Updated 11/18/2011
Abdominal Publications
Updated 11/18/2011
Abdominal Publications
Shear wave elastography of adrenal masses
Poster No.:
ECR 2011
Scientific Paper
R. Z. Slapa , A. A. Kasperlik-Zaluska , W. Jakubowski , A.
1 1
Piwowonski , T. Bednarczuk , K. T. Szopinski ; Warsaw/PL,
Adrenals, Elastography, Technology assessment, Tissue
characterisation, Endocrine disorders
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Abdominal Publications
The estimation of tissue hardness is a very ancient diagnostic tool in medicine. Palpation
- the earliest and most common form of tissue hardness estimation - was practiced by
Egyptian physicians as early as 2600 BCE [1].
In the era of advancement of ultrasound diagnostics there have been developed a method
called sonopalpation which involved monitoring of palpation with B-mode ultrasound.
A more recent and sophisticated method of imaging tissue hardness is technique known
as elastography. Roughly 20 years have elapsed since the production of the first
images depicting the local elastic properties of tissues. The first decade of development
produced a remarkable proliferation of techniques and optimization strategies. The
second decade continued this trend, but with the important extension to dedicated
platforms for conducting clinical trials in the hands of radiologists and skilled clinicians [2].
There are 3 main types of US elasticity imaging: elastography that tracks tissue
movement during compression to obtain an estimate of strain, sonoelastography that
uses color Doppler to generate an image of tissue movement in response to external
vibrations and tracking shear wave propagation through tissue to obtain the elastic
modulus [1].
The new generation of elasticity imaging called supersonic shear wave imaging has
already been introduced to imaging of superficial organs as breast and thyroid with high
frequency linear probes [3-5] (fig 1). This type of elastography does not require the
compression of the tissues during their elasticity examination and may be applied with
lower frequency convex probes for examination of deep laying organs and tissues in
abdominal cavity and retroperitoneum.
The aim of our study was to evaluate the feasibility of assessment of elasticity of adrenal
masses with supersonic shear wave elastography.
Images for this section:
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Abdominal Publications
Fig. 1: Shear wave elastography of the breast phantom. Hard inclusion in the phantom is
visible in color on elastographic image (uper image). Hardness of the object (circle ROI)
is measured in kPa. Hardness of the object can be also related to hardness of surounding
structures (dotted circle ROI) with ratio calculation. The lower image presents B-mode
presentation of the phantom.
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Abdominal Publications
Methods and Materials
We evaluated with ultrasound 14 consecutive patients with adrenal masses . The B
mode ultrasound revealed 16 adrenal masses that were examined with shear wave
elastography quantitatively, with Aixplorer ultrasound scanner (Supersonic, France) with
convex abdominal transducer. The final diagnosis was based on multiple CT or MRI and
biochemical studies.
Final diagnosis established: 1 myelolipoma, 7 hyperplastic nodules, 5
adenomas, 3 cysts.
In 1 patient with small left adrenal nodule ultrasound did not show the lesion.
All the solid lesions showed the elasticity map and measurements of their
hardness in kPa were possible.
Myelolipoma (fig 1) was harder than adenomas (fig 2) and hyperplastic
The cysts (fig 3) (some not obvious on B-mode imaging) did not show
elasticity signal, as shear waves do not propagate through liquids.
Images for this section:
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Abdominal Publications
Fig. 1: Myelolipoma of the left adrenal gland (arrows). LK - left kidney. On the upper
elastographic image myelolipoma is harder (circa 40 kPa) then adenoma (next figure).
On B-mode presentation (lower image) myelolipoma is distinctively hyperechoic.
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Abdominal Publications
Fig. 2: Non-hyperfunctioning adenoma (incidentaloma) of the right adrenal gland
(arrows). RK - right kidney. Liv - liver. On the elastographic image (upper) the
measurements of adenoma hardness (circa 25 kPa) and hardness of liver and kidney
parenchyma are marked with circle ROIs. The respective ratios of the hardness are also
calculated. On B-mode presentation (lower image) adrenal adenoma is isoechoic to liver.
Page 6 of 9
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Abdominal Publications
Fig. 3: Large reccurent cyst of the right adrenal gland with elasticity imaging (upper
image) and B-mode presentation (lower image). Main part of the cyst does not show
elasticity signal as shear waves do not propagate through liquids. Discrete dense material
within the upper pole of the cyst shows some signal of elastic structure.
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Abdominal Publications
Shear wave elastography with convex ultrasound probe is a feasible
technique for evaluation of adrenal masses.
Shear wave elastography shows the potential for differentiation of adrenal
Shear wave elastography indicates the liquid content of adrenal cystic
lesions, even these that do not present simple cyst features on B-mode
Further large scale studies evaluating the possibility of differentiation of
adrenal masses with shear wave elastography are warranted.
Garra BS: Imaging and estimation of tissue elasticity by ultrasound.
Ultrasound Quarterly 2007; 23: 255-268.
Parker KJ, Doyley MM, Rubens DJ: Imaging the elastic properties of tissue:
the 20 year perspective. Phys. Med. Biol. 2011; 56: R1-R29.
Tanter M, Bercoff J, Athanasiou A, Deffieux T, Gennisson J-L, Montaldo
G, Muller M, Tardivon A, Fink M: Quantitative assessment of breast lesion
viscoelasticity: Initial clinical results using supersonic shear imaging.
Ultrasound in Med. & Biol. 2008; 34: 1373-1386
Sebag F, Vaillant-Lombard J, Berbis J, Griset V, Henry JF, Petit P, Olivier
C: Shear wave elastography: a new ultrasound imaging mode for the
differential diagnosis of benign and malignant thyroid nodules. J Clin
Endocrinol Metab. 2010; 95: 5281-8.
Evans A, Whelehan P, Tomson K, McLean D, Brauer K, Purdie C, Jordan
L, Baker L, Thompson A: Quantitative shear wave ultrasound elastography:
initial experience in solid breast masses. Breast Cancer Research 2010;
Personal Information
Supported by the Ministry of Science and Higher Education
of Poland grant Nr N N402 481239 in years 2010-2013.
Corresponding author: Rafal Zenon Slapa
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Abdominal Publications
E-mail: [email protected]
Department of Diagnostic Imaging, Second Faculty of Medicine with the English Division
and the Physiotherapy Division, Medical University of Warsaw, ul. Kondratowicza 8,
03-242 Warsaw, Poland (RZS, WJ, KTS)
Department of Endocrinology, Centre for Posgraduate Medical Education, Warsaw,
Poland (AAK-Z)
NZOZ Almed, Jaroslaw, Poland (AP)
Department and Clinic of Internal Medicine and Endocrinology, First Faculty of Medicine,
Medical University of Warsaw, Warsaw, Poland (TB)
Interdisciplinary Centre for Mathematical and Computational Modelling, Warsaw
University, Warsaw, Poland (KTS)
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Shear Wave and Strain Elastography in Ultrasound Diagnosis of Thyroid Cancer
Slapa R,1* Jakubowski W,1 Piwowonski A,2,3 Bierca J,4 Szopinski K1,5 1Diagnostic Imaging, Medical University of Warsaw, Faculty of Medicine II, English Division, Physiotherapy Division,
Warsaw, Poland; 2Niepublicznych Zakladów Opieki Zdrowotnej
Almed, Jaroslaw, Poland; 3Samodzielny Publiczny Zaklad Opieki
Zdrowotnej, Przeworsk, Poland; 4Surgery, Solec Hospital, Warsaw, Poland; 5Interdisciplinary Center for Mathematical and
Computational Modeling, University of Warsaw, Warsaw, Poland
Objective. From a clinical background, hard nodules on palpation are more suspicious for thyroid cancer. So far, various variants of
ultrasound elastography have been developed: strain (correlation method
or tissue Doppler) and shear wave elastography. Ultrasound elastography,
as more precise and objective than palpation, should help indicate nodules for fine-needle aspiration (FNA). The purpose of this study was to
compare the usefulness of shear wave and strain elastography for evaluation of thyroid nodules.
Methods. With ultrasound, we evaluated 4 consecutive patients
with a single thyroid nodule (1) and nodular goiter (3). B-mode and power
Doppler ultrasound of the whole thyroid and neck lymph nodes was performed. Six dominant nodules (with regard to ultrasound features) were
evaluated with shear wave and strain elastography (tissue Doppler based)
qualitatively and quantitatively and with ultrasound using the contrast
agent SonoVue (Bracco) with following scanners: Aixplorer (Supersonic),
Aplio XG (Toshiba), and Technos (Esaote) with linear high-resolution
transducers. The final diagnosis was based on clinical evaluation, multiple FNA, or surgery.
Results. Final diagnoses established included 1 papillary carcinoma, 4 coloid nodules, and a benign nodule. Shear weave elastography
revealed 1 true-positive, 4 true-negative, and 1 false-positive diagnoses
with regard to thyroid cancer. Strain elastography revealed 5 false-positive
and 1 false-negative diagnoses. False-positive diagnoses with strain elastography were found in nodules with partly liquid content or necrosis visible on contrast-enhanced ultrasound or inferred from B-mode ultrasound.
Conclusions. (1) Shear wave elastography did better than strain
elastography in characterization of thyroid nodules, whether suspicious
for cancer or not. (2) False-positives on strain ultrasound were due to liquid or necrotic content in the nodules. (3) Further multicenter large-scale
studies of thyroid nodules evaluating different elastographic methods are
warranted. (Supported by grant N402 476437.)
Estimate of Effective Scatterer Diameter and Acoustic Concentration in Ultrasound Examination of the Cervix in
Pregnant Women as Predictors of Premature Delivery
Bigelow T,1* McFarlin B,2 Labyed Y,1 Abramowicz J3 1Electrical and Computer Engineering, Iowa State University, Ames,
Iowa USA; 2Women, Children, and Family Health Science, University of Illinois, Chicago, Illinois USA; 3Obstetrics and Gynecology, Rush University Medical Center, Chicago, Illinois
Objective. The cervix prepares for the delivery weeks to
months before labor by a process termed cervical ripening without any
signs or symptoms currently detectable noninvasively. As the cervix
ripens, the spacing between the collagen fibers increases and fills with
water, hyaluronan, decorin, and enzymes, suggesting that the ultrasound
scattering properties of the cervix should change. The objective of this
study was to assess the effective scatterer diameter and acoustic concentration as a function of the time to delivery to see if monitoring these quantitative ultrasound parameters could predict premature delivery.
Methods. A convenience sample of 33 pregnant women consented to a transvaginal scan of the cervix using a 5- to 9-MHz transducer
at a single time point during their pregnancy. Ultrasound radio frequency
data and corresponding beam-formed images were obtained with a
(Zonare) commercial ultrasound system. Then, the cervix attenuation was
estimated by comparing the echoes to the echoes from a tissue-mimicking phantom with known attenuation and scattering properties. Multiple attenuation estimates were obtained for regions throughout the cervix and
then averaged to get a single attenuation estimate for the entire cervix. The
attenuation estimate and echoes from the tissue-mimicking phantom were
then used to estimate the effective scatterer diameter and acoustic concentration for the cervix.
Results. The time from the ultrasound exam to delivery for the
patients varied from 0 to 29 weeks with a mean time to delivery of 16
weeks. There was a statistically significant decrease in attenuation (P <
.02), increase in effective scatterer diameter (P < .01), and decrease in
acoustic concentration (P < .025) as the delivery date approached.
Conclusions. The study validates the feasibility of using quantitative ultrasound parameters such as attenuation, effective scatterer diameter, and acoustic concentration to assess cervical ripening. In the
future, the goal will be to reduce some of the variability in the data by longitudinal studies and further improvement to the quantitative ultrasound algorithms.
Shear Wave Elastography During Sonography of Adrenal
and Liver Masses: Feasibility Study
Slapa R,1* Kasperlik-Zaluska A,2 Jakubowski W,1 Piwowonski A,3,4 Bednarczuk T,5 Szopinski K1,6 1Diagnostic Imaging,
Medical University of Warsaw, Faculty of Medicine II, English
Division, Physiotherapy Division, Warsaw, Poland; 2Endocrinology, Center for Postgraduate Medical Education, Warsaw, Poland; 3Niepublicznych Zakladów Opieki Zdrowotnej
Almed, Jaroslaw, Poland; 4Samodzielny Publiczny Zaklad
Opieki Zdrowotnej, Przeworsk, Poland; 5Internal Medicine and
Endocrinology, Medical University of Warsaw, Faculty of Medicine II, Warsaw, Poland; 6Interdisciplinary Center for Mathematical and Computational Modeling, University of Warsaw,
Warsaw, Poland
Objective. The elasticity of abdominal masses depends on their
composition (eg, amount of vascularity, fibrosis, necrosis, lipids, or fluid).
The purpose of this study was to evaluate the feasibility of assessment of
the elasticity of adrenal and liver masses with shear wave elastography
performed during ultrasound examination.
Methods. With ultrasound, we evaluated 16 consecutive patients with adrenal and/or liver masses. B-mode ultrasound revealed 16
adrenal masses that were examined with shear wave elastography quantitatively with an Aixplorer (Supersonic) and a convex abdominal transducer. Five liver masses (3 single and 2 dominant) were similarly
evaluated with shear wave elastography. The final diagnosis was based
on contrast-enhanced ultrasound, computed tomography, magnetic resonance imaging, follow-up, and biochemical studies.
Results. Final diagnoses of adrenal lesions established included
1 myelolipoma, 7 hyperplastic nodules, 5 adenomas, and 3 cysts. In 1 patient with a small left adrenal nodule, ultrasound did not show the lesion.
Final diagnoses of liver lesions established included 2 metastases (from
breast and adrenal cortex cancer), 1 focal nodular hyperplasia, 1 hemangioma, and 1 benign lesion. All the solid adrenal lesions showed an elasticity map. Adrenal myelolipoma was harder than adenomas and
hyperplastic nodules. The adrenal cysts (some not obvious on B-mode imaging) did not show an elasticity signal, as shear waves do not propagate
through liquids. Liver hemangioma was hard. Brest cancer metastasis was
partly hard and partly elastic. Other liver lesions were elastic.
Conclusions. (1) Shear wave elastography with an abdominal
convex ultrasound probe is a feasible technique that can be performed during ultrasound evaluation of adrenal and liver masses. (2) Shear wave elastography shows some potential for differential characterization of adrenal
and liver masses. (3) Shear wave elastography indicates the liquid con-
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American Institute of Ultrasound in Medicine Proceedings
J Ultrasound Med 30:S1–S120, April 2011
tent of adrenal cystic lesions, even those that do not present simple cyst
features on B-mode ultrasound. (4) Further large-scale studies evaluating
the possibility of differentiation of abdominal masses with shear wave
elastography are warranted. (Supported by grant N402 481239.)
Moderators: Liz Ladrido, RDMS, and
Tricia Turner, RDMS
Potential of Ultrasound Elasticity Measurements of the
Brachial Artery for Determining Arteriovenous Fistula
Sorace A,1* Hoyt K,1,2 Abts C,2 Robbin M,1,2 Lockhart M,2
Allon M3 1Biomedical Engineering, 2Radiology, 3Medicine,
University of Alabama, Birmingham, Alabama USA
Objective. To use ultrasound (US) to noninvasively measure
the elasticity of human brachial arteries and assess potential in determining the likelihood of arteriovenous (AV) fistula maturation in chronic kidney disease (CKD) patients.
Methods. US cine data were collected in the brachial artery of
both normal and potential AV fistula patients using a Philips iU22 scanner with an L17-5 transducer. The forearm was placed in a custom rest to
minimize any discomfort or patient motion. Simultaneous electrocardiographic (EKG) recordings of 10 cardiac cycles of US data were acquired.
Arterial Health prototype software (Siemens) was used to determine the
intima-media thickness (IMT) of the arterial wall during systole and diastole. Patient EKG data helped determine these extreme states of vessel
distension and contraction. Assuming a linear elastic medium, the modulus of elasticity for the vessel wall was estimated as the ratio of vascular
stress to strain. More specifically, stress was taken as the difference between systolic and diastolic pressure measurements. Tissue strain was derived from changes in IMT measurements (between systole and diastole)
and averaged over 6 different cardiac cycles.
Results. Preliminary results in normal healthy (non-CKD) patients were used to establish a database for comparison to patients scheduled for AV fistula surgical placement. Fistulas are tracked to either
maturation or failure on follow-up clinical examinations, and a comprehensive database is being compiled. To date, normal patient brachial artery
elasticity measurements were found to be 70.3 ± 8.8 kPa. The low SE
demonstrates feasibility and indicates low variability in healthy brachial artery elasticity. In comparison, CKD patient elasticity exhibits striations in
data, showing clusters near normal (78.1 kPa) and much stiffer (150.4
kPa). It is hypothesized that maturation outcomes will correlate with elasticity values. Comparison to AV fistula outcomes and histologic measures
of vascular fibrosis are pending.
Conclusions. US can be used to noninvasively measure the
elasticity of the brachial artery in human. A comprehensive database of
vascular elasticity measurements has great potential in helping determine
whether CKD patients will have complete AV fistula maturation.
Results. Thrombi were isolated to the common femoral vein
or femoral vein in 23.2% of extremities. Contiguous thrombi isolated to
the combination of the common femoral vein and femoral vein were present in 11.8% of extremities. In total, 35% of extremities with DVT did not
have thrombus located within the popliteal vein.
Conclusions. The conventional wisdom that lower extremity
thrombi begin in the calves and propagate centrally may not be correct in
a not-insignificant number of cases.
Transcranial Doppler Sonography to Evaluate Neurovascular Changes in Acute Blunt Cervical Vascular Injury
Purvis D,1* Aldaghlas T,3 Rizzo A,3 Sikdar S2 1Neuroscience,
Electrical and Computer Engineering, George Mason University, Fairfax, Virginia USA; 3Trauma Services, Inova Fairfax Hospital, Fairfax, Virginia USA
Objective. Complications of undetected blunt cervical vascular injury (BCVI) can lead to adverse neurologic sequelae. Screening for
BCVI with computed tomographic angiography (CTA) is more common
than conventional angiography. CTA is a validated screening modality;
the diagnosis remains imperfect due to high false-positive rates. Doppler
sonography has demonstrated high specificity in detecting vascular injuries. We are investigating bedside use of transcranial Doppler (TCD)
sonography during initial assessment and evaluation of BCVI in severely
injured trauma patients.
Methods. This is a prospective pilot study conducted at a large
level I trauma center. Patients enrolled were screened for BCVI with CTA,
followed by TCD. Positive CTA findings were followed up with traditional 4-vessel angiography. All extracranial cervical and intracranial vascular segments were insonated using a portable multigate power M-mode
TCD unit with a 2-MHz pencil probe.
Results. Nine trauma patients meeting study criteria were enrolled. Four were diagnosed with BCVIs: 2 internal carotid artery (ICA)
dissections and 2 vertebral artery (VA) dissections. Four had normal CTA
findings, and 1 had a probable injury. One had contralateral innominate
and subclavian artery pseudoaneursyms with ICA dissection. Another with
VA injury had a cerebellar infarct. TCD findings on these patients correlated with positive CTA results and included bruits, high-resistance flow,
tardus-parvus waveforms, steal phenomena, reverse flow, and to-and-fro
waveforms with retrograde diastolic flow. Abnormalities had a global effect, extending downstream beyond the local injury site to major intracranial vessels.
Conclusions. Preliminary results indicate abnormal TCD findings consistent with CTA results. To our knowledge, global neurovascular changes in BCVI are not well studied. Whereas CTA and angiography
provide definitive assessment of vascular injury, TCD provides rich flow
data regarding hemodynamic abnormalities and vessel wall integrity without contrast and patient risk. BCVI evaluation with portable TCD has huge
potential for field and bedside screening of injured patients. Additional
patients should be evaluated.
Distribution of Lower Extremity Thrombi at Ultrasound in
270 Extremities
Coursey C,1* Mittal P,1 Applegate K,1 Stein J2 1Radiology,
Internal Medicine, Emory Healthcare, Atlanta, Georgia USA
Objective. To determine the distribution of lower extremity
deep venous thromboses (DVT) seen at ultrasound.
Methods. Institutional Review Board approval was obtained,
and a waiver of informed consent was granted for this Health Insurance
Portability and Accountability Act–compliant study. Reports from 270 ultrasound studies that were positive for lower extremity DVT were reviewed, and the distribution of lower extremity thrombi was recorded.
Updated 11/18/2011
Abdominal Publications
WFUMB 2011
Shear Wave Elastography of Abdominal and
Retroperitoneal Masses and Inflammatory Processes: a
Feasibility Study
R.Z. Slapa1, W. Jakubowski1, A. Kasperlik-Zaluska1, A. Piwowonski2, K.T. Szopinski1;
Warsaw, Poland, 2Przeworsk, Poland
The purpose of the study was to evaluate the feasibility of assessment of elasticity of
abdominal and retroperitoneal masses and inflammatory processes with shear wave
elastography performed during sonographic examination.
Material & Methods
We evaluated with ultrasound 18 consecutive patients with adrenal and/or liver masses
and abdominal inflammatory processes. Quantitative shear wave elastography was
performed with Aixplorer (Supersonic) with convex abdominal transducer and/or linear
We evaluated with supersonic shear wave elastography 16 adrenal and 5 liver masses,
Crohn’s disease, ulcerative colitis and inflammatory changes related to arterial graft. All
the solid adrenal, liver masses and bowel inflammatory lesions showed the elasticity map.
The adrenal cysts (some not obvious on B-mode imaging) did not show elasticity signal,
as shear waves do not propagate through liquids.
Shear wave elastography of abdominal and retroperitoneal masses and inflammatory
processes is a feasible technique that can be performed during ultrasound examination
and has shown some potential for differential characterization of adrenal or liver masses
and inflammatory bowel diseases. Shear wave elastography may deliver the information
on the extent of inflammatory abdominal processes. Further large-scale studies
evaluating the possibility of differentiation and evaluation of extent of abdominal and
retroperitoneal lesions using shear wave elastography are warranted. Ultrasound
elastography is able to provide stiffness informations and is used since 2005 in thyroid
nodule examination. ShearWave elastography (SWE) is becoming available and provides
true quantitative measurement of stiffness with reduced variability between operators.
The purpose of our study was to evaluate SWE in routine clinical practice.
Updated 11/18/2011
Abdominal Publications
Updated 11/18/2011
Abdominal Publications
Eur Radiol
DOI 10.1007/s00330-011-2229-9
Detection of intrarenal microstructural changes
with supersonic shear wave elastography in rats
Marc Derieppe & Yahsou Delmas & Jean-Luc Gennisson &
Colette Deminière & Sandrine Placier & Mickaël Tanter &
Christian Combe & Nicolas Grenier
Received: 4 May 2011 / Revised: 25 July 2011 / Accepted: 28 July 2011
# European Society of Radiology 2011
Objectives To evaluate, in a rat model of glomerulosclerosis, whether ultrasonic shear wave elastography detects
kidney cortex stiffness changes and predicts histopathological development of fibrosis.
Materials and methods Three groups were studied transversally: a control group (n=8), a group after 4 weeks of
L-NAME administration (H4, n=8), and a group after
6 weeks (H6, n = 15). A fourth group was studied
longitudinally (n =8) before, after 4 weeks and after
7 weeks of L-NAME administration. Shear modulus of
renal cortex was quantified using supersonic shear
imaging technique. Urine was analysed for dosage of
protein/creatinine ratio. Kidneys were removed for histological quantification of fibrosis.
Results Diseased rats showed an increased urinary protein/
creatinine ratio. Cortical stiffness expressed as median
(interquartile range) was 4.0 kPa (3.3–4.5) in control kidneys.
It increased in all but one pathological groups: H4: 7.7 kPa
(5.5–8.6) (p<0.01); H6: 4.8 kPa (3.9–5.9) (not significant);
in the longitudinal cohort, from 4.5 kPa (3.1–5.9) to 7.7 kPa
(5.9–8.3) at week 4 (p<0.05) and to 6.9 kPa (6.1–7.8) at
week 7 (p<0.05). Stiffness values were correlated with the
proteinuria/creatininuria ratio (r=0.639, p<0.001).
Conclusions Increased cortical stiffness is correlated with
the degree of renal dysfunction. More experience in other
M. Derieppe (*)
Laboratory for Molecular and Functional Imaging: from
Physiology to Therapy, FRE 3313 CNRS
& University Bordeaux Segalen,
Bordeaux, France
e-mail: [email protected]
S. Placier
INSERM U489, Hôpital Tenon,
Paris, France
M. Derieppe : J.-L. Gennisson : M. Tanter
Institut Langevin – Ondes et Images, ESPCI ParisTech,
10 rue Vauquelin,
75005 Paris, France
Y. Delmas : C. Combe
Service de Néphrologie, Groupe Hospitalier Pellegrin,
Place Amélie Raba-Léon,
33076 Bordeaux Cedex, France
C. Deminière
Service d’Anatomopathologie, Groupe Hospitalier Pellegrin,
Place Amélie Raba-Léon,
33076 Bordeaux Cedex, France
Updated 11/18/2011
C. Combe
Unité INSERM 1026, Université Bordeaux Segalen,
Bordeaux, France
N. Grenier
Service d’Imagerie Diagnostique et Interventionnelle de l’Adulte,
Groupe Hospitalier Pellegrin,
Bordeaux, France
N. Grenier
Laboratory for Molecular and Functional Imaging:
from Physiology to Therapy,
FRE 3313, CNRS & University Bordeaux Segalen,
146 rue Léo Saignat,
33076 Bordeaux cedex, France
Abdominal Publications
Eur Radiol
models is necessary to understand its relationship with
microstructural changes.
Key Points
& Ultrasound elastography with supersonic shear wave
imaging can predict parenchymal microstructural
& In this rat model, cortical stiffness correlated with the
proteinuria/creatininuria ratio
& Quantification of cortical stiffness could be a useful
biomarker for chronic renal disease
& SSI should now be investigated in patients with native/
transplanted renal disease
Keywords Elastography . Renal fibrosis . Supersonic shear
wave imaging . L-NAME . Cortical stiffness
Chronic kidney disease (CKD) incidence and prevalence
are increasing in developed countries, particularly
diabetes and hypertension-related nephropathies [1].
Because it is a progressive disease, CKD may lead to
end-stage renal failure, with extensive morbidity, mortality and increasing health costs. This justifies developing
more efficient diagnostic strategies in patients with CKD
by using non-invasive methods. Non-invasive imaging
could participate in this challenge in the near future using
functional, structural or molecular approaches. However,
adequate imaging biomarkers have to be validated first. In
most types of renal disease, CKD progression is characterised by progressive fibrotic processes that may involve
first either glomeruli (glomerulosclerosis) or the interstitial space (interstitial fibrosis) depending on the initial
nephropathy [2, 3]. The detection of intrarenal fibrosis
and quantifying its progression with non-invasive methods
could be useful to nephrologists, in addition to current
methods used to evaluate CKD progression, which are
mainly based on quantification of the glomerular
filtration rate.
Among imaging methods used for that purpose,
diffusion-weighted MRI (DW–MRI) was recently proposed
in liver fibrosis [4, 5] and experimental interstitial renal
fibrosis [6]. Elastography is another attractive alternative, as
already demonstrated in the liver using ultrasound [7]. The
supersonic shear imaging (SSI) technique combines the
induction of mechanical vibrations by acoustic radiation
force pulses created by a focused ultrasound beam with a
very high ultrasound frame rate (up to 20,000 frames/s) to
capture the propagation of the shear waves [8, 9]. The
speed of the shear waves relates to Young’s modulus. This
method has already been applied in different organs for the
Updated 11/18/2011
diagnosis of different pathological conditions, such as
breast cancer [9], cornea diseases [10] or liver fibrosis,
and seems attractive for evaluating renal fibrosis.
Materials and methods
Animal protocol
This study involved 40 male Sprague Dawley®™ rats
(Harlan France and Charles River) with a mean body
weight of 50 g at the beginning of the experiments. These
were conducted in agreement with the European Commission guidelines and directives of the French Research
Ministry. Renal fibrosis was induced by administration of
L-NAME (Nω — Nitro — L — arginine methyl ester
hydrochloride, Sigma®) in drinking water [3, 4] at a dosage
of 20 mg/kg/day. Chronic administration of L-NAME was
previously shown to induce cortical vascular fibrosis and
glomerulosclerosis [11].
In a first step, three groups of rats were studied
before sacrifice for histological correlation: a control
group (Co, n = 8), a group undergoing imaging and
sacrificed at the fourth week of L-NAME administration
(H4, n=8), a group undergoing imaging and sacrificed at
the sixth week of L-NAME administration (H6, n=15). In
a second step, a longitudinal cohort (n=8) was studied
sequentially: before (L0), after 4 weeks (L4) and after
7 weeks (L7) of L-NAME administration, then sacrificed
after this last session.
The rats were anaesthetised with isoflurane (3% v/v
for induction and 1.5% v/v afterwards, Baxter, France).
After the last imaging session, rats under anaesthesia
were sacrificed using a lethal injection of pentobarbital
intraperitoneally. Blood and urine samples were collected for measurement of serum creatinine (automated
Jaffe method) and proteinuria normalised to urinary
creatinine concentration (ratio mg/mg) respectively, and
the imaged kidney was harvested. From the experimental work by Boffa et al. [11] we know that the mean
normal value of the urinary protein/creatinine ratio is 2.8±
0.7 mg/mg in rats of these strains.
Elastography sequence and data processing
An ultrafast ultrasound system (Aixplorer, SuperSonic
Imagine, Aix-en-Provence, France) was used with an
8-MHz probe. Principles of SSI have been described
elsewhere [8]. Briefly, a vibration force was generated by
four successive focusing ultrasound beams at different
depths with 5-mm spaces. Each focused beam, the socalled pushing beam, consisted of a 150 μs burst at 8 MHz.
Propagating shear waves were imaged at a very high frame
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Fig. 1 Elastic map of the left
kidney of a control rat
superimposed on the classical
ultrasound image in coronal
views. The elastic image is
colour-coded from 0 to 45 kPa,
corresponding to a shear waves
speed of 0 to 3.87 m/s. The
image size is about 42×25 mm²,
with a spatial resolution of
0.3 mm² for the ultrasound
image and 1.2 mm² for the
elastic image
rate (up to 20,000 frames/s) and raw radiofrequency data
were recorded. Using a speckle tracking correlation
technique, movies of displacements induced in tissues by
the shear wave were calculated. Then the shear wave speed
(cT) was locally deduced by using a time-of-flight algorithm. From the shear-wave speed in locally homogeneous
Fig. 2 Box plots illustrate the values of the urinary protein/creatinine
ratio 4 weeks (H4) and 6 weeks (H6) after L-NAME administration
for the transverse cohort, and 7 weeks (L7) after L-NAME
administration for the longitudinal cohort
Updated 11/18/2011
soft tissues, the elastic modulus, the so-called Young’s
modulus (E), is deduced from the following equation:
E 3m ¼ 3rc2T ;
where μ is the shear modulus and ρ is the density.
The results were displayed on a colour scale ranging
from 0 to 45 kPa (Young’s modulus) as presented in Fig. 1.
Fig. 3 Box plots illustrate cortical stiffness values (Young’s modulus)
in the transverse cohort: in the control group (C0) and in the groups
studied 4 weeks (H4) and 6 weeks (H6) after L-NAME administration
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Histopathological examination
Fig. 4 Box plots illustrate cortical stiffness values (Young’s modulus)
in the longitudinal cohort (9 kidneys) before (L0) and 4 weeks (L4)
and 7 weeks (L7) after L-NAME administration in the longitudinal
After the last elastography session, the imaged left kidney was
removed, fixed in buffered 4% acetic formalin, embedded in
paraffin and sectioned into 3-μm-thick coronal slices. Histological examination (C.D., 30 years’ experience) was
performed after haematoxylin-eosin and Masson trichrome
staining. Histological scoring was performed on x 400
sections by two observers in consensus (C.D. and Y.D.,
12 years’ experience), applying a semi-quantitative scale to
the following items: inflammation, vascular fibrosis, glomerular sclerosis, tubular sclerosis and interstitial sclerosis, each
item ranging from 0 to 5. Finally, a global score was calculated
by the addition of each grade (from 0 to 25).
Statistical analysis
In the following, all data were presented in terms of shear
modulus μ. The corresponding shear-wave speed thus
roughly ranged from 0 to 3.87 m/s. Spatial resolution was
0.3 mm² for the ultrasound image and 1.2 mm2 for the
elastic image. The left kidney was imaged in all cases
(N.G., 25 years’ experience in ultrasound). Three measurements were made for each animal at each session.
Data analysis
The colour scale stiffness map was positioned to cover the
entire kidney. Data analysis of stiffness values was
performed by using regions of interest within the cortex
only because the model induced a glomerulosclerosis
without involving the medulla. The regions of interest were
2×2 mm2 and drawn by one of the authors (N.G.) within
the cortex. Three separate measurements were performed
for each animal.
Values were expressed as mean ± standard deviations or
as median (interquartile range), as appropriate depending
on the normality of distribution. For each kidney, a
mean cortical stiffness value was calculated from the
three measurements. The intraoperator reproducibility
was evaluated by measuring the coefficient of variation
for the three measurements performed within the entire
It was verified that the logarithm of the proteinuria/
creatininuria ratio was normally distributed. It was then
compared with reference values in control rats (from
Boffa et al. [11]) using a t-test. Stiffness values between
groups of the transverse cohort (H4 and H6 groups versus
Co group) were compared using the Kruskal-Wallis
ANOVA. In the longitudinal cohort, comparison of
stiffness between baseline and values at 4 weeks and
7 weeks (L4 and L7) respectively was made using
Wilcoxon’s signed rank test. The relationships between
Fig. 5 Evolution of stiffness
values for each longitudinal rat:
homogeneous increase in the
shear modulus between the
baseline and the fourth week,
and a more variable evolution
between the fourth and the
seventh week
Updated 11/18/2011
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ƒFig. 6
Representative histopathological sections of the renal cortex in a
control rat (a) and in diseased rats after L-NAME administration (b, c)
using Masson trichrome staining (original magnification, x250). In the
control cortex (a), no glomerulosclerosis (arrow) and no interstitial
fibrosis is noted. Sections of diseased cortex demonstrate green staining
indicative of extracellular matrix due to inhibition of NO within the
interstitial space (double arrows in b and c), and shows mild
glomerulosclerosis (arrow in c) and mild infiltration of interstitium by
inflammatory cells (large arrow in b)
and p≤0.05 was considered to indicate a statistically
significant difference.
Biological results
Values of the urinary protein/creatinine ratio in diseased rats
from groups H4, H6 and L7, were 2.8 mg/mg (1.9–11.9),
2.3 mg/mg (1.6–3.8) and 10.4 mg/mg (4.5–15.4) respectively
(Fig. 2). These values were significantly increased for the L7
group only, compared with reference values (p<0.005).
Supersonic shear wave elastography
Cortical stiffness values measured in the three groups of the
transverse cohort and in the longitudinal cohort are
summarised in Figs. 3 and 4 respectively. Mean standard
deviation of the three measures was 0.85 kPa±068. In the
transverse cohort, mean cortical stiffness was 4.0 kPa (3.3–
4.5) in control kidneys versus 7.7 kPa (5.5–8.6) in the H4
group (p<0.01). However, the stiffness of the H6 group was
not significantly different from that of controls 4.8 kPa
(3.9–5.9). Considering the longitudinal cohort, the mean
cortical stiffness increased from 4.5 kPa (3.1–5.9) to
7.7 kPa (5.9–8.3) at week 4 (p<0.05) and to 6.9 kPa
(6.1–7.8) at week 7 (p<0.05), corresponding to a mean
increase of paired stiffness values for each individual of
62% (week 4 compared to week 0) and 35% (week 7
compared to week 0). The cortical stiffness values between
these two time points were not statistically significant.
However, Fig. 5 illustrates the evolution of stiffness values
for each longitudinal rat: it clearly shows a homogeneous
increase in the shear modulus between the baseline and the
fourth week, and a more variable evolution between the
fourth and the seventh week.
Histopathological analysis
stiffness and histopathological analyses, and between the
stiffness and the logarithm of the proteinuria/creatininuria
ratio, for all the kidneys analysed, were tested by Spearman’s rank coefficient. All statistical analyses were
performed with Statistica 9.1 (Statsoft, Tulsa, OK, USA)
Updated 11/18/2011
Diseased kidneys were characterised by mild pathological
changes associated with glomerulosclerosis, interstitial
fibrosis and infiltration by inflammatory cells (Fig. 6).
The mean histological global score was 5.5 (4.5–6.0) for
the H4 group and 6 (5–7) for the H6 group (Fig. 7). The
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Fig. 7 Box plots illustrate histopathological global score (addition of
5 items, ranging from 0 to 5: inflammation, vascular fibrosis,
glomerular sclerosis, tubular sclerosis and interstitial sclerosis) 4 weeks
(H4) and 6 weeks (H6) after L-NAME administration for the
transverse cohort, and 7 weeks (L7) after L-NAME administration
for the longitudinal cohort
difference between these two pathological scores was not
statistically significant. In the longitudinal cohort, the mean
histological global score was 7 (7–7) at week 7, which was
not statistically significant from the other groups.
Stiffness versus biology and histological score
Considering all the animals from the H4, H6 and L7
groups, SSI values were highly correlated with the
proteinuria/creatininuria ratio (Spearman’s rank coefficient:
r=0.6394, p<0.001, Fig. 8). However, neither individual
items from the histological scoring system (inflammation,
vascular fibrosis, glomerular sclerosis, interstitial sclerosis,
tubular and interstitial sclerosis), nor the global histological
score was correlated with the level of cortical stiffness
(p=0.16 for the global score).
Fig. 8 Graph illustrates relationship between cortical stiffness values
(Young’s modulus) and the logarithm of the protein/creatinine ratio;
data indicate a strong correlation (p<0.0001, r=0.64; Spearman’s rank
Updated 11/18/2011
An increase in the extracellular matrix synthesis, with
excessive fibrillary collagens, characterises the development of chronic lesions in the glomerular, interstitial and
vascular compartments [3], leading progressively to endstage renal failure. Mechanisms participating in these
processes are increasingly identified and various therapeutic
interventions have been shown to prevent or to favour
regression of fibrosis in several experimental models [12].
Therefore, development of new non-invasive methods for
identification and quantification of fibrosis would be
This study showed that cortical stiffness values, measured by ultrasound SSI, increase with the development of
intrarenal disease. When followed longitudinally, these
values increased to approximately 76% of their baseline
values 4 weeks after the onset of the model and remained
stable 3 weeks later, as suggested by the non significant
decrease at 7 weeks. All measurements performed in
pathological groups (except for the H6 transverse group
that showed a proteinuria not significantly greater than the
normal proteinuria) were significantly increased compared
with controls. The high degree of correlation between the
enhanced renal stiffness and the degree of renal dysfunction, measured by the proteinuria/creatininuria ratio, is very
encouraging. Histological changes associated with glomerular sclerosis, vascular fibrosis, interstitial sclerosis and
inflammation, were observed to be only small or mild in
pathological kidneys, because of the low level of fibrosis
induced by this model. The quantified global score ranged
between 1 and 8 on a 25-point scale. This is the reason why,
from our point of view, no correlation could be found
between the semi-quantitative scoring system (which is the
addition of several graded items evaluated qualitatively)
and SSI (which is a quantitative value changing linearly).
Conversely, the proteinuria/creatininuria ratio, which is an
early marker of glomerular dysfunction, is also a quantitative value changing linearly, suggesting that SSI is a
sensitive technique for detecting early intrarenal structural
Study of more fibrotic models is now mandatory to
evaluate how stiffness values increase according to the
degree of fibrosis. Unfortunately, such models with advanced fibrosis are difficult to obtain in rats. For example,
ureteral obstruction is a classical highly fibrotic model but
it has the disadvantage of associating fibrosis with a high
level of cellularity [13, 14] and with a decrease in the
tubular flow and water retention. Therefore, it could not be
applied easily to elastographic investigation because increased cellularity and increased intratubular and interstitial
hydrostatic pressure would change and bias the stiffness
values obtained within the renal parenchyma.
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Supersonic shear imaging has the advantage, compared with other ultrasound elastography approaches, of
providing dynamic two-dimensional quantitative stiffness
maps. Quantitative transient ultrasound elastography was
developed first, and is already used in clinics for
staging liver fibrosis (FibroScan®, Echosens, Paris,
France) [7]. Whereas this system was recently proposed
to detect fibrosis in renal transplants [15], the technique
has several limitations when used for renal purposes. First,
its sampling volume is fixed in depth and it is not imageguided, which poses a problem considering the complex
anatomy of the kidney with its cortical and medullary
portions and makes it difficult to focus samplings within
the cortex only. Second, the mechanical wave needs to be
applied to a rigid surface to get rid of compression effects
by the probe, which is impossible for the kidney. Acoustic
radiation force impulse (ARFI®, Siemens, Erlangen,
Germany) [16, 17] seems more promising because it is
quantitative and ultrasound-guided but limited to 5 cm in
depth. Finally, the one-dimensional characteristic of these
two systems is a major inconvenience knowing that the
development of this degenerative fibrotic process is
heterogeneous within tissues.
Experience of MR elastography of the kidney is
extremely limited [18]. It is based on the transmission of
low-frequency mechanical waves across the tissue of
interest, the wave propagation then being encoded in a
tridimensional way using phase data processing. This study
showed, in a rat model of nephrocalcinosis, an increase in
stiffness values with renal dysfunction. Intrarenal diffusion
coefficient value measured with MR imaging has also been
proposed as a surrogate marker of renal fibrosis, as
demonstrated recently in a model of unilateral ureteral
obstruction [6]. However, in this model, as for elastography,
changes in diffusion coefficients may also be due to
increased cellularity and decreased tubular flow and water
exchanges induced by obstruction. In the future, molecular
imaging could overcome these problems by specifically
targeting collagen fibres [19].
One of the main limitations of our study is the low
level of fibrosis induced by this model, as discussed
above. Second, measurements of stiffness were performed in the cortex only, without taking into account
medullary changes because of the small size of this
compartment in rats. The lack of a fibrosis score in
kidney diseases, that could be correlated with stiffness
values, is another limitation compared with liver
diseases. Finally, interobserver variability was not
evaluated in this first pilot study.
In conclusion, ultrasound elastography, using the twodimensional SSI system, appears to be an efficient
technique for the detection of parenchymal microstructural
changes responsible for renal dysfunction. These results
Updated 11/18/2011
suggest that quantification of cortical stiffness may be a
useful biomarker of the progression of chronic renal disease
in native or transplanted kidneys in humans. However,
more experience in fibrotic experimental models and in
chronic human renal diseases is still mandatory.
Acknowledgements We are grateful to Angélique Foucault-Simonin
and colleagues (UMR914, PNCA-INRA, AgroParisTech, Paris,
France) for technical support. This work was supported by Programme
National de Recherche en Imagerie 2007, Institut National de la Santé
et de la Recherche Médicale (INSERM), ELASTOREIN, France.
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2. Lee SB, Kalluri R (2010) Mechanistic connection between
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3. Ricardo SD, van Goor H, Eddy AA (2008) Macrophage diversity
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V (2008) Chronic hepatitis: role of diffusion-weighted imaging
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AJR Am J Roentgenol 189:799–806
6. Togao O, Doi S, Kuro-o M, Masaki T, Yorioka N, Takahashi M
(2010) Assessment of renal fibrosis with diffusion-weighted MR
imaging: study with murine model of unilateral ureteral obstruction. Radiology 255:772–780
7. Castera L, Forns X, Alberti A (2008) Non-invasive evaluation
of liver fibrosis using transient elastography. J Hepatol
8. Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a
new technique for soft tissue elasticity mapping. IEEE Trans
Ultrason Ferroelectr Freq Control 51:396–409
9. Athanasiou A, Tardivon A, Tanter M et al (2010) Breast lesions:
quantitative elastography with supersonic shear imaging–preliminary results. Radiology 256:297–303
10. Tanter M, Touboul D, Gennisson JL, Bercoff J, Fink M (2009)
High-resolution quantitative imaging of cornea elasticity using
supersonic shear imaging. IEEE Trans Med Imaging 28:1881–
11. Boffa JJ, Lu Y, Placier S, Stefanski A, Dussaule JC, Chatziantoniou C
(2003) Regression of renal vascular and glomerular fibrosis: role of
angiotensin II receptor antagonism and matrix metalloproteinases. J
Am Soc Nephrol 14:1132–1144
12. Chatziantoniou C, Boffa JJ, Tharaux PL, Flamant M, Ronco P,
Dussaule JC (2004) Progression and regression in renal vascular
and glomerular fibrosis. Int J Exp Pathol 85:1–11
13. Hauger O, Delalande C, Deminiere C et al (2000) Nephrotoxic nephritis and obstructive nephropathy: evaluation with
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iron oxide-preliminary findings in a rat model. Radiology
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15. Arndt R, Schmidt S, Loddenkemper C et al (2010) Noninvasive
evaluation of renal allograft fibrosis by transient elastography – a
pilot study. Transpl Int 23:871–877
16. Fahey BJ, Nightingale KR, McAleavey SA, Palmeri ML, Wolf
PD, Trahey GE (2005) Acoustic radiation force impulse imaging
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17. Friedrich-Rust M, Wunder K, Kriener S et al (2009) Liver fibrosis
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force impulse imaging versus transient elastography. Radiology
18. Shah NS, Kruse SA, Lager DJ et al (2004) Evaluation of renal
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Quantification of the Kidney Fibrosis Using Supersonic
Shear Wave Imaging: Experimental Study with Rabbit
SK Moon, DH Lee MD, SY Kim MD, JY Cho MD, SH Kim, KC Moon.
To evaluate the values and feasibility of ultrasonic shear wave elastography for the
quantification of renal fibrosis in an experimental rabbit model.
Materials and Methods
Thirty-eight kidneys of 19 rabbits were studied and categorized into three groups;
hydronephrosis group, renal vein thrombosis group and normal control group.
Hydronephrosis (n=9) and renal vein thrombosis (n=10) was surgically made in each left
kidney. Their right kidneys were control group (n=19).We repeatedly measured
viscoelasticity (Young’s modulus, kPa) at renal cortex using shear wave elastography and
evaluated sonographic findings of each kidney; size, echogenicity, other pathology,
perfusion degree, and resistive index (RI) measurement before operation, on 1st day
after operation, 3rd day, and weekly until 2nd week in hydronephrosis group, and until
4th week in vein thrombosis group. After sacrifice of the rabbits, degree of histologicallyquantified fibrosis and measured viscoelasticity was statistically compared.
Before surgery, initial mean viscoelasticity of renal cortex and conventional US findings in
three groups showed no significant difference (p> 0.05, 9.74kPa in control, 8.95kPa in
hydronephrosis, and 9.06kPa in thrombosis). However, in the last US exam, mean
viscoelasticity in each group were significantly different (p= 0.01, 9.77kPa in control,
10.91kPa in hydronephrosis, and 13.92kPa in thrombosis). Pathologically, degree of
fibrosis was significantly different among three groups (p< 0.001, 0.70% in control,
3.62% in hydronephrosis, and 11.70% in thrombosis), and the fibrosis degree and
viscoelasticity showed statistically good correlation (rho= 0.568, p= 0.01). In addition,
mean kidney size of the thrombosis group was significantly decreased as compared with
other two groups (p = 0.01). Of 39 kidneys, 19 control group kidneys had no fibrosis (<
1.5%, 0.70%), 12 minimal fibrosis (1~10%, 4.48%), and 7 mild fibrosis (> 10 %,
13.70%). In the prediction of fibrosis more than 10%, shear wave elastography showed
sensitivity 100% and specificity 87.1% at a cut-off value of 12.80kPa.
Ultrasonic shear wave elastography showed good correlation between viscoelasticity and
histologic degree of renal fibrosis. It can be the feasible tool in quantification of the renal
Clinical Relevance/Application
Ultrasonic shear wave elastography can be the noninvasive tool for the prediction of the
renal interstitial fibrosis.
Updated 11/18/2011
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