Accepted Manuscript

Biomechanical properties of low back myofascial tissue in

younger adult ankylosing spondylitis patients and matched
healthy control subjects

Allison White, Hannah Abbott, Alfonse T. Masi, Jacqueline

Henderson, Kalyani Nair

PII: S0268-0033(18)30201-8
DOI: doi:10.1016/j.clinbiomech.2018.06.006
Reference: JCLB 4549
To appear in: Clinical Biomechanics
Received date: 7 March 2018
Accepted date: 4 June 2018

Please cite this article as: Allison White, Hannah Abbott, Alfonse T. Masi, Jacqueline
Henderson, Kalyani Nair , Biomechanical properties of low back myofascial tissue in
younger adult ankylosing spondylitis patients and matched healthy control subjects. Jclb
(2017), doi:10.1016/j.clinbiomech.2018.06.006

This is a PDF file of an unedited manuscript that has been accepted for publication. As
a service to our customers we are providing this early version of the manuscript. The
manuscript will undergo copyediting, typesetting, and review of the resulting proof before
it is published in its final form. Please note that during the production process errors may
be discovered which could affect the content, and all legal disclaimers that apply to the
journal pertain.
 ACCEPTED MANUSCRIPT

Title:

Biomechanical Properties of Low Back Myofascial Tissue in Younger Adult

Ankylosing Spondylitis Patients and Matched Healthy Control Subjects

Author Names and Affiliations:

T
Allison Whitea
a

IP
Mechanical Engineering, Bradley University, Peoria, IL 61625 , USA
E-mail: awhite@mail.bradley.edu

CR
Hannah, Abbottb
b
Mechanical Engineering, Bradley University, Peoria, IL 61625, USA
E-mail: habbott@mail.bradley.edu

US
Alfonse T. Masi, MD, DR. PHc
c
University of Illinois College of Medicine, Peoria, IL 61656, USA
AN
E-mail: amasi@uic.edu

Jacqueline Henderson, PhDd

M

d
Mechanical Engineering, Bradley University, Peoria, IL 61625, USA
E-mail: jhenderson@bradley.edu
D

Kalyani Nair, PhDe

e
TE

Mechanical Engineering, Bradley University, Peoria, IL 61625, USA

E-mail: knair@bradley.edu
P

Corresponding author:
CE

Kalyani Nair, PhDf

Associate Professor
AC

f
Mechanical Engineering, Bradley University, Peoria, IL 61625, USA
E-mail: knair@bradley.edu

Word Count:

Abstract: 248 words

Main Text: 3,323 words

Page 1 of 24
 ACCEPTED MANUSCRIPT

ABSTRACT

Background

Ankylosing spondylitis is a degenerative and inflammatory rheumatologic disorder that

primarily affects the spine. Delayed diagnosis leads to debilitating spinal damage. This study

T
examines biomechanical properties of non-contracting (resting) human lower lumbar myofascia in

IP
ankylosing spondylitis patients and matched healthy control subjects.

CR
Methods

Biomechanical properties of stiffness, frequency, decrement, stress relaxation time, and

US
creep were quantified from 24 ankylosing spondylitis patients (19male, 5female) and 24 age- and
AN
sex-matched control subjects in prone position on both sides initially and after 10 minutes rest.

Concurrent surface electromyography measurements were performed to ensure resting state.

M

Statistical analyses were conducted, and significance was set at p < 0.05.
D

Findings
TE

Decreased lumbar muscle elasticity (inverse of decrement) was primarily correlated with
P

disease duration in ankylosing spondylitis subjects, whereas BMI was the primary correlate in
CE

control subjects. In ankylosing spondylitis and control groups, significant positive correlations

were observed between the linear elastic properties of stiffness and frequency as well as between
AC

the viscoelastic parameters of stress relaxation time and creep. The preceding groups also showed

significant negative correlations between the linear elastic and viscoelastic properties.

Interpretation

Findings indicate that increased disease duration is associated with decreased tissue

elasticity or myofascial degradation. Both ankylosing spondylitis and healthy subjects revealed

Page 2 of 24
 ACCEPTED MANUSCRIPT

similar correlations between the linear and viscoelastic properties which suggest that the disease

does not directly alter their inherent interrelations. The novel result that disease and duration

differentially affect stiffness and elasticity, respectively, deserves further investigation of the

biomechanical properties and their underlying mechanisms.

T
IP
Keywords: myofascia, linear elastic, viscoelastic, ankylosing spondylitis, low back, biomechanical

CR
properties

US
AN
M
D
P TE
CE
AC

Page 3 of 24
 ACCEPTED MANUSCRIPT

INTRODUCTION

Osteoligamentous complications commonly occur in ankylosing spondylitis (AS) and

spondyloarthritis (SpA) disorders, but little research has been done to determine whether passive

axial myofascial tone or stiffness play a role in the development of such disorders [1]. Human

resting muscle/myofascial tone (HRMT) is an intrinsic viscoelastic property which assists in

T
maintaining the spine’s stability. Current studies focus on active, contracting muscles, and little

IP
research has been published on HRMT or its effects on the biomechanics of human muscles,

CR
specifically those of the lower lumbar region [1].

Ankylosing spondylitis is a chronic degenerative and inflammatory disease that primarily

US
affects the spine and sacroiliac joints (SIJs) and typically manifests in the later teen or young adult
AN
years [2]. Later stages of AS of over 10 or more years of disease can exhibit clear manifestations

of spinal damage and loss of function [1]. In contrast, early signs of AS may be only symptomatic,
M

and definite diagnosis may be delayed for a period of 5 to 7 years or longer [1]. Our recent clinical
D

study on AS patients indicated increased muscle stiffness in the L3-L4 lumbar regions as measured
TE

by the MyotonPro [2].

P

Passive or resting (non-contractile) lumbar myofascial tissue behaves as both a linear

CE

elastic and viscoelastic material. Linear elastic materials differ from viscoelastic because the

linear elastic materials deform instantaneously with applied stress and are not time dependent.
AC

Viscoelastic materials return to their initial form after a period of time following the release of the

applied stress. Creep and stress relaxation time are time-dependent viscoelastic properties. Creep

is the material property in which progressive deformation occurs with time while a constant stress

is applied [3, 4]. Stress relaxation describes the phenomenon of decreasing stress with time, while

the applied strain is constant. Stress relaxation time is the recovery time for the material to return

Page 4 of 24
 ACCEPTED MANUSCRIPT

to its normal state after deformation [3, 5]. Muscle and other soft tissue behave both as linear

elastic and viscoelastic materials, depending upon the range of deformation [6-8].

Few studies have quantified both the linear elastic and viscoelastic properties of human

resting muscle tissue. For clinical trials of pre-school children with cerebral palsy, reference

measurements were obtained on 15 healthy children using MyotonPro, digital inclinometers,

T
ultrasound, and tape to develop a battery for comparison [9]. MyotonPro measurements of

IP
stiffness, frequency, decrement, creep, and stress relaxation time were performed on the posterior

CR
mid-lower leg. Repeated MyotonPro measurements of dynamic stiffness (ICC = 0.73) and

US
frequency (ICC = 0.74) were reliable [9]. A study in weightlessness during zero gravity flights

used the MyotonPro to measure stiffness, frequency, decrement, creep, and stress relaxation time
AN
of the gastrocnemius, m. erector spinae, and Achilles tendon in 11 healthy subjects [10]. Muscle
M

tissue was significantly more relaxed in microgravity than normal gravity (approximately 10%

lower) [10]. A further study quantified the effects of eccentric exercise (ECC) on upper trapezius
D

muscle stiffness and creep at the muscle belly and musculotendinous sites [11]. At the
TE

musculotendinous sites, muscle stiffness increased and creep decreased 24 hours after ECC, while
P

the reverse was observed at the muscle belly sites [11].

CE

None of the above published human studies performed correlational analysis between the
AC

different linear elastic and viscoelastic parameters to better understand and interpret the results.

No studies analyzed muscle properties at rest or of the lower back myofascial tissue in AS patients

or control (CN) subjects. Additionally, no studies have analyzed the association of BMI, age, and

disease duration with lower back myofascial tissue in AS patients.

The aim of this study is to analyze and compare AS and healthy subjects on their linear

elastic properties of stiffness, frequency (tone), and decrement (inverse of elasticity) and their

Page 5 of 24
 ACCEPTED MANUSCRIPT

viscoelastic properties of stress relaxation time and creep of the L3-L4 myofascia as measured by

the MyotonPro. In addition, correlational analyses were performed on all of the biomechanical

properties in the subject groups, and the associations of age, body mass index (BMI), and AS

disease duration with the five properties were investigated.

T
METHODS

IP
Approval of the research protocol was received from our Institutional Review Board (IRB).

CR
All subjects consented to participating in the project after being properly informed about the study.

The Assessment of SpondyloArthritis International Society’s (ASAS) criteria for axial

US
spondyloarthritis were used to select AS subjects [2]. Within each group (24 AS and 24 healthy
AN
controls), 19 male and 5 female age-comparable subjects were chosen, and the median age of the

total 48 subjects was 30 years old. Control subjects were excluded if they had pain or stiffness at
M

the time of the interview. All subjects were excluded if they suffered from chronic neurological or
D

musculoskeletal conditions, had a past spinal surgery, or had a BMI ≥ 35kg/m2. Of the 48
TE

subjects, 43 were right-handed [2].

P

MyotonPro® (Myoton AS, Tallinn, Estonia) was used to obtain non-invasive

CE

measurements to quantify the linear elastic and viscoelastic properties of the lower lumbar (L3-L4)

erector spinae muscles. Extensive data on the reliability of the device on a number of tissues has
AC

been reported [1, 2, 12-21]. The MyotonPro® applies a controlled pre-load of 0.18 N for an initial

compression of the subcutaneous tissue before imposing an additional 15 ms impulse of 0.40 N of

mechanical force, which induces a damped natural oscillation of the tissue [22]. The peak

acceleration (amax) of the natural oscillation is identified and measured using an accelerometer

located on the tip of the MyotonPro® probe. Velocity is derived from the first integration of the

Page 6 of 24
 ACCEPTED MANUSCRIPT

acceleration signal, and displacement is derived from the second integration [1]. The linear elastic

(dynamic stiffness and frequency) parameters, viscoelastic (stress relaxation time and creep)

parameters, and the inverse indicator of overall elasticity (decrement) are all acquired from the

acceleration signal. Dynamic stiffness (N/m) is quantified by the following equation,

𝑎𝑚𝑎𝑥 ∙𝑚𝑝𝑟𝑜𝑏𝑒
𝑆= (1)
∆𝑙

T
where amax is the maximum acceleration obtained from the acceleration curve of the

IP
impulse generated in the muscle by the MyotonPro, mprobe is the standardized mass of the

CR
MyotonPro’s probe, and Δl is the maximum displacement of the muscle tissue. Dynamic

US
stiffness characterizes the property of a muscle to resist an external force that deforms its initial

shape [22].
AN
The oscillation frequency (Hz) reflects the tone or the intrinsic tension of a muscle, which
M

is measured in this study in its passive or resting state without any voluntary contraction [22]. The

frequency is quantified mathematically by the maximum frequency obtained from a Fast Fourier
D

Transform (FFT) of the tissue’s acceleration curve [22].

TE

Using a logarithmic function, the MyotonPro® also quantifies a parameter called

P

decrement, which is inverse to the overall elasticity of the tissue. Decrement is measured as the
CE

damping ratio of the acceleration signal when the tissue recovers its shape after being deformed
AC

[22]. Decrement is quantified by the following equation,

𝑎
𝐷 = 𝑙𝑛 (𝑎1 ) (2)
3

where a1 is the first positive acceleration peak of the acceleration curve, and a3 is the second

positive acceleration peak. As the value of decrement increases, the elasticity of the tissue

decreases.

Stress relaxation time (SRT) is a viscoelastic property that is defined as the time (ms) for a

Page 7 of 24
 ACCEPTED MANUSCRIPT

material (muscle) to recover its shape after deformation following the removal of an external force

[22]. SRT is quantified by the equation,

𝑆𝑅𝑇 = 𝑡𝑅 − 𝑡1 (3)

where tR and t1 are represented in Figure 1. SRT is the time (ms) for the tissue to return to

rest (tR), after the point of maximum deformation (t1).

T
MyotonPro® quantifies another viscoelastic property called creep, which is expressed as

IP
the ratio of SRT to the initial deformation time. Biomechanically, creep is the continual

CR
deformation of a tissue over time when subjected to a constant tensile stress [22]. Creep is

US
quantified by the following equation,
𝑆𝑅𝑇
𝐶=𝑡 (4)
1 −𝑡𝑇
AN
where t1 and tT are represented in Figure 1. tT is the initial time, and t1 is the time at which
M

maximum deformation occurs.

D
P TE
CE
AC

Fig. 1: Acceleration curve generated in muscle tissue by MyotonPro  [12]

To ensure a passive state throughout the duration of data collection, surface

electromyography measurements (sEMG) were performed using the FlexComp Infiniti (Thought

Technology Ltd., Quebec, Canada). MyotonPro® measurements were performed only when the

Page 8 of 24
 ACCEPTED MANUSCRIPT

sEMG values were within the acceptable range of passive muscle state values of less than 5 μV [1,

23, 24]. The monitoring procedure consisted of attaching electrodes to the L3-L4 lumbar region of

each participant and connecting them to a computer through the FlexComp Infiniti hardware

components. The FlexComp Infiniti computer program then generated real-time waveforms of

sEMG behavior, which were monitored and recorded during all measurements, thereby confirming

T
a consistent passive muscle state. Four individual time and side measurements were recorded to

IP
quantify the studied variables at an initial point in time and after 10 minutes of rest on both the left

CR
and right sides of the subject’s lower back (L3-L4) [1, 2].

Nonparametric statistical analyses were performed using IBM SPSS Version 20. The

US
Mann Whitney U independent variables test was conducted on stiffness, frequency, decrement,
AN
SRT, and creep values between the different groups. The Wilcoxon dependent variables test was

performed to analyze data within groups (left vs. right side, initial vs. 10 minute). Bivariate
M

correlations were performed between the five biomechanical properties and the additional
D

variables of age, body mass index (BMI), and years duration since the AS patient was diagnosed
TE

with the disease. To evaluate the effects of disease duration in AS, as associated with age, both
P

subject groups were ranked by age within gender. The age-ranked disease duration of each AS
CE

patient was assigned to the paired CN subject. For example, the tenth ranked male AS had an age

of 32 years and disease duration of 10 years, which was assigned to the tenth ranked CN male.
AC

The intention of this disease duration analysis in AS patients is to determine how progression of

AS may clinically influence lumbar myofascial properties. The assigned disease duration value in

CN subjects is inferred to be incidental and non-significant and have no significant correlation

with the biomechanical properties.

Multivariable linear regression analysis between the variables of stiffness, frequency,

Page 9 of 24
 ACCEPTED MANUSCRIPT

decrement, SRT, creep, age, and BMI were also performed to determine correlation coefficients, as

well as their level of significance. Comparisons, correlations, and regressions which generated a

p-value within the accepted range of significance (p < 0.05) were recorded as significant.

RESULTS

T
Linear elastic and viscoelastic properties of lumbar myofascial tissue at the L3-L4 level are

IP
quantified and analyzed in this study. Correlation coefficients between the five listed

CR
biomechanical properties, age, and body mass index (BMI) values in the 24 AS and 24 CN

(combined gender, sides, and times) are shown in Table 1. Similar correlational analyses are

US
shown in Table 2 for 19 AS males and 5 AS females (combined sides and times) and in Table 3 for
AN
19 CN males and 5 CN females (combined sides and times). The combined data on sides and times

reveals a significant positive correlation between the linear elastic properties of stiffness and
M

frequency in all analyses, except for the 5 female control subjects (Tables 1-3). The viscoelastic
D

properties of SRT and creep also revealed significant positive correlations among all analyses
TE

(Tables 1-3). However, significant negative correlations were found between the linear elastic
P

properties of stiffness and frequency and the viscoelastic properties of SRT and creep in total AS
CE

and CN subjects (Table 1). A positive correlation of decrement (inverse of elasticity) and stiffness

was significant in CN males and females, but not in AS (Tables 1, 2, and 3).
AC

In 24 AS subjects, stiffness and frequency had a significant negative correlation with BMI,

but not in 24 CN subjects (Table 1). Of note, decrement (inverse of elasticity) had a significant

positive correlation with age in controls and AS subjects (Table 1). Decrement also had a

significant positive correlation with BMI in AS, but not in control subjects (Table 1).

Multivariate linear regression analysis revealed that decrement was significantly predicted

Page 10 of 24
 ACCEPTED MANUSCRIPT

by age, BMI, gender, and disease duration in AS subjects (r = 0.715, p = 0.007), but not in CN

subjects (r = 0.593, p = 0.071). When age was removed from the analysis, decrement was

significantly predicted by BMI, gender, and disease duration, and the correlation was stronger for

AS subjects (r = 0.664, p = 0.008) than for CN subjects (r = 0.565, p = 0.049). The significant

independent predictor for decrement in AS was disease duration (p = 0.012) and for CN subjects

T
was BMI (p = 0.038).

IP
CR
US
AN
M
D
P TE
CE
AC

Page 11 of 24
 ACCEPTED MANUSCRIPT

T
IP
CR
US
AN
M
D
P TE
CE
AC

Page 12 of 24
 ACCEPTED MANUSCRIPT

T
IP
CR
US
AN
M
D
P TE
CE
AC

The individual properties of stiffness, frequency, decrement (inverse of elasticity), SRT,

and creep of AS patients were compared to the healthy control subjects using Mann Whitney U

analyses (Table 4). Median dynamic stiffness (linear elastic) was significantly higher (p = 0.012)

in 24 AS than in 24 CN subjects when combining gender, sides, and times (Table 4). Significantly

higher median stiffness values were observed between the 5 AS and 5 CN females (p = 0.008), but

Page 13 of 24
 ACCEPTED MANUSCRIPT

between the 19 AS and 19 CN males (p = 0.130). Correspondingly, median frequency was

significantly (p = 0.014) higher in the 5 AS females than in the 5 CN females (Table 4).

Table 4: Comparison of median property values of study subjects

Total (N=48) Males (N=38) Females (N=10)
AS CN AS CN AS CN
(N=24) (N=24) (n=19) (n=19) (n=5) (n=5)
Stiffness (N/m) 272.2† 240.2† 270.2 266.3 274.2† 194.4†

T
Frequency (Hz) 14.5 13.9 14.6 14.5 14.3† 13.0†

IP
Decrement 1.2 1.1 1.2 1.0 1.5 1.1
Stress Relaxation Time(ms) 1.2 1.1 1.1 1.1 1.4 1.3

CR
Creep 18.9 20.3 18.7 19.4 22.0 23.0
†Mann-Whitney U Test significance noted for p-values < 0.05

US
Typical acceleration graphs of an AS and CN female subject are indicated in Figures 2a
AN
and 2b respectively. Stiffness, frequency, decrement, creep and stress relaxation values are derived

from acceleration curves using Eqns. (1), (2), (3) and (4) as explained previously [22], and are
M

displayed in Figure 2. The greater stiffness in the AS patient of 274 N/m is reflected in the higher
D

acceleration peak of almost 3500 mG, as compared to stiffness of 207 N/m and acceleration peak
TE

of 2500 mG for the control subject. The other physical properties can be interpreted by the

definitions in the Methods section.

P
CE
AC

Page 14 of 24
 ACCEPTED MANUSCRIPT

T
IP
CR
US
Fig 2a: Acceleration graph of an AS female subject (34yrs) from the left side initial measurement
AN
M
D
P TE
CE
AC

Fig 2b: Acceleration graph of a CN female subject (34yrs) from the left side initial measurement

Within the CN group, female SRT values were significantly (p < 0.031) higher than CN

males’ values by times and sides and when combining times and sides (Table 5). This trend was

Page 15 of 24
 ACCEPTED MANUSCRIPT

not observed in AS subjects.

Table 5: Median (25th - 75th percentile) SRT measurements (ms) in CN males and females
Time and Side CN Males (n=19) CN Females (n=5) p
Initial (Left and Right) 19.3 (17.6-22.2) 23.1 (21.8-25.9) 0.015†
10-Min (Left and Right) 19.3 (17.9-21.9) 23.0 (21.4-25.1) 0.030†
Left (Initial and 10-Min) 19.4 (17.9-21.7) 24.2 (21.6-26.7) 0.015†
Right (Initial and 10-Min) 19.1 (17.5-21.4) 22.1 (21.6-24.4) 0.030†
†Mann-Whitney U Test significance noted for p-values < 0.05

T
IP
CR
DISCUSSION

US
The positive correlation in this study between the linear elastic parameters of dynamic

stiffness and frequency (tone) measured at rest supports the validity of using MyotonPro to study
AN
myofascial lumbar tonicity. A significant positive correlation (p = 0.000) was observed between
M

these properties in the total 48 subjects. Biomechanically, stiffness is the amount of resistance a

tissue has to deformation, and frequency is the intrinsic tension that exists in the tissue at rest.
D

This direct relationship between dynamic stiffness and frequency was also observed in a study
TE

conducted on the trapezius muscle, though the authors did not report this finding [11].
P

A positive correlation between the viscoelastic parameters of stress relaxation time (SRT)
CE

and creep was also found in this study measured at rest. The significance was strong (p = 0.000)
AC

between the viscoelastic parameters of SRT and creep in the total 48 subjects. Both parameters are

mathematically derived from the time component of the acceleration curve generated by the

MyotonPro as shown in Fig. (1) and Eqns. (3) and (4). Biomechanically, SRT is the duration for

a tissue to recover its shape after deformation. The stiffer the tissue, the shorter the SRT, since the

tissue will more quickly restore the deformation. Creep is the degree of elongation of a

viscoelastic tissue over time under a constant tensile stress. The stiffer the tissue, the less the

Page 16 of 24
 ACCEPTED MANUSCRIPT

degree of creep. Since the MyotonPro derives creep from SRT using a positive ratio, as shown in

Eq. (4), both values are positively correlated. This relationship between SRT and creep was also

observed in a study conducted on the Achilles tendon, though the authors did not report this

finding [10].

A new finding in this study has been the significant negative correlations (p = 0.000)

T
observed between the linear elastic properties (stiffness and frequency) and the viscoelastic

IP
parameters (creep and SRT) of muscle measured at rest in all 48 subjects. This negative correlation

CR
between stiffness and SRT exists because as tissue stiffness increases, a shorter time period is

required to recover the tissue’s original shape.

US
Elasticity is defined as the ability to completely recover from deformation. Decrement,
AN
measured by the MyotonPro, is inversely proportional to elasticity, as shown in Eq. (2). Hence,

an increased decrement value indicates a decreased elasticity. The correlation of decrement

M

(inverse of elasticity) with stiffness is complex due to their respective biomechanical properties
D

and the possible confounding effects of age, gender, and other subject demographic measurements.
TE

For example, a significant positive correlation was observed between stiffness and decrement
P

values within CN subjects, but the correlation was not significant in AS (Table 1). However,
CE

decrement, but not stiffness, was significantly positively correlated with age in both AS and CN
AC

subjects (Table 1).

This study newly evaluates the effects of BMI and age on the linear elastic and viscoelastic

properties of low back myofascia in AS and CN subjects. In AS subjects, the linear elastic

properties of stiffness and frequency (tone) were negatively correlated with BMI, suggesting that

increased adiposity could be damping the higher myofascial stiffness and tone in the AS group.

Age had a significant negative correlation with frequency (tone) in AS subjects, but not in healthy

Page 17 of 24
 ACCEPTED MANUSCRIPT

CN subjects. These discriminating results may indicate that the AS disease duration effects

diminished lumbar myofascial changes in association with aging.

In AS subjects, decrement values significantly increase with disease duration, indicating

decreased elasticity (Table 1). When the AS subjects’ disease duration values were assigned to the

age-ranked CN subjects of the same sex, this variable was not found to correlate with elasticity.

T
Results from multivariate linear regression analyses indicate that elasticity of the tissue is

IP
significantly predicted by age, BMI, gender, and disease duration in AS subjects. When age was

CR
removed from the analyses, it was observed that the significant independent predictor for

decrement in AS was disease duration (p = 0.012). For CN subjects, the independent predictor was

BMI (p = 0.038).
US
AN
The significantly higher (p = 0.012) dynamic stiffness values of the total AS versus CN

groups (Table 4) were previously hypothesized as AS patients having increased resting muscle
M

tone as a genetic variant [2]. As the disease progresses, AS patients have muscle atrophy and
D

increased fibrous tissue replacement which may also decrease elasticity [2].
TE

This study also indicates the effects of gender on the viscoelastic properties of SRT of the
P

myofascia. In CN, female SRT values were significantly (p < 0.031) higher than male values
CE

(Table 5), but this trend was not observed in AS subjects. These results are consistent with the CN

female subjects having lower stiffness values than the CN males.

AC

A primary limitation of this study is the modest overall sample size. A total of 24 AS and

24 CN subjects were recruited, but only 5 female participants were included in each group.

Secondly, the MyotonPro can apply impulses only to superficial myofacial tissue (within 2 cm).

Further studies with advanced shear wave ultrasound elastography techniques that can quantify the

shear modulus properties of tissue at precise locations and varying depths may aid in supporting

Page 18 of 24
 ACCEPTED MANUSCRIPT

the hypothesis of AS subjects having altered myofacial properties compared to healthy control

subjects. Alteration of biomechanical properties of the low back myofascia may also be present in

non-AS patients such as subjects having low back pain (LBP). Our ongoing and future studies will

include nonspecific LBP patients to quantify and characterize their changes.

T
CONCLUSIONS

IP
This novel study quantifies and analyzes the linear elastic and viscoelastic properties of the

CR
L3-L4 myofascia in AS and healthy subjects. Multivariate linear regression analysis revealed that

disease duration in AS independently associated with decreased tissue elasticity (decrement). In

US
healthy subjects, BMI independently associated with decreased elasticity. The results in AS
AN
suggest that the disease has an increasing effect on tissue elasticity over time. Significant positive

correlations were found between the two linear elastic parameters of dynamic stiffness and
M

frequency. Also, the two viscoelastic parameters of SRT and creep were positively correlated,
D

which support trends in existing literature. The validity of the MyotonPro’s usage in
TE

biomechanical characterization of low back myofascia was supported in this study. Significant
P

negative correlations between the linear elastic and the viscoelastic parameters were comparable
CE

among both CN and AS subjects. Those data suggest underlying inverse relations between the

linear elastic and viscoelastic parameters which are not specifically altered by the AS disease.
AC

These preliminary results suggest that with continued disease duration the biomechanical

properties of elasticity and stiffness are altered in AS subjects. Preliminary data from this study

promise a better understanding of the interrelation of these five properties in AS patients versus

normal subjects. Future studies can recruit additional subjects to evaluate these preliminary

results. Shear wave elastography (SWE) can also quantify tissue properties and may be used to

Page 19 of 24
 ACCEPTED MANUSCRIPT

further test this study.

ACKNOWLEDGEMENTS

The authors would like to acknowledge funding from the NASA Illinois Space Grant Consortium,

the Office of Sponsored Programs at Bradley University, and the University of Illinois College of

T
Medicine at Peoria. We would also like thank Dr. Jean Aldag for providing her expertise in all

IP
statistical analyses and Dr. Sadia Ilahi for proof reading our manuscript.

CR
US
AN
M
D
P TE
CE
AC

Page 20 of 24
 ACCEPTED MANUSCRIPT

REFERENCES

[1] Nair K, Masi AT, Andonian BJ, et.al. Stiffness of resting lumbar myofascial in healthy young
subjects quantified using a handheld myotonometer and concurrently with surface
electromyography monitoring. Journal of Bodywork and Movement Therapies. 2016;
20(2):388-396. DOI: 10.1016/j.jbmt.2015.12.005

[2] Andonian BJ, Masi AT, Aldag JC, et.al. Greater resting lumbar extensor myofascial stiffness in
younger ankylosing spondylitis patients than age-comparable healthy volunteers quantified

T
by myotonometry. Archives of Physical Medicine and Rehabilitation. 2015; 96(11):2041-

IP
2047. DOI: 10.1016/j.apmr.2015.07.014

[3] Alev K, Vain A, Aru M, et.al. Glucocorticoid-induced changes in rat skeletal muscle

CR
biomechanical and viscoelastic properties: aspects of aging. Journal of Manipulative &
Physiological Therapeutics. 2018; 41(1):19-24. DOI: 10.1016/j.jmpt.2017.06.009

US
[4] Sanchez-Zuriaga D, Adams MA and Dolan P. Is activation of the back muscles impaired by
creep or muscle fatigue? Spine 2010; 35(5):517-525. DOI:
10.1097/BRS.0b013e3181b967ea
AN
[5] McHugh MP, Magnusson SP, Gleim GW, et. al. Viscoelastic stress relaxation in human
skeletal muscle. Medicine and Science in Sports and Exercise. 1992; 24(12):1375-1382.
M

[6] Delaine-Smith RM, Burney S, Balkwill Fr, et.al. Experimental validation of a flat punch
indentation methodology calibrated against unconfined compression tests for determination
D

of soft tissue biomechanics. Journal of the Mechanical Behavior of Biomedical Materials.

TE

2016; 60:401-415. DOI: 10.1016/j.jmbbm.2016.02.019

[7] Panda SK, Buist ML. A finite nonlinear hyper-viscoelastic model for soft biological tissues.
P

Journal of Biomechanics. 2018; 69:121-128. DOI: 10.1016/j.jbiomech.2018.01.025

CE

[8] Ates F, Hug F, Bouillard K, et.al. Muscle shear elastic modulus is linearly related to muscle
torque over the entire range of isometric contraction intensity. Journal of
Electromyography and Kinesiology. 2015; 25(4):703-708. DOI:
AC

10.1016/j.jelekin.2015.02.005

[9] Rapson R, Marsden J. Intra-rater reliability of clinical measures of leg function in typically
developing children aged 1-4 years. Association of Paediatric Chartered Physiotherapists.
2016; 7(1):14-22.

[10] Schneider S, Peipsi A, Stokes M, et. al. Feasibility of monitoring muscle health in
microgravity environments using Myoton technology. Medical & Biological Engineeering
& Computing. 2015; 53(1):57-66. DOI: 10.1007/s11517-014-1211-5
[11] Viir R, Virkus A, Laiho K, et. al. Trapezius muscle tone and viscoelastic properties in sitting

Page 21 of 24
 ACCEPTED MANUSCRIPT

and supine positions. Scandinavian Journal of Work, Environment, & Health. 2007;
suppl.(3):76-80.

[12] Bizzini M, Mannion AF. Reliability of a new, handheld device for assessing skeletal muscle
stiffness. Clinical Biomechanics. 2003; 18(5):459-461.

[13] Zinder SM, Padua DA. Reliability, validity, and precision of a handheld myometer for
assessing in vivo muscle stiffness. Journal of Sport Rehabilitation. 2011.
DOI: 10.1123/jsr.2010-0051

T
[14] Ditroilo M, Hunter AM, Haslam S, et. al. The effectiveness of two novel techniques in

IP
establishing the mechanical and contractile responses of biceps femoris. Physiological
Measurement. 2011; 32(8):1315-1326. DOI: 10.1088/0967-3334/32/8/020

CR
[15] Marusiak J, Jaskolska A, Koszewicz M, et. al. Myometry revealed medication-induced
decrease in resting skeletal muscle stiffness in Parkinson’s disease patients. Clinical

US
Biomechanics. 2012; 27(6):632-635. DOI: 10.1016/j.clinbiomech.2012.02.001
[16] Chuang LL, Wu CY, Lin KC, et. al. Quantitative mechanical properties of the relaxed biceps
and triceps brachii muscles in patients with subacute stroke: a reliability study of the
AN
Myoton-3 Myometer. Stroke Research and Treatment. 2012; 2012/617694. DOI:
10.1155/2012/617694
M

[17] Aird L, Samuel D, Stokes M. Quadriceps muscle tone, elasticity and stiffness in older males:
reliability and symmetry using the MyotonPRO. Archives of Gerontology and Geriatrics.
D

2012; 55(2):e31-e39. DOI: 10.1016/j.archger.2012.03.005

TE

[18] Bailey L, Samuel D, Warner MB, et. al. Parameters representing muscle tone, elasticity and
stiffness of biceps brachii in healthy older males: symmetry and within-session reliability
using the MyotonPRO. Journal of Neurological Disorders. 2013; 1(1):1-7.
P
CE

[19] Mullix J, Warner M, Stokes M. Testing muscle tone and mechanical properties of rectus
femoris and biceps femoris using a novel handheld MyotonPRO device: relative ratios and
reliability. Working Papers in Health Sciences. 2012; 1(1):1-8.
AC

[20] Liu CL, Feng YN, Zhang HQ, et. al. Assessing the viscoelastic properties of upper trapezius
muscle: intra-and inter-tester reliability and the effect of shoulder elevation. Journal of
Electromyography and Kinesiology. 2017. DOI: 10.1016/j.jelekin.2017.09.007

[21] Lo WLA, Zhao JL, Chen L, et. al. Between-days intra-rater reliability with a handheld
myotonometer to quantify muscle tone in the acute stroke population. Scientific Reports.
2017; 7(1):14173. DOI: 10.1038/s41598-017-14107-3
[22] MyotonPRO website: http://www.myoton.com/technology/ accessed on February 28, 2018.
[23] Coates B, Barry A, Dougherty J, et. al. Quantifying intrinsic properties of resting lumbar

Page 22 of 24
 ACCEPTED MANUSCRIPT

muscle in healthy subjects using a handheld myometer. Proceedings of the IEEE Annual
Northeast Bioengineering Conference, NEBEC. Institute of Electrical and Electronics
Engineers, Inc. 2014; December, 6972760. DOI: 10.1109/NEBEC.2014.6972760

[24] Thought Technology. ProComp InfinitiTM Hardware Manual, 2003. Retrieved May 15, 2011
from: http://www.thoughttechnology.com/pdf/manuals/SA7510%20Rev%206.pdf.

T
IP
CR
US
AN
M
D
P TE
CE
AC

Page 23 of 24
 ACCEPTED MANUSCRIPT

Highlights

Rationale and Core Findings

 Limited studies exist in the area of human resting muscle tone and its effects

 The role of muscle properties in ankylosing spondylitis has not been studied

T
 Few studies relate BMI, age, disease duration with muscle biomechanical properties

IP
 Disease duration alters low back elasticity and stiffness in ankylosing spondylitis

CR
 Relations between linear elastic and viscoelastic properties not altered by disease

US
AN
M
D
P TE
CE
AC

Page 24 of 24