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Journal of Sport Rehabilitation, 2011, e-pub only
© 2011 Human Kinetics, Inc.
Technical noTe
The authors are with the Dept of Exercise and Sport Science, University of North Carolina at Chapel
Hill, Chapel Hill, NC.
Reliability, Validity, and Precision
of a Handheld Myometer for Assessing
in Vivo Muscle Stiffness
Steven M. Zinder and Darin A. Padua
Biomechanically, muscle stiffness is the ratio of force response that results from
and resists mechanical stretch.1 The stiffness of the passive structures surrounding
a joint contributes little to its biomechanical stability except at the end ranges of
motion.2 Research has found, however, that the active stiffness properties of muscles
are essential to dynamic stability.3,4 Optimal levels of musculotendinous stiffness
are highly correlated to signicant increases in muscle performance.5 This increased
muscle stiffness surrounding a joint could limit the translation suffered by the joint
after an injurious perturbation.6 This in turn would limit strain on the ligamentous
structures, ultimately decreasing the incidence and severity of injury. Excessive
amounts of stiffness, such as the spasticity associated with cerebral palsy, can be
detrimental, however. Therefore, the ability to accurately quantify active muscle
stiffness in an attempt to identify the optimal level of stiffness is integral for both
clinicians and researchers.
To date, methods for measuring active muscle stiffness have used complicated
computer algorithms and sophisticated laboratory hardware, making accurate
assessment of muscle stiffness nearly impossible for clinicians. The oscillatory
method requires a sophisticated device to measure the frequency and decay of
transient motion oscillations at the joint along with a complicated mathematical
analysis to calculate the stiffness values. The passive force–position relationship,
wherein joint-force responses are measured at different passive joint angles, requires
a device that can accurately measure both joint position and force. In addition,
in both examples, the outcome measurement is essentially overall joint stiffness,
receiving contributions from the joint musculature, joint compression, and the
passive structures surrounding the joint. There is a need for clinicians to be able
to accurately measure the stiffness of individual muscles to isolate specic issues
to be addressed in rehabilitation.
A handheld myometer is a device purported to accurately measure muscle
stiffness in individual muscles. Previous research5,7–9 has shown that other methods
of muscle-stiffness measurement (e.g., damped oscillatory and passive length–
tension) are sensitive to levels of muscle force output. Sex differences have also been
observed using these other measures of stiffness.7,10,11 Thus, we hypothesized that if
a handheld myometer provides a valid assessment of stiffness that we would observe
2 Zinder and Padua
similar patterns. Therefore, the purpose of this investigation was to examine the reli-
ability and validity of a handheld myometer for assessing skeletal-muscle stiffness.
Methods
Subjects
20 subjects (6 men, 14 women; age 21.90 ± 2.93 y, height 170.46 ± 9.24 cm,
mass 72.01 ± 11.47 kg) with no known neuromuscular disorders volunteered to
participate in this study.
Instrumentation
All data were collected using the Myoton-3 (Müomeetria Ltd, Estonia, EU)
handheld myometer (Figure 1). The tip of the myometer was placed on the tissue
perpendicular to the underlying muscle. Slight pressure on the tip activated an
electromagnet in the device, which exerted a local impact on the tissue by means
of a brief mechanical impulse. This caused a minor deformation of the underly-
ing muscle tissue. After the impact, the tip was quickly released, and the damped
oscillatory behavior (Figure 2) of the tissue was recorded by an accelerometer in
the device. The viscoelastic stiffness of the underlying tissue was calculated using
the following equation12:
C = 4π2m2Y2 + (θ/4m)
where Y = the oscillation frequency, Y = 1/T Hz, and θ is the logarithmic decrement
of oscillation damping (Figure 2): θ = ln(a1/a3).
Procedures
All testing was performed in the sports medicine research laboratory at the
University of North Carolina at Chapel Hill. Each subject read and signed an
informed-consent form approved by the institutional review board and was given
the opportunity to ask questions if
any arose.
After we recorded demographic
data, subjects were positioned on a
Biodex System 3 isokinetic dyna-
mometer (Biodex Medical Systems,
Shirley, NY) per the manufactur-
er’s guidelines for knee extension
(Figure 1). The dynamometer arm
was locked with the subject’s knee
in 60° of exion for isometric test-
ing. Maximum voluntary isometric
contraction (MVIC) values were
calculated by averaging the peak
force output of three 5-second
maximal knee-extension contrac-
tions with 1 minute between exer-
tions. Five consecutive myometric
stiffness measurements were then Figure 1 — Myoton-3 and subject positioning.
Handheld Myometer to Assess in Vivo Muscle Stiffness 3
collected in a randomized order from the midbelly of the rectus femoris muscle
at each of 5 different activation levels: 10%, 20%, 30%, 40%, and 50% of the
subject’s MVIC. The subjects were given a 1-minute rest between testing con-
ditions. A visual display of percentage MVIC was provided to the subjects as
a reference for the graded contractions. They were permitted to practice until
they felt comfortable sustaining the specic level of contraction before testing
in each condition.
Statistical Analysis
Descriptive statistics were calculated for demographic information on age, height,
and body mass. A mixed-model repeated-measures ANOVA was computed to assess
rectus femoris viscoelastic-stiffness differences over the different load conditions
and across sexes. Separate intraclass correlation coefcients (ICC2,1) and standard
errors of measurement (SEMs) were performed across the 5 trials in each load
condition to assess trial-to-trial reliability and precision. All measurements were
collected by the same investigator (SMZ) and were analyzed with the Statistical
Package for the Social Sciences version 17.0 (SPSS, Chicago, IL).
Results
Mean stiffness values for each of the load conditions were consistent with pre-
vious literature (Table 1).13 Post hoc analysis revealed that stiffness values at
10% load were signicantly different than those at 20%, 30%, 40%, and 50%
Figure 2 — Damped oscillatory behavior of the rectus femoris muscle (adapted from Vain
and Kums12). T, time from peak 1 to peak 3; a1, amplitude peak 1; a2, amplitude peak 2.
4
Table 1 Muscle Stiffness for the Individual Trials, N/m
Trial
% MVIC Gender 1 2 3 4 5 Mean SD
P
ICC
2,1
SEM
10% men 410.50 374.50 389.50 386.33 395.00 391.17 74.96
women 276.07 278.79 280.64 282.57 290.29 281.67 30.76
total 316.40 307.50 313.30 313.70 321.70 314.52 69.11 .28 .92 23.34
20% men 445.17 442.83 443.00 422.83 428.83 436.53 84.64
women 296.21 306.29 307.07 304.07 313.36 305.40 49.88
total 340.90 347.25 347.85 339.70 348.00 344.74 85.96 .41 .96 19.38
30% men 461.00 461.83 463.50 441.50 457.33 457.03 89.34
women 313.50 323.14 314.29 334.14 323.14 321.64 73.58
total 357.75 364.75 359.05 366.35 363.40 362.26 99.28 .81 .94 26.69
40% men 520.20 451.60 436.00 453.40 459.00 464.04 102.05
women 332.21 329.93 334.14 325.07 333.71 331.16 66.59
total 387.80 367.55 367.45 363.70 366.68 370.64 99.11 .35 .86 46.78
50% men 514.83 485.17 545.17 508.00 506.83 512.00 127.86
women 330.36 334.07 328.93 340.71 331.57 333.13 67.56
total 385.70 379.40 393.80 390.90 384.15 386.79 120.40 .78 .91 38.00
MVIC, maximal voluntary isometric contraction.
Handheld Myometer to Assess in Vivo Muscle Stiffness 5
Figure 3 — Rectus femoris stiffness values across contraction levels. *10% < 20%, 30%,
40%, and 50%; 20% < 40% and 50%. MVIC, maximal voluntary isometric contraction.
loads and that 20% was signicantly different than stiffness levels at 40% and
50% MVIC (Figure 3). Men generated signicantly higher stiffness values than
women at each level of contraction (Figure 4). There was also a signicant load
× sex interaction that showed that the stiffness exhibited by men increased at a
greater rate at the higher level of contraction than did that of women, especially
at the 50% load level (Figure 4). Trial reliability and precision were excellent for
each load condition, with ICCs ranging from .86 to .96 and SEMs ranging from
19.38 to 46.78 N/m (Table 1).
Discussion
Active muscle stiffness has been shown to be an integral component in decreasing
injurious joint translations.3,4 It is therefore important to be able to easily and accu-
rately quantify skeletal-muscle stiffness. Previously this has been difcult because
of the specialized equipment and techniques needed, but the current investigation
evaluated the reliability, validity, and precision of a handheld myometer, a user-
friendly instrument, to quantify muscle stiffness.
Reliability Analysis
The current data show that the handheld myometer produced reliable and precise
measurements of active muscle stiffness. It has been suggested that ICCs above .75
demonstrate good reliability, and those below .75 indicate moderate to poor reli-
6 Zinder and Padua
ability.14 The very high ICCs in the current study (.86–.96 across the different load
conditions) demonstrate that when the manufacturer’s recommended procedures
are strictly followed, clinicians and researchers can obtain very consistent active
muscle-stiffness measures across multiple trials. These values are comparable
to reliability of other methods of stiffness calculation presented in the literature
demonstrating ICCs ranging from .88 to .96.15,16
The extremely low SEMs, ranging from 5.6% to 12.6% of the mean stiffness
values, demonstrate excellent precision of the measurement when compared across
trials. This is comparable to other methods presented in the literature that demon-
strated SEMs ranging from 5.7% to 8.0% of the mean stiffness values.16 Although
measures at all levels of submaximal voluntary contraction examined showed high
reliability and excellent precision, the stiffness measures at 20% and 30% of MVIC
produced the highest reliability and greatest precision, suggesting they may be the
best choices for submaximal stiffness measurements.
Validity Analysis
Construct validity of the handheld myometer active muscle-stiffness measures was
established by comparing the change in stiffness values relative to the change in
Figure 4 — Rectus femoris stiffness values across contraction levels and sex. *Men sig-
nicantly greater at each contraction level.
Handheld Myometer to Assess in Vivo Muscle Stiffness 7
level of muscle contraction across sexes. Many studies on both in vitro9,17 and in
vivo5,7,8 muscle tissue have demonstrated that active muscle stiffness is proportional
to the level of muscle activation. In the current study active muscle-stiffness mea-
sures were collected at 10%, 20%, 30%, 40%, and 50% of the subjects’ MVIC,
causing a systematic increase in motor-unit recruitment as the level of contraction
increased. Although not all the stiffness values were statistically different across
contraction levels, the data trended toward a linear increase (R2 of .95) in active
stiffness levels with the increase in contraction level (Figure 3). This is consistent
with previous research using the Myoton.13
It has also previously been demonstrated that males consistently have greater
musculotendinous-stiffness values than females7,10,18 and that those differences
widen as torque production in the underlying muscle increases.18 These results
are mirrored in the current study, in which men had signicantly greater stiffness
values at each level of background contraction, with the greatest difference at the
50% MVIC load. The combination of the ability to detect increased stiffness values
with a concomitant increase in background muscle activity and accurately portray-
ing the stiffness characteristics across sexes suggest that the Myoton 3 is a valid
instrument to measure viscoelastic-stiffness properties of the musculotendinous unit.
Another advantage of the Myoton over existing stiffness-measurement tech-
niques is its ability to measure isolated muscles. With the standard oscillatory
technique of assessing muscle stiffness it is nearly impossible to isolate specic
muscles and avoid cocontraction of antagonist musculature. Cocontraction has
been shown to be a signicant contributor to joint stiffness,11,19 so the Myoton may
allow for a more specic measure of isolated muscle stiffness than currently used
techniques for stiffness assessment. This could be an invaluable tool for clinicians
to isolate specic muscles to evaluate their individual contributions to joint stability.
Limitations
There are a few limitations and weaknesses to the current study. Most notably, only
1 aspect of validity, construct validity, was examined. There is no gold standard of
stiffness measurement in the literature, making comparisons to an accepted standard
difcult. Any of the previously used measures of stiffness use effective stiffness
measures that include contributions from all the surrounding musculature, passive
joint structures, joint compression, and so on. No other measurement technique we
are aware of allows for in vivo stiffness measures of individual muscles. There were
also unequal numbers of subjects in the gender groups. There was still adequate
statistical power to elucidate group differences, but future investigations should
place greater emphasis on similarity in sample size. Also, future studies should
examine other aspects of reliability, such as intratester and day-to-day reliability
of the measure, to get a more complete picture of the myometer’s reliability.
Conclusions
The results of this study suggest that a handheld myometer may be an effective
clinical measure of active muscle stiffness. The valid, reliable, and precise mea-
surements it collects combined with its ease of use and ability to measure active
muscle stiffness in specic, individual muscles make it a valuable tool to any
8 Zinder and Padua
practitioner or researcher interested in in vivo biomechanical properties of skeletal
muscle. Although myometry may not completely replace the computer algorithms
and sophisticated hardware needed in many applications, this simple device shows
promise as a tool in many research laboratories and therapy clinics.
References
1. Rack P, Westbury D. The effects of length and stimulus rate on tension in the isometric
cat soleus muscle. J Physiol (Lond). 1969;204(2):443–460.
2. Crisco JJ, Panjabi MM. Euler stability of the human ligamentous lumbar spine: part I
theory. Clin Biomech. 1992;7:19–26.
3. Duan XH, Allen RH, Sun JQ. A stiffness-varying model of human gait. Med Eng Phys.
1997;19:518–524.
4. Wagner H, Blickhan R. Stabilizing function of skeletal muscles: an analytical investiga-
tion. J Theor Biol. 1999;199:163–179.
5. Wilson GJ, Wood GA, Elliott BC. Optimal stiffness of series elastic component in a
stretch-shorten cycle activity. J Appl Physiol. 1991;70(2):825–833.
6. Wojtys EM, Ashton-Miller JA, Huston LJ. A gender-related difference in the contribu-
tion of the knee musculature to sagittal-plane shear stiffness in subjects with similar
knee laxity. J Bone Joint Surg Am. 2002;84(1):10–16.
7. Granata KP, Padua DA, Wilson SE. Gender differences in active musculoskeletal
stiffness: part II: quantication of leg stiffness during functional hopping tasks. J
Electromyogr Kinesiol. 2002;12(2):127–135.
8. McNair PJ, Hewson DJ, Dombroski E, Stanley SN. Stiffness and passive peak force
changes at the ankle joint: the effect of different joint angular velocities. Clin Biomech
(Bristol, Avon). 2002;17(7):536–540.
9. Rack PMH, Westbury DR. The short range stiffness of active mammalian muscle and
its effect on mechanical properties. J Physiol. 1974;240:331–350.
10. Blackburn JT, Padua DA, Weinhold PS, Guskiewicz KM. Comparison of triceps surae
structural stiffness and material modulus across sex. Clin Biomech (Bristol, Avon).
2006;21(2):159–167.
11. Granata KP, Padua DA, Wilson SE. Functional leg stiffness differences between genders.
J Electromyogr Kinesiol. 2002;12:127–135.
12. Vain A, Kums T. Criteria for preventing overtraining of the musculoskeletal system of
gymnasts. Biol Sport. 2002;19(4):329–346.
13. Bizzini M, Mannion AF. Reliability of a new, hand-held device for assessing skeletal
muscle stiffness. Clin Biomech (Bristol, Avon). 2003;18(5):459–461.
14. Portney LG, Watkins MP. Foundations of Clinical Research Applications to Practice.
2nd ed. Upper Saddle River, NJ: Pretice Hall Health; 2000.
15. Stanton TR, Kawchuk GN. Reliability of assisted indentation in measuring lumbar
spinal stiffness. Man Ther. 2009;14(2):197–205.
16. Zinder SM, Granata KP, Padua DA, Gansneder BM. Validity and reliability of a new
in vivo ankle stiffness measurement device. J Biomech. 2007;40(2):463–467.
17. Julian FJ, Sollins MR. Variation of muscle stiffness with force at increasing speeds of
shortening. J Gen Physiol. 1975;66:287–302.
18. Granata KP, Wilson SE, Padua DA. Gender differences in active musculoskeletal
stiffness: part I: quantication in controlled measurements of knee joint dynamics. J
Electromyogr Kinesiol. 2002;12(2):119–126.
19. Padua DA, Arnold BL, Perrin DH, Gansneder BM, Carcia CR, Granata KP. Fatigue,
vertical leg stiffness, and stiffness control strategies in males and females. J Athl Train.
2006;41(3):294–304.
