ARTICLE IN PRESS TagedEnFiur Available online at www.sciencedirect.com TagedEn TagedFiur TagedEn Journal of Sport and Health Science xxx (2021) xxx-xxx www.jshs.org.cn 1 TagedH1Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?TagedEn 3 4 5 6 7 agedPD1X XSasa XT Cigoja D2X X *, D3X XJared R. Fletcher D4X X , D5X XBenno M. Nigg D6X X TagedEn a, Q1 10 b a TagedP Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, T2N 1N4, Alberta, Canada b Department of Health and Physical Education, Mount Royal University, Calgary, T3E 6K6, Alberta, Canada a 8 9 53 Original article 2 TagedEn Available online xxx 13 2095-2546/Ó 2021 Published by Elsevier B.V. on behalf of Shanghai University of Sport. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) 16 17 18 19 20 21 22 23 24 25 26 27 28 29 56 57 58 59 60 61 62 64 65 66 14 15 55 63 11 12 54 TagedPAbstract 67 Objective: To investigate if changing the midsole bending stiffness of athletic footwear can affect the onset of lower limb joint work redistribution during a prolonged run. Methods: Fifteen trained male runners (10-km time of <44 min) performed 10-km runs at 90% of their individual speed at lactate threshold (i.e., when change in lactate exceeded 1 mmol during an incremental running test) in a control and stiff shoe condition on two occasions. Lower limb joint kinematics and kinetics were measured using a motion capture system and a force-instrumented treadmill. Data were acquired every 500 m. Results: Prolonged running resulted in a redistribution of positive joint work from distal to proximal joints in both shoe conditions. Compared to the beginning of the run, less positive work was performed at the ankle (approximately 9%; p  0.001) and more positive work was performed at the knee joint (approximately 17%; p  0.001) at the end of the run. When running in the stiff shoe condition, the onset of joint work redistribution at the ankle and knee joints occurred at a later point during the run. Conclusion: A delayed onset of joint work redistribution in the stiff condition may result in less activated muscle volume, because ankle plantar flexor muscles have shorter muscles fascicles and smaller cross-sectional areas compared to knee extensor muscles. Less active muscle volume could be related to previously reported decreases in metabolic cost when running in stiff footwear. These results contribute to the notion that footwear with increased stiffness likely results in reductions in metabolic cost by delaying joint work redistribution from distal to proximal joints. TagedPKeywords: Fatigue; Footwear; Mechanics; Performance; RunningTagedEn 68 69 70 71 72 73 74 75 76 77 78 79 80 81 30 82 31 83 84 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 TagedH11. IntroductionTagedEn T recent study reported that a prolonged (i.e., 10 km) run agedPA resulted in a redistribution of lower limb positive joint work, from distal (i.e., ankle) to more proximal (i.e., knee) joints, with increased running distance.1 Sanno et al.1 speculated that this redistribution occurred because ankle plantarflexor muscles might have fatigued to a greater extent during the prolonged run than the knee or hip extensor muscles. This was based on the notion that during the prolonged run calculated ankle joint moments were higher than calculated peak knee and hip joint moments relative to previously reported maximum joint moments assessed during isolated strength tests.2 This confirmed previous reports of the higher relative efforts 47 48 49 50 51 TagedEn Peer review under responsibility of Shanghai University of Sport. TagedEn *Corresponding author. E-mail address: sasa.cigoja1@ucalgary.ca (S. Cigoja). of the ankle extensors as compared to knee extensors during running.3 The authors further speculated that a redistribution of positive lower limb joint work toward more proximal joints is disadvantageous for long-distance running performance because muscletendon units (MTU) surrounding the ankle joint (e.g., triceps surae (TS) and Achilles tendon (AT)) are thought to be better equipped for storage and return of elastic energy than MTUs surrounding the knee joint.4 This conclusion was made under the assumption that tendons can store and return relevant amounts of strain energy during running,4,5 which may not necessarily be the case.6 Furthermore, if prolonged running resulted in increased positive work at the knee joint and the MTUs surrounding this joint are not as wellequipped for energy storage and return, the additional work must be performed by the muscle in series with the tendon.7 This muscle work would require a greater active muscle volume, thereby elevating the metabolic cost of running.7 This https://doi.org/10.1016/j.jshs.2020.12.007 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 52 Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 ARTICLE IN PRESS TagedEn2 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 could be disadvantageous for long-distance running performance because metabolic cost is one of the key determinants of distance running performance,8 and it increases as a function of running distance.911TagedEn TagedPIt can be speculated that if the onset of lower limb joint work redistribution was delayed, performance benefits could be achieved as the direct result of a mitigated increase in metabolic cost during long-distance running events. One footwear feature that has been shown to have large effects on biomechanical,12 physiological,13,14 and performance1517 variables is the midsole bending stiffness (MBS). Although the underlying sources behind performance improvements achieved by running in footwear with increased MBS (by means of inserting stiff carbon fiber plates) are not-well understood, multiple mechanisms have been proposed to explain its function: (a) by minimizing energy loss,15 (b) by storing and returning elastic energy,18,19 (c) by optimizing the function of the major ankle plantarflexor muscles,2022 and (d) by way of the “teeter-totter” effect.23,24 In brief, the principle of minimizing energy loss suggests that athletic performance can be improved by reducing the eccentric work performed by muscles. The principle of storing and returning elastic energy suggests that strain energy can be stored in the stiffening structures (e.g., carbon fiber plates) of running shoe midsoles as the metatarsophalangeal (MTP) joint undergoes extension (i.e., dorsiflexion). It is speculated that some of this stored energy is then returned to the athlete during the subsequent flexion of the MTP joint and recoil of the carbon fiber plates. The principle of optimizing ankle plantarflexor muscle function suggests that the TS muscle group is enabled to operate at slower shortening velocities when running in footwear with increased MBS due to changes in gear ratio25 (i.e., the ratio between external and internal moment arms) and longer stance times16,22,26; this is thought to reduce the muscle energy cost.7 Running in stiff footwear typically shifts the center of pressure further anteriorly during late stance.20 This increases the moment arm of the ground reaction force to the ankle while the AT moment arm remains unchanged, and therefore increases the gear ratio. This increase in ratio between the external and internal moment arm is believed to allow the ankle plantarflexor muscles to operate on a more favorable position of their forcevelocity relationship,27,28 which has been speculated to improve the energy cost of running.2022 The “teeter-totter” effect suggests that the ground reaction force produces a force at the heel due to the curvature of the carbon fiber plate as the center of pressure travels anteriorly during the stance phase of running. This heel force is supposed to act at the right location (heel of the foot), at the right time (during push-off), and with the right frequency to reduce the metabolic cost of running.24TagedEn TagedPIt was recently shown that running in footwear with increased MBS redistributed lower limb joint work from proximal to distal joints (i.e., opposite to the redistribution introduced by prolonged running).19 Compared to running in a control shoe, Cigoja et al.19 demonstrated that more positive work was performed at the MTP and less positive work was performed at the knee joint when running in stiff shoes. This S. Cigoja et al. was interpreted as a redistribution of positive lower limb joint work from proximal to distal joints; however, it remained unknown if such a redistribution could also be observed during a prolonged run and if it could be delayed by running in footwear with increased MBS.TagedEn TagedPFor this reason, the purpose of the present study was to investigate whether running in shoes with increased MBS affects the onset of lower limb joint work redistribution from distal to proximal joints during a prolonged run. It was hypothesized that running with increased MBS would mitigate the lower limb joint work redistribution during a 10-km run.TagedEn 162 163 164 165 166 167 168 169 170 171 172 173 TagedH12. MethodsTagedEn TagedH22.1. ParticipantsTagedEn T ifteen trained male runners (age: 28.5 § 6.7 years, height: agedPF 1.79 § 0.08 m, mass: 70.6 § 10.3 kg; mean § standard deviation) visited the laboratory on 3 separate occasions. Participants were included in this study if they reported the ability to run 10 km in less than 44 min, were free from lower limb injuries in the past 6 months, and fit Sizes 9, 10, or 11 US running shoes. This study was approved by the University of Calgary Conjoint Health Research Ethics Board (REB17-0171), and all subjects gave written informed consent prior to participating in this study. All procedures were performed in accordance with the Declaration of Helsinki.TagedEn 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 TagedH22.2. Footwear conditionsTagedEn T he control condition (Control) consisted of a Nike Free agedPT Run 2018 (Nike Inc., Beaverton, OR, USA) shoe. The stiff condition was achieved by inserting straight carbon fiber plates between the factory insole and the midsole, and along the full length of the control shoe. The stiff condition, however, varied between participants: 7 participants ran in footwear with carbon fiber plates of 1.5 mm thickness (Stiff), and 8 participants ran in footwear with plates of 2 mm thickness (Stiffer). There were no significant differences between participants who ran in Stiff compared to participants who ran in Stiffer with respect to age (Stiff: 27.43 § 6.90 years, Stiffer: 29.50 § 6.82 years, p = 0.285), height (Stiff: 1.78 § 0.08 m, Stiffer: 1.79 § 0.08 m, p = 0.390), mass (Stiff: 67.13 § 8.18 kg, Stiffer: 73.65 § 11.49, p = 0.117), speed at lactate threshold (sLT; Stiff: 4.25 § 0.22 m/s, Stiffer: 4.12 § 0.20 m/s, p = 0.132), or shoe size (Stiff: median = 9, range = 911, Stiffer: median = 9, range = 911, p = 0.430). The stiff condition differed between participants because previous studies have shown that there is a subject-specific optimal MBS of running shoes29,30; therefore, we sought to mitigate the risk of introducing a stiffness level that may be too low or too high for a given runner. Stiffer allowed us to compare the control shoe to a shoe with an extreme stiffness condition, which we speculated would result in large biomechanical effects during a prolonged run, whereas Stiff allowed us to compare the control shoe to a stiff footwear condition, one that is more likely to be encountered on the running footwear market.TagedEn Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 ARTICLE IN PRESS TagedEnShoe Stiffness Effects on Joint Work Redistribution 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 TagedPThe MBS of the shoe conditions was determined using a 3-point bending test.13,19 In brief, the forefoot was placed on a structure with two supporting pins, which were 160 mm apart. A vertical, compressive force was applied in the area of the Q2 MTP joint using an ElectroPuls X X E10000 Linear-Torsion testing machine (Instron, Norwood, MA, USA). The machine was set to displace the shoe by 15 mm at a speed of 10 mm/s. This was repeated 10 times for all shoe conditions. The force and displacement data were filtered using a dual pass second-order Butterworth filter with a cut-off frequency of 5 Hz. The slope of the force-displacement curve (i.e., stiffness) was determined for all 10 loading cycles. The stiffness values were first averaged between 70% and 90% of each loading curve (i.e., linear portion of the forcedisplacement curve) and then across all 10 cycles. The MBS for Control, Stiff, and Stiffer were 1.58, 6.46, 13.28 N/mm, respectively. The footwear conditions were weight matched by inserting a total of six masses (i.e., two at the rearfoot, two at the midfoot, and two at the forefoot) into the control shoe. Across all conditions, the masses were 259, 280, and 296 g for the size 9, 10, and 11 US shoes, respectively.TagedEn 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 TagedH22.3. Data collectionTagedEn TagedP2.3.1. Visit 1TagedEn TagedPOn the first visit, the individual sLT was determined based on methods described elsewhere31 while participants ran in the control shoe on a treadmill (Model Fully Instrumented Treadmill, Bertec Corp., Columbus, OH, USA) with no gradient. In brief, participants first performed a 5-min warm-up at a selfselected speed. Immediately after the warm-up, a fingertip blood sample was taken to determine resting blood lactate concentration (Lactate Pro, Sports Resource Group Inc., Minneapolis, MN, USA). After the warm-up, the treadmill belt speed was increased by 0.8 km/h every 2 min, after which blood lactate concentration was measured. This was repeated until blood lactate concentration rose more than 1 mmol from the previous sample. The sLT was determined as the speed at the stage preceding the final stage.TagedEn 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 TagedP2.3.2. Visits 2 and 3TagedEn TagedPOn the second and third visits, respectively, participants performed a 10-km run at 90% of the individual sLT while wearing a control or stiff running shoe. The order of shoe conditions was balance randomized, so that 8 participants first ran in the control condition and 7 participants first ran in their stiff condition. Twenty-four retroreflective markers (diameter: 12 mm) were applied to the pelvis and right lower limb according to methods described by Cigoja et al.19 Except for the shoe, all markers were applied directly to the skin overlying anatomical landmarks. The shoe markers were applied on the upper material of the shoe. Three-dimensional kinematic and kinetic data of the pelvis and right lower limb were recorded at 200 and 1000 Hz using 8 high speed cameras (Vicon Motion Systems Ltd., Oxford, UK) and a force-instrumented treadmill (Model Fully Instrumented Treadmill, Bertec Corp., Columbus, OH, USA), respectively. A 2-min familiarization trial was 3 performed to allow participants to get accustomed to the running speed and footwear condition. Baseline kinematic and kinetic data were measured for 30 s immediately after the familiarization trial and subsequently recorded every 500 m during the 10-km runs. This resulted in 21 bouts of approximately 35‒45 steps of the right leg, per subject and footwear condition. The stance phases (i.e., where vertical ground reaction forces exceeded a threshold of 20 N32) of the middle 30 steps were identified and used for further analyses.TagedEn 276 277 278 279 280 281 282 283 284 285 TagedH22.4. Data analysisTagedEn 286 T aw data were analyzed using a custom written MATLAB agedPR code (Version 2019a; The MathWorks Inc., Natick, MA, USA). To determine the three-dimensional MTP, ankle, knee, and hip joint kinematics and kinetics, marker and force data were filtered using a dual pass second-order Butterworth filter with a cut-off frequency of 50 Hz. The cut-off frequency was determined based on a residual analysis33 applied to marker trajectory data from 10 randomly chosen steps across all participants, shoe conditions, and distances. Then, the highest frequency across all markers was chosen as the cut-off frequency to guarantee that all relevant trajectory information was retained in the signal. Cardan angles were calculated to describe joint motion, and an inverse dynamics approach was used to estimate sagittal joint moments. Mechanical joint powers were calculated as the dot-product of joint moment and angular velocity. Positive and negative mechanical work were determined as the integral of the positive or negative joint powertime curves over the stance phase, respectively. Jointspecific positive work was expressed relative to total lower limb positive work performed during the stance phase of running. All variables of interest were first computed for each step across all participants, shoe conditions, and running distances. Then the variables were averaged across 30 steps, and the individual means were used for further comparisons between shoe conditions and running distances.TagedEn 287 TagedH22.5. StatisticsTagedEn 313 T hapiroWilk tests were used to test for normal distribuagedPS tions of all dependent variables. The variables of interest were joint-specific positive work contribution relative to total positive lower limb joint work, stance times, peak flexion (i.e., plantarflexion) moment, angular velocity and angle of the MTP joint, and peak extension moment, angular velocity, and angle of the ankle and knee joints. If variables were normally distributed, two-way repeated measures analysis of variance (ANOVA) was used to test for main effects of distance (i.e., 3 levels: 0, 5, and 10 km) and shoe condition (i.e., 2 levels: control and stiff), and for interaction effects between distance and shoe. Where significant (a = 0.05) distance main effects or interactions were found, univariate repeated measures ANOVAs with 20 (i.e., 0 km vs. every other timepoint) paired Student’s t tests were performed for each shoe condition for each lower limb joint. If variables were not normally distributed, Friedman’s tests were performed to test for significant running distance effects for each shoe condition. Multiple Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 ARTICLE IN PRESS TagedEn4 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 S. Cigoja et al. Wilcoxon signed-rank tests were then used where Friedman’s tests revealed significant distance effects. The significance level for multiple comparisons was adjusted using the Bonferroni correction and set to p = 0.003 (i.e., p = 0.05  20 = 0.003). Effect size estimates were calculated using Cohen’s d.34 The formula for calculating Cohen’s d was:     xi  xj    ffi d ¼ qffiffiffiffiffiffiffiffi 2 2 si þsj 2 Where xi and s2i are the sample mean and variance at baseline (i.e., 0 km), and xj and s2j are the sample mean and variance at any other time point during the prolonged run (i.e., 0.5  10 km). The minimal detectible change was calculated using the following formula35: pffiffiffi s MDC ¼ 1:96  2  pffiffiffi n where s is the sample standard deviation for each variable at baseline in the control condition and n is the sample size.TagedEn TagedPA mixed model ANOVA (between-subject factor: stiffness group (i.e., 2 levels: Stiff and Stiffer); within-subject factors: running distance (i.e., 3 levels: 0, 5, and 10 km) was used to test if joint work redistribution was affected differently in participants who ran in Stiff compared to Stiffer. Wilcoxon ranksum tests were used to identify whether the change in jointspecific positive work from the beginning to the end of the run differed between participants who ran in Stiff compared to Stiffer. All statistical analyses were performed in SPSS Statistics Version 26.0 (IBM Corporation, Armonk, NY, USA).TagedEn work during the runs. The two-way repeated measures ANOVA showed no significant interaction effect between shoe and distance for the positive work performed at the MTP (p = 0.152), ankle (p = 0.387), knee (p = 0.535), or hip (p = 0.777) joint. Significant distance main effects were found for the positive work performed at the MTP (p  0.001), ankle (p  0.001), knee (p  0.001), but not the hip (p = 0.111) joint. Significant shoe effects were found for the positive work performed at the MTP (p  0.001) but not for the ankle (p = 0.595), knee (p = 0.883), or hip (p = 0.491) joint (Table 1).TagedEn TagedPFriedman’s tests showed significant distance effects for the positive work performed at the MTP joint in the control (p  0.001) and stiff (p  0.001) condition (Supplementary Table 1). In the control condition, positive MTP joint work decreased at 9 km (p = 0.002, d = 1.07) for the first time compared to 0 km (Fig. 1). After correcting for multiple comparisons, no significant difference in positive MTP joint work was found for any timepoints compared to 0 km in the stiff condition (Table 1). Univariate tests showed significant distance effects on positive work at the ankle (control: p  0.001, stiff: p = 0.001) and knee (control: p  0.001, stiff: p  0.001) joints for both conditions. In the control condition, positive ankle joint work was significantly different from baseline for the first time at 5 km (p = 0.001, d = 0.43) (Fig. 2). In the stiff condition, positive ankle joint work was significantly reduced for the first time at 8 km (p = 0.002, d = 0.45). For the knee joint, positive work was increased for the first time at 5.5 km (p = 0.001, d = 0.28) and 7.5 km (p = 0.002, d = 0.34) in the control and stiff conditions, respectively (Fig. 2).TagedEn 366 367 368 369 370 373 374 375 376 377 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 421 TagedH23.2. Kinematics and kineticsTagedEn TagedH13. ResultsTagedEn T verage sLT measured at Visit 1 was 4.18 § 0.22 m/s, which agedPA corresponded to 39 min 59 s § 2 min 6 s on 10 km. The average running speed for Visit 2 and 3 (i.e., 90% of sLT) was 3.75 § 0.22 m/s, which corresponded to 44 min 36 s § 2 min 50 s.TagedEn 371 372 391 420 364 365 390 TagedH23.1. Relative joint workTagedEn T here were no shoe (p = 0.844), distance (p = 0.784), or agedPT interaction effects (p = 0.958) on total positive lower limb joint 422 T ignificant shoe (p  0.001) and distance (p  0.001) main agedPS effects but no interaction (p = 0.554) effects were found for stance times, with longer times observed in the stiff (216.58 § 2.76 ms) compared to the control (210.00 § 3.21 ms) condition, and with generally longer times (i.e., control: +3.31%, stiff: +2.15%) with increasing running distance (Supplementary Table 2). Compared to the beginning of the run (control: 206.27 § 18.47 ms, stiff: 214.18 § 16.83 ms), stance times were significantly longer at 10 km in both the control (213.11 423 424 425 426 427 428 429 430 431 432 433 TagedEnTable 1 434 435 379 Positive metatarsophalangeal, ankle, knee, and hip joint work at 0, 5, and 10 km in the control and stiff shoe condition relative to total positive lower limb joint work (mean § standard deviation). 380 Pos. work (%total Pos. work) 437 378 381 382 383 384 385 386 387 388 389 Control 0 km 5 km 10 km Stiff 0 km 5 km 10 km MTP Ankle Knee Hip 2.60 § 0.64 2.11 § 0.52 1.89 § 0.67* 52.06 § 8.41 48.45 § 8.20* 46.92 § 8.46* 25.13 § 9.28 27.30 § 9.36 29.89 § 9.96* 20.21 § 9.00 22.13 § 8.57 21.31 § 8.81 5.19 § 1.34 5.10 § 1.21 4.26 § 1.65 50.80 § 7.59 48.24 § 9.29 46.48 § 8.93* 25.29 § 8.72 26.46 § 9.28 29.42 § 10.86* 18.72 § 7.09 20.21 § 6.38 19.84 § 7.26 436 438 p  0.003, running distance effects within a shoe condition. Abbreviations: MTP = metatarsophalangeal; Pos. = positive. * Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 439 440 441 442 443 444 445 446 ARTICLE IN PRESS TagedEnTagedEnShoeTagedFiur Stiffness Effects on Joint Work Redistribution 5 447 504 448 505 449 506 450 507 451 508 452 509 453 510 454 511 455 512 456 513 457 514 458 515 459 516 460 517 461 518 462 519 463 520 464 521 465 522 466 467 468 Fig. 1. Mean § standard deviation positive metatarsophalangeal (A), ankle (B), knee (C), and hip (D) joint work in the control (blue squares) and stiff (red triangles) shoe condition during a 10-km run at 90% of individual speed at lactate threshold. Positive ankle joint work decreased and positive knee joint work increased earlier in the control compared to the stiff condition. *p  0.003, compared to the beginning of the run (i.e., 0 km). Pos. = positive; MTP = metatarsophalangeal.TagedEn 473 474 475 476 477 478 479 480 481 482 525 527 470 472 524 526 469 471 523 § 19.14 ms, p = 0.001, d = 0.36) and stiff (218.79 § 18.41 ms, p = 0.003, d = 0.26) condition (Supplementary Table 2).TagedEn TagedPSignificant distance main effects were found for the peak MTP flexion moments in the control (p  0.001) and stiff (p  0.001) conditions (Supplementary Table 3). Compared to the start of the run (control: 0.88 § 0.40 Nm/kg, stiff: 0.85 § 0.26 Nm/kg; Fig. 3), peak MTP flexion moments decreased in the stiff (0.80 § 0.27 Nm/kg, p = 0.001, d = 0.20) but not in the control (0.82 § 0.36 Nm/kg, p = 0.009, d = 0.17) condition after correcting for multiple TagedEn comparisons. Significant main effects for distance (p  0.001) but not shoe (p = 0.892) or interaction (p = 0.937) were found for peak ankle extension moments (Supplementary Table 4). Compared to 0 km (control: 2.99 § 0.53 Nm/kg, stiff: 2.96 § 0.43 Nm/kg), ankle joint moments were lower in the control (2.86 § 0.48 Nm/kg, p = 0.001, d = 0.27) but not stiff (2.86 § 0.42 Nm/kg, p = 0.010, d = 0.22) condition at 10 km. Although significant distance (p  0.001) main effects were observed for peak knee extension moment, no significant differences were TagedFiur 528 529 530 531 532 533 534 535 536 537 538 539 483 540 484 541 485 542 486 543 487 544 488 545 489 546 490 547 491 548 492 549 493 550 494 551 495 552 496 553 497 554 498 555 499 556 500 557 501 502 503 Fig. 2. Ensemble mean (n = 15) metatarsophalangeal, ankle, knee, and hip joint power over the stance phase of running at 90% of individual speed at lactate threshold for the control (top row) and stiff (bottom row) shoe condition. Green, yellow, and red lines represent joint power at the beginning, middle, and end of the 10-km run, respectively. MTP = metatarsophalangeal.TagedEn Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 558 559 560 ARTICLE IN PRESS TagedEnTagedEn6 TagedFiur S. Cigoja et al. 561 618 562 619 563 620 564 621 565 622 566 623 567 624 568 625 569 626 570 627 571 628 572 629 573 630 574 631 575 632 576 633 577 634 635 578 579 580 581 Fig. 3. Ensemble mean (n = 15) metatarsophalangeal, ankle, knee, and hip joint moments over the stance phase of running at 90% of individual speed at lactate threshold for the control (top row) and stiff (bottom row) shoe condition. Green, yellow, and red lines represent joint moments at the beginning, middle, and end of the 10-km run, respectively. MTP = metatarsophalangeal.TagedEn 584 585 586 587 588 589 590 591 592 593 594 595 596 637 638 639 582 583 636 found between the beginning and end of the run after correcting for multiple comparisons (Supplementary Table 5).TagedEn TagedPSignificant shoe (p  0.001), distance (p  0.001), and interaction (p  0.001) effects were found for peak MTP flexion velocity. Univariate tests revealed greater peak MTP flexion velocities in the control (1023.31 § 48.45 ˚/s) compared to the stiff (816.17 § 6.89 ˚/s) condition. Compared to the start of the run, peak MTP flexion velocities were higher at 8.5 km (p = 0.002, d = 0.57) in the control condition; no differences were observed in the stiff condition after correcting for multiple comparisons. Significant main effects of shoe (p = 0.002) and distance (p = 0.001) but not interaction (p = 0.210) were found for peak ankle extension velocity. Peak TagedEn TagedFiur ankle extension velocities were significantly lower in the stiff (497.38 § 7.55 ˚/s) than the control (561.69 § 11.94 ˚/s) condition. No shoe (p = 0.893), distance (p = 0.832), or interaction (p = 0.648) effects were observed for peak knee extension velocities (Fig. 4).TagedEn TagedPSignificant distance effects were found for the peak MTP extension angle in the control (p  0.001) and stiff (p  0.001) conditions. Compared to the start of the run (control: 24.8 § 4.1˚, stiff: 20.09 § 3.4˚), peak MTP joint extension angles were significantly larger at the end of the run in the control (27.0 § 4.6˚, p  0.001, d = 0.52) but not in the stiff (21.43 § 4.3˚, p = 0.008, d = 0.35) condition (Fig. 5). Significant distance (p  0.001) but no shoe (p = 0.152) or interaction 640 641 642 643 644 645 646 647 648 649 650 651 652 653 597 654 598 655 599 656 600 657 601 658 602 659 603 660 604 661 605 662 606 663 607 664 608 665 609 666 610 667 611 668 612 669 613 670 614 671 615 616 617 Fig. 4. Ensemble mean (n = 15) metatarsophalangeal, ankle, knee, and hip joint angular velocities over the stance phase of running at 90% of individual speed at lactate threshold for the control (top row) and stiff (bottom row) shoe condition. Green, yellow, and red lines represent joint angular velocities at the beginning, middle, and end of the 10-km run, respectively. MTP = metatarsophalangeal.TagedEn Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 672 673 674 ARTICLE IN PRESS TagedEnShoe Stiffness Effects on Joint Work Redistribution 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 (p = 0.785) effects were found for peak ankle extension angles. Compared to 0 km, peak ankle extension angles were higher at 8.5 (p = 0.003, d = 0.58), 9 (p = 0.002, d = 0.52), and 9.5 km (p = 0.002, d = 0.54) in the control condition, and at 9 km (p = 0.003, d = 0.59) in the stiff condition. Significant distance (p  0.001) but no shoe (p  0.001) or interaction (p = 0.822) effects were found for peak knee flexion angles. Peak knee flexion angles were significantly lower in the control (43.1 § 5.4˚, p = 0.003, d = 0.26) but not in the stiff (41.6 § 4.7˚, p = 0.006, d = 0.28) condition at the end compared to the beginning of the run (control: 41.6 § 5.7˚, stiff: 40.2 § 4.8˚) (Fig. 5).TagedEn TagedPThere were no significant effects of distance (p = 0.353) or shoe (p = 0.869), and no interaction effects (p = 0.405) on the striking pattern (i.e., determined as the sagittal plane ankle angle at heel-strike) (Supplementary Table 6).TagedEn 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 TagedH23.3. Subgroup analysisTagedEn T he mixed model ANOVA revealed significant distance agedPT effects on positive work performed at the MTP (p = 0.003), ankle (p  0.001), and knee (p = 0.001) but not hip (p = 0.210) joint. There were no interaction effects between distance and stiffness group on positive work performed at the MTP (p = 0.796), ankle (p = 0.572), knee (p = 0.775), or hip (p = 0.469) joints. Furthermore, there was no effect of stiffness group on the positive work performed at the MTP (p = 0.756), ankle (p = 0.639), knee (p = 0.731), and hip (p = 0.296) joints. There was no difference in the change of joint-specific positive work contribution from the beginning to the end of the run between the participants who ran in Stiff compared to Stiffer for the MTP (p = 0.867, d = 0.04), ankle (p = 0.536, d = 0.08), knee (p = 0.779, d = 0.26), or hip (p = 0.867, d = 0.19) joints (Supplementary Tables 7 and 8).TagedEn TagedEn TagedFiur 7 TagedH14. DiscussionTagedEn TagedH24.1. Muscle and tendon functionTagedEn T he purpose of this study was to investigate whether the agedPT onset of lower limb joint work redistribution from distal to proximal joints during a prolonged run can be affected by running in footwear with increased MBS. The findings of this study showed that the positive MTP and ankle joint work significantly decreased in the control condition from baseline at 9 km and 5 km, respectively; whereas, in the stiff condition, only positive ankle joint work decreased at 8 km with no significant changes at the MTP joint throughout the run. At the knee joint, positive work significantly increased from baseline at 5.5 km and 7.5 km for the control and stiff conditions, respectively. We interpret the finding that ankle joint work decreased while knee joint work increased sooner in the control condition than the stiff condition as an earlier onset of lower limb joint work redistribution. It needs to be acknowledged, however, that the interaction between shoe condition and distance was not significant, which could be related to the low sample size or use of different plates for the stiff condition. This delayed onset of redistribution in the stiff condition could be interpreted as a metabolically positive effect because a redistribution of positive work toward more proximal joints would require additional work to be performed by muscles surrounding these joints, thereby delaying the increase in metabolic cost normally seen during a run. Knee extensor muscles (i.e., quadriceps) were reported to have longer muscle fascicles and larger cross-sectional areas compared to ankle extensor muscles (i.e., TS),36 which would result in increased muscle volume activation. If similar activation levels between ankle and knee extensor muscles are assumed, it could then be speculated that greater active muscle volume would result in more adenosine triphosphate being consumed by the muscle, which could in turn increase the metabolic cost of muscle contraction 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 711 768 712 769 713 770 714 771 715 772 716 773 717 774 718 775 719 776 720 777 721 778 722 779 723 780 724 781 725 782 726 783 727 784 728 785 729 730 731 Fig. 5. Ensemble mean (n = 15) metatarsophalangeal, ankle, knee, and hip joint angles over the stance phase of running at 90% of individual speed at lactate threshold for the control (top row) and stiff (bottom row) shoe condition. Green, yellow, and red lines represent joint angles at the beginning, middle, and end of the 10-km run, respectively. MTP = metatarsophalangeal.TagedEn Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 786 787 788 ARTICLE IN PRESS TagedEn8 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 S. Cigoja et al. 7 and positive work generation . This could have substantial implications for long-distance running performance, as the active muscle volume has been shown to be a major determinant of the metabolic cost of running.37 Also, muscles with shorter fascicles have fewer sarcomeres in series and are thought to consume proportionally less adenosine triphosphate per unit force compared to muscles with longer fascicles under similar activation levels.27TagedEn TagedPUnder the assumption that tendons are able to store and return relevant amounts of strain energy, a delayed onset of joint work redistribution toward more proximal joints when running in stiff shoes could potentially indicate that the AT returns energy to the athlete over an extended period of time,1 thus reducing the need for additional muscle work.7 A recent study from our laboratory investigated the effects of MBS on in vivo gastrocnemius medialis (GM) muscle fascicle behaviour and estimated AT energy return. This unpublished study, which is currently under review, found that the GM muscle shortened less and with slower average shortening velocities when an individual was running in stiffer footwear. Ankle joint angles, however, remained similar between shoe conditions. This suggests that if the GM muscle shortened less but ankle angles did not change, the remaining shortening must have been performed by some other structure than the GM muscle. Based on findings from Lai et al.,38 it seems that all 3 TS muscles function similarly (i.e., they shorten throughout stance) during running. Therefore, it is plausible to speculate that the AT performed the remaining “shortening” in the stiff condition to maintain the same ankle joint angles and return more strain energy. These results indicated that this additional energy return by the AT could allow the GM (and potentially the entire TS muscle) to operate on a more favorable position of the muscle’s forcelengthvelocity relationship. This has been hypothesized to reduce muscle fatigue and delay the onset of joint work redistribution, therefore mitigating the steady increases in the energy cost of running that are typically observed during long-distance running events.911,39TagedEn TagedPA recently published study investigated how running in footwear with differently stiff carbon fiber plates can affect the soleus muscle fascicle dynamics and running economy.40 The authors did not find any differences in soleus fascicle pennation, force, length, velocity, or stride-average soleus active muscle volume due to altered MBS during running. Beck et al.40 therefore concluded that inserting carbon fiber plates in shoes may not improve running economy. Even though it seems that the soleus muscle function was not altered by footwear of various MBS when running at 3.5 m/s, there are two major reasons as to why it would still be possible to see differences in muscle function in a setup similar to our study. First, although the individual TS muscles are thought to function similarly during running, Lai et al.38 have demonstrated that there are subtle differences in fascicle length changes between the soleus and gastrocnemii muscles. Namely, the GM muscle fascicles exhibit the greatest length changes of all TS muscles during the stance phase of running. It is therefore reasonable to speculate that if changes in muscle fascicle shortening and/ or shortening velocity exist between stiffness conditions, they are more likely to be found at a muscle with greater absolute length changes during stance. Meaningful differences in muscle function could still exist between stiffness conditions, but maybe not at the soleus. Second, Beck et al.40 tested their participants while running at 3.5 m/s, whereas participants in our study ran at 90% of their individual sLT. Choosing a relative speed has the advantage that participants run at relative intensities, so it better represents their substrate utilization and energy yield per volume of oxygen.31 At higher relative speeds and intensities, it is possible that differences in muscle function are likelier to be found at muscles containing more Type II (or fast-twitch) fibers. Muscles of different fiber type composition could therefore be affected differently by inserting carbon fiber plates in shoes during running.TagedEn TagedPThe findings of this study showed that peak ankle extension moments decreased with increasing running distance. More importantly, these ankle joint moments started decreasing later in the stiff than in the control condition. This could be indicative of delayed fatigue of the major ankle plantarflexor muscles1 when running in footwear with increased MBS. Additionally, peak ankle extension velocities were lower and stance times were longer in the stiff condition. If it is assumed that ankle extension velocities can be descriptive of ankle extensor MTU function,22,25 these reduced velocities could indicate that the TS muscle and/or the AT operate at reduced shortening velocities. These speculations are supported by the increased stance times observed in this study when running in footwear with increased MBS, which would allow the MTU to shorten at slower velocities while maintaining similar shortening lengths.TagedEn 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866 867 868 869 870 871 872 873 874 875 876 TagedH24.2. Subgroup analysisTagedEn agedPIT n this study, a subgroup analysis was performed to determine if running shoes with extremely stiff carbon fiber plates (i.e., Stiffer, 13.28 N/mm) would affect joint-specific positive work differently from the beginning to the end of a prolonged run when compared to a footwear condition with carbon fiber plates more likely to be found on the current sporting goods market (i.e., Stiff, 6.46 N/mm). The findings of this study showed no significant difference in joint-specific positive work changes from the beginning to the end of the run between Stiff and Stiffer. This suggests that a delayed onset of joint work redistribution can already be achieved by using carbon fiber plates of moderate bending stiffness. It needs to be noted, however, that the carbon fiber plates embedded in commercially available marathon racing shoes are typically curved near the MTP joint. The carbon fiber plates used in this study, however, were straight. Results from a preliminary study showed that ankle push-off moments were higher when running in shoes with straight compared to curved carbon fiber plates.41 This suggests the likelihood that there are some differences in the functions of curved and straight carbon fiber plates. However, both curved14,16,17 and straight plates13,30 have been shown to improve the energy cost of running. Perhaps similar effects on the onset of lower limb joint work redistribution could be observed during a prolonged run in Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007 877 878 879 880 881 882 883 884 885 886 887 888 889 890 891 892 893 894 895 896 897 898 899 900 901 902 ARTICLE IN PRESS TagedEnShoe Stiffness Effects on Joint Work Redistribution 903 904 905 906 currently available marathon racing shoes, which have curved carbon fiber plates embedded. The effects of plate curvature on running mechanics will need to be investigated in more detail by future studies.TagedEn 907 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 TagedH24.3. LimitationsTagedEn T here are some limitations associated with this study. The agedPT sample used for comparing Stiff to Stiffer was low. This likely decreased the power of our statistical analysis, causing us to potentially underestimate the effects of differently stiff plates on joint work redistribution. Furthermore, not all participants were tested in all stiffness conditions. This would have allowed us to parse out subtle distinctions between different stiffnesses of carbon fiber plates. The control shoe used in this study had a low MBS. It is therefore possible that when running in other commercially available running shoes, which already have a higher MBS, the disparity in joint work redistribution may be smaller. The joint work considered in this study consisted of the sagittal plane work alone. Another recent study has shown that prolonged running can affect non-sagittal plane kinematics.42 It is unknown, however, if these changes in non-sagittal plane kinematics can alter the total work performed at joints as no kinetics were reported. Our study only reported sagittal plane joint work because the main focus of this investigation was to estimate the contribution of the joint flexor/extensor muscle groups. Also, the sagittal plane work has been shown to be the major determinant of total joint work during human gait.43 Furthermore, we did not control for the striking pattern of the runners. Although a recent study suggested that lower limb joint work may not be redistributed proximally during prolonged running in habitual rearfoot strikers,44 our study confirmed previous findings from Sanno et al.1 irrespective of striking pattern. Our analysis showed that the runners’ ankles were in a dorsiflexed position at heel-strike, suggesting a rearfoot striking pattern (Supplementary Table 6). More important, however, there was no effect of distance or shoe, and no interaction effect on the striking pattern. The changes in positive lower limb joint work from the beginning to the end of the run were 5.14% and 4.76% for the ankle and knee joints, respectively. This is smaller than the minimal detectible change, which is likely related to the high betweensubject variability in relative joint work contributions when running over a prolonged distance; however, the order of magnitude is well comparable to the findings by Sanno et al.1 (i.e., ankle: 8%, knee: 4%). The changes in relative joint work due to running in differently stiff shoes were of smaller magnitude than the changes observed due to the prolonged run (Table 1). This, however, was expected based on previously reported findings by Cigoja et al.19 Furthermore, we applied markers directly on the skin overlying anatomical landmarks, which may have resulted in vibration of the markers during running. This vibration, however, can be considered similar between shoe conditions and running distances as marker placements did not change. Therefore, marker vibrations are unlikely to have affected the conclusions of this study. Lastly, we did not directly assess muscle and/or whole-body metabolic cost over 9 the course of the prolonged run in both footwear conditions. Ultrasound imaging of the TS muscle (or its individual muscles) or of the AT would have enabled us to gain a deeper understanding of the ankle plantarflexor muscles and tendons, which would help with estimating the energy cost of muscle contraction and tendon energy return over the course of a prolonged run.45 The results reported in this study should be interpreted in the context of these limitations. If feasible, future studies should attempt to record expired gases and in vivo TS muscle fascicle or AT behaviour in order to determine the change in energy cost of running and to estimate muscle energy cost or tendon energy return.TagedEn 960 961 962 963 964 965 966 967 968 969 970 971 972 TagedH15. ConclusionTagedEn T rolonged running in footwear with increased MBS agedPP resulted in a delayed onset of lower limb joint work redistribution from distal to proximal joints as compared to a control condition. This delayed onset of joint work redistribution toward more proximal joints could be metabolically beneficial because MTUs crossing distal joints are thought to be better equipped for elastic energy storage and return and have smaller muscle volume compared to MTUs crossing more proximal joints. Furthermore, this delayed onset of lower limb joint work redistribution could also be related to previously reported performance benefits when running in footwear with increased MBS.TagedEn 973 974 975 976 977 978 979 980 981 982 983 984 985 986 987 TagedH1Authors’ contributionsTagedEn T C conceptualized the study, collected, processed, and anaagedPS lyzed the data, interpreted the results, and wrote the initial draft of the manuscript; JRF conceptualized the study, analyzed the data, interpreted the results, and revised the manuscript; BMN conceptualized the study, interpreted the results, and revised the manuscript. All authors have read and approved the final version of the manuscript, and agree with the order of presentation of the authors.TagedEn 988 989 990 991 992 993 994 995 996 997 998 TagedH1Declaration of Competing interestsTagedEn TagedPThe authors declare that they have no competing interests.TagedEn 999 1000 1001 1002 TagedH1AcknowledgmentsTagedEn T upported by the International Society of Biomechanics in agedPS Sports Student Mini Research Grant awarded to SC.TagedEn TagedH1Supplementary materialsTagedEn T upplementary material associated with this article can be agedPS found, in the online version, at doi:10.1016/j.jshs.2020.12.007.TagedEn TagedH1ReferencesTagedEn TagedP 1. Sanno M, Willwacher S, Epro G, Br€uggemann GP. Positive work contribution shifts from distal to proximal joints during a prolonged run. 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Farina EM, Haigh D, Luo G. Creating footwear for performance running. Footwear Sci 2019;11(Suppl. 1):134–5.TagedEn TagedP42. Willwacher S, Sanno M, Br€ uggemann GP. Fatigue matters: an intense 10 km run alters frontal and transverse plane joint kinematics in competitive and recreational adult runners. Gait Posture 2020;76:277–83.TagedEn TagedP43. Buczek FL, Kepple TM, Siegel KL, Stanhope SJ. Translational and rotational joint power terms in a six degree-of-freedom model of the normal ankle complex. J Biomech 1994;27:1447–57.TagedEn TagedP44. Melaro JA, Gruber AH, Paquette MR. Joint work is not shifted proximally after a long run in rearfoot strike runners. J Sports Sci 2020;13:1–6. doi:10.1080/02640414.2020.1804807.TagedEn TagedP45. Fletcher JR, MacIntosh BR. Theoretical considerations for muscle-energy savings during distance running. J Biomech 2018;73:73–9.TagedEn 1074 1075 1076 1077 1078 1079 1080 1081 1082 1083 1084 1085 1086 1087 1088 1089 1090 1091 1092 1093 1094 1095 1096 1097 1098 1099 1100 1101 1102 1103 1104 1105 1106 1107 1108 1109 1110 1111 1112 1113 1114 1115 1116 1117 1118 1119 1120 1121 1122 1123 1067 1124 1068 1125 1069 1126 1070 1127 1071 1128 1072 1129 1073 1130 Please cite this article as: Sasa Cigoja et al., Can changes in midsole bending stiffness of shoes affect the onset of joint work redistribution during a prolonged run?, Journal of Sport and Health Science (2021), https://doi.org/10.1016/j.jshs.2020.12.007