The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stability

Ross E Smith; Andrew D Shelton; Gregory S Sawicki; Jason R Franz

doi:10.1371/journal.pone.0302021

. 2024 Apr 16;19(4):e0302021. doi: 10.1371/journal.pone.0302021

The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stability

Ross E Smith ¹, Andrew D Shelton ¹, Gregory S Sawicki ^2,³, Jason R Franz ^1,^*

Editor: Laura-Anne Marie Furlong⁴

PMCID: PMC11020829 PMID: 38625839

Abstract

Falls among older adults are a costly public health concern. Such falls can be precipitated by balance disturbances, after which a recovery strategy requiring rapid, high force outputs is necessary. Sarcopenia among older adults likely diminishes their ability to produce the forces necessary to arrest gait instability. Age-related changes to tendon stiffness may also delay muscle stretch and afferent feedback and decrease force transmission, worsening fall outcomes. However, the association between muscle strength, tendon stiffness, and gait instability is not well established. Given the ankle’s proximity to the onset of many walking balance disturbances, we examined the relation between both plantarflexor strength and Achilles tendon stiffness with walking-related instability during perturbed gait in older and younger adults–the latter quantified herein using margins of stability and whole-body angular momentum including the application of treadmill-induced slip perturbations. Older and younger adults did not differ in plantarflexor strength, but Achilles tendon stiffness was lower in older adults. Among older adults, plantarflexor weakness associated with greater whole-body angular momentum following treadmill-induced slip perturbations. Weaker older adults also appeared to walk and recover from treadmill-induced slip perturbations with more caution. This study highlights the role of plantarflexor strength and Achilles tendon stiffness in regulating lateral gait stability in older adults, which may be targets for training protocols seeking to minimize fall risk and injury severity.

1. Introduction

Up to 35% of older adults fall annually, resulting in serious injuries and significant healthcare costs. Moreover, the likelihood of incurring severe injuries from a fall increase with age [1]. The nature of age-related falls risk is likely multifactorial, and the literature has catalogued numerous environmental and intrinsic factors that may precipitate or, with proper intervention, help prevent falls from occurring [2–5]. Unfortunately, despite these efforts, these concerns are accelerating; in the last 10 years, the death rate from falls has increased nearly 30% and fall-related hospitalizations among older adults has increased more than 200% [6]. Thus, there remains a critical need to identify novel, evidence-based, and modifiable factors to increase older adults’ resilience against balance challenges to mitigate the severity of fall-related injuries.

Balance perturbations precipitating falls are most commonly experienced during walking, where mitigation of instability requires rapid repositioning of the base of support and sufficient ground reaction forces from the musculoskeletal system to arrest momentum. In younger adults, dynamic balance recovery following gait perturbations are partly dependent on large, rapid leg extensor moments [7, 8]. With advanced age, adults experience sarcopenia [9, 10] and decreased muscle strength [11, 12], which would intuitively hinder balance recovery in older adults. Indeed, older adults with reduced maximal isometric leg press strength are more likely to fall [13]. Also, older adults are known to have age-related reductions in series elastic tissue stiffness [14–17]. In addition to disrupting metabolic walking cost and plantarflexor muscle neuromechanics [18], decreased tissue stiffness is associated with reducing maximal joint torque by increasing muscle shortening velocities [19–21] and increasing electromechanical delay [22], both of which likely impose further penalties to balance recovery in older adults.

The relationship between age-related declines in muscle-tendon unit (MTU) integrity and dynamic stability has been explored during a variety of tasks. Due to the nature of common, real-world balance perturbations (e.g. tripping, slipping) and the ankle’s proximity to the onset of such perturbations, the triceps surae and Achilles tendon are often the locus of investigation for this relationship. Onambele et al. [16] found older adults were more unstable, had weaker ankle plantaflexors and lesser Achilles tendon stiffness (k_AT) compared to younger adults showed during single-leg stance and tandem stance. During simulated forward falling, older adults took more steps to recover than younger adults, and had weaker knee and ankle extensors, as well as less stiff patellar tendons with no difference in k_AT [23, 24]. While neither of these experimental tasks involve gait, both indicate age-related declines in MTU integrity are important to postural stability. Considering gait stability in response to perturbations, Epro et al. [25] showed older adult women with stronger ankle plantarflexors and greater k_AT had better gait stability after unexpected treadmill belt accelerations. However, they later found increases in MTU capacity at the ankle through exercise had minimal effects on balance recovery in a similar population [26]. Most recently, Debelle et al. [8] showed that age-related declines in MTU integrity were not related to balance recovery, as older and younger adults showed similar margins of stability in the anteroposterior (AP) direction. This finding is unusual, as older adults are often reported to be more unstable in the AP direction than younger adults immediately following AP balance perturbations [24, 27, 28], which the authors attribute to a comparatively young “older adult” sample. Furthermore, recent literature demonstrated that AP gait perturbations were more closely correlated with compensatory efforts in the mediolateral (ML) direction during balance recovery [29]. Given that ML balance is disproportionately worsened with age [30, 31], related to increased falls risk [32], and is known to require greater active sensorimotor control from leg muscles [33], quantification of the relationship between MTU integrity and both AP and ML stability may provide novel insight into why older adults are more vulnerable to falls following gait perturbations.

Overall, the evidence concerning age-related declines in MTU integrity and their effect on older adults’ gait stability is not clear, as older adult groups have inconsistently reported age-range cutoffs; the existing literature differ among perturbation paradigms (e.g. forward falling, mechanical pulling or “trip”, and slip); of these studies concerned with gait perturbations, none report metrics concerning mediolateral stability in either young or older adults; and Achilles and patellar tendon stiffness are inconsistently different between older and younger adults when correlated with any of the various stability metrics. Therefore, our purpose was to determine whether ankle plantarflexor muscle strength and k_AT associated with vulnerability to walking treadmill-induced slip perturbations in both young and older adults, which is summarized in Fig 1. We first hypothesized that older adults would exhibit reduced plantarflexor strength and lesser k_AT. Additionally, reductions in plantarflexor strength and k_AT. would be correlated with larger perturbation-induced changes due to treadmill-induced slips when compared to younger adults. Ultimately, data in support of these associations would implicate age-related reductions in ankle plantarflexor muscle strength and k_AT as local MTU mechanisms, revealing potentially modifiable factors underlying the instability elicited by slips or the severity of falling-related injuries.

Fig 1 — A) The onset of a balance perturbation elicits a rapid change in joint position and thus muscle-tendon unit (MTU) lengthening. B) Lesser Achilles tendon stiffness (kAT) in older adults delays the transmission between ΔMTU length and muscle stretch (i.e., ΔLm), thereby delaying afferent detection of the perturbation compared to younger adults. C) Lesser plantarflexor muscle strength (FPF) in older adults reduces force responsiveness during perturbation recovery. D) Age-related decreases in kAT and FPF predispose older adults to increased vulnerability to unexpected balance disturbances.

2. Methods

2.1 Participants

22 healthy younger adults (10 female, age: 21.7 ± 2.0 yrs, height: 1.72 ± 0.08 m, mass: 66.4 ± 8.6 kg) and 21 healthy older adults (13 female, age: 74.0 ± 6.0 yrs, age range: 65–87, height: 1.69 ± 0.11 m, mass: 69.5 ± 18.6 kg) participated. Participants were included that had no history of neurological diseases, lower limb injury within the last 6 months, and who could walk without an assistive device. All experimental procedures and recruitment procedures were approved by the University of North Carolina at Chapel Hill Institutional Review Board (20–0555). Participant recruitment began on 4/14/20 and continued until 12/31/22. All participants gave their written informed consent prior to participation in the experimental protocols.

2.2 Experimental procedures

The laboratory visit began by recording participants’ preferred walking speed using photocells (Bower Timing Systems, Draper, Utah, USA) from the average time of four 30-meter walking trials. Participants then completed a 3-minute warm-up walking trial on a dual-belt, instrumented treadmill (Bertec, Columbus, Ohio, USA). Participants then completed two treadmill walking trials–namely, 2 minutes of usual, unperturbed walking and walking while responding to treadmill-induced slip perturbations of a duration (200 ms) and acceleration (6 m/s²) shown to elicit walking-related instability. The perturbations were applied randomly at 5 heel strikes on each leg, each separated by at least 10 steps [34–36]. For all walking trials after the warm-up, a 14-camera motion capture system (Motion Analysis Corporation, Rohnert Park, California, USA) operating at 100 Hz captured the 3D positions of retroreflective markers placed on the anterior and posterior iliac spines, sacrum, lateral femoral condyles, lateral malleoli, posterior calcanei, first and fifth metatarsal heads, acromial, 7^th cervical spine, 10^th thoracic spine, sternum, and the sternal notch plus an additional 14 tracking markers placed in clusters on the lateral thighs and shanks.

At the conclusion of the visit, we used in vivo ultrasound imaging to characterize plantarflexor strength and k_AT. For the former, participants performed two maximal voluntary isometric plantarflexion contractions (MVIC_PF) on a dynamometer (Biodex System 4 Pro, Shirley, New York, USA) with the ankle at 90° (neutral) and the knee flexed to 20°. All participants received identical verbal encouragement to give maximal effort (i.e. “push the ball of your foot like a gas pedal as hard as possible using only your calf muscles”), and adequate rest time was given between two repetitions to avoid fatigue. For the latter, we recorded the position of participants’ distal medial gastrocnemius musculotendinous junction (MTJ) with the Achilles tendon (AT) using B-mode ultrasound images while participants performed two passive, isokinetic ankle rotations (20°/s) from 20° plantarflexion to 30° dorsiflexion on the same dynamometer. The ultrasound system operated at 61 fps at a depth of 50 mm using a 60 mm linear array transducer (LV7.5/60/128Z-2, UAB Telemed, Vilnius, Lithuania) secured to the posterior shank using a custom probe mount and self-adhesive bandaging. Even bandage pressure over the probe was applied to so as not to alter muscle geometry within the image [37]. We collected motion capture from a posterior calcaneal marker as well as a marker triad rigidly affixed to the ultrasound transducer to estimate AT length change (detailed in Section 2.3.2).

2.3 Data processing and analysis

2.3.1 Kinematic data

All marker data were filtered using a 4^th order low-pass Butterworth filter with a cutoff frequency of 12 Hz. We also included a static standing calibration and hip circumduction task to establish segmental dimensions, knee and ankle joint centers, and functional hip joint centers.

2.3.2 Plantarflexor strength and Achilles tendon stiffness

We calculated plantarflexor strength from the greater of the two peak ankle moment values per participant measured during MVIC_PF trials. All MVIC_PF values are normalized to body mass. For k_AT, two investigators manually tracked the MTJ positions for both age groups, which were divided evenly between them to ensure scientific rigor (Tracker, V 6.0.10). The trackers selected the most distal location of the gastrocnemius muscle before intersection with the AT. Based on published experience [38], the positional change of MTJ during isokinetic ankle rotations is relatively linear. Thus we manually identified the orientation of the distal deep and superficial aponeuroses every fifth frame, and their intersection defined the MTJ position, then interpolated MTJ position over the range of ankle joint rotation. The tracked 2D MTJ position data were transformed into a common coordinate system using marker data from the ultrasound probe. The distance between the transformed 3D MTJ position and the posterior calcaneus marker (i.e., a surrogate for AT insertion) was used to estimate AT length. We calculated AT force by dividing the measured ankle moment by a generalized AT moment arm length from previously published literature [39]. We assumed constant values for Achilles tendon moment arms, though we acknowledge that these measures can vary with joint position and muscle loading [40]. However, our previously published data suggest that those variations are disproportionately small and insensitive to the effects of muscle loading in dorsiflexion. We opted to analyze only dorsiflexion ranges of motion for our estimates of Achilles tendon stiffness not only to avoid errors from the tendon’s dorsoventral curvature, but also from inter-individual variation in resting length. Finally, we calculated k_AT as the change in AT force divided by the change in AT length between 20 and 80% of passive dorsiflexion rotation range. For all participants, k_AT values were averaged between the two passive dorsiflexion trials.

2.3.3 Balance outcomes

We included two outcomes that quantify fundamentally-different content related to walking stability–namely, whole-body angular momentum (WBAM) and margin of stability (MoS). WBAM quantifies the summed maintenance and control of the momentum of individual body segments. Conversely, MoS quantifies a biophysical relation between the body’s center of mass (CoM) and the base of support. Both are critical features of walking balance and vulnerability to treadmill-induced slip perturbations.

To calculate WBAM, we used participant-specific computational simulations implemented in OpenSim to determine segmental center of mass (CoM) positions and velocities. WBAM was calculated using previously published methods [41]. We normalized WBAM values to participant body mass (kg), height (m), and walking speed (m/s). Values are reported as a percentage of the gait cycle and averaged across the unperturbed walking trial in the frontal, transverse, and sagittal planes. We extracted the range from minimum to maximum WBAM values during unperturbed and perturbed walking across the gait cycle in all planes (i.e. WBAM_SagRange, WBAM_FrontRange, WBAM_TransRange), as well as perturbation-induced effects as the difference from unperturbed walking in all planes (i.e. ΔWBAM_Sag, ΔWBAM_Front, ΔWBAM_Trans).

As a complement to WBAM, we also calculated MoS using previously published methods [42, 43]. Briefly, ML and AP MoS (MoS_Lat, MoS_Ant) were calculated as the lateral and anterior distance, respectively, between the BoS and the extrapolated CoM projected to the treadmill belt at heel strike. We defined the lateral and anterior margins of the base of support as the fifth and first metatarsal marker, respectively. For treadmill induced slips, the heel strike of interest was that of the recovery step after the application of the perturbation, whereas any heel strike was used for unperturbed walking. We also calculated perturbation-induced effects as the percent change from unperturbed walking (i.e., ΔMoS_Lat, ΔMoS_Ant) as a way to normalize MoS within subjects.

2.4 Statistics

Independent-samples t-tests assessed the effects of age on plantarflexor strength and k_AT. We then performed a series of multivariate linear regression analyses (SPSS V28, Chicago, Illinois, USA) to assess whether plantarflexor strength (i.e., peak ankle moment) and k_AT associated with MoS and WBAM during perturbed walking or their respective perturbation-induced changes (i.e., ΔMoS). We established statistical significance for all statistical tests at p ≤ 0.05. All results are reported as mean values ± standard deviation.

3. Results

Fig 2 summarizes plantarflexor strength and k_AT in younger and older adults. Older adults (0.75 ± 0.38 Nm/kg) exhibited lesser but statistically indistinguishable values of plantarflexor strength compared to younger adults (0.78 ± 0.34 Nm/kg) (p = 0.791). Conversely, we found that older adults averaged ~30% lesser k_AT than younger adults during passive rotation (4.33±1.78 N/mm vs. 6.12±2.82 N/mm, p = 0.016). Plantarflexor strength and k_AT were not correlated (see S1 Appendix).

Table 1 summarizes all individual associations between plantarflexor strength, k_AT, and balance outcomes, whereas Figs 3–6 highlights those associations and statistically significant results. We found no correlation between our predictive variables, k_AT and plantarflexor strength (S1 Appendix), and in all cases, the collinearity threshold of various inflation factor set at 3 was not crossed. Lesser plantarflexor strength among older adults was associated with greater MoS_Lat (Fig 3) (r² = 0.194, F(1,19) = 3.053, p = 0.023). There were no other significant correlations for any other MoS metric in any plane. Among OA, greater WBAM_TransRange was associated with lesser plantarflexor strength and greater k_AT (Fig 4) (Full model-r² = 0.372, F(2,18) = 5.332, p = 0.015; Plantarflexor Torque-r² = 0.266, p = 0.008; k_AT-r² = 0.165, p = 0.034). We found no significant correlations between any metric among younger adults, or for any perturbation-induced changes (Figs 5 and 6).

Table 1. Relations between Achilles tendon stiffness and plantarflexor torque and balance outcomes during perturbed walking.

	YA				OA
	K_AT		PF Torque		K_AT		PF Torque
	r	p	r	p	r	p	r	p
Margin of Stability (MoS)
MoS_Lat	-0.339	0.061	-0.077	0.366	0.313	0.084	-0.440	0.023
ΔMoS_Lat	-0.356	0.052	-0.063	0.390	-0.249	0.138	-0.019	0.467
MoS_Ant	-0.144	0.262	-0.204	0.181	0.084	0.359	-0.152	0.255
ΔMoS_Ant	-0.146	0.258	-0.237	0.144	-0.083	0.360	0.192	0.203
Whole-body Angular Momentum (WBAM)
WBAM_SagRange	-0.011	0.480	-0.180	0.212	0.018	0.469	-0.158	0.247
ΔWBAM_Sag	0.079	0.363	-0.232	0.150	0.003	0.495	-0.091	0.347
WBAM_FrontRange	-0.049	0.414	-0.203	0.182	0.155	0.311	-0.347	0.065
ΔWBAM_Front	0.064	0.388	-0.082	0.359	-0.135	0.279	-0.161	0.242
WBAM_TransRange	-0.001	0.498	-0.213	0.170	0.406	0.034	-0.516	0.008
ΔWBAM_Trans	0.341	0.060	-0.085	0.354	-0.015	0.474	-0.153	0.253

Open in a new tab

Fig 3 — Individual average peak plantarflexor torque, Achilles tendon stiffness (k_AT), mediolateral (MoS_Lat) and anteroposterior (MoS_Antt) direction margins of stability for older (solid line and solid dot, n = 21) and younger (dashed line and open dot, n = 22) adults during the recovery step following treadmill-induced slip perturbations. Lines of best fit for both groups are shown and significant correlations are depicted per group by their corresponding r-value accompanied by an asterisk. (p = 0.05).

Fig 6 — Individual average peak plantarflexor torque, Achilles tendon stiffness (k_AT), and relative whole-body angular momentum in the sagittal (ΔWBAM_SagRange), frontal (ΔWBAM_FrontRange), and transverse planes (ΔWBAM_TransRange) for older (solid line and solid dot, n = 21) and younger (dashed line and open dot, n = 22) adults during the recovery step following treadmill-induced slip perturbations. Lines of best fit for both groups are shown and significant correlations are depicted per group by their corresponding r-value accompanied by an asterisk. (p = 0.05).

Fig 4 — Individual average peak plantarflexor torque, Achilles tendon stiffness (k_AT), and whole-body angular momentum in the sagittal (WBAM_SagRange), frontal (WBAM_FrontRange), and transverse planes (WBAM_TransRange) for older (solid line and solid dot, n = 21) and younger (dashed line and open dot, n = 22) adults during during the recovery step following treadmill-induced slip perturbations. Lines of best fit for both groups are shown and significant correlations are depicted per group by their corresponding r-value accompanied by an asterisk. (p = 0.05).

Fig 5 — Individual average peak plantarflexor torque, Achilles tendon stiffness (k_AT), relative mediolateral (ΔMoS_Lat) and anteroposterior (ΔMoS_Ant) direction margins of stability for older (solid line and solid dot, n = 21) and younger (dashed line and open dot, n = 22) adults during the recovery step following treadmill-induced slip perturbations. Lines of best fit for both groups are shown and significant correlations are depicted per group by their corresponding r-value accompanied by an asterisk. (p = 0.05).

4. Discussion

Our purpose was to determine whether plantarflexor muscle strength and k_AT associated with the effect of walking treadmill-induced slip perturbations on dynamic balance recovery across a cohort of younger and older adults. Our results were in partial agreement with our hypotheses. First, older adults exhibited lesser k_AT but not lesser plantarflexor strength than younger adults. Second, we revealed associations between both plantarflexor strength and k_AT and key balance outcomes. For example, we found that weaker older adults generally exhibited greater vulnerability (i.e. larger WBAM) in the transverse plane following treadmill-induced slip perturbations. Together, these results reveal specific features of muscle-tendon units spanning the ankle that are relevant to walking balance control and which may be targeted through exercise interventions to mitigate the risk of falls among older adults.

In this study, older adults had similar plantarflexor strength as young adults during MVIC_PF contractions. Given the well-documented nature of age-related declines in muscle strength, similar values between age groups were surprising. We may attribute our uncharacteristically strong older adults as a potential feature of their high physical activity levels documented using a standard health screening. Another explanation may be that normalized ankle torque values among our younger adults are low when compared with previously reported values [8, 16, 24], which could result from misalignment of ankle joint rotation axes with that of the dynamometer or insufficient recruitment of ankle musculature in younger adults. As we accounted for alignment of dynamometer and ankle joint axes of rotation in our setup [44] and gave consistent vocal encouragement for maximal effort to all participants [45], it is unclear why MVIC_PF torque values among our younger adults were low in comparison with previous values. Nevertheless, only older adults with weaker plantarflexors had perturbation-induced changes to their stability, which we first discuss for WBAM and then for MoS. Regulation of sagittal-plane WBAM is considered a critical feature of walking stability [46, 47] and balance recovery [48, 49]. Notably, a hip-dominant strategy was previously identified for controlling sagittal-plane WBAM following combined slip and upper-body perturbations acting in opposite directions for healthy young adults [49]. Sagittal-plane WBAM was similar between fallers and non-fallers in a small sample of older adults walking at their preferred speed [50]. However, we also showed that plantarflexor strength can differentiate older adults’ ability to control WBAM in the transverse plane following a treadmill-induced slip perturbation. This idea is supported by findings that demonstrated the plantarflexors’ contributions to controlling WBAM in outside of the sagittal plane to counteract angular momentum of the body’s center of mass [51, 52]. Thus, stronger plantarflexors would provide a mechanism to mitigate increased transverse-plane WBAM following a treadmill-induced slip perturbation.

Older adults with weaker plantarflexors exhibited larger MoS_Lat when responding to treadmill-induced slip perturbations–an outcome that would represent a more stable gait by common interpretations [42, 43]. Although this finding is initially counterintuitive, it is not in itself novel. Mademli and Arampatzis [53] showed that older adults walk normally with higher MoS_Ant than younger adults. Those authors interpreted their findings as indicative of a more cautious strategy adopted by older adults. As evidenced by our results, we contend that this strategy also affects how relatively weaker adults attenuate perturbations, particularly in the ML direction. Ultimately, perhaps strength represents a measure of balance recovery confidence, where stronger older adults were more comfortable operating nearer their limits of stability when attenuating a treadmill-induced slip perturbation. This concept extends the interpretation of MoS to consider task context and habitual behaviors like walking speed when cataloging the literature on both steady-state gait behaviors and responses to walking balance perturbations.

Older adults exhibited ~30% less Achilles tendon stiffness than younger adults, consistent in magnitude with many previous reports on passive and active isolated contractions [16, 17]. We obtained k_AT values during passive rotations, which explains relative differences in the magnitude of our values compared to previous literature. We opted for passive rotations given the nature of sensing unexpected disturbances to ankle joint position. Nevertheless, this methodological decision also suggests that age-related decreases in tendon stiffness occur across a broad range of the stress-strain curve. Previous authors have reported no significant correlation between muscle strength and tendon stiffness for structures spanning the ankle [54] or knee [55] in sedentary or low-activity level young adults. Conversely, in trained cyclists and healthy young adults, respectively, Morrison et al. [56] and Muraoka et al. [57] found a significant correlation between plantarflexor strength and k_AT. Epro et al. [25] similarly found k_AT was significantly greater in a stronger group of older women. Notably, these prior k_AT values were taken from MVIC_PF in contrast to the k_AT from passive rotations reported here.

Authors with similar motivations to link MTU integrity to balance recovery have reported similar relationships in their work. For example, Epro et al. [25] differentiated two groups of older women via ankle plantarflexor strength (i.e., “strong” and “weak”). Those authors found that, following unexpected treadmill belt accelerations perturbations, stronger older women had higher k_AT and greater MoS_Ant than weaker older women in subsequent recovery steps. By contrast, Debelle et al. [8] found typical age-related differences in k_AT but no age-related differences in MoS_Ant during steady-state walking. Due to the nature of treadmill-induced slip perturbations, an anterior balance disturbance would intuitively require compensatory actions from the body in the sagittal plane. Ultimately, our data indicate similar balance responses to treadmill-induced slip perturbations in the direction of action across differences in age, muscle strength, and k_AT. However, our data reveals plantarflexor strength affects older adult’s vulnerability to treadmill-induced slip perturbations in the transverse and frontal planes. Recent findings from Leestma et al. [29] using multi-directional, ground translation perturbations found that increases in WBAM following perturbations were more strongly correlated with mediolateral balance recovery metrics like step width than with anteroposterior balance recovery metrics (i.e. step width). These results indicate that walking balance and balance recovery following perturbations in the AP direction are dependent upon ML recovery strategies. Thus, while literature has focused largely on AP-direction recovery strategies during perturbed walking, future study is warranted to examine the neuromechanical responses of leg muscles acting primarily in the frontal and transverse planes following AP walking balance perturbations.

We hypothesized that higher k_AT would be associated with better stability following treadmill-induced slip perturbations. We instead found that older adults with stiffer Achilles tendons had greater WBAM_TransRange in response to treadmill-induced slips. As plantarflexor strength and k_AT were not correlated in our study, we cannot attribute the increase in WBAM_TransRange to be another consequence of faster walking speeds. Intuitively, a stiffer Achilles tendon might increase the strut-like function of the ankle by increasing force transmission from the plantarflexors at the perturbation, acting to vault the body forward. However, this affect would presumably also be apparent in WBAM_SagRange or ΔWBAM_Sag, where we saw no correlation with k_AT. Thus, considering this and previous work exploring similar motivations, the relationship between tendon stiffness and perturbed walking balance control is still unclear. As balance control following a perturbation is a multi-faceted neuromuscular process, it may be that tendon stiffness at a single joint is not sufficient to explain whole-body mechanics. However, due to the well-established declines in proprioceptive acuity among older adults, future investigations may benefit from examining the effect of tendon stiffness on local muscle reflex responses and balance perturbation detection.

The results of this study may be immediately applicable to clinicians seeking to mitigate falls and fall injury severity. Notably, Debelle et al. [8] concluded that training would likely have minimal effects on balance recovery after finding correlations between neither k_AT nor plantarflexor strength and MoS_Ant. Our data corroborate this suggestion pertaining to balance recovery in the AP direction, but we provide novel insight into the importance of plantarflexor strength for balance recovery in the frontal and transverse planes in older adults. These findings seem especially pertinent as older adults’ anteroposterior stability is largely regulated by pendular mechanics, while frontal stability is largely regulated through muscular recruitment and is disproportionately afflicted during normal walking and following balance perturbations in older adults [31, 32].

This study has several experimental limitations. First, we examined WBAM in a model that neglected the arm segments and thus the specific magnitude of our outcomes and associations may differ modestly with their inclusion. Another possible limitation is that participants completed all walking trials at their preferred speed, which yielded a slower walking speed for older than younger adults. However, we believe this improves the ecological validity of our findings. Finally, we used only one perturbation paradigm (treadmill-induced slips) and treadmill-induced slip perturbation responses are likely to vary significantly between various contexts. Our study focused only on measures of MTU integrity and their relationship to gait stability following balance perturbation. However, there are many other sensory feedback mechanisms that are equally or even more involved in regulating walking balance (e.g. vestibular, visual). Our measures of Achilles tendon elongation assume a straight-line distance between the MTJ and calcaneal insertion. While there is curvature of the Achilles tendon, it primarily affects tendon force-length curves at larger values of plantarflexion, which our ankle rotation data purposefully excludes. In conclusion, we have presented novel findings indicating a potentially modifiable factor relevant to accommodating treadmill-induced slip perturbations. Plantarflexor strength can be improved through targeted training in older adults and may provide vital protection against fall risk and helping mitigate the severity of fall-related injuries. Future research should seek to identify if other muscles with mechanical actions specific to the frontal plane are also related to walking balance recovery, and if older adults have improved balance recovery following training protocols that improve plantarflexor strength. Additionally, investigating the ability of stiffer tendons to impact local muscle neural responses to balance perturbations may provide mechanistic insights into the relationship between tendon stiffness and balance control.

Supporting information

S1 Appendix. Plantarflexor strength and Achilles tendon stiffness relations.

Individual average peak plantarflexor torque and Achilles tendon stiffness (k_AT) for older (solid line, n = 21) and younger (dashed line, n = 22) adults. Lines of best fit for both groups are shown and significant correlations are depicted per group by their corresponding r-value accompanied by an asterisk. (p = 0.05).

(TIF)

pone.0302021.s001.tif^{(412.6KB, tif)}

Acknowledgments

We would like to acknowledge Yujin Kwon for their assistance in data processing.

Data Availability

A .mat master data file is available here: https://cdr.lib.unc.edu/concern/data_sets/6d5707327.

Funding Statement

This project was supported by NIH Grants R01AG058615 to JRF and GSS and R21AG067388 to JRF. National Institutes of Health (nih.gov). These sponsors played no role in study design, data collection or analysis, decision to publish, or preparation of the manuscript.

References

1.Hartholt KA, van Beeck EF, Polinder S, van der Velde N, van Lieshout EM, Panneman MJ, et al. Societal consequences of falls in the older population: injuries, healthcare costs, and long-term reduced quality of life. Journal of Trauma. 2011;71(3):748–53. doi: 10.1097/TA.0b013e3181f6f5e5 . [DOI] [PubMed] [Google Scholar]
2.Graafmans WC, Ooms ME, Hofstee HM, Bezemer PD, Bouter LM, Lips P. Falls in the elderly: a prospective study of risk factors and risk profiles. American Journal of Epidemiology. 1996;143(11):1129–36. doi: 10.1093/oxfordjournals.aje.a008690 . [DOI] [PubMed] [Google Scholar]
3.De Almeida ST, Chaves Soldera CL, De Carli GA, Gomes I, Lima Resende TD. Análise de fatores extrínsecos e intrínsecos que predispõem a quedas em idosos. Revista da Associação Médica Brasileira. 2012;58(4):427–33. doi: 10.1590/s0104-42302012000400012 [DOI] [PubMed] [Google Scholar]
4.Kelsey JL, Procter-Gray E, Hannan MT, Li W. Heterogeneity of Falls Among Older Adults: Implications for Public Health Prevention. American Journal of Public Health. 2012;102(11):2149–56. doi: 10.2105/AJPH.2012.300677 [DOI] [PMC free article] [PubMed] [Google Scholar]
5.Nyman SR, Ballinger C, Phillips JE, Newton R. Characteristics of outdoor falls among older people: a qualitative study. BMC Geriatrics. 2013;13(1):125. doi: 10.1186/1471-2318-13-125 [DOI] [PMC free article] [PubMed] [Google Scholar]
6.CDIS D. Falls Injury Data 2022 [7/12/2023]. Available from: https://injuryfreenc.dph.ncdhhs.gov/DataSurveillance/FallsData.htm#:~:text=As%20our%20population%20ages%2C%20fall,for%20individuals%2065%20and%20older.
7.Debelle H, Harkness-Armstrong C, Hadwin K, Maganaris CN, O’Brien TD. Recovery From a Forward Falling Slip: Measurement of Dynamic Stability and Strength Requirements Using a Split-Belt Instrumented Treadmill. Frontiers in Sports and Active Living. 2020;2. doi: 10.3389/fspor.2020.00082 [DOI] [PMC free article] [PubMed] [Google Scholar]
8.Debelle H, Maganaris CN, O’Brien TD. Role of Knee and Ankle Extensors’ Muscle-Tendon Properties in Dynamic Balance Recovery from a Simulated Slip. Sensors. 2022;22(9):3483. doi: 10.3390/s22093483 [DOI] [PMC free article] [PubMed] [Google Scholar]
9.Rosenberg JG, Ryan ED, Sobolewski EJ, Scharville MJ, Thompson BJ, King GE. Reliability of panoramic ultrasound imaging to simultaneously examine muscle size and quality of the medial gastrocnemius. Muscle & nerve. 2014;49(5):736–40. Epub 2013/09/17. doi: 10.1002/mus.24061 . [DOI] [PubMed] [Google Scholar]
10.Abellan van Kan G, Cderbaum JM, Cesari M, Dahinden P, Fariello RG, Fielding RA, et al. Sarcopenia: biomarkers and imaging (International Conference on Sarcopenia research). Journal of Nutrition Health and Aging. 2011;15(10):834–46. doi: 10.1007/s12603-011-0365-1 . [DOI] [PubMed] [Google Scholar]
11.Bäckman E, Johansson V, Häger B, Sjöblom P, Henriksson KG. Isometric muscle strength and muscular endurance in normal persons aged between 17 and 70 years. Scandanavian Journal of Rehabilitation Medicine. 1995;27(2):109–17. . [PubMed] [Google Scholar]
12.Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G. Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle and Nerve. 2002;25(6):858–63. doi: 10.1002/mus.10113 . [DOI] [PubMed] [Google Scholar]
13.Pijnappels M, Van Der Burg JCE, Reeves ND, Van Dieën JH. Identification of elderly fallers by muscle strength measures. European Journal of Applied Physiology. 2008;102(5):585–92. doi: 10.1007/s00421-007-0613-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
14.Franz JR, Krupenevich RL, Gray AJ, Batsis JA, Sawicki GS. Reduced Achilles tendon stiffness in aging persists at matched activations and associates with higher metabolic cost of walking. 2023. [DOI] [PMC free article] [PubMed] [Google Scholar]
15.McCrum C, Leow P, Epro G, König M, Meijer K, Karamanidis K. Alterations in Leg Extensor Muscle-Tendon Unit Biomechanical Properties With Ageing and Mechanical Loading. Frontiers in Physiology. 2018;9. doi: 10.3389/fphys.2018.00150 [DOI] [PMC free article] [PubMed] [Google Scholar]
16.Onambele GL, Narici MV, Maganaris CN. Calf muscle-tendon properties and postural balance in old age. Journal of Applied Physiology. 2006;100(6):2048–56. Epub 20060202. doi: 10.1152/japplphysiol.01442.2005 . [DOI] [PubMed] [Google Scholar]
17.Reeves ND. Adaptation of the tendon to mechanical usage. Journal of Musculoskeletal and Neuronal Interaction. 2006;6(2):174–80. . [PubMed] [Google Scholar]
18.Krupenevich RL, Beck ON, Sawicki GS, Franz JR. Reduced Achilles Tendon Stiffness Disrupts Calf Muscle Neuromechanics in Elderly Gait. Gerontology. 2022;68(3):241–51. doi: 10.1159/000516910 [DOI] [PMC free article] [PubMed] [Google Scholar]
19.Narici MV, Maffulli N, Maganaris CN. Ageing of human muscles and tendons. Disabil Rehabil. 2008;30(20–22):1548–54. doi: 10.1080/09638280701831058 . [DOI] [PubMed] [Google Scholar]
20.Alcazar J, Csapo R, Ara I, Alegre LM. On the Shape of the Force-Velocity Relationship in Skeletal Muscles: The Linear, the Hyperbolic, and the Double-Hyperbolic. Frontiers in Physiology. 2019;10. doi: 10.3389/fphys.2019.00769 [DOI] [PMC free article] [PubMed] [Google Scholar]
21.Quinlan JI, Maganaris CN, Franchi MV, Smith K, Atherton PJ, Szewczyk NJ, et al. Muscle and Tendon Contributions to Reduced Rate of Torque Development in Healthy Older Males. The Journals of Gerontology: Series A. 2018;73(4):539–45. doi: 10.1093/gerona/glx149 [DOI] [PMC free article] [PubMed] [Google Scholar]
22.Nordez A, Gallot T, Catheline S, Guevel A, Cornu C, Hug F. Electromechanical delay revisited using very high frame rate ultrasound. J Appl Physiol (1985). 2009;106(6):1970–5. Epub 20090409. doi: 10.1152/japplphysiol.00221.2009 . [DOI] [PubMed] [Google Scholar]
23.Karamanidis K, Arampatzis A. Age-related degeneration in leg-extensor muscle-tendon units decreases recovery performance after a forward fall: compensation with running experience. Eur J Appl Physiol. 2007;99(1):73–85. Epub 20061025. doi: 10.1007/s00421-006-0318-2 . [DOI] [PubMed] [Google Scholar]
24.Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008;18(6):980–9. Epub 20070618. doi: 10.1016/j.jelekin.2007.04.003 . [DOI] [PubMed] [Google Scholar]
25.Epro G, McCrum C, Mierau A, Leyendecker M, Brüggemann G-P, Karamanidis K. Effects of triceps surae muscle strength and tendon stiffness on the reactive dynamic stability and adaptability of older female adults during perturbed walking. Journal of Applied Physiology. 2018;124(6):1541–9. doi: 10.1152/japplphysiol.00545.2017 [DOI] [PubMed] [Google Scholar]
26.Epro G, Mierau A, McCrum C, Leyendecker M, Brüggemann GP, Karamanidis K. Retention of gait stability improvements over 1.5 years in older adults: effects of perturbation exposure and triceps surae neuromuscular exercise. Journal of Neurophysiology. 2018;119(6):2229–40. doi: 10.1152/jn.00513.2017 [DOI] [PubMed] [Google Scholar]
27.König M, Epro G, Seeley J, Potthast W, Karamanidis K. Retention and generalizability of balance recovery response adaptations from trip perturbations across the adult life span. Journal of Neurophysiology. 2019;122(5):1884–93. doi: 10.1152/jn.00380.2019 [DOI] [PubMed] [Google Scholar]
28.McCrum C, Karamanidis K, Grevendonk L, Zijlstra W, Meijer K. Older adults demonstrate interlimb transfer of reactive gait adaptations to repeated unpredictable gait perturbations. GeroScience. 2020;42(1):39–49. doi: 10.1007/s11357-019-00130-x [DOI] [PMC free article] [PubMed] [Google Scholar]
29.Leestma JK, Golyski PR, Smith CR, Sawicki GS, Young AJ. Linking whole-body angular momentum and step placement during perturbed human walking. Journal of Experimental Biology. 2023;226(6). doi: 10.1242/jeb.244760 [DOI] [PMC free article] [PubMed] [Google Scholar]
30.Schrager MA, Kelly VE, Price R, Ferrucci L, Shumway-Cook A. The effects of age on medio-lateral stability during normal and narrow base walking. Gait & Posture. 2008;28(3):466–71. doi: 10.1016/j.gaitpost.2008.02.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
31.Dean JC, Alexander NB, Kuo AD. The Effect of Lateral Stabilization on Walking in Young and Old Adults. IEEE Transactions on Biomedical Engineering. 2007;54(11):1919–26. doi: 10.1109/TBME.2007.901031 [DOI] [PubMed] [Google Scholar]
32.Hilliard MJ, Martinez KM, Janssen I, Edwards B, Mille M-L, Zhang Y, et al. Lateral Balance Factors Predict Future Falls in Community-Living Older Adults. Archives of Physical Medicine and Rehabilitation. 2008;89(9):1708–13. doi: 10.1016/j.apmr.2008.01.023 [DOI] [PMC free article] [PubMed] [Google Scholar]
33.Bauby CE, Kuo AD. Active control of lateral balance in human walking. J Biomech. 2000;33(11):1433–40. doi: 10.1016/s0021-9290(00)00101-9 . [DOI] [PubMed] [Google Scholar]
34.Crenshaw JR, Grabiner MD. The influence of age on the thresholds of compensatory stepping and dynamic stability maintenance. Gait Posture. 2014;40(3):363–8. Epub 2014/06/04. doi: 10.1016/j.gaitpost.2014.05.001 . [DOI] [PubMed] [Google Scholar]
35.Lee A, Bhatt T, Pai YC. Generalization of treadmill perturbation to overground slip during gait: Effect of different perturbation distances on slip recovery. Journal of biomechanics. 2016;49(2):149–54. Epub 2015/12/15. doi: 10.1016/j.jbiomech.2015.11.021 ; PubMed Central PMCID: PMC4793378. [DOI] [PMC free article] [PubMed] [Google Scholar]
36.Liu X, Bhatt T, Pai Y-C. Intensity and generalization of treadmill slip training: High or low, progressive increase or decrease? Journal of Biomechanics. 2016;49(2):135–40. doi: 10.1016/j.jbiomech.2015.06.004 [DOI] [PMC free article] [PubMed] [Google Scholar]
37.Wakeling JM, Jackman M, Namburete AI. The effect of external compression on the mechanics of muscle contraction. Journal of Applied Biomechanics. 2013;29(3):360–4. Epub 20120822. doi: 10.1123/jab.29.3.360 . [DOI] [PubMed] [Google Scholar]
38.Krupenevich RL, Clark WH, Sawicki GS, Franz JR. Older adults overcome reduced triceps surae structural stiffness to preserve ankle joint quasi-stiffness during walking. Journal of applied biomechanics. 2020;5:1–8. doi: 10.1123/jab.2019-0340 [DOI] [PMC free article] [PubMed] [Google Scholar]
39.Rasske K, Franz JR. Aging effects on the Achilles tendon moment arm during walking. Journal of biomechanics. 2018;77:34–9. doi: 10.1016/j.jbiomech.2018.06.001 [DOI] [PMC free article] [PubMed] [Google Scholar]
40.Franz JR, Khanchandani A, McKenny H, Clark WH. Ankle Rotation and Muscle Loading Effects on the Calcaneal Tendon Moment Arm: An In Vivo Imaging and Modeling Study. Annals of Biomedical Engineering. 2019;47(2):590–600. doi: 10.1007/s10439-018-02162-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
41.Silverman AK, Neptune RR. Differences in whole-body angular momentum between below-knee amputees and non-amputees across walking speeds. Journal of Biomechanics. 2011;44(3):379–85. Epub 20101111. doi: 10.1016/j.jbiomech.2010.10.027 . [DOI] [PubMed] [Google Scholar]
42.McAndrew PM, Wilken JM, Dingwell JB. Dynamic stability of human walking in visually and mechanically destabilizing environments. Journal of biomechanics. 2011;44(4):644–9. doi: 10.1016/j.jbiomech.2010.11.007 ; PubMed Central PMCID: PMC3042508. [DOI] [PMC free article] [PubMed] [Google Scholar]
43.Hof AL, Gazendam MG, Sinke WE. The condition for dynamic stability. Journal of biomechanics. 2005;38(1):1–8. Epub 2004/11/03. doi: 10.1016/j.jbiomech.2004.03.025 . [DOI] [PubMed] [Google Scholar]
44.Arampatzis A, Morey-Klapsing G, Karamanidis K, DeMonte G, Stafilidis S, Bruggemann GP. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech. 2005;38(4):885–92. doi: 10.1016/j.jbiomech.2004.04.027 . [DOI] [PubMed] [Google Scholar]
45.Tod D, Iredale F, Gill N. ???Psyching-Up??? and Muscular Force Production. Sports Medicine. 2003;33(1):47–58. doi: 10.2165/00007256-200333010-00004 [DOI] [PubMed] [Google Scholar]
46.Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm and leg movements during human locomotion. European Journal of Neuroscience. 2001;14(11):1906–14. doi: 10.1046/j.0953-816x.2001.01813.x [DOI] [PubMed] [Google Scholar]
47.Herr H, Popovic M. Angular momentum in human walking. Journal of Experimental Biology. 2008;211(4):467–81. doi: 10.1242/jeb.008573 [DOI] [PubMed] [Google Scholar]
48.Marigold DS, Bethune AJ, Patla AE. Role of the unperturbed limb and arms in the reactive recovery response to an unexpected slip during locomotion. Journal of neurophysiology. 2003;89(4):1727–37. Epub 2003/03/04. doi: 10.1152/jn.00683.2002 . [DOI] [PubMed] [Google Scholar]
49.van Mierlo M, Ambrosius JI, Vlutters M, van Asseldonk EHF, van der Kooij H. Recovery from sagittal-plane whole body angular momentum perturbations during walking. Journal of Biomechanics. 2022;141:111169. Epub 20220603. doi: 10.1016/j.jbiomech.2022.111169 . [DOI] [PubMed] [Google Scholar]
50.Simoneau GC, Krebs DE. Whole-Body Momentum during Gait: A Preliminary Study of Non-Fallers and Frequent Fallers. Journal of Applied Biomechanics. 2000;16(1):1–13. doi: 10.1123/jab.16.1.1 [DOI] [Google Scholar]
51.Neptune RR, McGowan CP. Muscle contributions to whole-body sagittal plane angular momentum during walking. Journal of Biomechanics. 2011;44(1):6–12. doi: 10.1016/j.jbiomech.2010.08.015 [DOI] [PMC free article] [PubMed] [Google Scholar]
52.Neptune RR, McGowan CP. Muscle contributions to frontal plane angular momentum during walking. Journal of Biomechanics. 2016;49(13):2975–81. doi: 10.1016/j.jbiomech.2016.07.016 [DOI] [PMC free article] [PubMed] [Google Scholar]
53.Mademli L, Arampatzis A. Lower safety factor for old adults during walking at preferred velocity. AGE. 2014;36(3). doi: 10.1007/s11357-014-9636-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
54.Kubo K, Kanehisa H, Fukunaga T. Gender differences in the viscoelastic properties of tendon structures. European Journal of Applied Physiology. 2003;88(6):520–6. doi: 10.1007/s00421-002-0744-8 [DOI] [PubMed] [Google Scholar]
55.Onambélé GNL, Burgess K, Pearson SJ. Gender-specific in vivo measurement of the structural and mechanical properties of the human patellar tendon. Journal of Orthopaedic Research. 2007;25(12):1635–42. doi: 10.1002/jor.20404 [DOI] [PubMed] [Google Scholar]
56.Morrison SM, Dick TJM, Wakeling JM. Structural and mechanical properties of the human Achilles tendon: Sex and strength effects. Journal of Biomechanics. 2015;48(12):3530–3. doi: 10.1016/j.jbiomech.2015.06.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
57.Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H. Elastic properties of human Achilles tendon are correlated to muscle strength. J Appl Physiol (1985). 2005;99(2):665–9. Epub 20050324. doi: 10.1152/japplphysiol.00624.2004 . [DOI] [PubMed] [Google Scholar]

PLoS One. doi: 10.1371/journal.pone.0302021.r001

Decision Letter 0

Laura-Anne Marie Furlong

2 Jan 2024

PONE-D-23-30928The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stabilityPLOS ONE

Dear Dr. Franz,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. I request that you address the comments raised by both reviewers, in particular adding to/editing the presented literature where identified. A second major area which needs to be addressed are some of the issues raised related to quantification of tendon stiffness during passive rotation. I appreciate addressing this in full is ultimately a different study, but please acknowledge some of the potential measurement issues with this technique as used here.

Please submit your revised manuscript by Feb 16 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Laura-Anne Marie Furlong

Academic Editor

PLOS ONE

Journal requirements:

When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

2. Thank you for stating the following in the Acknowledgments Section of your manuscript:

“We would like to acknowledge Yujin Kwon for their assistance in data processing. This study was supported by grants from the National Institutes of Health (R21AG067388, R01AG058615).”

We note that you have provided funding information that is currently declared in your Funding Statement. However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form.

Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows:

“This project was supported by NIH Grants R01AG058615 to JRF and GSS and R21AG067388 to JRF.

National Institutes of Health (nih.gov). These sponsors played no role in study design, data collection or analysis, decision to publish, or preparation of the manuscript.”

Please include your amended statements within your cover letter; we will change the online submission form on your behalf.

3. We note that your Data Availability Statement is currently as follows: [All relevant data are within the manuscript and its Supporting Information files.]

Please confirm at this time whether or not your submission contains all raw data required to replicate the results of your study. Authors must share the “minimal data set” for their submission. PLOS defines the minimal data set to consist of the data required to replicate all study findings reported in the article, as well as related metadata and methods (https://journals.plos.org/plosone/s/data-availability#loc-minimal-data-set-definition).

For example, authors should submit the following data:

- The values behind the means, standard deviations and other measures reported;

- The values used to build graphs;

- The points extracted from images for analysis.

Authors do not need to submit their entire data set if only a portion of the data was used in the reported study.

If your submission does not contain these data, please either upload them as Supporting Information files or deposit them to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. For a list of recommended repositories, please see https://journals.plos.org/plosone/s/recommended-repositories.

If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially sensitive information, data are owned by a third-party organization, etc.) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. If data are owned by a third party, please indicate how others may request data access.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This manuscript describes an interesting study into the relationships between plantarflexor strength (a modifiable risk factor) and Achilles tendon stiffnesson gait stability in an younger and aged populations. Overall the manuscript is very well constructed, I have a few suggestions listed below.

1) I would recommend introducing the current state of knowledge on Achilles tendon stiffness (and perhaps changes with age) in the introduction.

2) In the methods section (around line 102) it may be beneficial to include a range of ages instead of just a mean/stdev given the potential variability in an older adult cohort.

3) Were any repeatability/reliability studies conducted for the process of the ultrasound image collections and stiffness calculations? Both between investigators and between sessions? If so, please include information on the reliability of this approach.

4) Having seen the data figures, I am curious if your team has performed any assessments on the variability between subjects in each group? Are the data points for each perturbed step within an individual as variable as the data between subjects? Or are there any metrics that can inform the variability (sex, age, walking speed, strength, reported activity level, body size...)?

5) Were any analyses performed comparing male and female data? I see that the subject pool was divided evenly so I'm wondering if these groups were treated separately or together in statistical comparisons.

Reviewer #2: PONE-D-23-30928

The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stability

General comments

The present study aimed to examine whether there is any association between triceps surae muscle (TS) strength as well as Achilles tendon (AT) stiffness and balance recovery responses following a slip-like perturbation in older and younger adults. The authors analysed the joint moments from maximal voluntary isometric plantarflexion contractions and the elongation of the GM MTJ during passive ankle joint rotation using an isokinetic device and simultaneous ultrasonography. AP and ML margin of stability as well as whole-body angular momentum were determined post slip-like perturbations on an instrumented treadmill using optical motion capture system. The main outcomes were that older compared to younger adults had no differences in muscle strength but revealed lower passive tendon stiffness. Among the older adults, lower muscle strength was associated with greater whole-body angular momentum following slip-like perturbations. Although the overall topic is interesting for the scientific community this manuscript is in parts weak, with several methodological limitations. Moreover, the overall topic of effects of TS MTU on balance recovery responses following a perturbation has been addressed already by several previous publications and therefore does perhaps not provide significant innovation in the current form. Below I have provided detailed feedback and listed my concerns related to the current manuscript:

Specific Comments:

1. The results concerning the lack of age-related effects on TS muscle strength are not in accordance with most of the literature. In particular the reported average maximal joint moment values in younger adults seem to be quite low (less than 1 Nm/kg) and may be attributed to a lack of maximal muscle activation in the younger adults and / or to a potential misalignment between joint axis of rotation and rotational axis of the dynamometer during MVC which was not taken into account in the current study (see Arampatzis et al. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech 2005 38(4):885-92).

2. The overall topic of effects of TS MTU on balance recovery responses post perturbations has been addressed already by several previous publications e.g.

a. Debelle et al. Role of Knee and Ankle Extensors' Muscle-Tendon Properties in Dynamic Balance Recovery from a Simulated Slip. Sensors (Basel). 2022 3;22(9):3483;

b. Epro et al. Retention of gait stability improvements over 1.5 years in older adults: effects of perturbation exposure and triceps surae neuromuscular exercise. J Neurophysiol. 2018 1;119(6):2229-2240;

c. Epro et al. Effects of triceps surae muscle strength and tendon stiffness on the reactive dynamic stability and adaptability of older female adults during perturbed walking. J Appl Physiol (1985). 2018 Jun 1;124(6):1541-1549;

d. Karamanidis et al. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008 Dec;18(6):980-9;

e. Karamanidis and Arampatzis, Age-related degeneration in leg-extensor muscle-tendon units decreases recovery performance after a forward fall: compensation with running experience. Eur J Appl Physiol. 2007 99(1):73-85;

f. Onambele et al. Calf muscle-tendon properties and postural balance in old age. J Appl Physiol 2006 100(6):2048-56;

g. Debelle et al. Recovery From a Forward Falling Slip: Measurement of Dynamic Stability and Strength Requirements Using a Split-Belt Instrumented Treadmill. Front Sports Act Living. 2020 21;2:82.

3. Most of the above-mentioned manuscripts have not been included and referred to in the introduction which clearly weakens the current section.

4. Accordingly, several statements in the introduction section such as in line 64 “However, relations between age-related decreases in tendon stiffness and walking balance control are not well-detailed in literature” or line 74 “Clearly, the literature elucidating the relationship between muscle strength and balance recovery following a perturbation is generally focused on the entire lower limb” are not correct and require amendments.

5. Page 12, hypothesis #B: “Lesser Achilles tendon stiffness (kAT) in older adults delays the transmission between ΔMTU length and muscle stretch (i.e., ΔLm), thereby delaying afferent detection of the perturbation compared to younger adults.” The provided hypothesis cannot be addressed by the current experimental design. Moreover, I argue that other sensory feedback information are perhaps more relevant to recover balance and rapidly execute effective postural corrections following a perturbation e.g. the vestibular or the visual system.

6. Line 1154: “which were interpolated over the gait cycle.” I am not sure why the elongation of the tendon over the AT force assessed during passive angle joint angular rotation on an isokinetic device was interpolated over the gait cycle.

7. The assessment of AT stiffness during passive ankle joint rotation has several limitations. For instance, during passive joint moment measurements, the measured joint moments correspond to all structures surrounding the ankle joint including muscles, ligaments, and other tendons. This is perhaps relevant at more dorsiflexed joint angle configurations potentially affecting the calculated AT force. Given that the joint moments during passive rotation were approximately less than 10 Nm (considering an AT lever arm of around 4 cm) this is a significant limitation and cannot be ignored.

8. The length change of the AT during passive ankle joint rotation as ssessed by assuming a straight line (distance between GM MTJ and AT insertion to the calcaneus) neglecting any effects of AT curvature on tendon length changes. This can significantly affect the calculated force-length relationship of the tendon.

9. Tendon resting length as well as AT lever arm affects tendon elongation during passive joint angular rotation and hence could potentially affect subject group comparison and correlation analysis. Both variables were not considered in the current approach.

10. The authors often state that they have assessed balance responses following gait perturbations. To provide more clarity, I suggest changing this to slip-like perturbations throughout the manuscript.

11. Several statements concerning previous findings and citations are wrong e.g.

a. Page 21: Mademli and Arampatzis did not assess MoS in the ML direction during walking (they determined AP MOS);

b. Page 22: Epro et al. did not assess slip-like perturbations (the authors analysed tripping).

c. Page 22: In addition, the statement “Those authors found that, following slip-like balance perturbations, stronger older women had higher kAT but did not differ in MoSAnt from weaker older women.” is not correct as weaker adults had a lower MoS during the recovery steps following first trip perturbation.

12. Description of figure 3 and 5: “… mediolateral (MoSLat) and anteroposterior (MoSLat) direction margins of stability….” and “relative mediolateral (ΔMoSLat) and anteroposterior (ΔMoSLat) direction margins of stability…”. Anteroposterior MoS is referred as MOSLat hence not correct.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Apr 16;19(4):e0302021. doi: 10.1371/journal.pone.0302021.r002

Author response to Decision Letter 0

1 Mar 2024

Response to Reviewers for PONE-D-23-30928

“The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stability”

Reviewer #1:

We appreciate the reviewer’s thoughtful and constructive recommendations. We have incorporated each in the revised version of our manuscript as outlined in our responses that follow.

1) I would recommend introducing the current state of knowledge on Achilles tendon stiffness (and perhaps changes with age) in the introduction.

We thank the reviewer for this helpful suggestion. Much of the current state of knowledge on Achilles tendon stiffness focuses on its effect on metabolic walking cost or its relationship to sport performance. Given the scope of our study, we took this recommendation to focus on including additional references regarding tendon stiffness the changes thereof due to age (e.g., lines 62-66) . For example: “Also, older adults are known to have age-related reductions in series elastic tissue stiffness [1-4]. In addition to disrupting metabolic walking cost and calf muscle neuromechanics [5], decreased tissue stiffness is associated with reducing maximal joint torque by increasing muscle shortening velocities [6-8] and increasing electromechanical delay [9], both of which likely impose further penalties to balance recovery in older adults.”

2) In the methods section (around line 102) it may be beneficial to include a range of ages instead of just a mean/stdev given the potential variability in an older adult cohort.

This is another helpful inclusion, in addition to the descriptive statistics, we have also now added “age range: 65-87” to line 121.

The specific methodological approach and outcome measures we used in this study have been previously validated in the literature. These include those covering ultrasound image collection in younger and older adults across a range of tendon force magnitudes (e.g., doi: 10.1111/j.1469-7580.2011.01365.x, doi: 10.1002/jcsm.12210) and those covering the measurement of tendon stiffnesses by combining ultrasound and dynamometry (e.g., doi: 10.1016/j.ultrasmedbio.2021.01.002, doi: 10.1519/JSC.0b013e31825bb47f).

We performed all of our ultrasound measurements in a single experimental session, avoiding the potential for errors due to poor between-session reliability. We also did not design our study to include any repeatability/reliability measurements between investigators. Rather, our design ensured that only one investigator collected the ultrasound images. We did have two investigators identify muscle-tendon junction (MTJ) positions from the recorded ultrasound images. Compared to other anatomical features, such as a fascicle length and pennation, the position of the MTJ is very highly recognizable. In addition, to mitigate the potential influence of this methodological decision, we randomly and evenly divided participants from each age group to each of the two investigators assigned to track the MTJ positions. Although we cannot report on inter-rater reliability, we are extremely confident in the rigor of these measurements. Nevertheless, we will consider including reliability measures in our future work and appreciate the recommendation.

We have not performed any formal analyses subject-to-subject variability. We do commend this interesting comment though and may pursue future investigations into covariates (such as those listed) to explain variability in perturbed gait balance. However, analyzing these differences in response are outside the scope of this investigation. As to the variability within subjects, the first perturbation has a larger response due to its novelty, and subsequent deliveries of the perturbation elicit lesser responses, generally.

The subject pool was indeed divided evenly in accordance with SaGER guidelines. We have not yet performed any sex-specific analyses and have thus far been exclusively focused on group-average differences between younger and older adults. For this reason, we also opted not to include those exploratory results in the revised version of this manuscript. However, based on the reviewers interesting idea, we intend to pursue an exploratory post-hoc analysis of those differences as a follow-up and will use any identified trends to pursue additional studies designed with the power to identify the influence of sex on these associations.

Reviewer #2:

We appreciate the reviewers’ attention to detail and highly productive comments and recommendations, which we believe have greatly strengthened our revised manuscript in our effort to make a meaningful contribution to the literature. We have adopted all of the reviewer’s suggestions as outlined in our responses that follow.

We fully agree with the reviewer and appreciate the advice on potential explanations for the lack of age-related differences in TA muscle strength. We first took the opportunity to revisit our raw data to confirm the accuracy of our experimental data, to include reviewing the analog data files, mV to Nm conversions, and analysis code. We did note a minor error in our mV to Nm conversions, wherein we were estimating TS muscle strength ~12% different than actual values. In doing so, we also noted a loss of significance for one of the lesser correlations; namely, the one between PF strength and frontal plane WBAM. PF torque values have been updated throughout, to include Figures 2-6 and the appendix, the results on lines 219-220, and all instances in our revised discussion on lines 303-308, 347, 355, and 377-381. We also note here in response to the reviewer a bit more about our experimental approach. Specifically, the rotational axis of the dynamometer was well-matched to the rotation axis of each participant’s ankle, and all participants were given the same verbal instructions for the MVIC trials (i.e., “push the ball of your foot like a gas pedal as hard as possible using only your calf muscles” with loud motivational vocal cues (i.e., “push, push, push”) provided in a consistent manner to all participants. These details are included in our revised methods section on lines 146-147, which reads: “All participants received identical verbal encouragement to give maximal effort (i.e. “push the ball of your foot like a gas pedal as hard as possible using only your calf muscles”)”. Nevertheless, given the lack of an age-related difference in strength, we cannot exclude the possibility that younger adults failed to maximally activate their plantarflexors during these trials. Thus, we have added a note to address this possibility in the revised discussion section on lines 289-295, which now reads: “Another explanation may be that normalized ankle torque values among our younger adults are low when compared with previously reported values [3, 10, 11], which could result from misalignment of ankle joint rotation axes with that of the dynamometer or insufficient recruitment of ankle musculature in younger adults. As we accounted for alignment of dynamometer and ankle joint axes of rotation in our setup [12] and gave consistent vocal encouragement for maximal effort to all participants [13], it is unclear why MVIC torque values among our younger adults were low in comparison with previous values.”

2. The overall topic of effects of TS MTU on balance recovery responses post perturbations has been addressed already by several previous publications e.g.

a. Debelle et al. Role of Knee and Ankle Extensors' Muscle-Tendon Properties in Dynamic Balance Recovery from a Simulated Slip. Sensors (Basel). 2022 3;22(9):3483;

d. Karamanidis et al. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008 Dec;18(6):980-9;

f. Onambele et al. Calf muscle-tendon properties and postural balance in old age. J Appl Physiol 2006 100(6):2048-56;

g. Debelle et al. Recovery From a Forward Falling Slip: Measurement of Dynamic Stability and Strength Requirements Using a Split-Belt Instrumented Treadmill. Front Sports Act Living. 2020 21;2:82.

3. Most of the above-mentioned manuscripts have not been included and referred to in the introduction which clearly weakens the current section.

We agree with this a fair and insightful comment. We especially appreciate the reviewer’s generosity in recommending several articles, one of which was unknown to our team. We originally omitted many of these articles in our introduction to provide a background more focused on the theoretical contributions of ankle muscle-tendon integrity to balance recovery, in favor of having incorporated more empirical results from these studies into the discussion. However, upon reading the introduction again with the benefit of the reviewer’s comments, we agreed that incorporating those relevant manuscripts would strengthen the revised introduction – especially in the context of other revisions we’ve adopted throughout. Thus, we have edited the introduction (lines 55-85) to more completely summarize the existing understanding of how muscle strength and tendon stiffness contribute to balance recovery, which now reads, in full for the reviewer’s convenience:

“Balance perturbations precipitating falls are most commonly experienced during walking, where mitigation of instability requires rapid repositioning of the base of support and sufficient ground reaction forces from the musculoskeletal system to arrest momentum. In younger adults, dynamic balance recovery following gait perturbations are partly dependent on large, rapid leg extensor moments [7, 8]. With advanced age, adults experience sarcopenia [9, 10] and decreased muscle strength [11, 12], [13, 14]which would intuitively hinder balance recovery in older adults. Indeed, older adults with reduced maximal isometric leg press strength are more likely to fall [15]. Also, older adults are known to have age-related reductions in series elastic tissue stiffness [13, 14, 16, 17]. In addition to disrupting metabolic walking cost and calf muscle neuromechanics [18], decreased tissue stiffness is [13, 14, 16, 17] associated with reducing maximal joint torque by increasing muscle shortening velocities [19-21] and increasing electromechanical delay [22], both of which likely impose further penalties to balance recovery in older adults. [15]

The relationship between age-related declines in muscle-tendon unit (MTU) integrity and dynamic stability has been explored during a variety of tasks. Due to the nature of common, real-world balance perturbations (e.g. tripping, slipping) and the ankle’s proximity to the onset of such perturbations, the triceps surae and Achilles tendon are often the locus of investigation for this relationship. Onambele et al. [14] found older adults were more unstable, had weaker ankle plantaflexors and less stiff Achilles tendons compared to younger adults showed during single-leg stance and tandem stance. During simulated forward falling, older adults took more steps to recover than younger adults, and had weaker knee and ankle extensors, as well as less stiff patellar tendons with no difference in Achilles tendon stiffness [23, 24]. While neither of these experimental tasks involve gait, both indicate age-related declines muscle-tendon integrity are important to postural stability [24-26]. Considering gait stability in response to perturbations, Epro et al. [27] showed older adult women with stronger ankle plantarflexors and stiffer Achilles tendons had better gait stability after unexpected treadmill gait perturbations. However, they later found increases in muscle-tendon capacity at the ankle through exercise had minimal effects on balance recovery in a similar population [28]. Most recently, Debelle et al. [8] showed that age related declines in muscle-tendon integrity were not related to balance recovery, as older and younger adults showed similar MoSAnt¬. This finding is unusual, as older adults are often reported to be more unstable in the AP direction than younger adults immediately following AP balance perturbations [24-26], which the authors attribute to a comparatively young “older adult” sample.”

We now emphasize the existing literature and more explicitly describe how it motivates the need for our study. Indeed, we continue to believe that there is a significant need for additional study in this area, specifically in regards to how older adults attenuate balance challenges applied during walking – which can be fundamentally different than postural responses during standing or simulated falling, particularly regarding mediolateral stability as evidenced by Leestma et al (https://doi.org/10.1242/jeb.244760). We specifically point this out in our revised introduction as well, stating in lines 86-92:

“Furthermore, recent literature demonstrated that AP gait perturbations were more closely correlated with compensatory efforts in the mediolateral direction during balance recovery [14]. Given that mediolateral (ML) balance is disproportionately worsened with age [15, 16], related to increased falls risk [17], and is known to require greater active sensorimotor control from leg muscles [18], quantification of the relationship between MTU integrity and both AP and ML stability may provide novel insight into why older adults are more vulnerable to falls following gait perturbations.”.

We of course also agree with this comment – as we had, for example, originally omitted our intended contrast was to highlight need for additional study in walking as opposed to standing or simulated falling.

In addition to revising our introduction to include the relevant literature suggested, we have amended these statements to more properly acknowledge the existing literature and better define the need for and novelty of our study in lines 93-99:

“Overall, the evidence concerning age-related declines in MTU integrity and their effect on older adults’ gait stability is not clear, as older adult groups have inconsistently reported age-range cutoffs; the existing literature differ in perturbation paradigms (e.g. forward falling, mechanical pulling or “trip”, and slip); of these studies concerned with gait perturbations, none report metrics concerning mediolateral stability in either young or older adults; and Achilles and patellar tendon stiffness are inconsistently different between older and younger adults when correlated with any of the various stability metrics.”

We fully agree with the reviewer that the current experiment is not to designed to fully test the mechanistic origins of the theoretic premise we outline to describe the ways in which lesser Achilles tendon stiffness can influence the detection of muscle stretch as means of influencing vulnerability to perturbations. Fortunately, we did not design our study to test this statement itself and we are careful not to describe this theoretical premise as a specific hypotheses in our manuscript. We carefully reviewed the manuscript in full to make sure our phrasing was not in any way misleading for the reader. That said, we certainly do not disagree with the reviewer that other sensor feedback information may be perhaps more relevant to recover balance. Indeed, we have other paradigms in the lab to test, for example, the role of the visual system in controlling balance correcting responses. Thus, we sought to better acknowledge this other sensory feedback information to better place the focus of our study in the broader context of how sensory information is used to recover balance. Specifically, our revised discussion section (lines 388-391) now includes: “Our study focused only on measures of MTU integrity and their relationship to gait stability following balance perturbation. However, there are many other sensory feedback mechanisms that are equally or even more involved in regulating walking balance (e.g. vestibular, visual).”

We thank the reviewer for identifying this typo. We have corrected this sentence on line 170 to read: “then interpolated MTJ position over the range of ankle joint rotation.”

We have carefully revised our manuscript to ensure that readers fully understand and appreciate the methodological limitations of our study. As we describe in our next response, we purposefully designed our stiffness calculations to involve a dorsiflexion range of motion. We also opted for passive joint rotations in particular due to, in our past experience, the potential for heel-rise during isometric contractions of higher magnitude to preclude accurate measurements of Achilles tendon stiffness. However, we agree with the reviewer that the dynamometer torque measurements during this task are in aggregate not only of the Achilles tendon but also other periarticular structures. We have revised our discussion section to disclose this potential source of error. We also fully appreciate the complex behavior of the Achilles tendon moment arm, not only as a function of ankle joint rotation, but also as a function of muscle loading. Indeed, we have published several studies characterizing these effects across multiple subject cohorts (e.g., Rasske et al. 2017, Rasske and Franz 2018, Franz et al. 2019). Thus, even in past studies using fixed-end (isometric) contractions and higher force magnitudes to estimate Achilles tendon stiffness, these complex variations in Achilles tendon moment arm are unaccounted for. Fortunately, our previously published data in Franz et al. (doi: 10.1007/s10439-018-02162-4) demonstrate that while the AT moment arm varies with ankle joint posture – these variations are dominated by changes in plantarflexion. Indeed, the moment arm is relatively invariant with posture and insensitive to the effects of muscle loading in dorsiflexion. Thus, we believe our estimates of Achilles tendon force and thus stiffness are unlikely to be affected by our decision to assume a constant moment arm. Nevertheless, we have revised our discussion of limitations to clarify these details. Specifically, we now include on lines 176-179: “We assumed constant values for Achilles tendon moment arms, though we acknowledge that these measures can vary with joint position and muscle loading [40]. However our previously-published data suggest that those variations are disproportionately small and insensitive to the effects of muscle loading in dorsiflexion”.

8. The length change of the AT during passive ankle joint rotation as assessed by assuming a straight line (distance between GM MTJ and AT insertion to the calcaneus) neglecting any effects of AT curvature on tendon length changes. This can significantly affect the calculated force-length relationship of the tendon.

We appreciated the opportunity to clarify our methodological approaches and assumptions. We agree that the dorsoventral curvature of the Achilles tendon can – in some ankle joint postures - preclude accurate estimates of Achilles tendon elongation using a straight-line representation. We are also aware of published techniques that allow for correction of this curvature. This curvature is disproportionately problematic in ankle joint postures in larger values of plantarflexion (i.e., ≥20°). Indeed, the straight-line representation can be sufficiently rigorous when in ankle dorsiflexion. We designed our experiment with this specifically in mind and excluded all estimates of tendon elongation at postures beyond 10° of plantarflexion. Although we believe this leads to sufficiently accurate estimates to test our hypotheses, we also want to be fully transparent for the reader. Thus, we have taken the reviewer’s recommendation and added the following to our revised discussion of limitations on line 391-395-: “Our measures of Achilles tendon elongation assume a straight-line distance between the MTJ and calcaneal insertion. While there is curvature of the Achilles tendon, it primarily affects tendon force-length curves at larger values of plantarflexion, which our ankle rotation data purposefully excludes.”

We refer the reviewer to our earlier response in which we outline in detail consideration of the Achilles tendon lever/moment arm. We were also careful to consider tendon resting length in the design of our experiment, and appreciated the opportunity to clarify those details in our revised manuscript. We opted to analyze ankle ranges of motion for our estimates of Achilles tendon stiffness not only to avoid errors from the tendon’s dorsoventral curvature, but also from inter-individual variation in resting length. The ankle angle at which Achilles tendon resting length occurs, assuming a knee flexion angle similar to the one used in this study, range between 10° and 20° plantarflexion. Thus, we believe our methodological approach avoided these errors. That said, we have revised our methods section to be clearer about the motivation underlying our experimental design. Specifically, we now state in lines 179-181: “We opted to analyze primarily dorsiflexion ranges of motion for our estimates of Achilles tendon stiffness not only to avoid errors from the tendon’s dorsoventral curvature, but also from inter-individual variation in resting length.”.

We have taken this recommendation and revised our perturbation descriptions throughout the manuscript to “treadmill-induced slip perturbations”.

11. Several statements concerning previous findings and citations are wrong e.g.

a. Page 21: Mademli and Arampatzis did not assess MoS in the ML direction during walking (they determined AP MOS);

b. Page 22: Epro et al. did not assess slip-like perturbations (the authors analysed tripping).

We appreciate the reviewer for identifying these errors in our original manuscript and certainly apologize for the oversight. We have corrected all of these errors, and also used the opportunity to review the manuscript in full to ensure we are accurately describing the available literature. Specific revisions made in response to the reviewer’s notes here include:

a. We have corrected the subscript on line 314 to refer to anteroposterior margin of stability, consistent with the work of Mademli and Arampatzis.

b. As the reviewer notes, Epro et al. did not analyze slip-like perturbations. However, upon closer review, we noticed that those authors do not refer to their perturbations as a tripping paradigm. To keep the spirit of the author’s phrasing and include the reviewer’s comment, we suggest the term “unexpected treadmill belt accelerations”, which we have used in lieu of “slip-like perturbations" on line 79 in the introduction and 339 in the discussion.

c. Again, the reviewer is correct. After review, we believe that the source of our original description was that both groups had the same MoS at the heel strike immediately before perturbation onset. We have revised this sentence to correctly manuscript state the results of the study regarding differing MoS after perturbation onset during the recovery steps in lines 339-341: “Those authors found that, following unexpected gait perturbations, stronger older women had higher kAT and greater MoSAnt than weaker older women in subsequent recovery steps.”

These revised discussion points – which allow us to more accurately place our research discoveries in the context of the available literature – have greatly strengthened our manuscript.

We have revised both figure captions to correct these errors.

References for reviewer responses

1. Franz JR, Krupenevich RL, Gray AJ, Batsis JA, Sawicki GS. Reduced Achilles tendon stiffness in aging persists at matched activations and associates with higher metabolic cost of walking. 2023.

2. McCrum C, Leow P, Epro G, König M, Meijer K, Karamanidis K. Alterations in Leg Extensor Muscle-Tendon Unit Biomechanical Properties With Ageing and Mechanical Loading. Frontiers in Physiology. 2018;9. doi: 10.3389/fphys.2018.00150.

3. Onambele GL, Narici MV, Maganaris CN. Calf muscle-tendon properties and postural balance in old age. Journal of Applied Physiology. 2006;100(6):2048-56. Epub 20060202. doi: 10.1152/japplphysiol.01442.2005. PubMed PMID: 16455811.

4. Reeves ND. Adaptation of the tendon to mechanical usage. Journal of Musculoskeletal and Neuronal Interaction. 2006;6(2):174-80. PubMed PMID: 16849829.

5. Krupenevich RL, Beck ON, Sawicki GS, Franz JR. Reduced Achilles Tendon Stiffness Disrupts Calf Muscle Neuromechanics in Elderly Gait. Gerontology. 2022;68(3):241-51. doi: 10.1159/000516910.

6. Narici MV, Maffulli N, Maganaris CN. Ageing of human muscles and tendons. Disabil Rehabil. 2008;30(20-22):1548-54. doi: 10.1080/09638280701831058. PubMed PMID: 18608375.

7. Alcazar J, Csapo R, Ara I, Alegre LM. On the Shape of the Force-Velocity Relationship in Skeletal Muscles: The Linear, the Hyperbolic, and the Double-Hyperbolic. Frontiers in Physiology. 2019;10. doi: 10.3389/fphys.2019.00769.

8. Quinlan JI, Maganaris CN, Franchi MV, Smith K, Atherton PJ, Szewczyk NJ, et al. Muscle and Tendon Contributions to Reduced Rate of Torque Development in Healthy Older Males. The Journals of Gerontology: Series A. 2018;73(4):539-45. doi: 10.1093/gerona/glx149.

9. Nordez A, Gallot T, Catheline S, Guevel A, Cornu C, Hug F. Electromechanical delay revisited using very high frame rate ultrasound. J Appl Physiol (1985). 2009;106(6):1970-5. Epub 20090409. doi: 10.1152/japplphysiol.00221.2009. PubMed PMID: 19359617.

10. Debelle H, Maganaris CN, O’Brien TD. Role of Knee and Ankle Extensors’ Muscle-Tendon Properties in Dynamic Balance Recovery from a Simulated Slip. Sensors. 2022;22(9):3483. doi: 10.3390/s22093483.

11. Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008;18(6):980-9. Epub 20070618. doi: 10.1016/j.jelekin.2007.04.003. PubMed PMID: 17574441.

12. Arampatzis A, Morey-Klapsing G, Karamanidis K, DeMonte G, Stafilidis S, Bruggemann GP. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech. 2005;38(4):885-92. doi: 10.1016/j.jbiomech.2004.04.027. PubMed PMID: 15713310.

13. Tod D, Iredale F, Gill N. ???Psyching-Up??? and Muscular Force Production. Sports Medicine. 2003;33(1):47-58. doi: 10.2165/00007256-200333010-00004.

14. Leestma JK, Golyski PR, Smith CR, Sawicki GS, Young AJ. Linking whole-body angular momentum and step placement during perturbed human walking. Journal of Experimental Biology. 2023;226(6). doi: 10.1242/jeb.244760.

15. Schrager MA, Kelly VE, Price R, Ferrucci L, Shumway-Cook A. The effects of age on medio-lateral stability during normal and narrow base walking. Gait & Posture. 2008;28(3):466-71. doi: 10.1016/j.gaitpost.2008.02.009.

16. Dean JC, Alexander NB, Kuo AD. The Effect of Lateral Stabilization on Walking in Young and Old Adults. IEEE Transactions on Biomedical Engineering. 2007;54(11):1919-26. doi: 10.1109/tbme.2007.901031.

17. Hilliard MJ, Martinez KM, Janssen I, Edwards B, Mille M-L, Zhang Y, Rogers MW. Lateral Balance Factors Predict Future Falls in Community-Living Older Adults. Archives of Physical Medicine and Rehabilitation. 2008;89(9):1708-13. doi: 10.1016/j.apmr.2008.01.023.

18. Bauby CE, Kuo AD. Active control of lateral balance in human walking. J Biomech. 2000;33(11):1433-40. doi: 10.1016/s0021-9290(00)00101-9. PubMed PMID: 10940402.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0302021.s002.docx^{(52.3KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0302021.r003

Decision Letter 1

Laura-Anne Marie Furlong

27 Mar 2024

The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stability

PONE-D-23-30928R1

Dear Dr. Franz,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Laura-Anne Marie Furlong

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #1: (No Response)

Reviewer #2: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

**********

PLoS One. doi: 10.1371/journal.pone.0302021.r004

Acceptance letter

Laura-Anne Marie Furlong

2 Apr 2024

PONE-D-23-30928R1

PLOS ONE

Dear Dr. Franz,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Laura-Anne Marie Furlong

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Appendix. Plantarflexor strength and Achilles tendon stiffness relations.

(TIF)

pone.0302021.s001.tif^{(412.6KB, tif)}

Attachment

Submitted filename: Response to Reviewers.docx

pone.0302021.s002.docx^{(52.3KB, docx)}

Data Availability Statement

A .mat master data file is available here: https://cdr.lib.unc.edu/concern/data_sets/6d5707327.

[pone.0302021.ref001] 1.Hartholt KA, van Beeck EF, Polinder S, van der Velde N, van Lieshout EM, Panneman MJ, et al. Societal consequences of falls in the older population: injuries, healthcare costs, and long-term reduced quality of life. Journal of Trauma. 2011;71(3):748–53. doi: 10.1097/TA.0b013e3181f6f5e5 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref002] 2.Graafmans WC, Ooms ME, Hofstee HM, Bezemer PD, Bouter LM, Lips P. Falls in the elderly: a prospective study of risk factors and risk profiles. American Journal of Epidemiology. 1996;143(11):1129–36. doi: 10.1093/oxfordjournals.aje.a008690 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref003] 3.De Almeida ST, Chaves Soldera CL, De Carli GA, Gomes I, Lima Resende TD. Análise de fatores extrínsecos e intrínsecos que predispõem a quedas em idosos. Revista da Associação Médica Brasileira. 2012;58(4):427–33. doi: 10.1590/s0104-42302012000400012 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref004] 4.Kelsey JL, Procter-Gray E, Hannan MT, Li W. Heterogeneity of Falls Among Older Adults: Implications for Public Health Prevention. American Journal of Public Health. 2012;102(11):2149–56. doi: 10.2105/AJPH.2012.300677 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref005] 5.Nyman SR, Ballinger C, Phillips JE, Newton R. Characteristics of outdoor falls among older people: a qualitative study. BMC Geriatrics. 2013;13(1):125. doi: 10.1186/1471-2318-13-125 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref006] 6.CDIS D. Falls Injury Data 2022 [7/12/2023]. Available from: https://injuryfreenc.dph.ncdhhs.gov/DataSurveillance/FallsData.htm#:~:text=As%20our%20population%20ages%2C%20fall,for%20individuals%2065%20and%20older.

[pone.0302021.ref007] 7.Debelle H, Harkness-Armstrong C, Hadwin K, Maganaris CN, O’Brien TD. Recovery From a Forward Falling Slip: Measurement of Dynamic Stability and Strength Requirements Using a Split-Belt Instrumented Treadmill. Frontiers in Sports and Active Living. 2020;2. doi: 10.3389/fspor.2020.00082 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref008] 8.Debelle H, Maganaris CN, O’Brien TD. Role of Knee and Ankle Extensors’ Muscle-Tendon Properties in Dynamic Balance Recovery from a Simulated Slip. Sensors. 2022;22(9):3483. doi: 10.3390/s22093483 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref009] 9.Rosenberg JG, Ryan ED, Sobolewski EJ, Scharville MJ, Thompson BJ, King GE. Reliability of panoramic ultrasound imaging to simultaneously examine muscle size and quality of the medial gastrocnemius. Muscle & nerve. 2014;49(5):736–40. Epub 2013/09/17. doi: 10.1002/mus.24061 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref010] 10.Abellan van Kan G, Cderbaum JM, Cesari M, Dahinden P, Fariello RG, Fielding RA, et al. Sarcopenia: biomarkers and imaging (International Conference on Sarcopenia research). Journal of Nutrition Health and Aging. 2011;15(10):834–46. doi: 10.1007/s12603-011-0365-1 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref011] 11.Bäckman E, Johansson V, Häger B, Sjöblom P, Henriksson KG. Isometric muscle strength and muscular endurance in normal persons aged between 17 and 70 years. Scandanavian Journal of Rehabilitation Medicine. 1995;27(2):109–17. . [PubMed] [Google Scholar]

[pone.0302021.ref012] 12.Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G. Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle and Nerve. 2002;25(6):858–63. doi: 10.1002/mus.10113 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref013] 13.Pijnappels M, Van Der Burg JCE, Reeves ND, Van Dieën JH. Identification of elderly fallers by muscle strength measures. European Journal of Applied Physiology. 2008;102(5):585–92. doi: 10.1007/s00421-007-0613-6 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref014] 14.Franz JR, Krupenevich RL, Gray AJ, Batsis JA, Sawicki GS. Reduced Achilles tendon stiffness in aging persists at matched activations and associates with higher metabolic cost of walking. 2023. [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref015] 15.McCrum C, Leow P, Epro G, König M, Meijer K, Karamanidis K. Alterations in Leg Extensor Muscle-Tendon Unit Biomechanical Properties With Ageing and Mechanical Loading. Frontiers in Physiology. 2018;9. doi: 10.3389/fphys.2018.00150 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref016] 16.Onambele GL, Narici MV, Maganaris CN. Calf muscle-tendon properties and postural balance in old age. Journal of Applied Physiology. 2006;100(6):2048–56. Epub 20060202. doi: 10.1152/japplphysiol.01442.2005 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref017] 17.Reeves ND. Adaptation of the tendon to mechanical usage. Journal of Musculoskeletal and Neuronal Interaction. 2006;6(2):174–80. . [PubMed] [Google Scholar]

[pone.0302021.ref018] 18.Krupenevich RL, Beck ON, Sawicki GS, Franz JR. Reduced Achilles Tendon Stiffness Disrupts Calf Muscle Neuromechanics in Elderly Gait. Gerontology. 2022;68(3):241–51. doi: 10.1159/000516910 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref019] 19.Narici MV, Maffulli N, Maganaris CN. Ageing of human muscles and tendons. Disabil Rehabil. 2008;30(20–22):1548–54. doi: 10.1080/09638280701831058 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref020] 20.Alcazar J, Csapo R, Ara I, Alegre LM. On the Shape of the Force-Velocity Relationship in Skeletal Muscles: The Linear, the Hyperbolic, and the Double-Hyperbolic. Frontiers in Physiology. 2019;10. doi: 10.3389/fphys.2019.00769 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref021] 21.Quinlan JI, Maganaris CN, Franchi MV, Smith K, Atherton PJ, Szewczyk NJ, et al. Muscle and Tendon Contributions to Reduced Rate of Torque Development in Healthy Older Males. The Journals of Gerontology: Series A. 2018;73(4):539–45. doi: 10.1093/gerona/glx149 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref022] 22.Nordez A, Gallot T, Catheline S, Guevel A, Cornu C, Hug F. Electromechanical delay revisited using very high frame rate ultrasound. J Appl Physiol (1985). 2009;106(6):1970–5. Epub 20090409. doi: 10.1152/japplphysiol.00221.2009 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref023] 23.Karamanidis K, Arampatzis A. Age-related degeneration in leg-extensor muscle-tendon units decreases recovery performance after a forward fall: compensation with running experience. Eur J Appl Physiol. 2007;99(1):73–85. Epub 20061025. doi: 10.1007/s00421-006-0318-2 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref024] 24.Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008;18(6):980–9. Epub 20070618. doi: 10.1016/j.jelekin.2007.04.003 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref025] 25.Epro G, McCrum C, Mierau A, Leyendecker M, Brüggemann G-P, Karamanidis K. Effects of triceps surae muscle strength and tendon stiffness on the reactive dynamic stability and adaptability of older female adults during perturbed walking. Journal of Applied Physiology. 2018;124(6):1541–9. doi: 10.1152/japplphysiol.00545.2017 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref026] 26.Epro G, Mierau A, McCrum C, Leyendecker M, Brüggemann GP, Karamanidis K. Retention of gait stability improvements over 1.5 years in older adults: effects of perturbation exposure and triceps surae neuromuscular exercise. Journal of Neurophysiology. 2018;119(6):2229–40. doi: 10.1152/jn.00513.2017 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref027] 27.König M, Epro G, Seeley J, Potthast W, Karamanidis K. Retention and generalizability of balance recovery response adaptations from trip perturbations across the adult life span. Journal of Neurophysiology. 2019;122(5):1884–93. doi: 10.1152/jn.00380.2019 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref028] 28.McCrum C, Karamanidis K, Grevendonk L, Zijlstra W, Meijer K. Older adults demonstrate interlimb transfer of reactive gait adaptations to repeated unpredictable gait perturbations. GeroScience. 2020;42(1):39–49. doi: 10.1007/s11357-019-00130-x [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref029] 29.Leestma JK, Golyski PR, Smith CR, Sawicki GS, Young AJ. Linking whole-body angular momentum and step placement during perturbed human walking. Journal of Experimental Biology. 2023;226(6). doi: 10.1242/jeb.244760 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref030] 30.Schrager MA, Kelly VE, Price R, Ferrucci L, Shumway-Cook A. The effects of age on medio-lateral stability during normal and narrow base walking. Gait & Posture. 2008;28(3):466–71. doi: 10.1016/j.gaitpost.2008.02.009 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref031] 31.Dean JC, Alexander NB, Kuo AD. The Effect of Lateral Stabilization on Walking in Young and Old Adults. IEEE Transactions on Biomedical Engineering. 2007;54(11):1919–26. doi: 10.1109/TBME.2007.901031 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref032] 32.Hilliard MJ, Martinez KM, Janssen I, Edwards B, Mille M-L, Zhang Y, et al. Lateral Balance Factors Predict Future Falls in Community-Living Older Adults. Archives of Physical Medicine and Rehabilitation. 2008;89(9):1708–13. doi: 10.1016/j.apmr.2008.01.023 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref033] 33.Bauby CE, Kuo AD. Active control of lateral balance in human walking. J Biomech. 2000;33(11):1433–40. doi: 10.1016/s0021-9290(00)00101-9 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref034] 34.Crenshaw JR, Grabiner MD. The influence of age on the thresholds of compensatory stepping and dynamic stability maintenance. Gait Posture. 2014;40(3):363–8. Epub 2014/06/04. doi: 10.1016/j.gaitpost.2014.05.001 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref035] 35.Lee A, Bhatt T, Pai YC. Generalization of treadmill perturbation to overground slip during gait: Effect of different perturbation distances on slip recovery. Journal of biomechanics. 2016;49(2):149–54. Epub 2015/12/15. doi: 10.1016/j.jbiomech.2015.11.021 ; PubMed Central PMCID: PMC4793378. [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref036] 36.Liu X, Bhatt T, Pai Y-C. Intensity and generalization of treadmill slip training: High or low, progressive increase or decrease? Journal of Biomechanics. 2016;49(2):135–40. doi: 10.1016/j.jbiomech.2015.06.004 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref037] 37.Wakeling JM, Jackman M, Namburete AI. The effect of external compression on the mechanics of muscle contraction. Journal of Applied Biomechanics. 2013;29(3):360–4. Epub 20120822. doi: 10.1123/jab.29.3.360 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref038] 38.Krupenevich RL, Clark WH, Sawicki GS, Franz JR. Older adults overcome reduced triceps surae structural stiffness to preserve ankle joint quasi-stiffness during walking. Journal of applied biomechanics. 2020;5:1–8. doi: 10.1123/jab.2019-0340 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref039] 39.Rasske K, Franz JR. Aging effects on the Achilles tendon moment arm during walking. Journal of biomechanics. 2018;77:34–9. doi: 10.1016/j.jbiomech.2018.06.001 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref040] 40.Franz JR, Khanchandani A, McKenny H, Clark WH. Ankle Rotation and Muscle Loading Effects on the Calcaneal Tendon Moment Arm: An In Vivo Imaging and Modeling Study. Annals of Biomedical Engineering. 2019;47(2):590–600. doi: 10.1007/s10439-018-02162-4 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref041] 41.Silverman AK, Neptune RR. Differences in whole-body angular momentum between below-knee amputees and non-amputees across walking speeds. Journal of Biomechanics. 2011;44(3):379–85. Epub 20101111. doi: 10.1016/j.jbiomech.2010.10.027 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref042] 42.McAndrew PM, Wilken JM, Dingwell JB. Dynamic stability of human walking in visually and mechanically destabilizing environments. Journal of biomechanics. 2011;44(4):644–9. doi: 10.1016/j.jbiomech.2010.11.007 ; PubMed Central PMCID: PMC3042508. [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref043] 43.Hof AL, Gazendam MG, Sinke WE. The condition for dynamic stability. Journal of biomechanics. 2005;38(1):1–8. Epub 2004/11/03. doi: 10.1016/j.jbiomech.2004.03.025 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref044] 44.Arampatzis A, Morey-Klapsing G, Karamanidis K, DeMonte G, Stafilidis S, Bruggemann GP. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech. 2005;38(4):885–92. doi: 10.1016/j.jbiomech.2004.04.027 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref045] 45.Tod D, Iredale F, Gill N. ???Psyching-Up??? and Muscular Force Production. Sports Medicine. 2003;33(1):47–58. doi: 10.2165/00007256-200333010-00004 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref046] 46.Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm and leg movements during human locomotion. European Journal of Neuroscience. 2001;14(11):1906–14. doi: 10.1046/j.0953-816x.2001.01813.x [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref047] 47.Herr H, Popovic M. Angular momentum in human walking. Journal of Experimental Biology. 2008;211(4):467–81. doi: 10.1242/jeb.008573 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref048] 48.Marigold DS, Bethune AJ, Patla AE. Role of the unperturbed limb and arms in the reactive recovery response to an unexpected slip during locomotion. Journal of neurophysiology. 2003;89(4):1727–37. Epub 2003/03/04. doi: 10.1152/jn.00683.2002 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref049] 49.van Mierlo M, Ambrosius JI, Vlutters M, van Asseldonk EHF, van der Kooij H. Recovery from sagittal-plane whole body angular momentum perturbations during walking. Journal of Biomechanics. 2022;141:111169. Epub 20220603. doi: 10.1016/j.jbiomech.2022.111169 . [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref050] 50.Simoneau GC, Krebs DE. Whole-Body Momentum during Gait: A Preliminary Study of Non-Fallers and Frequent Fallers. Journal of Applied Biomechanics. 2000;16(1):1–13. doi: 10.1123/jab.16.1.1 [DOI] [Google Scholar]

[pone.0302021.ref051] 51.Neptune RR, McGowan CP. Muscle contributions to whole-body sagittal plane angular momentum during walking. Journal of Biomechanics. 2011;44(1):6–12. doi: 10.1016/j.jbiomech.2010.08.015 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref052] 52.Neptune RR, McGowan CP. Muscle contributions to frontal plane angular momentum during walking. Journal of Biomechanics. 2016;49(13):2975–81. doi: 10.1016/j.jbiomech.2016.07.016 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref053] 53.Mademli L, Arampatzis A. Lower safety factor for old adults during walking at preferred velocity. AGE. 2014;36(3). doi: 10.1007/s11357-014-9636-1 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref054] 54.Kubo K, Kanehisa H, Fukunaga T. Gender differences in the viscoelastic properties of tendon structures. European Journal of Applied Physiology. 2003;88(6):520–6. doi: 10.1007/s00421-002-0744-8 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref055] 55.Onambélé GNL, Burgess K, Pearson SJ. Gender-specific in vivo measurement of the structural and mechanical properties of the human patellar tendon. Journal of Orthopaedic Research. 2007;25(12):1635–42. doi: 10.1002/jor.20404 [DOI] [PubMed] [Google Scholar]

[pone.0302021.ref056] 56.Morrison SM, Dick TJM, Wakeling JM. Structural and mechanical properties of the human Achilles tendon: Sex and strength effects. Journal of Biomechanics. 2015;48(12):3530–3. doi: 10.1016/j.jbiomech.2015.06.009 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0302021.ref057] 57.Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H. Elastic properties of human Achilles tendon are correlated to muscle strength. J Appl Physiol (1985). 2005;99(2):665–9. Epub 20050324. doi: 10.1152/japplphysiol.00624.2004 . [DOI] [PubMed] [Google Scholar]

PERMALINK

The effects of plantarflexor weakness and reduced tendon stiffness with aging on gait stability

Ross E Smith

Andrew D Shelton

Gregory S Sawicki

Jason R Franz

Roles

Abstract

1. Introduction

Fig 1. Conceptual model for how age-related differences in ankle muscle-tendon unit function can increase the vulnerability to unexpected balance disturbances.

2. Methods

2.1 Participants

2.2 Experimental procedures

2.3 Data processing and analysis

2.3.1 Kinematic data

2.3.2 Plantarflexor strength and Achilles tendon stiffness

2.3.3 Balance outcomes

2.4 Statistics

3. Results

Fig 2. Plantarflexor strength and Achilles tendon stiffness for older and younger adults.

Table 1. Relations between Achilles tendon stiffness and plantarflexor torque and balance outcomes during perturbed walking.

Fig 3. Plantarflexor strength and Achilles tendon stiffness relations to margins of stability during perturbed walking.

Fig 6. Plantarflexor strength and Achilles tendon stiffness relations to relative whole-body angular momentum during perturbed walking.

Fig 4. Plantarflexor strength and Achilles tendon stiffness relations to whole-body angular momentum during perturbed walking.

Fig 5. Plantarflexor strength and Achilles tendon stiffness relations to relative margins of stability during perturbed walking.

4. Discussion

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Laura-Anne Marie Furlong

Roles

Author response to Decision Letter 0

Decision Letter 1

Laura-Anne Marie Furlong

Roles

Acceptance letter

Laura-Anne Marie Furlong

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases