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Older adults with history of falls are unable to perform walking and prehension movements simultaneously

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The aim of this study was to investigate the combined task of walking and prehension with different levels of manual task difficulty in older adults with and without a history of falls.. Ab

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5 N M RINALDIa,b*AND R MORAESb,c

6 a Ribeirao Preto Medical School, University of Sao Paulo, Brazil

7 bResearch Support Center on Chronic-Degenerative

8 Diseases, University of Sao Paulo, Brazil

9 cBiomechanics and Motor Control Lab, School of Physical

10 Education and Sport of Ribeirao Preto, University of Sao Paulo, Brazil

11 Abstract—Older adults have a greater incidence of falls, and

risk of falls will increase when combining two motor tasks.

Thus, it is interesting to investigate the effect of fall history

on motor performance in older adults when combining

walk-ing with another task such as graspwalk-ing an object The aim of

this study was to investigate the combined task of walking

and prehension with different levels of manual task difficulty

in older adults with and without a history of falls Thirty

older adults participated in this study; groups were

desig-nated as fallers ( n = 15) and non-fallers (n = 15)

Partici-pants were asked to reach-to-grasp a dowel during quiet

standing and during walking Level of manual task difficulty

was manipulated by the type of dowel support and obstacles

located at different distances to the sides of the dowel Fall

history influenced the performance of this combined task

for the most difficult manual conditions Fallers were able

to be identified due to differences in the grasping strategies

used while walking compared to non-fallers In addition,

walking and grasping were mutually modulated due to the

level of difficulty of the manual task Ó 2015 Published by

Elsevier Ltd on behalf of IBRO.

Key words: aging, falls, locomotion, prehension, dual task.

12

14 It is estimated that one-third of community-dwelling

15 people aged 65 and older fall every year (O’loughlin

16

et al., 1993; Perracini and Ramos, 2002) Consequently,

17 fall-related injuries are associated with a poorer quality

18

of life due to restricted mobility and functional decline

19 (Tideiksaar, 1996) In addition, one of the major intrinsic

20 risk factors for falls in older adults is deficit in static and

21 dynamic postural control (Verghese et al., 2007)

Impor-22 tantly, more than 50% of falls occur during locomotion

23 (Barak et al., 2006)

24 Older adults with a history of falls (FOA) present some

25 gait impairments (Hausdorff et al., 2001), such as a

26 decrease in stride length and velocity, and an increase in

27 gait variability and double support time (Kirkwood et al.,

28 2011; Toebes et al., 2012) These changes in the walking

29 pattern are even more evident when two motor tasks are

30 combined (Nordin et al., 2010) FOA have a slower swing

31 time and step velocity than older adults without a history of

32 falls in a dual task paradigm (Springer et al., 2006) These

33 results suggest that FOA may have problems switching

34 their attention between two motor tasks due to

neuromus-35 cular problems (Hawkes et al., 2012) The changes in the

36 walking behavior during a dual task paradigm can predict

37 falls in older adults (Beauchet et al., 2009) Moreover,

38 the level of difficulty of the secondary task can also

influ-39 ence how dual-task-related changes are associated with

40

a history of falls (Chu et al., 2013) Nordin et al (2010)

41 investigated, in FOA, gait changes during dual task

condi-42 tions at different levels of difficulty They found that FOA

43 increased their step width in the two most difficult tasks

44 (task 1: carry a saucer with a coffee cup in one hand; task

45 2: perform serial subtractions by three starting from 50)

46 These results indicated the usage of sensory-motor

47 resources in a flexible manner to decrease the risk of falls

48 (i.e., a protective strategy).Hall et al (2011)investigated

49 the impact of cognitive task level of difficulty on walking

50

of FOA FOA reduced gait speed when cognitive task

51 demand increased, suggesting that the more difficult the

52 secondary task is, the greater the impact on gait

perfor-53 mance Furthermore, FOA performed the alphabet and

54 alternate letters tasks more slowly in walking than in the

55 seated condition With an increase in task difficulty, older

56 adults must allocate more attentional resources to walking

57

to compensate for the reduction in sensory-motor control

58 (Stelmach et al., 1990)

59 The combined task of walking and prehension (i.e.,

60 reach-to-grasp) is widely performed during activities of

61 daily life Older adults exhibit smaller peak wrist velocity

62 and greater movement times than young adults when

63 reaching for an object (Roy et al., 1996) Furthermore,

http://dx.doi.org/10.1016/j.neuroscience.2015.12.037

0306-4522/ Ó 2015 Published by Elsevier Ltd on behalf of IBRO.

*Correspondence to: N M Rinaldi, Faculdade de Medicina de

Ribeira˜o Preto, Programa de Po´s-Graduac¸a˜o em Reabilitac¸a˜o e

Desempenho Funcional, Universidade de Sa˜o Paulo, Avenida dos

Bandeirantes, 3900 Ribeira˜o Preto, SP 14049-900, Brazil Tel:

+55-16-3315-0359; fax: +55-16-3315-0551.

E-mail address: narinaldi@yahoo.com.br (N M Rinaldi).

Abbreviations: ANOVAs, analysis of variances; AP, anterior–posterior;

COM, center of mass; FOA, Older adults with a history of falls; HCs,

heel contacts; MDS, margin of dynamic stability; ML, medial–lateral;

MMSE, Mini Mental State Examination; OA, older adults with no history

of falls; SB, stable base; SLD, stable base with obstacles at long; SSD,

stable base with obstacles at short; UB, unstable base; WT, walking

baseline.

Neuroscience xxx (2015) xxx–xxx

1

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64 older adults have reduced tactile sensitivity and,

conse-65 quently, increase the grip force as a compensatory

strat-66 egy (Gorniak et al., 2011) During walking aging has been

67 found to affect prehension.Diermayr et al (2011)

investi-68 gated the aging effects on grasp control when walking and

69 transporting an object They found an increase in grip

70 force while walking, indicating a decline in manual

dexter-71 ity while performing functional tasks

72 Interestingly,Delbaere et al (2004)found that walking

73 and reaching are the most avoided tasks in older adults

74 with fear of falling When reaching for an object in an

75 upright position older adults adopted a hip strategy to

per-76 form the task, which is different than that of young adults

77 who preferred an ankle strategy (Delbaere et al., 2004)

78 Additionally, Huang and Brown (2015) found that older

79 adults showed a larger center of pressure excursions

80 compared to young individuals when combining upright

81 stance with reach-to-grasp These different strategies

82 are likely to compensate for constraints in balance-related

83 functions Thus, it becomes interesting to combine these

84 two tasks because they have the potential to challenge

85 dynamic stability due to mechanical constraints and, at

86 the same time, increase cognitive load because this

com-87 bined task is also a dual task

88 Many studies have investigated the interference of

89 motor/cognitive tasks on walking and the relationship to

90 fall risk in older adults (Menant et al., 2014) However,

91 most of these studies involving dual task paradigms and

92 FOA investigated primarily the main task (i.e., walking)

93 (Beauchet et al., 2009) Recently, we found modifications

94 in walking and prehension when combining these two

95 tasks in young adults (Rinaldi and Moraes, 2015) We

96 suggested that prehension was superimposed on gait,

97 although the adaptations in motor behavior were global

98 because both motor patterns were modified to guarantee

99 the execution of prehension with different levels of

diffi-100 culty while walking without stopping Then, in this context

101 of dual task and falls, it is important to analyze both tasks

102 to investigate the level of interference between these two

103 motor tasks in FOA Possible changes in the prehension

104 control, such as, reduced movement time, wrist velocity

105 and grip aperture velocity could be related to changes in

106 walking control Changes in gait stability could be part of

107 a compensatory strategy to accommodate the control of

108 upper body movements toward an object in FOA

Further-109 more, this combined motor task is different from other

110 dual task paradigms in the literature (Yamada et al.,

111 2011), because most studies have older adults perform

112 the secondary task during the entire pathway (e.g.,

carry-113 ing a tray) Thus, they do not need to change their motor

114 strategy to perform the secondary task, since they could

115 preprogram their movement from the beginning of the

116 walking task However, to perform daily life activities,

117 older adults are required to change their walking patterns

118 to accommodate other tasks (e.g., prehension) Based on

119 these assumptions, our combined motor task can

con-120 tribute to investigate the motor strategies used by FOA

121 when they have to disrupt the walking pattern to

superim-122 pose a voluntary, discrete task

123 Based on these considerations, this study presents two

124 main research questions: (1) what are the changes in

125 prehension and walking when these tasks are combined

126

in FOA? (2) Do these changes occur as a function of the

127 manual task difficulty? To answer these questions, we

128 analyzed variables based on whole body center of mass

129 (COM) (including stability measures) and spatiotemporal

130 gait parameters to describe the possible changes in

131 walking of the FOA due to manual task difficulty We

132 analyzed two steps before object grasping to investigate

133 the changes in walking during the approach phase In

134 relation to reach-to-grasp, we analyzed the reaching and

135 grasping components, such as reaching duration and

136 velocity, and hand grip aperture and velocity We also

137 investigated prehension variables in the upright stance to

138 identify changes in reach-to-grasp due to the addition of

139 walking Therefore, the aim of this study was to

140 investigate the combined task of walking and prehension

141 with different levels of manual task difficulty in older

142 adults with and without a history of falls

143 EXPERIMENTAL PROCEDURES

144 Participants

145 Thirty individuals participated in this study They were

146 distributed in two groups (n = 15): older adults with no

147 history of falls (OA) (15 females); older adults who

148 experienced at least one fall in the 12-month period

149 prior to data collection (FOA) (15 females) Participants

150 were screened before starting the experimental task by

151 filling out a clinical questionnaire to check the history of

152 falls, health status, physical activity level (Baecke)

153 (Voorrips et al., 1991), cognitive function (Mini Mental

154 State Examination, MMSE) (Folstein et al., 1975) and

bal-155 ance performance (Mini-BESTest) (Maia et al., 2013)

156 Participants were excluded if they had cognitive

impair-157 ment (<24 points in the MMSE), vestibular dysfunction,

158 and/or if they were unable to walk without assistance

159

We invited participants through local media (newspaper,

160 television and radio) Forty-eight older adults returned to

161 our invitation We did an initial contact by phone and we

162 asked them whether or not they experienced a fall in the

163 last 12 months, after explaining to them that a fall was

164

an event in which they came to the ground or to some

165 lower level unintentionally, regardless of the

conse-166 quences of the fall After this screening, 28 older adults

167 reported a recent history of fall and 20 older adults did

168 not experience a fall in the last 12 months However,

169 regarding the FOA, seven individuals did not attend to

170 the inclusion criteria (visual problem [n = 1] and use of

171 assistive devices [n = 6]) Yet, six individuals refused to

172 participate in the study For the OA, five individuals did

173 not attend to the inclusion criteria (neurological disorders

174 [n = 3] and musculoskeletal problems [n = 2])

175 All participants had normal or corrected-to-normal

176 vision and no neurological/musculoskeletal disorders

177 that would affect task performance The local ethics

178 committee approved all procedures and participants

179 signed a consent form before starting the experiment

180 Experimental protocol

181 For data collection, we used an 8-camera motion analysis

182 system (MX-T40S, Vicon) with a sampling rate of 100 Hz

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183 Passive reflective markers were placed on participants’

184 skin at predefined landmarks according to the

Plug-in-185 Gait Full Body model (Vicon) and two markers were

186 placed on the index finger and thumb, respectively

187 Moreover, we positioned two video cameras (Bonita,

188 Vicon) in front of and on the left side of the participants

189 We used the video camera images to determine dowel

190 contact (visual inspection), defined as the first contact of

191 the fingers with the dowel

192 Participants performed two experimental tasks:

193 reaching-to-grasping a dowel (a wood cylinder,

194 diameter: 4.5 cm, height: 10 cm, mass: 105 g) during

195 quiet standing (stationary) and during walking We

196 positioned the dowel on the top of a base made of wood

197 and placed over a support located approximately 3 m

198 from the starting position We adjusted the height of the

199 support to height of the participants’ greater trochanter

200 We positioned the support on the right side of the

201 walkway, with a distance corresponding to 50% of the

202 participants’ right arm length This distance was also

203 used for the stationary task and, in this task,

204 participants stood behind the object at a distance of

205 30% of their right upper limb length The base of the

206 dowel could be stable (wide base) and unstable (narrow

207 base) We made the manual task more difficult by

208 placing the dowel between two wooden obstacles such

209 that for each type of support there were three obstacle

210 conditions: no obstacle, short distance, and long

211 distance The short and long distances of the obstacles

212 corresponded to three and five times the right hand

213 thickness, respectively The combination of type of base

214 and obstacle resulted in six grasping conditions: stable

215 (SB) and unstable (UB) bases without obstacles, stable

216 base with obstacles at short (SSD) and long (SLD)

217 distances, and unstable base with obstacles at short

218 (USD) and long (ULD) distances (Fig 1) Participants

219 also performed a baseline walking condition (WT)

220 without grasping (control condition) More details about

221 the experimental procedures are available in our

222 previous study (Rinaldi and Moraes, 2015)

223 We asked participants to reach-to-grasp the dowel as

224 they walked, without stopping, at a self-selected speed

225 After grasping the dowel, participants were instructed to

226 hold it and walk normally until the end of the pathway

227 For the stationary task, we instructed them to stand as

228 quietly as possible In both tasks, participants were not

229 allowed to contact the obstacles and knock down the

230 support Participants performed 21 trials for the walking

231 task, and 18 trials for the stationary task We collected

232 these tasks in separate blocks and counterbalanced

233 them within each group Trials were completely

234 randomized within each block We repeated those trials

235 with errors at the end of each block without participants’

236 awareness

237 Data analysis

238 The tridimensional coordinates of the individual markers

239 were digitally filtered using a 4th-order Butterworth filter

240 with a 6-Hz cut-off frequency For the walking task, all

241 variables were calculated for the step at the period of

242 contact with the dowel (N) and two steps before contact

243 (N-2 and N-1) to verify possible gait adjustments during

244 the approach phase For the WT condition, the dowel

245 was kept on the support to use as a reference to

246 identify the region corresponding to steps N-2, N-1,

247 and N

248 Spatiotemporal gait parameters Step width and step

249 length were calculated as the absolute difference

250 between heel markers of the right and left feet at

251 subsequent heel contacts (HCs) in each direction,

252 medial–lateral (ML) and anterior–posterior (AP),

253 respectively Step duration corresponded to the frame

254 difference between each HC divided by the sampling

255 frequency The division of step length by step duration

256 resulted in step velocity

257 COM variables and margin of dynamic stability (MDS)

258 Nexus software (Vicon) computed the tridimensional

259 COM coordinates based on the tridimensional

260 coordinates of the 39 markers, which defined a

261 15-segment model (Winter, 2005) COM velocity

corre-262 sponded to the first derivative of the COM position

263 (central difference procedure) We identified the minimum

264 COM AP velocity during the approach phase until dowel

265 contact for all walking conditions After that, we computed

266 the percentage of COM AP velocity reduction as the

dif-267 ference between minimum COM AP velocity in the WT

268 condition and in the walking combined with prehension

269 conditions (Fig 3A) We also calculated the temporal

dif-270 ference between the time of dowel contact and minimum

271 COM AP velocity (Fig 3A)

272 For the computation of the MDS, we first calculated

273 the extrapolated COM position (XcoM) (Hof et al.,

274

2005) Based on XcoM, MDS was calculated according

275

toRinaldi and Moraes (2015), where metatarsal and heel

276 markers on both feet were used to define the outside

277 boundaries of the foot (foot edge) in the AP and ML

direc-278 tions We calculated the MDS by the difference between

279 foot edge and XcoM position (AP and ML directions) A

280 positive value for the MDS indicates that XcoM is located

281 before the foot edge and the system is dynamically stable

282 Reaching-to-grasping variables We used the interval

283 between reaching onset and dowel contact to calculate

284 the reach-to-grasp variables The methods used to

285 detect reaching onset for walking and stationary tasks

286 were the same as the ones used byRinaldi and Moraes

287 (2015) The reaching variables analyzed were: movement

288 time (temporal difference between reaching onset and

289 dowel contact), peak wrist velocity (maximum value

290 obtained in the resultant wrist velocity curve), and

time-291 to-peak wrist velocity (time of occurrence of the peak wrist

292 velocity adjusted to movement time, %) The peak wrist

293 velocity was calculated based on the relative position of

294 the right wrist to the right iliac crest (i.e., relative to the

295 person’s body position in space, as used by Carnahan

296

et al (1996)) The grasping variables analyzed were:

297 peak grip aperture (maximum distance between the

mark-298 ers on thumb and index finger), time-to-peak grip aperture

299 (time of occurrence of peak grip aperture adjusted to

300 movement time, %), peak grip aperture velocity

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(maxi-301 mum value obtained in the resultant velocity curve of the

302 distance thumb-finger, which was determined as the first

303 derivative of the thumb-finger distance), and time-to-peak

304 grip aperture velocity (time of occurrence of peak grip

305 aperture velocity adjusted to movement time, %)

306 We also analyzed the relationship between reaching

307 onset and gait events For that, we calculated the

308 temporal difference between the last right HC before

309 dowel contact and reaching onset Negative values

310 indicated that the participant touched the ground before

311 starting the reaching movement

312 Statistical analysis

313 One-way analysis of variances (ANOVAs) were

314 computed to compare age, anthropometric (height and

Fig 1 (A) Transverse view of the experimental set-up for the walking and stationary tasks It shows the three steps (N-2, N-1, and N) selected for data analysis and dowel’s location for walking and stationary tasks (B) Illustration of the six prehension conditions Dowel is shown in white, obstacles in black and base in gray colors ( Rinaldi and Moraes, 2015 ).

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315 body mass) and clinical characteristics (MMSE,

Mini-316 BESTest, and Baecke scores) between groups For the

317 remaining data, five MANOVAs and three ANOVAs

318 were performed Three-way MANOVAs (group [FOA,

319 OA] conditions [SB, SLD, SSD, UB, ULD, USD,

320 WT] step [N-2, N-1, N]) with repeated measures in the

321 last two factors were carried out for the following set of

322 dependent variables: (1) step length and step width; (2)

323 step duration and step velocity; and (3) MDS in the AP

324 and ML directions Two-way ANOVAs (group

325 conditions) with repeated measures for the last factor

326 were carried out for the following dependent variables:

327 (1) temporal difference between HC and reaching onset;

328 (2) temporal difference between dowel contact and

329 minimum COM AP velocity; and (3) AP velocity

330 reduction For reaching and grasping variables, two

331 three-way MANOVAs were calculated (group

332 conditions [SB, SLD, SSD, UB, ULD, USD] task

333 [walking and stationary]) with repeated measures in the

334 last two factors for the following set of dependent

335 variables: (1) movement time, peak wrist velocity, and

336 time-to-peak wrist velocity; and (2) peak grip aperture,

337 time-to-peak grip aperture, peak grip aperture velocity,

338 and time-to-peak grip aperture velocity MANOVAs were

339 followed by univariate analyses, which revealed main

340 and interaction effects; therefore we focused on group

341 and interaction effects Post hoc tests with Bonferroni

342 adjustments were performed for main and interaction

343 effects We computed the effect size using the eta

344 squared (g2) parameter The cut-off criteria for the effect

345 size (partial eta squared [g2]) were: small effect

346 (0.206 g2

< 0.50), medium effect (0.506 g2

< 0.80),

347 and large effect (g2P 0.80) as suggested by Cohen

348 (1992) The level of significance was set at p6 0.05

350 We present results of the MANOVAs and ANOVAs in

351 Tables 1 and 2 Since there was no interaction between

352 step*condition and task*condition for any of the

353 dependent variables, we exclude the statistical results of

354 these interactions from bothTables 1 and 2

355 Sample characteristics

356 ANOVA showed difference between groups for the

Mini-357 BESTest (F1,28= 112.7, p6 0.001) FOA (22.2 pts)

358 scored lower than OA (27.3 pts), indicating impaired

359 balance However, groups were similar in age

360 (FOA = 71.8 years|OA = 70.1 years), height (FOA =

361 1.55 m|OA = 1.54 m), body mass (FOA = 65.7 kg|

362 OA = 59.9 kg), MMSE (FOA = 27 pts|OA = 28.2 pts)

363 and physical activity level (FOA = 4.2 pts|OA =

364 4.1 pts) In addition, FOA presented a mean of 2.1 falls

365 in the last 12 months

366 Spatiotemporal gait parameters

367 Step width was greater for FOA (0.09 m) than for OA

368 (0.06 m) (p = 0.003) (Fig 2A) Step length was greater

369 in WT (0.58 m) than in all grasping conditions (0.47 m)

370 (p = 0.001) (Fig 2B) Relative to the step effect, step

371 width was greater in step N (0.09 m) than N-2 (0.07 m)

372 and N-1 (0.06 m) (p = 0.001) (Fig 2A) However, step

373 length was greater in step N-2 (0.54 m) than N-1

374 (0.48 m) and N (0.46 m) (p6 0.001) (Fig 2B)

375 Step duration was greater for FOA (0.62 s) than for OA

376 (0.52 s) (p = 0.03) (Fig 2C) FOA (0.64 m/s) presented a

377 lower step velocity than OA (0.93 m/s) in step N

378 (p6 0.001) (Fig 2D) For the effect of condition, step

379 duration was greater for the stable base with obstacles

380

at short distance (0.61 s) and the stable base with

381 obstacles at long distance (0.58 s) conditions than for

382 walking through (0.51 s) (p6 0.001) (Fig 2C) However,

383 step velocity was lower in the grasping conditions

384 (0.88 m/s) than in walking through (1.15 m/s) (p6 0.001)

385 (Fig 2D) Step duration was lower in steps N-2 (0.52 s)

386 and N-1 (0.53 s) than in step N (0.66 s) (p = 0.002)

387 (Fig 2C) Step velocity was greater in steps N-2 (1.04 m/

388 s) and N-1 (0.93 m/s) than in step N (0.78 m/s) (Fig 2D)

389 COM variables and MDS

390 For the percentage of COM AP velocity, FOA (60%)

391 presented a greater reduction in AP velocity than OA

392 (30%) (Fig 3B) For the effect of condition, COM AP

393 velocity reduction was greater in the obstacle (stable

394 base with obstacles at short distance: 56.5%; stable

395 base with obstacles at long distance: 45.7%; unstable

396 base with obstacles at short distance: 59.7%; unstable

397 base with obstacles at long distance: 47.9%) than in the

398 no-obstacle conditions (stable base: 28.9%; unstable

399 base: 32.4%) (p6 0.001) (Fig 3B) In absolute values,

400 the mean COM AP velocity for FOA was equal to

401 0.39 m/s and 0.75 m/s for the OA

402 The temporal difference between minimum velocity

403 and dowel contact was greater for FOA (3.51 s) than

404

OA (2.58 s) (Fig 3B) This result showed that FOA

405 exhibited a minimum velocity earlier than OA before

406 dowel contact (Fig 3B) In addition, the minimum

407 velocity occurred earlier in the stable base condition

408 (2.71 s) than in the stable base at short distance

409 condition (3.31 s) (p = 0.001) (Fig 3B)

410

In both directions, MDS was greater for FOA (AP:

411 0.07 m, ML: 0.04 m) than OA (AP: 0.02 m, ML: 0.01 m)

412 (p = 0.002) (Fig 3C) The MDS AP was greater in the

413 stable base with obstacles at short distance (0.07 m)

414 and the unstable base with obstacles at short distance

415 (0.06 m) conditions than in walking through (0.01 m)

416 (p = 0.002) (Fig 3C) In addition, the MDS AP was

417 greater in step N-1 (0.07 m) than in step N (0.03 m)

418 (p = 0.017) (Fig 3C)

419 Reaching-to-grasping variables

420 FOA presented a greater movement time and a lower

421 peak wrist velocity (1.57 s|27.7 m/s) than OA (1.21 s|

422 31.7 m/s) (p = 0.001) (Fig 4A, B) Movement time and

423 peak wrist velocity were greater for stationary (1.62 s|

424 0.46 m/s) than for the walking (1.16 s|0.38 m/s,

425 respectively) task (p6 0.001) (Fig 4A , B) In addition,

426 the time- to- peak wrist velocity occurred earlier in

427 walking (18.3%) than in the stationary (41.2%) task

428 (p6 0.001) (Fig 4C) Regarding the condition effect, the

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429 movement time was lower for conditions without

430 obstacles (stable base: 1.25 s|unstable base: 1.28 s)

431 than with obstacles (stable base with obstacles at short

432 distance: 1.55-s|unstable base with obstacles at short

433 distance: 1.56 s) (p6 0.001) (Fig 4A) In addition, the

434 movement time was greater for conditions with

435 obstacles at short (stable base with obstacles at short

436 distance: 1.55-s|unstable base with obstacles at short

437 distance: 1.56 s) versus long distances (stable base with

438 obstacles at long distance: 1.36-s|unstable base with

439 obstacles at long distance: 1.36 s) (p6 0.001) (Fig 4A)

440 Peak wrist velocity and time-to-peak wrist velocity were

441 greater in the stable base (0.45 m/s|32%) than in the

442 stable base with obstacles at short distance (0.39 m/s|

443 26%) condition (p = 0.010) (Fig 4B, C) For the

444 unstable base, peak wrist velocity and time- to- peak

445 wrist velocity were lower for the unstable base with

446 obstacles at short distance (0.39 m/s|27%) than for the

447 unstable base with obstacles at long distance (0.43 m/s|

448 33%) condition (p = 0.008) (Fig 4B, C)

449 The temporal difference between right HC and

450 reaching onset was greater for FOA (0.36 s) than for OA

451 ( 0.14 s) This indicated that FOA touched the ground

452 before reaching onset (Fig 4D)

Table 1 F- and p-values for main and interaction effects (condition, step and condition*step interaction) of the MANOVAs and the univariate ANOVAs for the spatiotemporal gait parameters (step length, step width, step duration and step velocity), margin of dynamic stability in AP and ML directions, temporal difference between minimum velocity and dowel contact, and AP velocity reduction (%)

Variables Group Condition Step Condition*group Step*group

MANOVA Wilk’s Lambda = 0.629,

F 2,27 = 7.95, p = 0.002,

g 2

= 0.371

Wilk’s Lambda = 0.121,

F 12,17 = 10.28,

p 6 0.0001,

g 2 = 0.879

Wilk’s Lambda = 0.232,

F 4,25 = 20.66,

p 6 0.0001,

g 2 = 0.768

Wilk’s Lambda = 0.365,

F 12,17 = 2.46,

p = 0.044,

g 2 = 0.635

Wilk’s Lambda = 0.717,

F 4,25 = 2.47,

p = 0.070,

g 2 = 0.283 Follow-up univariate

Step length F1,28= 3.09,

p = 0.09,

g 2 = 0.094

F6,168= 25.63,

p 6 0.0001,

g 2 = 0.478

F2.56= 28.98,

p 6 0.0001,

g 2 = 0.509

F6,636= 1.88,

p = 0.132,

g 2 = 0.063

F2,56= 4.31,

p = 0.018,

g 2 = 0.283 Step width F1,28= 10.80,

p = 0.003,

g 2 = 0.278

F6,168= 3.39,

p = 0.017,

g 2 = 0.108

F2.56= 8.78,

p = 0.002,

g 2 = 0.239

F6,636= 2.46,

p = 0.061,

g 2 = 0.081

F2,56= 0.55,

p = 0.525,

g 2 = 0.133 MANOVA Wilk’s Lambda = 0.67,

F 2,27 = 6.59,

p = 0.005,

g 2

= 0.328

Wilk’s Lambda = 0.120,

F 12,17 = 10.38,

p 6 0.0001,

g 2

= 0.880

Wilk’s Lambda = 0.163,

F 4,25 = 32.16,

p 6 0.0001,

g 2

= 0.837

Wilk’s Lambda = 0.393,

F 12,17 = 2.19,

p = 0.068,

g 2

= 0.325

Wilk’s Lambda = 0.675,

F 4,25 = 3.04,

p = 0.037,

g 2

= 0.607 Follow-up univariate

Step duration F1,28= 10.63,

p = 0.030,

g 2 = 0.275

F6,168= 4.31,

p = 0.007,

g 2 = 0.133

F2,56= 13.73,

p 6 0.0001,

g 2 = 0.329

F6,168= 1.55,

p = 0.206,

g 2 = 0.053

F2.56= 3.78,

p = 0.060,

g 2 = 0.119 Step velocity F 1,28 = 10.62,

p = 0.020,

g 2

= 0.293

F 6,168 = 52.03,

p 6 0.0001,

g 2

= 0.650

F 2,56 = 64.32,

p 6 0.0001,

g 2

= 0.697

F 6,168 = 1.57,

p = 0.193,

g 2

= 0.054

F 2.56 = 5.08,

p = 0.014,

g 2

= 0.154 MANOVA Wilk’s Lambda = 0.528,

F2,27= 12.06,

p 6 0.0001,

g 2 = 0.472

Wilk’s Lambda = 0.338,

F2,27= 12.06,

p 6 0.0001,

g 2 = 0.662

Wilk’s Lambda = 0.451,

F4,25= 7.61,

p 6 0.0001,

g 2 = 0.549

Wilk’s Lambda = 0.604,

F12,17= 0.93,

p = 0.541,

g 2 = 0.596

Wilk’s Lambda = 0.919,

F4,25= 0.55,

p = 0.698,

g 2 = 0.081 Follow-up univariate

MDS AP F 1,28 = 5.85,

p = 0.022,

g 2

= 0.173

F 6,168 = 4.86,

p 6 0.0001,

g 2

= 0.148

F 2,56 = 6.78,

p = 0.002,

g 2

= 0.195

F 6,168 = 0.559,

p = 0.521,

g 2

= 0.020

F 2,56 = 0.546,

p = 0.582,

g 2

= 0.019 MDS ML F 1,28 = 18.53,

p 6 0.0001,

g 2

= 0.398

F 6,168 = 2.51,

p = 0.061,

g 2

= 0.082

F 2,56 = 1.54,

p = 0.227,

g 2

= 0.052

F 6,168 = 1.292,

p = 0.282,

g 2

= 0.044

F 2,56 = 1.443,

p = 0.245,

g 2

= 0.049 ANOVA

Temporal

difference

F1,28= 9.681,

p = 0.004,

g 2 = 0.257

F2,28= 6.391,

p 6 0.0001,

g 2 = 0.186

p = 0.545,

g 2 = 0.027

ANOVA

% AP velocity

reduction

F 1.28 = 14.13,

p 6 0.0001,

g 2

= 0.335

F 5.140 = 43.67,

p 6 0.0001,

g 2

= 0.609

p = 0.360,

g 2

= 0.037

Trang 7

453 Peak grip aperture was unaffected by group, condition

454 and task (Fig 5A) However, time-to-peak grip aperture

455 was lower for FOA (73.2%) than for OA (86.8%) in the

456 walking task (Fig 5B) Time-to-peak grip aperture was

457 lower for conditions without obstacles than for

458 conditions with obstacles at both short and long

459 distances (stable base: 72.2%|stable base with

460 obstacles at long distance: 78.6%|stable base with

461 obstacles at short distance: 78.7%|unstable base:

462 71.9%|unstable base at long distance: 79.9%|unstable

463 base at short distance: 79.1%) (p6 0.001) (Fig 5B) In

464 addition, time-to-peak grip aperture was greater in

465 walking (79.9%) than in stationary (73.6%) task

466 (p = 0.001) (Fig 5B)

467 The peak grip aperture velocity and the time-to-peak

468 grip aperture velocity were lower for FOA (0.12 m/s|

469 37.2%) than for OA (0.15 m/s|47.3%) (p6 0.001)

470 (Fig 5C, D) The peak grip aperture velocity was greater

471 in the stationary (0.18 m/s) than in the walking task

472 (0.09 m/s) (p = 0.01) (Fig 5C) For the condition effect,

473 the time- to- peak grip aperture velocity was lower in

474 conditions without obstacles than in conditions with

475 obstacles at short and long distances (stable base:

476 31.6%|stable base with obstacles at long distance:

477 45.2%|stable base with obstacles at short distance:

478 48.2%|unstable base: 29.6%|unstable base with

479 obstacles at long distance: 47.7%|unstable base with

480 obstacles at short distance: 52.2%) (p6 0.001) (Fig 5D)

481 DISCUSSION

482

We investigated the motor performance of walking

483 combined with prehension at varying levels of manual

484 task difficulty in older adults with and without a history of

485 falls FOA performed worse than OA in the

486 MiniBESTest, which indicates poor balance and

487 mobility This result supports the findings that FOA have

488 poor balance control (Cebolla et al., 2015) History of falls

489 did influence motor performance during the combined

Table 2 F- and p-values for main and interaction effects (condition, step and condition*step interaction) of the MANOVAs and the univariate ANOVAs for reaching (movement time, peak wrist velocity, time-to-peak wrist velocity, temporal difference) and grasping (peak grip aperture, time-to-peak grip aperture, peak grip aperture velocity, time-to-peak grip aperture velocity) variables

Variables Group Condition Task Task*group

MANOVA Wilk’s

Lambda = 0.618,

F 3,25 = 5.15,

p = 0.007,

g 2 = 0.402

Wilk’s Lambda = 0.110,

F 3,25 = 7.04,

p = 0.0001,

g 2 = 0.883

Wilk’s Lambda = 0.121,

F 3,25 = 60.27,

p 6 0.0001,

g 2 = 0.877

Wilk’s Lambda = 0.880,

F 3,25 = 1.13,

p = 0.354,

g 2 = 0.110 Follow-up univariate

Movement time F1,27= 4.37,

p = 0.046,

g 2 = 0.159

F5,135= 21.78,

p 6 0.0001,

g 2 = 0.452

F1,27= 35.27,

p 6 0.0001,

g 2 = 0.573

F1,27= 0.77,

p = 0.389,

g 2 = 0.030 Peak wrist velocity F 1,27 = 15.57,

p = 0.0001,

g 2

= 0.385

F 5,135 = 6.89,

p 6 0.0001,

g 2

= 0.226

F 1,27 = 21.15,

p 6 0.0001,

g 2

= 0.458

F 1,27 = 1.08,

p = 0.307,

g 2

= 0.053 Time-to-peak wrist velocity F 1,27 = 2.68,

p = 0.113,

g 2

= 0.098

F 5,135 = 7.04,

p 6 0.0001,

g 2

= 0.168

F 1,27 = 120.95,

p 6 0.0001,

g 2

= 0.817

F 1,27 = 2.29,

p = 0.142,

g 2

= 0.049 ANOVA

Temporal difference F1,28= 11.98,

p = 0.002,

g 2 = 0.300

F5,140= 1.92,

p = 0.145,

g 2 = 0.064

MANOVA Wilk’s

Lambda = 0.572,

F 4,24 = 4.48,

p = 0.008,

g 2

= 0.428

Wilk’s Lambda = 0.033,

F 20,8 = 11.84,

p = 0.001,

g 2

= 0.976

Wilk’s Lambda = 0.283,

F 4,24 = 15.22,

p 6 0.0001,

g 2

= 0.717

Wilk’s Lambda = 0.658,

F 4,24 = 3.12,

p = 0.034,

g 2

= 0.342 Follow-up univariate

Peak grip aperture F1,27= 0.18,

p = 0.674,

g 2 = 0.007

F5,135= 1.87,

p = 0.167,

g 2 = 0.065

F1,27= 2.58,

p = 0.120,

g 2 = 0.087

F1, 27= 0.11,

p = 0.746,

g 2 = 0.004 Time-to-peak grip aperture F1,27= 12.43,

p = 0.002,

g 2 = 0.315

F5,135= 9.05,

p 6 0.0001,

g 2 = 0.251

F1,27= 14.45,

p = 0.001,

g 2 = 0.349

F1, 27= 5.77,

p = 0.023,

g 2 = 0.176 Peak grip aperture velocity F1,27= 4.55,

p = 0.042,

g 2 = 0.144

F5,135= 2.77,

p = 0.064,

g 2 = 0.093

F1,27= 52.13,

p = 0.001,

g 2 = 0.659

F1, 27= 6.08,

p = 0.020,

g 2 = 0.184 Time-to-peak grip aperture velocity F 1,27 = 8.38,

p = 0.007,

g 2

= 0.237

F 5,135 = 26.56,

p 6 0.0001,

g 2

= 0.496

F 1,27 = 0.16,

p = 0.695,

g 2

= 0.006

F 1, 27 = 3.16,

p = 0.087,

g 2

= 0.105

Trang 8

490 task of walking and prehension, and will be discussed

491 below

492 FOA exhibited a more conservative walking strategy

493 and decoupled the combined task when compared to

494 OA

495 Walking performance in FOA was observed to be

496 impaired These impairments included: reduced step

497 velocity and increased step width and duration when

498 compared to OA These findings are in agreement with

499 other studies on gait changes in FOA (Barak et al.,

500 2006; Kirkwood et al., 2011; Toebes et al., 2012) The

501 slowness of FOA may indicate the need for extra time

502 to pick up necessary sensory information to assist with

503 movement performance (Chapman and Hollands, 2007)

504 Although the spatial-temporal gait parameters could allow

505 inferences about the control of stability, the MDS is a

506 more appropriate measurement to investigate dynamic

507 stability control Our results showed an increase in the

508 MDS of FOA to ensure body stability Consequently,

509 FOA preferred a more conservative strategy to increase

510 their dynamic stability compared to OA

511 When walking was combined with prehension, FOA

512 presented a greater reduction in AP velocity than OA

513 Moreover, FOA exhibited the minimum AP velocity

514 earlier than OA before dowel contact Considering the

515 AP velocity, FOA almost stopped walking to perform the

516 prehension task Altogether, these results suggest that

517 FOA decouple the walking and prehension tasks, which

518 may represent a loss of automaticity to superimpose a

519 discrete motor task on walking Similarly to our task, in

520 activities that require movement transitions in sequence,

521 such as sit-to-walk, FOA have been observed to also

522 divide this motor task into two phases (i.e., sit-to-stand

523 and stand-to-walk) to achieve a more upright position

524 before initiating gait to ensure body stability (Chen et al.,

525

2013)

526 FOA began moving their hand toward the dowel

527

360 ms after HC, whereas OA started at 140 ms before

528

HC The behavior of OA was more similar to young

529 adults (Rinaldi and Moraes, 2015), although hand

move-530 ment in young adults started 460 ms before HC The

531 beginning of hand movement 460 ms before HC

repre-532 sents the appropriate timing to exploit the upper limb

for-533 ward momentum (Rinaldi and Moraes, 2015) The short

534 time for OA could be related to a smaller range of motion

535

of their upper limbs For FOA, the beginning of hand

536 movement after HC is one more indication of the

decou-537 pling of walking and prehension FOA may prefer to slow

538 down, almost to the point of terminating gait, before

initi-539 ating hand movement toward the dowel These changes

540 indicate a conservative motor strategy to achieve the goal

541

of the task Older adults with fear of falling present an

542 extended anticipatory postural adjustment (APA) during

543 gait initiation under dual-task condition (Uemura et al.,

544

2012) to compensate for deficits in balance control Thus,

545 FOA have to compensate for balance deficits when

per-546 forming the combined task by dividing it in two phases:

547

a preparatory phase to gain stability followed by the

548 grasping execution

549 History of falls affected prehension movement

550 Changes in motor performance of FOA were not

551 restricted to walking alone, but also occurred in the

552 prehension task FOA presented slower movement time

553 and lower peak wrist velocity, peak grip aperture

554 velocity, and time-to-peak grip aperture To the best of

555 our knowledge, this is the first study to show

556 modifications in prehension movement in FOA, which

557 indicates a generalized slowing down in movement

Fig 2 Mean and standard error for step width (A), step length (B), (C) step duration and (D) step velocity for fallers and non-fallers for all experimental conditions (SB: stable base, SLD: stable base with obstacles at long distance, SSD: stable base with obstacles at short distance, UB: unstable base, ULD: unstable base with obstacles at long distance, USD: unstable base with obstacles at short distance, WT: walking baseline).

Trang 9

558 performance This slowness suggests that FOA need

559 more time to gain sensory information to accomplish the

560 manual task successfully, as has been suggested for

561 walking tasks (Chapman and Hollands, 2007) Although

562 most of studies that investigate the performance of FOA

563 showed changes in walking (primary task) (Hall et al.,

564 2011), we also found changes in the secondary motor

565 task (prehension) We suggest that FOA may have

prob-566 lems in switching attention between two motor tasks due

567 to neuromuscular problems, which may be related to a

568 loss of function in the frontal subcortical pathways

569 (Viswanathan and Sudarky, 2011)

570 Additionally, the time-to-peak grip aperture occurred

571 earlier for FOA than for OA only during the walking task,

572 indicating a strategy to increase the time available for

573 online control of hand configuration before dowel

574 contact The need for this additional time in FOA

575 appeared only during the combined task This may have

576 occurred due to the complexity of planning a movement

577 while concurrently performing another movement Thus,

578 they preprogrammed less their grasping movement in

579 the walking task and relied more on online control for

580 performing grasping successfully

581 Gait and prehension were mutually modified due to

582 the level of difficulty of the manual task in both

583 groups

584 Most of the studies have shown a decline in gait

585 performance of older adults during dual task conditions

586 (Hall et al., 2011) However, some studies did not show

587 when older adults changed their walking pattern due to

588 the addition of a secondary task Our results show that

589 older adults made modifications in the walking pattern in

590 the step of object grasping and the previous step before

591

it Similarly,Rinaldi and Moraes (2015)found that young

592 adults made modifications in their walking due to the

addi-593 tion of prehension one-step before it In this context, the

594 level of difficulty of the prehension task influenced the gait

595

of older adults We found a decrease in both step length

596 and speed with the addition of the prehension task Yet,

597 the different levels of difficulty of the manual task affected

598 more some variables; COM AP velocity reduction was

599 more pronounced for the conditions with obstacles,

600 whereas the MDS increased for conditions with obstacles

601

at short distance as compared to WT Thus, participants

602 adjusted their walking to accommodate the accurate

exe-Fig 3 Time series of COM AP velocity for one faller and one non-faller in walking combined to grasping and walking through conditions (A) The vertical dashed lines indicate minimum velocity and dowel contact, respectively The AP velocity reduction (%) is indicated by the difference between the combined condition (thick line) and the baseline walking condition (thin line) The temporal difference is calculated by the difference between the time of minimum velocity and dowel contact, mean and standard error for AP velocity reduction (left side), temporal difference between minimum velocity and dowel contact (right side) (B) and margin of dynamic stability in AP (left side) and ML direction (right side) for experimental conditions (SB: stable base, SLD: stable base with obstacles at long distance, SSD: stable base with obstacles at short distance, UB: unstable base, ULD: unstable base with obstacles at long distance, USD: unstable base with obstacles at short distance, WT: walking through).

Trang 10

603 cution of the manual task that may challenge their body

604 stability, as found in young adults (Rinaldi and Moraes,

605 2015) As a result, they adopted a more conservative

606 strategy to allow them to allocate more attention to the

607 grasping task and avoid errors Previous studies also

608 found changes in the walking behavior of older adults

609 for the secondary tasks with the highest level of difficulty

610 (Nordin et al., 2010; Hall et al., 2011) In synthesis,

611 reaching-to-grasping affected postural control by

chang-612 ing the gait behavior

613 Different conditions and tasks influenced prehension

614 Participants presented a greater movement time and a

615 lower peak wrist velocity for conditions with obstacles

616 (short and long distance) Relative to grasping, the

time-Fig 4 Mean and standard error for movement time (A), peak wrist velocity (B), time-to-peak wrist velocity (C) and temporal difference between heel contact and reaching onset (D) for fallers and non-fallers for all experimental conditions (SB: stable base, SLD: stable base with obstacles at long distance, SSD: stable base with obstacles at short distance, UB: unstable base, ULD: unstable base with obstacles at long distance, USD: unstable base with obstacles at short distance).

Fig 5 Mean and standard error for peak grip aperture (A), time-to-peak grip aperture (B), peak grip aperture velocity (C), and time-to-peak grip aperture velocity (D) for fallers and non-fallers for all experimental conditions (SB: stable base, SLD: stable base with obstacles at long distance, SSD: stable base with obstacles at short distance, UB: unstable base, ULD: unstable base with obstacles at long distance, USD: unstable base with obstacles at short distance).

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