables, gain and phase,that together represent how the participant responded to thesensory stimuli motions. Changes in the  sensitivity  and   tim-ing   of the postural sway response to the unique vision/touchmotion frequencies (0.2 Hz/0.28 Hz) were indicated by  gain and   phase  values, respectively. The postural sway response atall frequencies other than the 2 stimulus frequencies is theresidual COM displacement and was used to calculate 2 ad-ditional variables, position variability and velocity variabil-ity. Hence, the 6 dependent variables in the MSR analysiswere vision and touch gain, vision and touch phase, posi-tion variability, and velocity variability. Supplemental DigitalContent 1, Appendix 4, http://links.lww.com/JNPT/A202, de-scribes these measures and the rationale for their inclusion inthis study. Supplemental Digital Content 1, Appendix 5,http://links.lww.com/JNPT/A202, contains a list of definitionsfor many terms used in this article that may or may not befamiliar to the reader. Statistical Analysis All statistical analyses were performed using SPSS Ver-sion 12. Multisensory reweighting gain and phase data wereanalyzed with a Test by Condition (3 × 5) repeated measures(RM) multivariate analysis of variance (MANOVA). Positionvariability and velocity variability were examined separatelywith a Test by Condition (3  ×  5) RM-MANOVA. Each RMMANOVA was followed by planned multiple pairwise com- parisons with Bonferroni correction to  P  ≤ 0.05.DifferencesinscoresfromtheABCScaleandBBSwereanalyzed using Freidman test, with planned multiple pairwisecomparisons performed using related samples paired   t   testswith Bonferroni correction to  P   ≤  0.016. Four compositescores were compiled from the (1) bilateral lower extremityrange of motion, (2) bilateral lower extremity strength mea-sures, (3) the SOT Equilibrium scores, and (4) the LOS Max-imum Excursion scores. These composite scores were exam-ined using a 3  ×  3 (Test by Trainer) RM MANOVA. Unlessotherwise noted, significance was set at 0.05 or less for allanalyses. Nonsignificant results are not reported. RESULTS Of the 33 participants who were enrolled in the study, 20completed all training and testing sessions. Participants had a history of 1 or more unexplained falls within the past year (range: 1-6, mean  =  3). The first stage of screening was aquestionnaire; 95/104 were returned. Thirty-three volunteerswereexcludedatthisstageduetomedicalconditions(N = 23)andmajorpolypharmacy(N = 10).Telephonecallsweremadeto the remaining 62 volunteers; at this stage, 16 volunteers de-clined to participate further. Forty-six volunteers underwentclinical screening, and 13 of these were excluded due to sen-sory loss (N = 11) and frailty (N = 2). Thirty-three fall-proneolderadultswereacceptedintothestudy.Twenty-eightpartici- pants(22female;meanageof83 ± 5years)beganthetraining program and 20 finished all 16 sessions. The primary reasonsreported for discontinuing the study were problems related toage: health status changes (N = 6) and caregiver burden (N = 4). The exercise program was well tolerated, with partici- pantsreportingtemporaryfatigueafterexercisebutnoadverseeffects. Multisensory Reweighting Outcome Measures At all 3 test periods, we saw decreasing vision gainswithincreasingvisualmotionamplitudesandincreasingtouchgains with decreasing touch motion amplitudes (Figure 5AandB).SignificantdifferencesbetweenConditionswerefound  Copyright © 2018 Academy of Neurologic Physical Therapy, APTA. Unauthorized reproduction of this article is prohibited. C  2018 Academy of Neurologic Physical Therapy, APTA  87
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