Skip to main content
PLOS One logoLink to PLOS One
. 2023 Mar 22;18(3):e0283333. doi: 10.1371/journal.pone.0283333

Relationship between stair ascent gait speed, bone density and gait characteristics of postmenopausal women

Ali Dostan 1,*,#, Catherine A Dobson 1,#, Natalie Vanicek 2,#
Editor: John Leicester Williams3
PMCID: PMC10032478  PMID: 36947573

Abstract

Stair ascent is a biomechanically challenging task for older women. Bone health may affect gait stability during stair walking. This study investigated the gait biomechanics associated with stair ascent in a group of postmenopausal women in relation to walking speed and bone health, quantified by T-score. Forty-five healthy women (mean (SD) age: 67 (14) years), with bone density ranging from healthy to osteoporotic (T-score range +1 to -3), ascended a custom-made five-step staircase with two embedded force plates, surrounded by 10 motion capture cameras, at their self-selected speed. Multivariate regression analyses investigated the explained variance in gait parameters in relation to stair ascent speed and T-score of each individual. Stair ascent speed was 0.65 (0.1) m·s-1 and explained the variance (R2 = 9 to 47%, P ≤ 0.05) in most gait parameters. T-score explained additional variance in stride width (R2 = 20%, P = 0.014), pelvic hike (R2 = 19%, P = 0.011), pelvic drop (R2 = 21%, P = 0.007) and hip adduction (R2 = 7%, P = 0.054). Increased stride width, and thereby a wider base of support, accompanied by increased frontal plane hip kinematics, could be important strategies to improve dynamic stability during stair ascent among this group of women. These findings suggest that targeted exercises of the hip abductors and adductors, including core trunk musculature, could improve dynamic stability during more challenging locomotor tasks. Balance exercises that challenge base of support could also benefit older women with low bone mineral density who may be at risk of falls.

Introduction

Negotiating stair ascent is more physically and mechanically challenging than level walking [1] and presents a greater risk of falling, especially for older women [2, 3]. A fall on stairs can have serious consequences, and in the most severe cases may lead to hospitalisation and loss of independence and quality of life [4]. Osteoporosis increases the likelihood of fractures at the hip, wrist and vertebrae [5]. Although changes in bone mineral density (BMD) cannot be considered the sole risk factor in osteoporotic fractures [6], a previous study identified that loss of BMD in the femoral neck region was an important predictor of fracture risk in older women [7]. Day-to-day load-bearing activities, such as stair climbing, can help to maintain and attenuate further bone loss in older adults [8].

Negotiating stairs safely becomes more challenging as we age. The underlying biomechanical reasons are associated with decreased musculoskeletal capacity and consequently reduced gait speed [9]. Older adults have demonstrated greater hip frontal plane moments when compared to younger adults and maintain lateral stability by relying mainly on the hip abductors [10]. They also operate at a higher relative capacity compared to younger adults when it comes to utilising extensor moments [9] and consequently develop compensatory strategies to meet the biomechanical demands of stair ascent. For example, by redirecting energy from the knee distally towards the ankle, they are able to generate a greater plantarflexor moment [9]. It is unclear whether different compensatory stair ascent strategies exist for older women with low BMD, as a fall could have more severe consequences in this group (e.g., a fracture).

There are a limited number of studies that have investigated the relationships between level walking gait parameters and BMD in older women [1116].To the best of our knowledge, no study to date has investigated the biomechanics of stair ascent in relation to low BMD or osteoporosis. Research in this area would help make evidence-based recommendations for improved functional capacity of older women with low BMD during common daily activities. The aim of this study was to explore the gait, biomechanics in relation to comfortable stair ascent speed and T-score (a standardised level of BMD) in older women with a broad range of T-scores, spanning from healthy to osteoporotic, during stair climbing. It was hypothesised that speed would be the most important predictor and explain most of the variance in both joint kinematic and kinetic parameters. However, it was anticipated that inclusion of the T-score in the regression model would explain additional variance for kinematic and kinetic parameters, especially related to the knee and ankle in the sagittal plane, and pelvis and hip in the frontal plane.

Methods

Participants

Forty-five healthy postmenopausal women, aged between 65–70 years with a BMI between 18–30 kg/m2 and various levels of BMD (ranging from +1 to −3 T-score), were recruited from the local Centre for Metabolic Bone Disease. T-score compares the BMD at a specific site with that of a young, healthy sex-matched group and expresses the relative level of BMD as a deviation from the mean peak value. The same technician measured the BMD (expressed as T-score) at the femoral neck with a DXA scan for all participants, resulting in n = 13 with healthy BMD (-1 SD ≤ T-score ≤ +1 SD), n = 26 with osteopenia (-2.5 SD ≤ T-score ≤ −1 SD) and n = 6 with osteoporosis (T-score ≤ −2.5 SD). Therefore, 29% of the participants a healthy BMD, while 71% were considered to have low BMD.

Eligibility criteria were set to exclude any participant who presented with gait abnormalities, neurological disorders, any cardiac failure, or if they had received a treatment course of hormone replacement therapy, glucocorticoids, teriparatide and/or bisphosphonate within the five years prior to study enrolment. Favourable ethical opinion was granted by the NHS Local Research Ethics Committee (Ref. 11/YH/0347) and all participants gave their written informed consent prior to participation. Participants’ demographics are reported in Table 1. Based on the World Health Organization guidelines (WHO) [17], 81% of participants self-reported achieving at least 150 minutes of moderate intensity, or 75 minutes of vigorous intensity, or a combination of both, of physical activity every week.

Table 1. Participant (n = 45) characteristics.

Mean (SD) Range
Age (years) 67.3 (1.4) 65 to 70
Height (cm) 161.4 (4.9) 151 to 172.5
Mass (kg) 63.5 (8.6) 47.8 to 80.4
BMI (kg/m2) 24.1 (2.8) 18.6 to 29.2
Femoral neck T-score -1.5 (0.8) 1 to -3
Number of days physically active [a] (days per week) 5 (2.3) 0 to 7
Commencement of menopause (age in years) 50 (4.5) 38 to 58
Number of falls (last 12 months) 1 (0.6) 0 to 3
Number of fractures (>50 years old) 1 (0.9) 0 to 4

[a] Activities included walking, Zumba, badminton, golf and general gym exercises.

Protocol

Participants wore their own tight-fitting clothing and normal, flat walking shoes during one visit to the laboratory. Forty-four retroreflective markers (14 mm), including clusters of four markers on the thigh and leg, were secured bilaterally onto the lower limb segments according to the six degrees of freedom (6DoF) marker set [18].

Three-dimensional kinematic data were collected using twelve Pro-Reflex MCU1000 motion capture cameras (Qualisys, Gothenburg, Sweden) sampling at 100 Hz while participants ascended a 5-step custom-built wooden staircase (step height: 20cm tread 30cm, width: 80cm) surrounded by a separate wooden handrail structure (Fig 2). Two Kistler piezoelectric force plates (model 9286AA, Kistler, Winterthur, Switzerland) were embedded into the second and third steps of the stairway and synchronised with the motion capture system. Ground reaction forces (GRFs) were sampled at 500 HZ. Participants walked along a 5-metre level walkway to achieve a steady pace before ascending the staircase at their preferred pace and 10 trials were recorded. No adverse events (trips or falls) occurred.

Fig 2. Ensemble mean (± 1SD: Dashed lines) of lower limb joint powers during stair ascent.

Fig 2

Power bursts are labelled (H1-H4, K1-K4, A1-A3) according to McFadyen and Winter (1988) [18]. Positive [+ve] joint power values indicate power generation while negative [-ve] values indicate power absorption.

Data analysis

Marker coordinates were first processed in Qualisys Track Manager Software (version 2.09) before being analysed in Visual 3D v3.0™ (C-Motion, Rockville, USA). 3D marker coordinate data were interpolated using a cubic-spline algorithm. Marker trajectory and GRF data were filtered using a low-pass 4th order Butterworth filter with a cut-off frequency of 6 Hz and 25 Hz, respectively. A lower limb, 7-segment 6DOF model was built in Visual 3D based on the static calibration file with bilateral virtual feet segments and CODA and Visual 3D pelvis segments. Gait speed was computed in Visual 3D using the actual stride length / actual stride time. Joint moments and powers were calculated using inverse dynamics analysis. The ankle joint moment was calculated considering the effects of the gravitational force on the centre of mass, and GRF acting through the centre of pressure as well as the joint reaction force [19]. The segment’s centre of mass location and moment of inertia were based on Dempster’s (1955) values [20]. The results were then incorporated to determine the subsequent proximal joint moments. Joint moment and angular velocity were utilised to determine the joint powers. The X-Y-Z Cardan sequence defined the order of rotations following the Right Hand Rule about the segment coordinate system axes.

Stair ascent gait data were normalised to the gait cycle. The trail limb data started with foot contact on the second step and terminated on the fourth step. The lead limb data started with foot contact on the third step and terminated on the top, fifth step. This allowed us to analyse steady-state stair ascent for both limbs. Gait events (initial contact and toe-off) of the lead and trail limbs were identified using the kinetic data from the force plates embedded into the third and second step, respectively (Fig 1). The foot contact terminating the gait cycle for each limb was identified by examining the kinematic profile of the 1st metatarsal marker, as initial contact was made with the forefoot. Gait events for the subsequent trials were identified using an automatic event identification pipeline command in Visual 3D, and also checked manually.

Fig 1.

Fig 1

a) Laboratory staircase, force plates 1 and 2 were embedded in the second and third steps of the staircase, respectively, b) Schematic demonstration of the lead (blue line) and trail (red line) limb gait cycles during stair ascent.

Temporal-spatial and sagittal plane kinematic data are presented, including frontal plane pelvis and hip data. All kinetic data were normalised to body mass, with joint moments presented as internal moments [21]. GRF data (N/kg), load and decay rate (N/kg/s) are presented relative to the stance phase; sagittal joint moments (Nm/kg) and powers (W/kg) are presented relative to the gait cycle (GC). Throughout this paper, we have defined the following stair ascent sub-phases, according to McFadyen and Winter (1988), and assuming a stance: swing ratio of 60:40: weight acceptance (~0–10% of the GC), pull-up (~10–32% of the GC), forward continuance (~32–60% of the GC), foot clearance (~60–80% of the GC), and foot placement (~80–100% of the GC). The sub-phases were used to label joint power bursts according to McFadyen and Winter (1988). The following joint power bursts occurred during these sub-phases: weight acceptance (H1, K1, A1), pull-up (A2), forward continuance (K2, A3), foot clearance (H3, K3) and foot placement (H4, K4).

Statistical analysis

The Stata statistical computer package v15.0 (Stata Corp, Texas, USA) was used to carry out normal distribution testing and multivariate regression analyses. Normal distribution of the data was confirmed using skewness to measure the asymmetry and kurtosis to determine the ‘peakedness’ in histogram of residuals [22, 23].

Two regression models were created to investigate the explained variance in gait biomechanics parameters. Temporal-spatial data and the peak values of joint angles, GRFs, joint moments and powers (averaged from each participant’s 10 trials) were treated as dependant variables while comfortable stair ascent speed and femoral neck T-score were considered to be the predictor (independent) variables. Collinearity between T-score and speed was examined by testing the variance inflation factor (VIF). The VIF was determined to be 1.05 which was within the acceptable limit (<10) [24]. The first regression model used stair ascent speed as the predictor variable. The femoral neck T-score was added to the second regression model using blockwise-entry method to explore the relationships between the predictor variables and biomechanics parameters in our cohort of older postmenopausal females. The coefficient of multiple determination (R2) was used to measure at what level the model explained the variability of the response data in relation to the gradient of the regression line (B). The result was deemed statistically significant when P ≤ 0.05.

Results

Temporal-spatial and kinematics

The mean (SD) stair ascent speed 0.65 (0.1) m·s-1 explained the variance (R2 = 9–47%, P ≤ 0.05) in most temporal spatial parameters (Table 2). When T-score was included in the regression model, the shared explanatory power of the model only increased for stride width to (R2 = 20%, P = 0.014), with a slope coefficient of B = 0.01 and 95% CI: [0.001 to 0.019] which can be indicative of high precision of this result (Table 2).

Table 2. Explained variance (R2) and slope coefficient for temporal-spatial and joint kinematics during stair ascent.

Gaitparameter Mean (SD) Predictor variable R2% Predictor variable Slope coefficient (B) 95% Confidence interval
Stride width (m) 0.08 (0.02) GS 9 GS 0.04* 0.007: 0.08
GS & TS 20 TS 0.01** 0.001: 0.01
Cycle time (s) 1.15 (0.15) GS 47 GS -0.54*** -0.72: -0.37
GS & TS 47 TS -0.008 -0.04: 0.04
Stance phase (%) 68 (12) GS 46 GS -0.44*** -0.59: -0.29
GS & TS 47 TS 0.01 -0.02: 0.04
Double limb support time (s) 0.22 (0.07) GS 35 GS -0.21*** -0.30: -0.12
GS & TS 35 TS -0.006 -0.02: 0.02
Degrees (°)
Pelvic obliquity hike (Pull-up) 6.84 (1.24) GS 5 GS 1.52 -0.42: 3.47
GS & TS 19 TS 0.56** -0.56: 3.10
Pelvic obliquity drop (Foot clearance) -6.37 (1.51) GS 9 GS -2.37* -4.67: -0.07
GS & TS 21 TS -0.63** -4.27: 0.09
Pelvic anterior tilt (Foot clearance) 11.25 (5) GS 5 GS -5.82 -13.73: 2.07
GS & TS 6 TS -0.36 -2.23: 1.51
Hip adduction (Pull-up) 13.29 (2.6) GS 1 GS 0.72 -3.37: 4.81
GS & TS 7 TS -0.86* -1.82: 0.08
Hip abduction (Foot clearance) -4.77 (2.71) GS 1 GS -1.16 -5.46: 3.13
GS & TS 2 TS -0.38 -1.40: 0.64
Hip frontal RoM 18.06 (3.2) GS 1 GS 1.66 -3.52: 6.86
GS & TS 2 TS -0.42 -1.65: 0.80
Hip extension (Forward continuance) -5.35 (5.15) GS 1 GS -3.50 -13.25: 6.24
GS & TS 1 TS 0.22 -2.11: 2.56
Hip flexion (Foot placement) 71.4 (6.14) GS 5 GS -7.15 -16.7: 2.39
GS & TS 5 TS -0.66 -2.94: 1.61
Hip sagittal RoM 66.08 (4.74) GS 2 GS -3.68 -11.15: 3.79
GS & TS 5 TS -0.88 -2.65: 0.88
Knee flexion (Weight acceptance) 70.03 (5.49) GS 16 GS -11.29*** -19.32: -3.27
GS & TS 16 TS 0.15 -1.77: 2.07
Knee flexion (Foot clearance) 108.8 (6.93) GS 1 GS -0.68 -11.73: 10.35
GS & TS 3 TS -1.43 -4.04: 1.18
Knee sagittal RoM 94.8 (7.08) GS 1 GS -0.99 -12.28: 10.28
GS & TS 6 TS -2.19* -4.81: 0.42
Ankle dorsiflexion (Pull-up) 18.73 (3.6) GS 3 GS -3.47 -9.11: 2.15
GS & TS 4 TS -0.15 -1.50: 1.19
Ankle plantarflexion (Foot clearance) -15.5 (4.78) GS 1 GS -0.44 -8.22: 7.33
GS & TS 1 TS -0.52 -2.32: 1.26
Ankle sagittal RoM 34.28 (4.8) GS 2 GS -3.16 -11.59: 5.25
GS & TS 2 TS 0.44 -1.54: 2.43

Slope coefficients (B) are presented for stair ascent gait speed (GS) and T-score (TS). Significant findings areas were shaded whereby the point estimate of the regression slope (B) was significantly different from 0 at the following alpha levels

* P ≤ 0.05

** P ≤ 0.01, and

*** P ≤ 0.001

Speed explained (R2 = 9%, P = 0.011) and (R2 = 16%, P = 0.007) of the variance for pelvic drop (during foot clearance) and knee flexion (during the weight acceptance), respectively (Table 2). Adding T-score jointly with speed into the regression model significantly increased the shared explained variance for pelvic hike during pull-up and pelvic drop during foot clearance to (R2 = 19%, P = 0.011) and (R2 = 21%, P = 0.017), hip adduction during pull-up to (R2 = 7%, P = 0.054), and knee range of motion (RoM) in the sagittal plane to (R2 = 6%, P = 0.051) (Table 2).

Ground reaction force and joint moments

Stair ascent speed significantly explained the variance in peak posterior GRF during pull-up (R2 = 28%, P ≤ 0.001), first vertical GRF peak (Fz1) during pull-up (R2 = 37%, P ≤ 0.001), and load rate (R2 = 36%, P ≤ 0.001) (Table 3). Inclusion of T-score in the second regression model increased the shared explained variance for load rate to (R2 = 41%, P = 0.054) (Table 3). Speed significantly explained of the variance in the hip abductor moment (during pull-up) (R2 = 15%, P = 0.009), hip adductor moment (during foot clearance) (R2 = 22%, P ≤ 0.001) and knee flexor moment (during forward continuance) (R2 = 15%, P ≤ 0.001) (Table 3). Adding T-score did not have any significant effects on the explanatory power of the regression models for the joint moments (Table 3).

Table 3. Explained variance (R2) and slope coefficient for peak ground reaction forces and peak joint moment during stair ascent.

Gait parameter Mean (SD) Predictor variable R2% Predictor variable Slope coefficient (B) 95% Confidence interval
GRF (N·kg-1) & loading/decay rates (N·kg-1·s-1)
Posterior GRF (Pull-up) -0.03 (0.03) GS 28 GS -0.15*** -0.23: -0.07
GS & TS 28 TS 0.001 -0.009: 0.01
Anterior GRF (Forward continuance) 0.12 (0.01) GS 1 GS 0.01 -0.02: 0.06
GS & TS 2 TS -0.001 -0.007: 0.004
1st vertical GRF peak (Fz1) (Pull-up) 1.03 (0.08) GS 37 GS 0.48*** 0.29: 0.68
GS & TS 41 TS -0.01 -0.04: 0.005
2nd vertical GRF peak (Fz2) (Forward continuance) 1.26 (0.11) GS 1 GS 0.11 -0.23: 0.47
GS & TS 1 TS -0.007 -0.05: 0.03
Load rate 5.26 (1.8) GS 36 GS 10.63*** 6.25: 15.02
GS & TS 41 TS -0.50* -1.03: 0.03
Decay rate -10.10 (1.65) GS 4 GS 3.50 -1.44: 8.44
GS & TS 6 TS -0.26 -0.88: 0.35
N·m·kg-1
Hip abductor (Pull-up) 0.55 (0.25) GS 15 GS 0.47** 0.14: 0.85
GS & TS 18 TS -0.04 -0.13: 0.03
Hip adductor (Foot clearance) -0.12 (0.05) GS 22 GS -0.12*** -0.20: -0.04
GS & TS 23 TS -0.006 -0.02: 0.01
Hip extensor (Weight acceptance) 0.91 (0.2) GS 1 GS 0.002 -0.36: 0.36
GS & TS 1 TS 0.31 -0.05: 0.11
Hip flexor (Forward continuance) -0.48 (0.2) GS 4 GS 0.26 -0.11: 0.64
GS & TS 8 TS -0.05 -0.14: 0.03
Knee extensor (Pull-up) 0.83 (0.2) GS 1 GS 0.18 -0.10: 0.47
GS & TS 5 TS -0.02 -0.09: 0.04
Knee flexor (Forward continuance) -0.23 (0.1) GS 15 GS -0.25*** -0.44: -0.06
GS & TS 20 TS 0.03 -0.01: 0.07
Ankle plantarflexor (Forward continuance) 1.28 (0.2) GS 1 GS 0.07 -0.17: 0.32
GS & TS 1 TS 0.01 -0.04: 0.07

Slope coefficients (B) are presented for stair ascent gait speed (GS) and T-score (TS). Significant findings areas were shaded whereby the point estimate of the regression slope (B) was significantly different from 0 at the following alpha levels

* P ≤ 0.05

** P ≤ 0.01, and

*** P ≤ 0.001

Joint powers

A substantial amount of the variance in joint powers was explained by STA speed (P ≤ 0.01) (Table 4). Speed explained (R2 = 18%, P = 0.004) of the variance in H1 (hip extensor power generation during weight acceptance), (R2 = 13%, P = 0.016) in H3 (hip flexor power generation during foot clearance), (R2 = 14%, P = 0.012) in H4 (hip extensor power generation during foot placement), (R2 = 15%, P = 0.012) in K3 (knee extensor power absorption during foot clearance), (R2 = 32%, P ≤ 0.001) in K4 (knee flexor power absorption during foot placement), (R2 = 38%, P ≤ 0.001) in A1 (ankle plantarflexor power absorption during weight acceptance) and (R2 = 19%, P ≤ 0.001) in A2 (ankle plantarflexor power generation during pull-up). Inclusion of T-score in the regression model did not explain any additional variance in joint powers. Ensemble mean (SD) joint power profiles of the participants during stair ascent are presented Fig 2.

Table 4. Explained variance (R2) and slope coefficient for peak joint powers during stair ascent.

Joint power parameter Mean (SD) Predictor variable R2% Predictor variable Slope coefficient (B) 95% Confidence interval
W·kg-1
H1 (Weight acceptance) 2.18 (0.88) GS 18 GS 1.94*** 0.66: 3.22
GS & TS 18 TS -0.67 -0.37: 0.23
H3 (Foot clearance) 0.79 (0.28) GS 13 GS 0.51** 0.10: 0.92
GS & TS 13 TS 0.02 -0.07: 0.12
H4 (Foot placement) 0.45 (0.36) GS 14 GS 0.69** 0.16: 1.23
GS & TS 14 TS -0.01 -0.14: 0.11
K1 (Weight acceptance) 1.81 (0.56) GS 4 GS 0.59 -0.27: 1.46
GS & TS 7 TS -0.11 -0.32: 0.08
K2 (Forward continuance) 1.3 (0.69) GS 1 GS 0.38 -0.71: 1.47
GS & TS 2 TS 0.08 -0.18: 0.34
K3 (Foot clearance) -0.4 (0.23) GS 15 GS -0.44** -0.77: -0.11
GS & TS 15 TS 0.18 -0.06: 0.09
K4 (Foot placement) -0.76 (0.5) GS 32 GS -1.48*** -2.16: -0.81
GS & TS 34 TS 0.06 -0.15: 0.46
A1 (Weight acceptance) -0.68 (0.5) GS 38 GS -1.71*** -2.38: -1.04
GS & TS 39 TS 0.07 -0.08: 0.23
A2 (Pull-up) 0.99 (0.19) GS 19 GS 0.75*** 0.27: 1.23
GS & TS 19 TS -0.01 -0.12: 0.10
A3 (Forward continuance) 3.19 (1.05) GS 1 GS 0.60 -1.05: 2.26
GS & TS 1 TS 0.06 -0.33: 0.46

The joint power bursts are labelled (H1-H4, K1-K4, A1-A3) according to McFadyen and Winter (1988) [18].

Slope coefficients (B) are presented for stair ascent gait speed (GS) and T-score (TS). Significant findings areas were shaded whereby the point estimate of the regression slope (B) was significantly different from 0 at the following alpha levels

* P ≤ 0.05

** P ≤ 0.01, and

*** P ≤ 0.001

Discussion

To our knowledge, this study is the first to explore the relationships between stair ascent speed, T-score and biomechanical gait parameters of older postmenopausal women with BMD levels ranging from healthy to osteoporotic. As hypothesised, speed remained the most important variable to explain most of the variance for temporal-spatial, GRFs, joint kinematic and kinetic data. When T-score was introduced into the regression model, it explained the variance in some gait parameters associated with dynamic stability in both the sagittal and frontal planes.

A review of the literature has found that only a few studies reported speed or cadence during stair ascent [2534], making it difficult to compare the findings from different studies. This is because our findings have demonstrated that self-selected stair ascent speed is an influential predictor variable. In the present study, participants’ mean (SD) stair ascent speed was 0.65 (0.10) m·s-1. Another gait study involving older women (mean age = 82.2 years) who climbed a 5-step staircase reported an average speed of 0.49 (0.13) m·s-1 [25], while a different study investigating younger women (mean age = 23.9 years) ascending a 3-step staircase reported a speed of 0.65 (0.03) m·s-1 [26]. These findings indicate that our participants were functioning at a high physical level despite their age and varied bone health. Our participants also exhibited a high cadence of 107 (17) steps/min, compared to another study [27] involving older women (mean age = 74.9 years) climbing a 4-step staircase at a rate of 92 (10) steps/min. The fast stair ascent speed in our study was attributed to the high cadence, and not step length, as step length was naturally constrained by the staircase dimensions.

The first regression model with speed as the only predictor variable significantly explained the variance in many of the temporal-spatial parameters (e.g., stride width, cycle time, stance phase and double limb support time) and only two of the joint angles (e.g., pelvic drop and knee flexion). Similar to our previous research, where we explored the relationship between speed, T-score and gait parameters during level walking [11], gait speed was found to be one of the most important predictor variables when analysing the gait biomechanics in postmenopausal women with varied BMD. Therefore, we recommend that future studies quantify stair ascent speed, and specify whether it is self-selected/comfortable or standardised, when examining the effects of other predictor variables, such as BMD, on gait parameters.

Older adults have demonstrated a tendency to increase their stride width to enhance dynamic stability during level walking [11, 35]. In line with our previous study on level walking [11], we observed increased stride width during stair ascent in the same group of postmenopausal women (Table 2). The T-score explained additional variance in stride width (Table 2) associated with low BMD or osteoporosis. Considering the biomechanical challenges and falls risk associated with stair climbing, it is not surprising to observe an increased base of support amongst participants with low bone mineral density. It should be acknowledged that participants were aware of their T-score and bone health, so it was possible that increased stride width served as a compensatory strategy to improve dynamic stability (and therefore reduce falls risk) during stair ascent. We are unable to establish the cause and effect relationship due to the cross-sectional nature of study design. However, we believe load-bearing exercises that challenge stride width during dynamic tasks (e.g., balancing with a narrow base of support on a compliant or moving surface) should be incorporated into an exercise programmes tailored to people with low BMD.

Combining the T-score with speed in the second regression model increased the explanatory power of models for pelvic hike and drop, and hip adduction during pull-up (Table 2). These parameters are related to pelvic control and dynamic stability in the frontal plane during stair ascent, and demand sufficient strength from the hip abductors and adductors and the deeper core muscles of the trunk. These findings suggest older women with low BMD may benefit from weight-bearing exercise programmes aimed at strengthening these muscle groups to enhance dynamic stability during more challenging ambulatory tasks. The complex interaction of the hip abductor and adductors, which have multiple points of insertion on the femur, may generate a strain distribution responsible for driving bone remodelling. These muscles, primarily the gluteus medius and minimus, may also help to compress the entire femoral neck due to co-contraction of the surrounding musculature. The compressive stress due to this co-contraction may be structurally beneficial to induce bone remodelling in the femur [36] and help maintain bone density in this population.

Significant slope coefficient for the first regression model (speed as the only predictor) showed a linear and positive relationship between stair ascent speed with the first vertical GRF peak (Fz1) and load rate (Table 3). Inclusion of T-score increased the explanatory power of the regression model for load rate, indicating older women with low BMD tended to load the lower limbs less during the stair ascent task. This may be a compensatory strategy to decrease the effect of cyclic loading during stair walking, which is a more challenging task than level walking, with a higher risk for bone micro-fractures. It is well understood that bone remodelling is stimulated by the loading rate [37, 38] and physical activities with loading intensity beyond certain level of threshold (10–15 BW/s) improve bone density in healthy women [39]. Although high-impact exercises have been reported to improve bone density in older females with low BMD [40], it should be acknowledged that loading at high rates may increase the risk of bone micro-fracture in older postmenopausal women and should not be performed if dynamic stability is challenged and the risk of falls is increased.

Addition of T-score to the regression model did not increase the explanatory power of the model for the lower limb joint power bursts. However, stair ascent speed significantly explained the variance in hip and ankle peak joint power generation (H1, H3, H4, A2) (Table 4) and in knee and ankle peak joint power absorption (K3, K4, A1) (Table 4). To our knowledge, only two studies have previously explored the three-dimensional biomechanics of postmenopausal women with low BMD during level walking [11, 12]. One of these studies [12] identified H1, H2, H3, K4 and A2 as the main gait parameters to predict low BMD. However, it is not possible to compare their results with the current study because the two studies explored different locomotor tasks and one study [12] did not report or include gait speed in their statistical models. The current results indicate that older postmenopausal women are capable of producing sufficient joint power outputs regardless of their level of BMD. Walking at a faster pace (beyond comfortable walking speed) during uphill activities, including stair ascent, could provide the mechanical stimulus to positively influence the stress/strain distribution on the long bones of the lower limbs. However, care should be taken during stair negotiation and light handrail use could help with safety without compromising mechanical stimuli and stability.

Some limitations of this study must be acknowledged. Based on the WHO definition [17], 81% of the participants were considered to be active, as many of them were engaged in regular physical activity (Table 1). It is possible that a group of older postmenopausal women, leading a more sedentary lifestyle, could exhibit slower stair ascent speed and different gait outcomes. Our findings may not be generalisable to men and younger women with low BMD. Finally, due to the cross-sectional nature of this study, cause and effect of gait biomechanics in relation to BMD (T-score) could not be identified.

Conclusion

Most of the gait variance during stair ascent was explained by speed, while T-score mainly explained the variance in gait parameters related to dynamic stability associated with hip and pelvic kinematics in the frontal plane. Furthermore, our findings suggest increased stride width and decreased load rate could be associated with low BMD. Based on these findings, a weight-bearing exercise programme that incorporates a combination of balance activities and hip abductor/adductor strengthening could improve dynamic stability to benefit older women with low BMD during more challenging daily tasks, such as stair walking.

Supporting information

S1 Data

(XLSX)

Data Availability

Data are all contained within the manuscript and the supporting information file.

Funding Statement

This research was funded through a charitable donation by Osteoporosis Research in East Yorkshire (OSPREY) (charity commission number: 1013289). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  • 1.Nadeau S., McFadyen B. J., and Malouin F., “Frontal and sagittal plane analyses of the stair climbing task in healthy adults aged over 40 years: What are the challenges compared to level walking?,” Clin. Biomech., vol. 18, no. 10, pp. 950–959, 2003, doi: 10.1016/s0268-0033(03)00179-7 [DOI] [PubMed] [Google Scholar]
  • 2.Startzell J. K., a Owens D., Mulfinger L. M., and Cavanagh P. R., “Stair negotiation in older people: a review.,” J. Am. Geriatr. Soc., vol. 48, no. 5, pp. 567–580, 2000, doi: 10.1111/j.1532-5415.2000.tb05006.x [DOI] [PubMed] [Google Scholar]
  • 3.Lythgo N., Begg R., and Best R., “Stepping responses made by elderly and young female adults to approach and accommodate known surface height changes,” Gait Posture, vol. 26, no. 1, pp. 82–89, 2007, doi: 10.1016/j.gaitpost.2006.07.006 [DOI] [PubMed] [Google Scholar]
  • 4.Jacobs J. V., “A review of stairway falls and stair negotiation: Lessons learned and future needs to reduce injury,” Gait Posture, vol. 49, pp. 159–167, 2016, doi: 10.1016/j.gaitpost.2016.06.030 [DOI] [PubMed] [Google Scholar]
  • 5.Warriner A. H. et al. , “Which fractures are most attributable to osteoporosis?,” J. Clin. Epidemiol., vol. 64, no. 1, pp. 46–53, 2011, doi: 10.1016/j.jclinepi.2010.07.007 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.William D. L., Morin S. N., and Lix L. M., “Rate of bone density change does not enhance fracture prediction in routine clinical practice,” J. Clin. Endocrinol. Metab., vol. 97, no. 4, pp. 1211–1218, 2012, doi: 10.1210/jc.2011-2871 [DOI] [PubMed] [Google Scholar]
  • 7.Nguyen T. V., Center J. R., and Eisman J. A., “Femoral neck bone loss predicts fracture risk independent of baseline BMD,” J. Bone Miner. Res., vol. 20, no. 7, pp. 1195–1201, 2005, doi: 10.1359/JBMR.050215 [DOI] [PubMed] [Google Scholar]
  • 8.Segev D., Hellerstein D., and Dunsky A., “Physical Activity-does it Really Increase Bone Density in Postmenopausal Women? A Review of Articles Published Between 2001–2016,” Curr. Aging Sci., 2018, doi: 10.2174/1874609810666170918170744 [DOI] [PubMed] [Google Scholar]
  • 9.Reeves N. D., Spanjaard M., Mohagheghi A. A., Baltzopoulos V., and Maganaris C. N., “Older adults employ alternative strategies to operate within their maximum capabilities when ascending stairs,” J. Electromyogr. Kinesiol., vol. 19, no. 2, pp. e57–e68, 2009, doi: 10.1016/j.jelekin.2007.09.009 [DOI] [PubMed] [Google Scholar]
  • 10.Novak A. C. and Brouwer B., “Sagittal and frontal lower limb joint moments during stair ascent and descent in young and older adults.,” Gait Posture, vol. 33, no. 1, pp. 54–60, Jan. 2011, doi: 10.1016/j.gaitpost.2010.09.024 [DOI] [PubMed] [Google Scholar]
  • 11.Dostanpor A., Dobson C. A., and Vanicek N., “Relationships between walking speed, T-score and age with gait parameters in older post-menopausal women with low bone mineral density,” Gait Posture, vol. 64, pp. 230–237, 2018, doi: 10.1016/j.gaitpost.2018.05.005 [DOI] [PubMed] [Google Scholar]
  • 12.ElDeeb A. M. and Khodair A. S., “Three-dimensional analysis of gait in postmenopausal women with low bone mineral density.,” Neuroengineering Rehabil., vol. 11, no. 1, p. 55, 2014, doi: 10.1186/1743-0003-11-55 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Löfgren N., Halvarsson A., Ståhle A., and Franzén E., “Gait characteristics in older women with osteoporosis and fear of falling,” Eur. J. Physiother., vol. 15, no. 3, pp. 139–145, Sep. 2013, doi: 10.3109/21679169.2013.827238 [DOI] [Google Scholar]
  • 14.Palombaro K. M. et al. , “Gait variability detects women in early postmenopause with low bone mineral density.,” Phys. Ther., vol. 89, pp. 1315–1326, 2009, doi: 10.2522/ptj.20080401 [DOI] [PubMed] [Google Scholar]
  • 15.Lou Bareither M., Troy K. L., and Grabiner M. D., “Bone mineral density of the proximal femur is not related to dynamic joint loading during locomotion in young women.,” Bone, vol. 38, no. 1, pp. 125–9, Jan. 2006, doi: 10.1016/j.bone.2005.07.003 [DOI] [PubMed] [Google Scholar]
  • 16.Moisio K. C., Hurwitz D. E., and Sumner D. R., “Dynamic loads are determinants of peak bone mass.,” J. Orthop. Res., vol. 22, no. 2, pp. 339–45, Mar. 2004, doi: 10.1016/j.orthres.2003.08.002 [DOI] [PubMed] [Google Scholar]
  • 17.Bull F. C. et al. , “World Health Organization 2020 guidelines on physical activity and sedentary behaviour,” British Journal of Sports Medicine, vol. 54, no. 24. 2020, doi: 10.1136/bjsports-2020-102955 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Cappozzo A., Catani F., Della Croce U., and Leardini A., “Position and orientation in space of bones during movement: anatomical frame definition and determination,” Clin. Biomech., vol. 10, no. 4, pp. 171–178, 1995, doi: 10.1016/0268-0033(95)91394-t [DOI] [PubMed] [Google Scholar]
  • 19.Kirtley C., Clinical Gait Analysis: Theory and Practice. Elsevier Health Sciences, 2006. [Google Scholar]
  • 20.Dempster W. T., “Space Requirements of the Seated Operator,” Am. J. Phys. Anthro, vol. 22, no. March, pp. 1–254, 1955, doi: citeulike-article-id:437004. [Google Scholar]
  • 21.McFadyen B. J. and Winter D. A., “An integrated biomechanical analysis of normal stair ascent and descent,” J. Biomech., vol. 21, no. 9, pp. 733–744, 1988, doi: 10.1016/0021-9290(88)90282-5 [DOI] [PubMed] [Google Scholar]
  • 22.West S., Finch J., and Curran P., “Structural equation models with nonnormal variables: Problems and remedies.,” 1995. [Google Scholar]
  • 23.Kim H.-Y., “Statistical notes for clinical researchers: assessing normal distribution (2) using skewness and kurtosis,” Restor. Dent. Endod., vol. 38, no. 1, p. 52, 2013, doi: 10.5395/rde.2013.38.1.52 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Hair J. F., Black W. C., Babin B. J., and Anderson R. E., “Multivariate Data Analysis (3rd ed).,” New York Macmillan, 1995. [Google Scholar]
  • 25.Hamel K. A. and Cavanagh P. R., “Stair Performance in People Aged 75 and Older,” J. Am. Geriatr. Soc., vol. 52, no. 4, pp. 563–567, 2004, doi: 10.1111/j.1532-5415.2004.52162.x [DOI] [PubMed] [Google Scholar]
  • 26.Vallabhajosula S., Tan C. W., Mukherjee M., Davidson A. J., and Stergiou N., “Biomechanical analyses of stair-climbing while dual-tasking,” J. Biomech., vol. 48, no. 6, pp. 921–929, 2015, doi: 10.1016/j.jbiomech.2015.02.024 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Reeves N. D., Spanjaard M., Mohagheghi A. A., Baltzopoulos V., and Maganaris C. N., “Influence of light handrail use on the biomechanics of stair negotiation in old age,” Gait Posture, vol. 28, no. 2, pp. 327–336, 2008, doi: 10.1016/j.gaitpost.2008.01.014 [DOI] [PubMed] [Google Scholar]
  • 28.Chen J., Wang J., Wang J., Liu X., Li T., and Lin P., “An Experimental Study of Individual Ascent Speed on Long Stair,” Fire Technol., vol. 53, no. 1, 2017, doi: 10.1007/s10694-016-0579-1 [DOI] [Google Scholar]
  • 29.Oh J., Kuenze C., Jacopetti M., Signorile J. F., and Eltoukhy M., “Validity of the Microsoft Kinect TM in assessing spatiotemporal and lower extremity kinematics during stair ascent and descent in healthy young individuals,” Med. Eng. Phys., vol. 60, 2018, doi: 10.1016/j.medengphy.2018.07.011 [DOI] [PubMed] [Google Scholar]
  • 30.Waiteman M. C., de Oliveira Silva D., Azevedo F. M., Pazzinatto M. F., Briani R. V., and Bazett-Jones D. M., “Women with patellofemoral pain and knee crepitus have reduced knee flexion angle during stair ascent,” Phys. Ther. Sport, vol. 48, 2021, doi: 10.1016/j.ptsp.2020.12.013 [DOI] [PubMed] [Google Scholar]
  • 31.Weiss A., Brozgol M., Giladi N., and Hausdorff J. M., “Can a single lower trunk body-fixed sensor differentiate between level-walking and stair descent and ascent in older adults? Preliminary findings,” Med. Eng. Phys., vol. 38, no. 10, 2016, doi: 10.1016/j.medengphy.2016.07.008 [DOI] [PubMed] [Google Scholar]
  • 32.Pitcairn S., Lesniak B., and Anderst W., “In vivo validation of patellofemoral kinematics during overground gait and stair ascent,” Gait Posture, vol. 64, 2018, doi: 10.1016/j.gaitpost.2018.06.028 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Moyer R., Birmingham T., Marriott K., Leitch K., and Giffin J., “Effects of combined custom valgus knee brace and custom lateral wedge foot orthotic use during stair ascent,” Osteoarthr. Cartil., vol. 22, 2014, doi: 10.1016/j.joca.2014.02.207 [DOI] [Google Scholar]
  • 34.Catelli D. S., Bedo B. L. S., Beaulé P. E., and Lamontagne M., “Pre- and postoperative in silico biomechanics in individuals with cam morphology during stair tasks,” Clin. Biomech., vol. 86, 2021, doi: 10.1016/j.clinbiomech.2021.105387 [DOI] [PubMed] [Google Scholar]
  • 35.McAndrew Young P. M. and Dingwell J. B., “Voluntary changes in step width and step length during human walking affect dynamic margins of stability,” Gait Posture, vol. 36, no. 2, pp. 219–224, 2012, doi: 10.1016/j.gaitpost.2012.02.020 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Rudman K. E., Aspden R. M., and Meakin J. R., “Compression or tension? The stress distribution in the proximal femur.,” Biomed. Eng. Online, vol. 5, no. 1, p. 12, Jan. 2006, doi: 10.1186/1475-925X-5-12 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Frost H. M, “From Wolff’s law to the Utah paradigm: Insights about bone physiology and its clinical applications,” Anatomical Record, vol. 262, no. 4. pp. 398–419, 2001, doi: 10.1002/ar.1049 [DOI] [PubMed] [Google Scholar]
  • 38.Christen P. et al. , “Bone remodelling in humans is load-driven but not lazy,” Nat. Commun., 2014, doi: 10.1038/ncomms5855 [DOI] [PubMed] [Google Scholar]
  • 39.Chahal J., Lee R., and Luo J., “Loading dose of physical activity is related to muscle strength and bone density in middle-aged women,” Bone, vol. 36, no. 67, pp. 41–45, 2014, doi: 10.1016/j.bone.2014.06.029 [DOI] [PubMed] [Google Scholar]
  • 40.James M. M. S. and Carroll S., “Effects of different impact exercise modalities on bone mineral density in premenopausal women: A meta-analysis,” Journal of Bone and Mineral Metabolism. 2010, doi: 10.1007/s00774-009-0139-6 [DOI] [PubMed] [Google Scholar]

Decision Letter 0

John Leicester Williams

7 Sep 2022

PONE-D-22-11086Stair ascent in postmenopausal women: A regression analysis exploring the relationships between walking speed and T-score with sagittal and frontal plane gait biomechanicsPLOS ONE

Dear Dr. Dostan,

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.

The reviewers have raised a number of questions related to the study design and statistical approach that need to be adequately addressed.

Please submit your revised manuscript by Oct 22 2022 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,

John Leicester Williams, Ph.D.

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. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

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

“We would like to thank and acknowledge Osteoporosis Research in East Yorkshire (OSPREY) (charity commission number: 1013289) who funded this research.”

We note that you have provided funding information that is not 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:

“AD, CAD, NV received funding from Osteoporosis Research in East Yorkshire (OSPREY) (charity commission number: 1013289).

There are no grant number.

URL:https://www.osprey.org.uk/index.php

The funders had no role in study design, data collection and 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.

4. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability.

Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized.

Important: If there are ethical or legal restrictions to sharing your data publicly, please explain these restrictions in detail. Please see our guidelines for more information on what we consider unacceptable restrictions to publicly sharing data: http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. Note that it is not acceptable for the authors to be the sole named individuals responsible for ensuring data access.

We will update your Data Availability statement to reflect the information you provide in your cover letter.

5. We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For more information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions.

In your revised cover letter, please address the following prompts:

a) 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.

b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories.

We will update your Data Availability statement on your behalf to reflect the information you provide.

[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: Partly

Reviewer #2: Yes

**********

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

Reviewer #1: No

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: The manuscript examined the relationship between the gait related biomechanical variables and stair ascent speed and T-scores using multiple regression analyses. The study included relatively large number of participants. However, I have major reservations for the research question and analysis method of the regression model and variable selection method.

General comments –

1. The main hypothesis does not match the purpose of the student. It is well known that gait speed is highly correlated with many biomechanical gait variables. It is not worthwhile to investigate the relationship between the gait speed and gait related variables, even though it has not been explored extensively in the population as stated by the authors.

2. The regression analysis used in the study is sufficient enough to answer the research question. The inclusion of all variables (Tables 2-4) in the analyses are not appropriate without proper justifications as many of the included variables are more likely highly correlated with each other. Such an approach is not that different from running correlation coefficients among the variables. Correlation analysis is not sufficient in addressing the research question. More importantly, inclusion of all lower limb biomechanical variables and special and temporal gait variables in the analyses is too broad without focus. There are many stair gait biomechanical research studies and the authors should be able to draw sufficient information to narrow down the more important variables related to hip biomechanics that are more relevant to the hip fracture related to osteoporosis.

3. The gait speed determination was not provided in the method section but it was used as a main predictor of the regression models.

4. It seems that the authors included data from both limbs, trailing limb on the second step and leading limb in the third step, in their analysis. Did the authors used 10 individual trials and both limb’s data in the regression analysrs? This may inflate the sample size and violation of regression analysis as individual trials of the same condition for an individual participant are not considered independent of each other.

Specific comments –

Ln 74-76 The hypothesis is not a novel one as it is commonly known that gait speed is a main factor for changes in gait biomechanics, especially the gait kinetics.

Ln 84-85 the sample size is relatively small for the osteoporosis patients.

Ln 100-101 A picture of the stair system would be helpful.

Ln 105 It is important to have a consistent stair ascent speed. Did the authors monitor the speed?

Ln 105 Did the authors used the data of the average of 10 trials or data of the 10 dividual trials in the regression analyses? See also my general comment on this.

Ln 114 Change this to “Inverse dynamics analysis”.

Ln 118-121 It is not clear how the phases of stair ascent was defined. Later the authors referred to “pull-up” and “load rate” which were never mentioned that how there phases were defined. Although they referred to McFadyen and Winter (1988), but these should be defined in the methods.

Reviewer #2: General comments

The submitted manuscript is an observational study aimed at investigating the gait biomechanics of stair ascent for older, postmenopausal women. Forty-five women underwent DEXA to assessment bone health quality, and were subsequently categorised as either: healthy, osteopenic, or osteoporotic. On a separate occasion they then ascended aa five-step stair to capture kinematics and kinetics. Finally, regression analyses were conducted, revealing that gait speed was the most important characteristic in explaining variance in all biomechanical measures. T-score, or bone density score, explained variance for gait measures relating to dynamic stability, and has implications targeting the hip adductors and abductors, and core musculature for future exercise interventions for falls prevention in older women.

The study methodology is appropriate to satisfy the aims, the findings are original and would interest the journal’s readership.

Specific comments

Title

The title is currently verbose, and particularly throughout the manuscript, the use of ‘T-score’ may lose the reader. Although correct and scientific, many PLOS One readers from the natural and social sciences may not understand what T-score is without explanation.

Introduction

The aim could be written with greater clarity, and appears not to directly transfer to the aim stated in the abstract.

Methods

Participants

Page 4

I recommend presenting data for the measurement error associated with the DEXA scans. A minor point would also be to add the % proportion of ‘healthy’, ‘osteopenic’, etc.

You mention ‘strict criteria’ were used to exclude potential participants. However, the specific inclusion and exclusion criteria is not clearly stated, nor is there any information on whether i) any did not complete testing, ii) there were any adverse events (particularly trips), or iii) data was lost incomplete/lost for any participants. For the latter, if so, then what methods were used for data handling.

Protocol

Page 5

Consider including a pictorial / reproduction diagram of the stair set-up, including the gait cycle. This would benefit the paper in readability and help interpret the precise gait cycle.

Data analysis

Page 5

There is scant information on how joint moments and powers were calculated. Please expand on the inverse dynamic analyses. Also, the specific gait cycle could be better described, specifying the left / right foot contact for each gait phase.

Page 6

You give reference to McFadyen and Winter (1988), but there is no explanation of STA, H1, H2, etc, in the Method. These need succinctly adding.

Results

The results for joint power are not written in an accessible, easily interpretable manner. The use of H1, etc, do not really illustrate the gait cycle events. This subsection could be clearer.

Also, include exact P values and check that the significant variables highlighted in tables 2 and 3 are consistent with descriptions in the text.

Discussion

Page 12

I recommend briefly confirming whether limb length was an influential factor in step cadence and other temporo-spatial characteristics.

Page 113, line 222: “we recommend future studies quantify stair ascent speed…”, and based on the preceding sentence walking gait too.

Line 226: typo “level walk”

Line 241-244: It would be insightful to illustrate the trunk’s role in the ascent gait cycle (e.g. stance) for interpretation.

Page 15

The authors highlight the importance of physical activity in human gait in their limitations, but given there is a wealth of evidence to support those ‘highly’ physical active or ‘active’ in having greater gait ability, it is worth providing data on how many (n, %) were classified as: very active, active, low active, or sedentary.

**********

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: Yes: James P. Gavin

**********

[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. 2023 Mar 22;18(3):e0283333. doi: 10.1371/journal.pone.0283333.r002

Author response to Decision Letter 0


30 Dec 2022

Response to the editor's specific comments:

We would like to confirm that our revised manuscript meets the PLOS ONE's style requirements.

There are no grant numbers associated with the funding that we have received as this research was funded through a charitable donation by Osteoporosis Research in East Yorkshire (OSPREY) (charity commission number: 1013289).

Could you please amend the funding statement to: “This research was funded through a charitable donation by Osteoporosis Research in East Yorkshire (OSPREY) (charity commission number: 1013289). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.”

We have also amended the acknowledgment section to read “We would like to thank Osteoporosis Research in East Yorkshire (OSPREY) (charity commission number: 1013289) for their support.”

We would also like to confirm that we have now uploaded the minimal anonymized data set that is required to replicate the results of this study.

Response to the reviewer's specific comments:

Specific Comments Reviewer #1:

Ln 74-76 - The hypothesis is not a novel one as it is commonly known that gait speed is a main factor for changes in gait biomechanics, especially the gait kinetics.

The focus of the study is not to study the effects of gait speed on the biomechanics of this population. Instead we focused on identifying the level at which bone mineral density (T-score) explained the variance in gait parameters by also considering the effects of gait speed.

We used gait speed as one of our independent variables to consider its effects when investigating the relationship between gait parameters and T-score (level of bone density). Without the inclusion of gait speed in our regression model and consideration for its effect, we may run the risk of inflated results similar to a previous study published by ElDeeb and Khodair (2014) (ElDeeb & Khodair, 2014).

ElDeeb and Khodair (2014) reported many gait parameters such as hip adductor and extensor moments, and joint power bursts (H1, H2, H3, K4 and A2) to be significant predictors for low bone density in postmenopausal women without accounting for the effects of walking speed. In addition to that, our previous study (2) demonstrated that gait speed was an important predictor variable and must be taken into account when considering other factors that could affect gait performance (e.g. bone density (T-score), age, etc).

Ln 84-85 the sample size is relatively small for the osteoporosis patients.

Our participants included 26 women with osteopenia and 6 with osteoporosis. Therefore 71% of our participants have low BMD scores (We have included a statement, please see P4, lines 90-92). The low number of participants with osteoporosis does not affect our statistics/results as the participants were not assigned into different groups. Instead, we conducted a multi-regression analysis and studied the level of explained variance for each gait parameter. We then identified gait parameters that were related to participants with low BMD when T-score significantly explained the variance in the gait parameter.

Ln 100-101 A picture of the stair system would be helpful.

Additional figure has been added (figure 1).

Ln 105 It is important to have a consistent stair ascent speed. Did the authors monitor the speed?

Yes, the participants were instructed to climb the stairs at their comfortable preferred walking speed to capture data related to their usual biomechanics and to avoid any potential falls related to walking too quickly or slowly.

Ln 105 Did the authors used the data of the average of 10 trials or data of the 10 dividual trials in the regression analyses? See also my general comment on this.

The average value for the trials was used.

Ln 114 Change this to “Inverse dynamics analysis”.

This has been amended (please see P6, line 126)

Ln 118-121 It is not clear how the phases of stair ascent was defined. Later the authors referred to “pull-up” and “load rate” which were never mentioned that how there phases were defined. Although they referred to McFadyen and Winter (1988), but these should be defined in the methods.

We have now introduced the terms in the method section. (Please see 7 lines 147- 154)

Specific Comments Reviewer #2:

Title

The title is currently verbose, and particularly throughout the manuscript, the use of ‘T-score’ may lose the reader. Although correct and scientific, many PLOS One readers from the natural and social sciences may not understand what T-score is without explanation.

The title has been amended.

We have included a description to define T-score in the method section in P4, lines 86-88.

Introduction

The aim could be written with greater clarity, and appears not to directly transfer to the aim stated in the abstract.

This has been amended (please see P3, lines 74-75)

Methods

Participants

Page 4

I recommend presenting data for the measurement error associated with the DEXA scans. A minor point would also be to add the % proportion of ‘healthy’, ‘osteopenic’, etc.

You mention ‘strict criteria’ were used to exclude potential participants. However, the specific inclusion and exclusion criteria is not clearly stated, nor is there any information on whether i) any did not complete testing, ii) there were any adverse events (particularly trips), or iii) data was lost incomplete/lost for any participants. For the latter, if so, then what methods were used for data handling.

The reliability of DEXA measurements for bone mineral density are reported to be (r = 0.98) during supine scanning (Lohman et al., 2009). We agree that due to the differences in X-ray energy generation/absorption and bone edge detection paradigms, the BMD level reported in g/cm2 differs amongst DEXA manufacturers. To avoid these issues, we used the same DEXA scanning device throughout the study and utilised the T-score to report BMD level which provides a normalised value.

We have added a sentence to state the number of healthy and low BMD participants in percentage (please see P4, lines 91-92).

The exclusion criteria are listed P4, lines 93-96 as the following: “gait abnormalities, neurological disorders, any cardiac failure, or if they had received a treatment course of hormone replacement therapy, glucocorticoids, teriparatide and/or bisphosphonate within the five years prior to the study enrolment”.

We have now added further information in the “participants” section (P4, lines 84-86) to describe our inclusion criteria. “Our inclusion criteria included postmenopausal females aged between 65-70 years with a BMI between 18-30 kg/m2 and various levels of BMD (ranging from +1 to −3 T-score).”

i) We can confirm that every participant successfully completed the study during a single visit to our laboratory. Please see P5 lines 105-106.

ii) All participants were otherwise healthy and there were no falls or any other incident to be reported. Please see P5 line 117.

iii) Marker dropout, ghost markers, and marker movement were the more prominent notes. To fix the issue marker trajectory data were interpolated using a cubic-spline algorithm. This was referred to in “data analysis” section, P6, line 121.

Protocol

Page 5

Consider including a pictorial / reproduction diagram of the stair set-up, including the gait cycle. This would benefit the paper in readability and help interpret the precise gait cycle.

A figure has now been included (figure 1).

Data analysis

Page 5

There is scant information on how joint moments and powers were calculated. Please expand on the inverse dynamic analyses. Also, the specific gait cycle could be better described, specifying the left / right foot contact for each gait phase.

We have added a description on P6, lines 126- 131.

We have now included more information in P6, line 137-141. Please also see figure 1 for further information.

Page 6

You give reference to McFadyen and Winter (1988), but there is no explanation of STA, H1, H2, etc, in the Method. These need succinctly adding.

We have now introduced the terms in the method section. (Please see P7 lines 147-154)

Results

The results for joint power are not written in an accessible, easily interpretable manner. The use of H1, etc, do not really illustrate the gait cycle events. This subsection could be clearer.

Also, include exact P values and check that the significant variables highlighted in tables 2 and 3 are consistent with descriptions in the text.

We have described the joint power bursts with the corresponding gait cycle event for these terms, e.g. H1 (hip extensor power generation during weight acceptance).

We have now reported the exact P-vales and double checked the descriptions in Table 2 and 3 are consistent with text.

Discussion

Page 12

I recommend briefly confirming whether limb length was an influential factor in step cadence and other temporo-spatial characteristics.

The data are normalised to the participant’s height therefore limb length should not affect cadence or any other temporal-spatial data.

Page 113, line 222: “we recommend future studies quantify stair ascent speed…”, and based on the preceding sentence walking gait too.

That’s correct, however, we would like to keep the focus of this study on stair climbing. We have previously published a paper with a focus on level walking gait (Dostanpor et al., 2018) where we discussed the effects of walking speed and low BMD on gait parameters.

Line 226: typo “level walk”

Amended.

Line 241-244: It would be insightful to illustrate the trunk’s role in the ascent gait cycle (e.g. stance) for interpretation.

Unfortunately, we only focused on the lower limb and we do not have any information about the trunk. We now collect trunk and upper limb motion regularly to ensure sufficient data from trunk and upper limbs are collected for our current and future studies.

Page 15

The authors highlight the importance of physical activity in human gait in their limitations, but given there is a wealth of evidence to support those ‘highly’ physical active or ‘active’ in having greater gait ability, it is worth providing data on how many (n, %) were classified as: very active, active, low active, or sedentary.

We have used the WHO guidelines on physical activity and sedentary behaviour to report the (self-reported) activity levels of our participants. Please see P4, lines 99-101, and P15 lines 310-311.

References:

Benedetti, M. G., Furlini, G., Zati, A., & Mauro, G. L. (2018). The Effectiveness of Physical Exercise on Bone Density in Osteoporotic Patients. In BioMed Research International. https://doi.org/10.1155/2018/4840531

Dostanpor, A., Dobson, C. A., & Vanicek, N. (2018). Relationships between walking speed, T-score and age with gait parameters in older post-menopausal women with low bone mineral density. Gait and Posture, 64, 230–237. https://doi.org/10.1016/j.gaitpost.2018.05.005

ElDeeb, A. M., & Khodair, A. S. (2014). Three-dimensional analysis of gait in postmenopausal women with low bone mineral density. Neuroengineering and Rehabilitation, 11(1), 55. https://doi.org/10.1186/1743-0003-11-55

Frost, H. M. (1994). Wolff’s Law and bone’s structural adaptations to mechanical usage: an overview for clinicians. In Angle Orthodontist (Vol. 64, Issue 3, pp. 175–188). https://doi.org/10.1043/0003-3219(1994)064<0175:WLABSA>2.0.CO;2

Frost, H M. (1990). Skeletal structural adaptations to mechanical usage (SATMU): 1. Redefining Wolff’s law: the bone modeling problem. The Anatomical Record, 226(4), 403–413. https://doi.org/10.1002/ar.1092260402

Frost, Harold M. (2004). A 2003 Update of Bone Physiology and Wolff ’ s Law for Clinicians. 74(1), 3–15.

Hair, J. F., Black, W. C., Babin, B. J., & Anderson, R. E. (1995). Multivariate Data Analysis (3rd ed). New York: Macmillan.

Lohman, M., Tallroth, K., Kettunen, J. A., & Marttinen, M. T. (2009). Reproducibility of dual-energy x-ray absorptiometry total and regional body composition measurements using different scanning positions and definitions of regions. Metabolism: Clinical and Experimental, 58(11). https://doi.org/10.1016/j.metabol.2009.05.023

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 1

John Leicester Williams

7 Mar 2023

Relationship between stair ascent gait speed, bone density and gait characteristics of postmenopausal women

PONE-D-22-11086R1

Dear Dr. Dostan,

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 for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, 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,

John Leicester Williams, Ph.D.

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 #2: All comments have been addressed

**********

2. 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 #2: Yes

**********

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

Reviewer #2: Yes

**********

4. 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 #2: Yes

**********

5. 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 #2: Yes

**********

6. 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 #2: I commend the authors in their clear and logical responses to the reviewers. I feel they have adequately addressed the major and minor comments of the two reviewers.

**********

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 #2: Yes: James P. Gavin

**********

Acceptance letter

John Leicester Williams

13 Mar 2023

PONE-D-22-11086R1

Relationship between stair ascent gait speed, bone density and gait characteristics of postmenopausal women

Dear Dr. Dostan:

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

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 plosone@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. John Leicester Williams

Academic Editor

PLOS ONE


Articles from PLOS ONE are provided here courtesy of PLOS

RESOURCES