超声弹性成像测量正常大鼠肝脏的粘弹性：与振荡流变法比较资源-CSDN文库

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UNCORRECTED PROOF

Biorheology 00 (20xx) 1–15 1

DOI 10.3233/BIR-16091

IOS Press

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Viscoelastic properties of normal rat liver

measured by ultrasound elastography:

Comparison with oscillatory rheometry

Haoming Lin

a,b,c,∗

, Yuanyuan Shen

a,b,c,∗

,XinChen

a,b,c,∗∗

,YingZhu

, Yi Zheng

Xinyu Zhang

a,b,c

, Yanrong Guo

,TianfuWang

a,b,c

and Siping Chen

a,b,c

School of Biomedical Engineering, Shenzhen University, Shenzhen, China

National-Regional Key Technology Engineering Laboratory for Medical Ultrasound, Shenzhen,

China

Guangdong Key Laboratory for Biomedical Measurements and Ultrasound Imaging, Shenzhen, China

Department of Electrical and Computer Engineering, St. Cloud State University, St. Cloud, MN,

56301, USA

Received 1 January 2016

Accepted 31 October 2016

Abstract.

BACKGROUND: Ultrasound elastography has been widely used to measure liver stiffness. However, the accuracy of liver

viscoelasticity obtained by ultrasound elastography has not been well established.

OBJECTIVE: To assess the accuracy of ultrasound elastography for measuring liver viscoelasticity and compare to conven-

tional rheometry methods. In addition, to determine if combining these two methods could delineate the rheological behavior

of liver over a wide range of frequencies.

METHODS: The phase velocities of shear waves were measured in livers over a frequency range from 100 to 400 Hz using

the ultrasound elastography method of shearwave dispersion ultrasound vibrometry (SDUV), while the complex shear moduli

were obtained by rheometry over a frequency range of 1 to 30 Hz. Three rheological models, Maxwell, Voigt, and Zener, were

ﬁt to the measured data obtained from the two separate methods and from the combination of the two methods.

RESULTS: The elasticity measured by SDUV was in good agreement with that of rheometry. However, the viscosity measured

by SDUV was signiﬁcantly different from that of rheometry.

CONCLUSIONS: The results indicate that the high frequency components of the dispersive data play a much more important

role in determining the dispersive pattern or the viscous value than the low frequency components. It was found that the Maxwell

model is not as appropriate as the Voigt and Zener models for describing the rheological behavior of liver.

Keywords: Viscoelasticity, liver, elastography, rheometry, dispersion, shearwave dispersion ultrasound vibrometry

These authors contributed equally.

Address for correspondence: Xin Chen, School of Biomedical Engineering, Shenzhen University, Shenzhen, China.

Fax: +86-755-86671920; E-mail: chenxin@szu.edu.cn.

[research-article] p. 1/15

UNCORRECTED PROOF

2 H. Lin et al. / Viscoelastic properties of normal rat liver measured by ultrasound elastography

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1. Introduction

Elastography is an emerging branch of medical imaging for noninvasively quantifying the biomechan-

ical properties of soft biological tissues [1]. A number of elastography techniques, primarily based on

a variety of imaging modalities such as ultrasound, magnetic resonance imaging (MRI), and optical co-

herence tomography (OCT), have been developed over the past two decades [1]. Because ultrasound has

unique advantages such as being noninvasive, applicable to real time imaging and ease of accessibil-

ity, elastography based on this modality has attracted considerable attention. A diversity of ultrasound

elastography methods have been proposed, including quasi-static elastography [2], transient elastogra-

phy (TE) [3], sonoelastography [4], acoustic radiation force impulse imaging (ARFI) [5], shear wave

elasticity imaging (SWEI) [6], supersonic shear imaging (SSI) [7], harmonic motion imaging [8], shear

wave induced resonance elastography (SWIRE) [9], vibro-elastography [10] and shearwave dispersion

ultrasound vibrometry (SDUV) [11]. Some of these have been integrated into commercial ultrasound

systems and have been widely applied in clinical applications [12,13].

Elastography has been applied to measure the mechanical properties of various human tissues and or-

gans, including muscle, breast, brain, liver, etc. [12,14]. Assessment of liver status is one of the most suc-

cessful applications of elastography and is becoming a common application in clinical practice [15,16].

Studies using ultrasound elastography demonstrated that the mechanical properties of liver have signif-

icant correlations with diseases such as ﬁbrosis [17–19] and non-alcoholic fatty liver disease (NAFLD)

[20,21]. Most studies applying elastography to liver assessment used a linear elastic model that contains

only elasticity. However, living liver contains ﬂuid and, thus, naturally exhibits both elastic and viscous

(i.e. rheological) behavior. Hence, a viscoelastic description of the mechanical behavior of liver is more

accurate and physically correct than a linear elastic one. Furthermore, the viscosity, as well as the elas-

ticity, can provide useful information about liver status [21]. Several ultrasound elastography methods

have been developed to measure the viscoelastic properties of soft tissues [8,11,22,23], and a few of them

were applied to the assessment of liver [18,19,21]. These methods have usually been applied in a multi-

frequency approach to measure the dispersive shear-wave properties. Some representative frequencies

were 95–380 Hz [18], 60–600 Hz [19], and 100–400 Hz [21],

The ultrasound elastography methods that measure the viscoelastic properties of tissues usually in-

volve ﬁtting the dispersive shear-wave velocity and attenuation coefﬁcients to a rheological model [24].

Several models, including Voigt [18], Maxwell [25], and Zener [26]

models have been applied to the as-

sessment of liver properties. However, most of the studies assumed a speciﬁc model in advance and did

not investigate the issue of model selection. A few preliminary studies, however, investigated different

rheological models for liver characterization. For instance, ultrasound elastography was used to measure

the propagation velocity of shear waves in porcine liver and evaluated the performance of three models,

Voigt, Maxwell, and Zener, in ﬁtting the measured shear wave velocity [25,27]. Nevertheless, insofar as

we are aware, no general agreement has been reached as to which model is the most appropriate for the

application of ultrasound elastography to liver.

Conventional methods for investigating the biomechanical properties of soft tissue include rheological

tests such as dynamic mechanical analysis (DMA) and oscillatory rheometry. Some studies have com-

pared elastography techniques with these conventional methods for assessing the viscoelastic properties

of biological tissue. For example, Chatelin et al. [28] measured the shear modulus of liver by both tran-

sient elastography (TE) (50 Hz) and dynamic mechanical analysis (DMA) (0.1–4 Hz) and studied the

inﬂuence of the test conditions on the liver viscoelastic properties. Klatt et al. [29] investigated bovine

liver specimens by oscillatory rheometry and multi-frequency magnetic resonance elastography (MRE)

[research-article] p. 2/15

UNCORRECTED PROOF

H. Lin et al. / Viscoelastic properties of normal rat liver measured by ultrasound elastography 3

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in a common frequency range between 25.0 and 62.5 Hz and validates MRE as a method for investi-

gating the rheology of liver tissue. Bernal et al. [30] used SSI (20–400 Hz) to measure the viscoelastic

properties of blood clots and carried out classical rheometry experiments (0.25–25 Hz) on the same

blood samples taken within the ﬁrst few seconds of coagulation. A similar work was conducted earlier

by Schmitt et al. to characterize blood clot viscoelasticity by dynamic ultrasound elastography [31].

The studies mentioned above showed that elasticity measured by elastography was in good agreement

with that measured by rheological tests. However, few studies have tried to validate the viscosity ob-

tained by elastography. Speciﬁcally, elastography and rheological tests usually use different frequency

bands that typically range from 100 to 600 Hz for elastography and 0 to 50 Hz for rheometry. This raises

the question of the effect of frequency on the viscoelastic results as measured by the two methods. More

importantly, with complementary frequency ranges, would the two methods provide mutual information

about the rheological behavior of the tissue, and better characterize its elastic and viscous components,

compared with a single method? Addressing these questions could considerably advance the develop-

ment and application of ultrasound elastography and, consequently, contribute to better understanding

of the rheological behavior of the tissue.

The present study used an ultrasound elastography method called shearwave dispersion ultrasound

vibrometry (SDUV) and classic rheometry test to measure the shear viscoelastic modulus of rat liver.

Because the frequency ranges of the two methods were different, we could not directly compare the

results of the two methods. Instead, the dispersive data from the two methods were combined to assess

the viscoelastic properties of liver in a reasonable way. The goal was twofold. First, we aimed to demon-

strate the validity of SDUV for quantitatively measuring liver viscoelasticity by correlating it with the

conventional rheometric techniques. Second, we combined the dispersive data from both methods to

explore the rheological behavior of liver over a broader frequency range.

2. Methods

2.1. Theory

Rheological tests measure the dynamic mechanical behavior of biological tissues. A sinusoidal shear

strain ε(t) = ε

iωt

is imposed on the tissue to induce a sinusoidal shear stress σ(t) = σ

i(ωt+δ)

.The

ratio of stress to strain is represented as the complex shear modulus [32]:

G(ω) =

i(ωt+δ)

iωt

(cos δ + i sin δ) = G



(ω) + iG



(ω), (1)

where ε

is the shear strain amplitude, σ

is the shear stress amplitude, ω is the angular frequency, δ is

the phased-shifted angle, and G



and G



are the storage modulus and loss modulus, respectively. The

complex modulus can be related to elasticity and viscosity by different rheological models. In this study,

we used the following rheological models (Fig. 1), which consist of different combinations of a spring

and a dashpot.

The relationship between the complex modulus and the viscoelastic parameters are as follows [33]:

G(ω) = G



+ iG



⎧

⎪

⎨

⎪

⎩

μη

+ω

+ i

ηω

+ω

Maxwell,

μ + iηω Vo i g t ,

+ω

(μ

+μ

)

+ω

+ i

ηω

+ω

Zener,

(2)

[research-article] p. 3/15

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