See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/277599377

The Inter-day Measurement Consistency of and Relationships Between

Hamstring and Leg Musculo-articular Stiffness

Article in Journal of Applied Biomechanics · June 2015

DOI: 10.1123/jab.2014-0289 · Source: PubMed

CITATIONS READS

2 185

3 authors:

Justin Phillip Waxman Randy Schmitz

SEA Limited University of North Carolina at Greensboro
33 PUBLICATIONS 173 CITATIONS 134 PUBLICATIONS 3,985 CITATIONS

SEE PROFILE SEE PROFILE

Sandra J Shultz
University of North Carolina at Greensboro
222 PUBLICATIONS 11,667 CITATIONS

SEE PROFILE

All content following this page was uploaded by Justin Phillip Waxman on 20 January 2016.

The user has requested enhancement of the downloaded file.

Journal of Applied Biomechanics, 2015, 31, 340  -348
http://dx.doi.org/10.1123/jab.2014-0289
© 2015 Human Kinetics, Inc. Original Research

The Interday Measurement Consistency of and Relationships

Between Hamstring and Leg Musculo-articular Stiffness
Justin P. Waxman, Randy J. Schmitz, and Sandra J. Shultz
The University of North Carolina at Greensboro

Hamstring stiffness (KHAM) and leg stiffness (KLEG) are commonly examined relative to athletic performance and injury risk.
Given these may be modifiable, it is important to understand day-to-day variations inherent in these measures before use in
training studies. In addition, the extent to which KHAM and KLEG measure similar active stiffness characteristics has not been
established. We investigated the interday measurement consistency of KHAM and KLEG, and examined the extent to which KLEG
predicted KHAM in 6 males and 9 females. KHAM was moderately consistent day-to-day (ICC2,5 = .71; SEM = 76.3 N·m–1), and
95% limits of agreement (95% LOA) revealed a systematic bias with considerable absolute measurement error (95% LOA = 89.6
± 224.8 N·m–1). Day-to-day differences in procedural factors explained 59.4% of the variance in day-to-day differences in KHAM.
Bilateral and unilateral KLEG was more consistent (ICC2,3 range = .87–.94; SEM range = 1.0–2.91 kN·m–1) with lower absolute
error (95% LOA bilateral= –2.0 ± 10.3; left leg = –0.36 ± 3.82; right leg = –1.05 ± 3.61 kN·m–1). KLEG explained 44% of the
variance in KHAM (P < .01). Findings suggest that procedural factors must be carefully controlled to yield consistent and precise
KHAM measures. The ease and consistency of KLEG, and moderate correlation with KHAM, may steer clinicians toward KLEG when
measuring lower-extremity stiffness for screening studies and monitoring the effectiveness of training interventions over time.
Keywords: spring-mass model, free-oscillation, musculo-articular stiffness, leg stiffness, musculoskeletal

Measures of lower-extremity stiffness have often been exam- concentric and eccentric rate of force development.13–16 It has also been
ined for their relative contribution to performance and injury risk.1–4 demonstrated that anterior cruciate ligament (ACL) deficient individu-
Stiffness describes the relationship between an applied load and the als with higher KHAM possess greater knee functional stability than
amount of elastic deformation that occurs within a given structure.4 those with more compliant hamstrings,8 and that uninjured healthy
In terms of the human body, stiffness can be described from the individuals with higher KHAM display characteristics associated with
macroscopic level of the whole body all the way to the microscopic reduced ACL loading during controlled perturbations and dynamic
level of a single muscle fiber. Although a number of in vitro and in landing tasks.17,18 Further, ACL-reconstructed individuals with higher
vivo methods exist, 2 in vivo measures commonly employed are leg levels of KLEG have been reported to be more functional and able to
stiffness (KLEG) and hamstring musculo-articular stiffness (KHAM). participate in more demanding physical activity with fewer symptoms
KHAM and KLEG are measures of active stiffness that rely on mod- of joint pain and instability.19 Thus, it appears that higher levels of KLEG
eling the hamstring muscle-tendon unit and entire lower extremity, and KHAM may be beneficial for enhancing performance and reducing
respectively, as mass-spring systems.5–8 KHAM is assessed using the injury risk. However, other research suggests that there may actually
free-oscillation technique,6 whereby the hamstring muscle-tendon be an optimal range for stiffness, where either too much or too little
unit represents the massless linear spring and the lower leg (shank) stiffness may lead to increased risk of bony injuries20–22 or soft tissue
and applied load represent the mass; a perturbation is then applied injuries,23,24 respectively. Although additional work is needed to gain
to the joint and the ensuing oscillations are measured.7,8 Similarly, a greater understanding of how stiffness measures are related to per-
KLEG is commonly assessed using functional bilateral or unilateral formance and injury risk, the ability to modify this neuromechanical
hopping test protocols, whereby the leg(s) represents the massless property makes stiffness an important variable to consider from injury
linear spring and the rest of the body represents the mass.5,9 Given prevention, rehabilitation, and performance perspectives.
the in vivo nature of these methods, the values obtained represent Because of the potential for stiffness to be modified through
global measures of stiffness for the system being modeled, which training,25–27 it is important to understand the inherent day-to-day
includes the stiffness of the muscle-tendon unit(s), skin, ligaments, consistency and precision of these measures before progressing to
bones, and articular capsule(s).1,10 intervention strategies. The reliability of KLEG has previously been
Evidence suggests that these measures of lower-extremity stiff- established, with reported interday intraclass correlation coef-
ness are related to both athletic performance and injury risk. KLEG ficients (ICCs) and coefficients of variation (CV) ranging from
has previously been shown to be positively related to running perfor- .82 to .94 and from 4.2% to 13.9%, respectively, during bilateral
mance.11,12 In addition, both KLEG and KHAM are positively related to and unilateral hopping tasks.28–30 However, less is known about
the reliability of KHAM. Of the 5 investigations that have examined
KHAM measurement consistency, 4 studies17,25,31,32 reported intraday
Justin P. Waxman, Randy J. Schmitz, and Sandra J. Shultz are with the consistency, while only 2 studies16,25 examined interday consistency.
Applied Neuromechanics Research Laboratory, Department of Kinesiology, Blackburn and Norcross25 examined the day-to-day measurement
The University of North Carolina at Greensboro, Greensboro, NC. Address consistency of KHAM over a 6-week time period and reported a reli-
author correspondence to Justin P. Waxman at [email protected]. ability estimate (ICC) of .86 and measurement precision (standard

340
 Hamstring and Leg Stiffness Measurement Consistency   341

error of measurement [SEM]) of 1.69 N/m·kg–1. Similarly, Ditroilo Schiller Park, IL) at a cadence of 70–80 revolutions per minute and
et al16 examined the day-to-day measurement consistency of KHAM a target rating of perceived exertion of ≥ 3 on a Borg CR-10 scale.34
within a 1-week time period and reported ICCs ranging from .66 After the warm-up, the following assessments were performed in
to .89. Ditroilo et al16 also reported the CV as an index of measure- identical fashion during both testing sessions: (1) KHAM, (2) bilateral
ment precision, which ranged from 5.1% to 13.1% under different KLEG, and (3) unilateral KLEG.
methodological conditions. Given the more moderate estimates of KHAM was measured using the free-oscillation technique,
KHAM day-to-day measurement consistency and precision compared whereby the leg is modeled as a single degree of freedom mass-
with KLEG, methodological factors inherent to the measurement of spring system. The damping effect that the hamstring muscles
KHAM (ie, subtle variations in perturbation magnitude and hip and impose on oscillatory flexion/extension of the knee joint is then
knee joint angles) may, in part, impact measurement precision. To quantified, following a perturbation.8,18,31 Because KHAM does not
the best of our knowledge, however, the influence of such method- differ between limbs in healthy individuals,35 all data were obtained
ological factors on the measurement precision of KHAM has not yet from the left leg. Participants were instrumented with clusters of 4
been investigated. optical LED markers (Phase Space, San Leandro, CA), each placed
Furthermore, we are unaware of any studies that have examined on the lateral thigh and shank of the left limb. Three-dimensional
the extent to which KHAM and KLEG are related. Although KHAM and kinematic data were obtained via an 8-camera IMPULSE motion
KLEG are assessed using fundamentally different procedures (eg, tracking system (Phase Space, San Leandro, CA). Participants were
closed vs. open kinetic chain), both measures are based on the under- positioned prone, with the trunk and thigh supported in 30° of hip
lying construct that the muscle-tendon unit(s) can be independently flexion and the lower leg free to move (Figure 1). A thermoplastic
or collectively modeled as a linear mass-spring system.7 Further, splint was secured to the plantar aspect of the foot and posterior
because KHAM is inherently a more difficult measurement technique shank to standardize ankle position at approximately 90°. A 10%
for both the participant and researcher, having a simpler, clinically- body mass load was then attached to the distal shank, at the level
accessible measure of lower-extremity stiffness could be of great of the malleoli, using cuff-style ankle weights. The investigator
value when attempting to evaluate large samples in a minimal amount then passively positioned the participant’s shank parallel to the
of time. Therefore, the primary purposes of this study were to: (1) floor, placing the knee in approximately 30° of flexion, and the
assess the interday measurement consistency of KHAM and KLEG and participant was required to hold this position via isometric ham-
(2) examine the relationships between these measures. A secondary string contraction. Within 5 seconds of the participant holding
purpose of this study was to examine potential procedural factors this position, an anterior perturbation was manually applied to the
that could introduce sources of measurement error in KHAM. Based posterior aspect of the calcaneus, resulting in slight knee exten-
on previously published work, we hypothesized that KHAM and KLEG sion and subsequent damped oscillatory knee flexion and exten-
would both display acceptable interday measurement consistency but sion.17,18,31,36 This damped oscillatory motion was characterized as
that KLEG would have superior consistency given the greater relative the tangential acceleration of the shank and foot segment, captured
simplicity of the measure. In addition, we hypothesized that KHAM via a triaxial accelerometer (sensor dimensions: 2.54 × 2.54 × 1.91
and KLEG would be moderately correlated with one other given that cm; NeuwGhent Technology, Lagrangeville, NY) attached to the
both measures are based on the same underlying construct. thermoplastic splint. Participants were verbally instructed not to
interfere with or voluntarily produce the oscillations following the
perturbation, and to attempt to keep the hamstring muscles active
Methods only to a level necessary to support the mass of the shank and foot
segment, and the applied load, in the testing position.17,31 Follow-
Participants ing 3–5 practice trials, 5 test trials were recorded for analysis.
Fifteen healthy college-aged individuals (6 male, 9 female; age = Test trials were separated by 30-second rest intervals to reduce
21.5 ± 2.5 years, height = 1.7 ± 0.1 m, mass = 69.3 ± 11.0 kg) vol- the likelihood of fatigue.
unteered to participate. Participants were: (1) recreationally active (≥
90 minutes physical activity per week), (2) free from lower-extremity
injury for a minimum of 6 months before participation, (3) free from
any history of lower-extremity surgery, (4) without known medical
conditions that would affect connective tissue, and (5) without any
history of cardiovascular or pulmonary problems. To ensure that all
participants met the inclusion criteria, physical activity and health
history questionnaires were administered before enrollment in the
study. Before participation, participants signed an informed consent
approved by the university’s institutional review board.

Procedures
All participants visited the laboratory for testing on 2 separate
occasions separated by 2–5 days to minimize the risk of carryover
effects between testing sessions (eg, muscle fatigue, soreness).33 All
testing sessions were administered by the same investigator (JW).
Upon arrival to each testing session, participants were outfitted with
laboratory compression shorts and an athletic top, and measures of
body height and mass were obtained. Participants then performed Figure 1 — Participant positioning during hamstring musculo-articular
a 5-minute warm-up on a stationary cycle ergometer (Life Fitness, stiffness (KHAM) assessments.

JAB Vol. 31, No. 5, 2015

342  Waxman, Schmitz, and Shultz

KLEG was assessed via barefoot hopping in place on a force Hamstring Stiffness (KHAM). The time interval between the first
plate (Type 4060–130; Bertec Corporation, Columbus, OH) at 2 oscillatory peaks (t1 and t2) of the accelerometer time series was
a hopping frequency of 2.2 Hz under 3 different conditions: (1) used to calculate the damped frequency of oscillation (1/[t2 – t1])
bilateral, (2) unilateral left leg, and (3) unilateral right leg. Bilateral for each trial (Figure 2). KHAM was then calculated using the equa-
hopping was always performed first. Unilateral hopping order was tion, KHAM = 4π2mƒ2, where m is the summed mass of the shank and
assigned in a counterbalanced fashion; once order was assigned, foot segment (6.1% body mass)39 and the applied load (10% body
participants alternated legs each trial to minimize the likelihood mass), and ƒ is the damped frequency of oscillation.35 In addition,
of fatigue. Participants performed unilateral hopping trials in the the following kinetic and kinematic variables were obtained from
same order during both testing sessions. Participants were verbally each KHAM trial to examine the influence of procedural factors on
instructed to stand tall with their hands placed on their hips and measurement error: (1) perturbation magnitude, (2) initial knee
their eyes looking straight ahead. Once the metronome began to flexion angle, and (3) initial tibia rotation angle. Perturbation magni-
sound, participants were instructed to begin hopping while attempt- tude was defined as the product of the peak downward acceleration
ing to synchronize their hops with the tone. Because variations in immediately following perturbation onset and the total system mass
ground contact time can affect stiffness regulation at a given hop- (shank and foot segment weight + applied load [N]). Perturbation
ping frequency,37 participants were asked to hop with as short a onset was defined as the instant at which downward acceleration of
ground contact time as possible. Before data collection, participants the shank and foot segment exceeded 3 standard deviations of the
were allowed to practice until they felt comfortable with the task. mean acceleration before the perturbation. Initial knee flexion and
Three 10-second trials, separated by 30-second rest intervals, were tibia rotation angles were defined as the average angles (in degrees)
then recorded for each condition. At 2.2 Hz, the interval between obtained 100 milliseconds before perturbation onset. All variables
vertical ground reaction force peaks should be 455 milliseconds. were then averaged across 5 trials and used for analysis.
Peak ground reaction force intervals that fell within 5% (± 23 mil-
liseconds) of 455 milliseconds were considered valid data to be Leg Stiffness (KLEG). KLEG was calculated from the vertical ground
used for comparisons.38 reaction force and the effective ground contact time.9 Effective con-
tact time is defined as the amount of time that the vertical ground
reaction force is greater than body weight during the stance phase of
Data Sampling and Reduction
hopping, and is expressed as T/2, where T equals the period of oscil-
Accelerometer and force plate data were sampled at 1000 Hz, lation (Figure 3).3,9,23 From this, the natural frequency of oscillation
whereas kinematic data were sampled at 240 Hz. Kinetic and kine- (ω) and spring constant of the spring-mass system were calculated
matic instrumentation was time synchronized and interfaced with as, KLEG = Mgω2, with ω = 2π/T and where M is the participant’s
Motion Monitor software (Innovative Sports Training, Chicago, IL). body mass. Data collected during 5 consecutive hops, between the
Left limb kinematics were modeled using Motion Monitor software. sixth and tenth hop of 15 hops, were used to calculate KLEG for each
All data were later exported from Motion Monitor software and trial.40,41 Ground contact time (tc) and flight time (tf) were determined
processed using custom written Matlab code (Mathworks, Inc., using the vertical ground reaction force. The beginning and end
Natick, MA). Accelerometer and force plate data were low-pass of ground contact was defined as the instants at which the vertical
filtered at 10 Hz, while kinematic data were low-pass filtered at 12 ground reaction force was above and below 5 N. The 3 trials for
Hz, using a fourth-order zero-lag Butterworth filter. each condition were then separately averaged and used for analysis.

Figure 2 — Example time series data obtained from the accelerometer during a hamstring musculo-articular stiffness (KHAM) assessment. Point A
represents perturbation onset. Point B represents peak downward acceleration resulting from perturbation. t1 and t2 represent the time points at which
the first 2 oscillatory peaks occur; these time points are then used to calculate the frequency of oscillation.

JAB Vol. 31, No. 5, 2015

 Hamstring and Leg Stiffness Measurement Consistency   343

Figure 3 — Typical example of a vertical ground reaction force (vGRF) time curve during hopping at 2.2 Hz. Kleg was calculated by measuring one-
half of a resonant period (T/2) and then using the equation listed above. The T/2 is the amount of time that the vGRF is greater than one body weight
(BW). Ground contact time (tc) and aerial/flight time (tf) were also calculated for each hop to evaluate hopping frequency.

Statistical Analyses KHAM demonstrated moderate interday measurement consis-

tency (ICC2,5 = .71) with an SEM (76.27 N·m–1) that represented
All statistical analyses were performed using SPSS version 20.0 7.67% of the overall mean value (993.82 N·m–1). LOA analysis
for Windows (IBM Inc., Chicago, IL). Interday measurement (absolute measurement error) revealed a relatively large system-
consistency was determined using a repeated-measures analysis of atic bias (mean difference from day 1 to day 2 = 89.57 N·m–1),
variance (ANOVA) and calculating ICCs, using the ICC2,k model as with considerable variability (± 224.8 N·m–1) around this mean
described by Shrout and Fleiss.42 Although there is no clear consen- difference (Table 1, Figure 4). Specifically, in 95% of the cases,
sus on ICC interpretation, it is generally accepted that ICC values the actual test-retest difference for KHAM could be expected to
greater than .75 represent good measurement consistency, whereas range from 135.3 N·m–1 lower to 314.4 N·m–1 higher on day 2
ICCs less than .75 reflect moderate to poor consistency.43 Precision as compared with day 1. In contrast, KLEG demonstrated good
of measurement was then evaluated by computing the SEM and to excellent measurement consistency (ICC2,3 range = .87–.94)
LOA for each variable. SEM was calculated as: , and relatively low SEMs (range = 1.00–2.91 kN·m–1) across all
where SD is the sample standard deviation. LOA were obtained 3 hopping conditions (Table 2). LOA analysis revealed little
by calculating the mean and standard deviation of the differences systematic bias between testing sessions (bilateral = –2.0, left
(SDdiff) between testing sessions (ie, day 2 – day 1). We then calcu- leg = 0.4, right leg = –1.1 kN·m–1), and in 95% of the cases (95%
lated 68% and 95% confidence limits around the mean difference LOA), the actual test-retest differences for bilateral and unilateral
as the mean difference ± 1⋅SDdiff and ± 1.96⋅SDdiff, respectively.44 KLEG ranged from being 12.3 kN·m–1 and 4.7 kN·m–1 lower to 8.3
To examine the extent to which day-to-day differences in KHAM kN·m–1 and 2.5 kN·m–1 higher on day 2 as compared with day 1
could be attributed to day-to-day differences in procedural factors (Table 2, Figure 5).
(ie, perturbation magnitude and initial knee flexion and tibia rota- All procedural factors associated with the KHAM assessment
tion angles), a multiple linear regression analysis was conducted demonstrated good to excellent day-to-day measurement consis-
on the test-retest difference scores (day 2 –day 1) for each measure. tency (Table 1). Although we attempted to carefully standardize
Finally, simple linear regression was used to determine the extent to these procedural factors during the assessment of KHAM, repeated-
which KLEG predicted KHAM on the first day of testing. This regres- measures ANOVA and LOA analyses revealed a small systematic
sion analysis was performed on body mass normalized values to bias for peak perturbation magnitude and initial knee flexion angle,
account for the influence of body size. In addition, because KHAM where peak perturbation magnitude values were on average 1.0 N
was assessed only on the left leg, KLEG during unilateral left leg lower (P = .03) and initial knee flexion angles were on average 3.4°
hopping was used as the predictor. higher (P < .01) on day 2 as compared with day 1 (Table 1). In 95%
of the cases, the actual test-retest differences for peak perturba-
Results tion magnitude and initial knee flexion angle could be expected
to range from 4.2 N lower to 2.2 N higher, and from 3.0° lower to
Interday measurement consistency (ICC2,k) and precision (SEM 9.7° higher, respectively.
and LOA) and test-retest means ± standard deviations for KHAM and When examining the extent to which day-to-day measure-
KLEG are presented in Table 1 and Table 2, respectively. ment error in KHAM could be attributed to day-to-day changes in

JAB Vol. 31, No. 5, 2015

344  Waxman, Schmitz, and Shultz

Table 1 Interday reliability results for hamstring musculo-articular stiffness (KHAM) variables
Mean Difference
Day 1 Day 2
Mean ± SD Mean ± SD ICC2,5 SEM 68% LOA 95% LOA
KHAM (N⋅m–1) 949.03 ± 134.13 1038.61 ± 141.83 .71 76.27 89.57 ± 114.70 89.57 ± 224.82
Perturbation magnitude (N) 139.60 ± 22.86 138.59 ± 22.33 .99 0.94 –1.01 ± 1.61 –1.01 ± 3.17
Initial knee flexion angle (°) 38.38 ± 4.89 41.73 ± 5.85 .82 2.48 3.35 ± 3.22 3.35 ± 6.32
Initial tibial rotation angle (°) –0.27 ± 8.54 0.92 ± 8.63 .93 2.34 1.19 ± 4.48 1.19 ± 8.78
Abbreviations: SD = standard deviation; ICC = intraclass correlation coefficient; SEM = standard error of measurement; LOA = limits of agreement.
Note. The term mean difference denotes day 2 – day 1 mean differences.

Table 2 Interday reliability results for bilateral and unilateral leg stiffness (KLEG) measures

Day 1 Day 2 Mean Difference

Mean ± SD Mean ± SD ICC2,3 SEM 68% LOA 95% LOA
KLEG (kN⋅m–1)
Bilateral 37.23 ± 8.13 35.23 ± 7.99 .87 2.91 –2.00 ± 5.27 –2.00 ± 10.32
Left leg 25.45 ± 4.13 25.09 ± 4.24 .94 1.00 –0.36 ± 1.95 –0.36 ± 3.82
Right leg 25.65 ± 4.16 24.59 ± 4.57 .94 1.10 –1.05 ± 1.84 –1.05 ± 3.61
Abbreviations: SD = standard deviation; ICC = intraclass correlation coefficient; SEM = standard error of measurement; LOA = limits of agreement.
Note. The term mean difference denotes day 2 – day 1 mean differences.

Figure 4 — Interday reliability for hamstring musculo-articular stiffness (KHAM). This Bland-Altman plot shows the difference between values for the
first and second day of testing on the vertical axis, and the mean of the first and second day of testing on the horizontal axis for each participant during
KHAM assessments. The thin dashed line represents the mean difference (bias) between testing days (day 2 – day 1), while the thick dashed lines and
solid lines represent the 68% and 95% limits of agreement, respectively. The mean difference is greater than zero, indicating systematic bias between
the first and second day of testing.

procedural factors, multiple linear regression analysis revealed magnitude) + 21.60(∆initial knee flexion angle) – 15.05(∆initial
that the linear combination of the difference scores (day 2 – day 1) tibia rotation angle). All 3 predictors uniquely contributed to the
for peak perturbation magnitude, and initial knee flexion and tibia overall model after controlling for all other predictors (Table 3).
rotation angles, explained 59.4% of the variance in the difference When examining the relationship between KHAM and KLEG,
score for KHAM (P = .02). The regression equation for the 3-predic- KLEG explained 44.2% of the variance in KHAM (P < .01), with a
tor model was: predicted ∆KHAM = 72.06 + 36.66(∆perturbation prediction equation of KHAM = 2.093 + 0.665(KLEG).
JAB Vol. 31, No. 5, 2015
Figure 5 — Interday reliability of bilateral and unilateral leg stiffness (KLEG) measurements: (A) bilateral, (B) left, and (C) right. These Bland-Altman
plots show the differences between values for the first and second day of testing on the vertical axis, and the mean of the first and second day of testing
on the horizontal axis for each participant during each of the 3 hopping conditions. The thin dashed line represents the mean difference (bias) between
testing days (day 2 – day 1), while the thick dashed lines and solid lines represent the 68% and 95% limits of agreement, respectively.
JAB Vol. 31, No. 5, 2015 345
346  Waxman, Schmitz, and Shultz

Table 3 Results of multiple linear regression analysis examining the extent to which day-to-day
differences in musculo-articular stiffness (KHAM) could be attributed to day-to-day differences in
procedural factors
Unstandardized Coefficients Correlations
Model B Standard Error P Zero-Order Partial Semipartial
Constant 72.057 35.648 .068
∆ Perturbation magnitude 36.662 14.441 .028 .404 .608 .488
∆ Initial knee flexion angle 21.599 7.386 .014 .453 .661 .562
∆ Initial tibia rotation angle –15.050 5.578 .021 –.188 –.631 –.518
Multiple R2 = .594; F(3,14) = 5.369; p = .016.
∆ = day 2 – day 1 difference.

Discussion group. In contrast, expressing the magnitude of the day-to-day

mean differences for bilateral and unilateral KLEG relative to the
Previous research suggests that higher levels of hamstring and leg deviation in scores obtained on day 1 (Table 2) resulted in much
musculo-articular stiffness (KHAM and KLEG, respectively) may be smaller estimated effect sizes (bilateral = 0.25, left = 0.09, right =
beneficial for: (1) enhancing athletic performance through increased 0.25), which suggests that the simpler assessment of KLEG may be
concentric and eccentric rate of force development11,12,14–16 and (2) a more sensitive measure for detecting changes over time.
reducing lower-extremity injury risk by helping counteract deleteri- The lower measurement consistency and precision observed for
ous loading and helping shield the ligaments from bearing the full KHAM is likely due to its more complex procedural characteristics.
responsibility of dynamic joint stability.8,17–19 Fortunately, stiffness Our results revealed that the linear combination of test-retest dif-
can be modified though training,25–27 and thus may be an important ferences for 3 procedural factors explained 59.4% of the variance
factor to consider from both injury prevention and rehabilitation in the difference in scores from day 1 to day 2 for KHAM. Given that
perspectives. Therefore, obtaining consistent measures of KHAM such a large amount of the day-to-day variability in KHAM could be
and KLEG is essential for the ability to distinguish between random attributed to these procedural factors, it is plausible that magnitude
variation in the measurement (random error) and changes attribut- of absolute measurement error could be dramatically reduced in
able to external factors such as training interventions or injury future research efforts if: (1) attempts are made to better standardize
over time.45 Although the interday measurement consistency for the application of the manual perturbation and (2) stricter control is
the assessment of KLEG during bilateral and unilateral hopping has placed over initial knee joint positioning. However, it is important
previously been established, less is known about the measurement to note that 40.6% of the variance remained unexplained by these
consistency of KHAM. factors. Carryover effects, such as effects due to familiarization,
Our primary findings were that KHAM and KLEG both demon- muscle fatigue, or muscle soreness, may have also contributed to
strated acceptable interday measurement consistency, but that KHAM the magnitude of absolute measurement error observed in this study.
was less consistent than KLEG. To our knowledge, only 2 studies16,25 Thus, measurement consistency of KHAM may also be improved
have previously examined the interday measurement consistency of by allowing additional time for participants to become adequately
KHAM, and these studies have reported ICCs ranging from .66 to .89. familiarized to the task in future work. Furthermore, it has previ-
In addition, previous investigations on the interday measurement ously been demonstrated that the method by which the assessment
consistency of KLEG have reported ICCs of .93 and .9429,30 during load is determined also contributes to KHAM variability.46 Different
bilateral barefoot hopping, .8228 during bilateral shod hopping, and methods of assigning the applied limb load include: (1) standard-
.84 to .8928 during unilateral shod hopping, at similar frequencies izing the load as 10% of the participant’s body mass (as in the
(2.0–2.5 Hz). Thus, our current findings are in agreement with prior current study),31,32 (2) standardizing the load as a percentage of the
work and support our hypothesis that, although KHAM and KLEG participant’s maximal isometric voluntary contraction (MVIC),16,25
would both display acceptable interday measurement consistency, or (3) using a single fixed load for all participants (eg, 6.5 kg).16
KLEG would display superior measurement consistency compared Ditroilo et al46 reported that assigning load as a percentage of the
with KHAM. participant’s MVIC introduces greater variability to the measure-
We also constructed Bland-Altman plots and calculated the ment of KHAM when compared with the use of a single fixed load.
68% and 95% LOA for KHAM (Table 1, Figure 4) and KLEG (Table Therefore, future studies should also carefully consider the method
2, Figure 5) to gain a better picture of the magnitude of absolute by which limb load is assigned when attempting to assess longitu-
measurement error (ie, systematic and random error) that one could dinal changes in KHAM.
expect when performing repeated measurements over time, in the Because of the complexity and equipment needed to measure
absence of any training intervention or injury. When considering KHAM, we were also interested in examining the extent to which
the magnitude of the day-to-day mean difference (systematic error the more clinically-accessible and global measure of KLEG was
= 89.6 N·m–1) for KHAM relative to the deviation in scores obtained associated with KHAM. KHAM and unilateral KLEG measures on day
on day 1 (134.1 N·m–1), this yields an estimated effect size of 0.67. 1 were found to be moderately correlated with one another (R = .67,
This moderately large estimated effect size for KHAM may mask a P < .01), with KLEG predicting 44% of the variance in KHAM. While
potential treatment effect, or suggest that a treatment effect has these findings suggest that KLEG and KHAM are related measures, we
occurred when in fact there is not one. Thus, future studies aiming acknowledge that this finding is based on a relatively small sample
to assess longitudinal changes in KHAM should include a control size (n = 15) which includes both male (n = 6) and female (n = 9)
JAB Vol. 31, No. 5, 2015
 Hamstring and Leg Stiffness Measurement Consistency   347

participants in the same analysis. It has previously been shown References

that KHAM and KLEG, as well as underlying factors that contribute
to these measures, can differ in males and females.25,47,48 Hence, 1. Butler RJ, Crowell HP, Davis IM. Lower extremity stiffness:
in certain situations, between-sex differences can create artificial Implications for performance and injury. Clin Biomech (Bris-
relationships when male and female participants are grouped into tol, Avon). 2003;18(6):511–517. PubMed doi:10.1016/S0268-
a single analysis. However, there were no between-sex differences 0033(03)00071-8
observed for KHAM (P = .34) or KLEG (P = .24), and within-sex cor- 2. Serpell BG, Ball NB, Scarvell JM, Smith PN. A review of models
relations were similar (males: R = .66, P = .15; females: R = .63, P of vertical, leg, and knee stiffness in adults for running, jumping or
= .07), confirming that this relationship was not simply driven by hopping tasks. J Sports Sci. 2012;30(13):1347–1363. PubMed doi:1
between-sex differences. 0.1080/02640414.2012.710755
As mentioned previously, the procedures associated with the 3. Brughelli M, Cronin J. A review of research on the mechanical stiff-
assessment of KHAM can be somewhat cumbersome, and the need ness in running and jumping: Methodology and implications. Scand
for adequate familiarization can be time-consuming. In contrast, J Med Sci Sports. 2008;18(4):417–426. PubMed doi:10.1111/j.1600-
the assessment of KLEG requires little familiarization, and collect- 0838.2008.00769.x
ing data on 3 trials in each condition (ie, bilateral, left, right) can 4. Ditroilo M, Watsford M, Murphy A, De Vito G. Assessing musculo-
easily be accomplished in under 10 minutes. Although these 2 mea- articular stiffness using free oscillations: Theory, measurement
sures are assessed using fundamentally different procedures, both and analysis. Sports Med. 2011;41(12):1019–1032. PubMed
assessment methods are based on the underlying construct that the doi:10.2165/11591470-000000000-00000
muscle-tendon unit(s) can be independently or collectively modeled 5. Blickhan R. The spring-mass model for running and hopping. J
as a linear mass-spring system.7 Given the impact that procedural Biomech. 1989;22(11-12):1217–1227. PubMed doi:10.1016/0021-
factors had on the day-to-day measurement consistency of KHAM, 9290(89)90224-8
it is possible that improving the measurement precision of KHAM 6. Cavagna GA. Elastic bounce of the body. J Appl Physiol.
may reveal a stronger relationship than what we observed in the 1970;29(3):279–282. PubMed
current study. In addition, participants were instructed to minimize 7. Shorten MR. Muscle elasticity and human performance. Med Sport
quadriceps muscle activation during the KHAM assessment, whereas Sci. 1987;25:18.
cocontraction of the quadriceps and hamstring muscles is inherent to 8. McNair PJ, Wood GA, Marshall RN. Stiffness of the hamstring
the assessment of KLEG.49 Hence, differences in cocontraction mag- muscles and its relationship to function in anterior cruciate ligament
nitude may also contribute to this unexplained variance. Because of deficient individuals. Clin Biomech (Bristol, Avon). 1992;7(3):131–
the potential for KLEG to be used in large screening studies, future 137. PubMed doi:10.1016/0268-0033(92)90027-2
research should continue to explore these factors to determine the 9. Farley CT, Blickhan R, Saito J, Taylor CR. Hopping frequency in
extent to which KLEG may be appropriately representative of KHAM. humans: a test of how springs set stride frequency in bouncing gaits.
In summary, findings of the current study show that KLEG is a J Appl Physiol. 1991;71(6):2127–2132. PubMed
consistent measure during bilateral and unilateral hopping at 2.2 10. Granata KP, Wilson SE, Massimini AK, Gabriel R. Active stiffness of
Hz, and that KLEG can adequately be assessed with relatively little the ankle in response to inertial and elastic loads. J Electromyogr Kine-
familiarization. In contrast, KHAM demonstrated lower interday siol. 2004;14(5):599–609. PubMed doi:10.1016/j.jelekin.2004.03.005
measurement consistency, which was found to be largely due to 11. Chelly SM, Denis C. Leg power and hopping stiffness: relation-
day-to-day variations in the magnitude of the manual perturba- ship with sprint running performance. Med Sci Sports Exerc.
tion as well as initial knee joint positioning. Other factors, such 2001;33(2):326–333. PubMed doi:10.1097/00005768-200102000-
as familiarization, muscle fatigue, or muscle soreness, and simple 00024
performance inconsistencies in isometrically holding the load may 12. Arampatzis A, Brüggemann GP, Metzler V. The effect of speed
also have contributed to the lower interday measurement consistency on leg stiffness and joint kinetics in human running. J Bio-
observed for KHAM. As such, researchers interested in assessing mech. 1999;32(12):1349–1353. PubMed doi:10.1016/S0021-
longitudinal changes in KHAM are encouraged to allow time for 9290(99)00133-5
additional familiarization, attempt to standardize the manual per- 13. Walshe AD. The validity and reliability of a test of lower body
turbation, place strict control over initial knee joint positioning, musculotendinous stiffness. Eur J Appl Physiol Occup Physiol.
and include a control group in future work. In addition, researchers 1996;73:332–339. PubMed doi:10.1007/BF02425495
may find these results helpful for sample size estimation or when 14. Wilson GJ. Murphy a J, Pryor JF. Musculotendinous stiffness: its
comparing day-to-day measurement consistency using alternative relationship to eccentric, isometric, and concentric performance. J
procedures. Furthermore, this study shows a relationship between Appl Physiol. 1994;76(6):2714–2719. PubMed
KHAM and KLEG, which suggests that the simpler measure of KLEG 15. Watsford M, Ditroilo M, Fernández-Peña E, D’Amen G, Lucertini F.
has the potential to serve as a reliable, time-efficient, and clinically- Muscle stiffness and rate of torque development during sprint cycling.
accessible measure of lower extremity stiffness that could be of great Med Sci Sports Exerc. 2010;42(7):1324–1332. PubMed doi:10.1249/
value when attempting to evaluate large samples with limited time MSS.0b013e3181ce509d
(eg, when conducting preseason athlete screenings). Further work 16. Ditroilo M, Watsford M, De Vito G. Validity and inter-day reliability
is needed to examine the extent of the KHAM and KLEG relationship of a free-oscillation test to measure knee extensor and knee flexor
after addressing methodological factors that may introduce error musculo-articular stiffness. J Electromyogr Kinesiol. 2011;21(3):492–
(thus unexplained variance) in the measure, such as subtle trial-to- 498. PubMed doi:10.1016/j.jelekin.2010.11.004
trial variations in knee joint positioning and perturbation magnitude. 17. Blackburn JT, Norcross MF, Cannon LN, Zinder SM. Hamstrings
stiffness and landing biomechanics linked to anterior cruciate
ligament loading. J Athl Train. 2013;48(6):764–772. PubMed
Acknowledgments
doi:10.4085/1062-6050-48.4.01
The authors thank Mridula Manoj and Hsin-Min Wang for their valuable 18. Blackburn JT, Norcross MF, Padua DA. Influences of hamstring
assistance with this project. stiffness and strength on anterior knee joint stability. Clin Biomech
JAB Vol. 31, No. 5, 2015
348  Waxman, Schmitz, and Shultz

(Bristol, Avon). 2011;26(3):278–283. PubMed doi:10.1016/j.clinbio- 34. Borg G. Borg’s perceived exertion and pain scales. Champaign, IL:
mech.2010.10.002 Human Kinetics; 1998.
19. Bryant AL, Kelly J, Hohmann E. Neuromuscular adaptations and cor- 35. Jennings AG, Seedhom BB. The measurement of muscle stiffness
relates of knee functionality following ACL reconstruction. J Orthop in anterior cruciate injuries - An experiment revisited. Clin Biomech
Res. 2008;26(1):126–135. PubMed doi:10.1002/jor.20472 (Bristol, Avon). 1998;13(2):138–140. PubMed doi:10.1016/S0268-
20. Williams DS, Davis IM, Scholz JP, Hamill J, Buchanan TS. High- 0033(97)00085-5
arched runners exhibit increased leg stiffness compared to low-arched 36. Granata KP, Wilson SE, Padua DA. Gender differences in
runners. Gait Posture. 2004;19(3):263–269. PubMed doi:10.1016/ active musculoskeletal stiffness. Part I. Quantification in con-
S0966-6362(03)00087-0 trolled measurements of knee joint dynamics. J Electromyogr
21. Williams DS, McClay IS, Hamill J. Arch structure and injury pat- Kinesiol. 2002;12(2):119–126. PubMed doi:10.1016/S1050-
terns in runners. Clin Biomech (Bristol, Avon). 2001;16(4):341–347. 6411(02)00002-0
PubMed doi:10.1016/S0268-0033(01)00005-5 37. Arampatzis A, Schade F, Walsh M, Brüggemann GP. Influence of
22. Milner CE, Ferber R, Pollard CD, Hamill J, Davis IS. Biomechanical leg stiffness and its effect on myodynamic jumping performance. J
factors associated with tibial stress fracture in female runners. Med Electromyogr Kinesiol. 2001;11(5):355–364. PubMed doi:10.1016/
Sci Sports Exerc. 2006;38(2):323–328. PubMed doi:10.1249/01. S1050-6411(01)00009-8
mss.0000183477.75808.92 38. Bishop M, Fiolkowski P, Conrad B, Brunt D, Horodyski M. Ath-
23. Granata KP, Padua DA, Wilson SE. Gender differences in active letic footwear, leg stiffness, and running kinematics. J Athl Train.
musculoskeletal stiffness. Part II. Quantification of leg stiffness during 2006;41(4):387–392. PubMed
functional hopping tasks. J Electromyogr Kinesiol. 2002;12:127–135. 39. Winter DA. Anthropometry. In: Biomechanics of Human Movement.
PubMed doi:10.1016/S1050-6411(02)00003-2 New York, NY: John Wiley & Sons; 1990:51–74.
24. Watsford ML, Murphy AJ, McLachlan KA, et al. A prospective 40. Hobara H, Kimura K, Omuro K, et al. Determinants of difference in leg
study of the relationship between lower body stiffness and hamstring stiffness between endurance- and power-trained athletes. J Biomech.
injury in professional Australian rules footballers. Am J Sports Med. 2008;41:506–514. PubMed doi:10.1016/j.jbiomech.2007.10.014
2010;38(10):2058–2064. PubMed doi:10.1177/0363546510370197 41. Hobara H, Inoue K, Kobayashi Y, Ogata T. A comparison of com-
25. Blackburn JT, Norcross MF. The effects of isometric and isotonic putation methods for leg stiffness during hopping. J Appl Biomech.
training on hamstring stiffness and anterior cruciate ligament loading 2014;30(1):154–159. PubMed doi:10.1123/jab.2012-0285
mechanisms. J Electromyogr Kinesiol. 2014;24(1):98–103. PubMed 42. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reli-
doi:10.1016/j.jelekin.2013.10.010 ability. Psychol Bull. 1979;86(2):420–428. PubMed doi:10.1037/0033-
26. Burgess KE, Connick MJ, Graham-Smith P, Pearson SJ. Plyometric 2909.86.2.420
vs. isometric training influences on tendon properties and muscle 43. Portney LG, Watkins MP. Reliability. In: Foundations of clinical
output. J Strength Cond Res. 2007;21(3):986–989. PubMed research: applications to practice. 2nd ed. New Jersey: Prentice Hall
27. Kubo K, Morimoto M, Komuro T, et al. Effects of plyometric and Health; 2000:53–68.
weight training on muscle-tendon complex and jump performance. 44. Bland JM, Altman DG. Statistical methods for assessing agreement
Med Sci Sports Exerc. 2007;39(10):1801–1810. PubMed doi:10.1249/ between two methods of clinical measurement. Lancet. 1986;1:307–
mss.0b013e31813e630a 310. PubMed doi:10.1016/S0140-6736(86)90837-8
28. Joseph C, Bradshaw E, Clark R. Inter-Day Reliability Leg, Knee 45. Atkinson G, Nevill AM. Statistical methods for assessing measurement
and Ankle Stiffness Measures During Hopping. Port J Sport Sci. error (reliability) in variables relevant to sports medicine. Sports Med.
2011;11(2):989–992. 1998;26(4):217–238. PubMed doi:10.2165/00007256-199826040-
29. McLachlan KA, Murphy AJ, Watsford ML, Rees S. The interday 00002
reliability of leg and ankle musculotendinous stiffness measures. J 46. Ditroilo M, Watsford M, Murphy A, De Vito G. Sources of vari-
Appl Biomech. 2006;22(4):296–304. PubMed ability in musculo-articular stiffness measurement. PLoS One.
30. Lloyd RS, Oliver JL, Hughes MG. Williams C a. Reliability and 2013;8(5):e63719. PubMed doi:10.1371/journal.pone.0063719
validity of field-based measures of leg stiffness and reactive strength 47. Hobara H, Kato E, Kobayashi Y, Ogata T. Sex differences in relation-
index in youths. J Sports Sci. 2009;27(14):1565–1573. PubMed ship between passive ankle stiffness and leg stiffness during hop-
doi:10.1080/02640410903311572 ping. J Biomech. 2012;45(16):2750–2754. PubMed doi:10.1016/j.
31. Blackburn JT. Sex comparison of extensibility, passive, and active stiff- jbiomech.2012.09.008
ness of the knee flexors. Clin Biomech (Bristol, Avon). 2004;19(1):36– 48. Blackburn JT, Bell DR, Norcross MF, Hudson JD, Kimsey MH. Sex
43. PubMed doi:10.1016/j.clinbiomech.2003.09.003 comparison of hamstring structural and material properties. Clin
32. Bell DR, Blackburn JT, Norcorss MF, et al. Estrogen and muscle Biomech (Bristol, Avon). 2009;24(1):65–70. PubMed doi:10.1016/j.
stiffness have a negative relationship in females. Knee Surg Sports clinbiomech.2008.10.001
Traumatol Arthrosc. 2012;20(2):361–367. PubMed doi:10.1007/ 49. Hobara H, Inoue K, Muraoka T, Omuro K, Sakamoto M, Kanosue
s00167-011-1577-y K. Leg stiffness adjustment for a range of hopping frequencies in
33. Bompa TO, Haff G. Periodization: Theory and Methodology of Train- humans. J Biomech. 2010;43(3):506–511. PubMed doi:10.1016/j.
ing. 5th ed. Champaign, IL: Human Kinetics; 2009. jbiomech.2009.09.040

JAB Vol. 31, No. 5, 2015

View publication stats