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actors associated with the impossibility to obtain reliable livertiffness measurements by means of Acoustic Radiation Force ImpulseARFI) elastography—Analysis of a cohort of 1031 subjects
imona Bota ∗, Ioan Sporea1, Roxana Sirli 1, Alina Popescu1, Mirela Danila1,na Jurchis1, Oana Gradinaru-Tascau1
epartment of Gastroenterology and Hepatology, “Victor Babes” University of Medicine and Pharmacy Timisoara, Romania
r t i c l e i n f o
rticle history:eceived 7 August 2013eceived in revised form1 November 2013ccepted 17 November 2013
Introduction: Acoustic Radiation Force Impulse (ARFI) elastography is a non-invasive technique for liverfibrosis assessment.Aim: To assess the feasibility of ARFI elastography in a large cohort of subjects and to identify fac-tors associated with impossibility to obtain reliable liver stiffness (LS) measurements by means of thistechnique.Methods: Our retrospective study included 1031 adult subjects with or without chronic liver disease. Ineach subject LS was assessed by means of ARFI elastography. Failure of ARFI measurements was definedif no valid measurement was obtained after at least 10 shots and unreliable in the following situations:fewer than 10 valid shots; or median value of 10 valid measurements with a success rate (SR) < 60% and/oran interquartile range interval (IQR) ≥ 30%.Results: Failure of LS measurements by means of ARFI was observed in 4 subjects (0.3%), unreliable mea-surements in 66 subjects (6.4%), so reliable measurements were obtained in 961 subjects (93.3%). Inunivariant analysis, the following risk factors were associated with failed and unreliable measurements:
age over 58 years (OR = 0.49; 95% CI 0.30–0.80, p = 0.005), male gender (OR = 0.58; 95% CI 0.34–0.94,p = 0.04), BMI > 27.7 kg/m2 (OR = 0.23, 95% CI 0.13–0.41, p < 0.0001). In multivariate analysis all the factorsmentioned above were independently associated with the risk of failed and unreliable measurements.Conclusions: Reliable LS measurements by means of ARFI elastography were obtained in 93.3% of cases.Older age, higher BMI and male gender were associated with the risk of failed and unreliable measure-ments, but their influence is limited as compared with Transient Elastography.
. Introduction
Acoustic Radiation Force Impulse (ARFI) elastography is aon-invasive method for liver fibrosis assessment, valuable for pre-
icting significant and severe fibrosis and with excellent results forredicting liver cirrhosis [1–3]. This elastographic technique has
∗ Corresponding author at: Department of Gastroenterology, University ofedicine and Pharmacy, 2, Intrarea Martir Angela Sava str., 300742 Timisoara,
applications also in other organs, such as spleen [4,5], thyroid [6,7],breast [8], kidney [9] or prostate [10].
The principle of ARFI elastography is based on the compressionof the examined tissue that induces a smaller strain in hard tissuesthan in soft ones. The ultrasound probe automatically produces anacoustic “push” pulse that generates shear-waves which propagateinto the tissue. Their speed, measured in meters/second (m/s), isdisplayed on the screen. Also, shear wave speed may be quantified,in a precise anatomical region, focused on a region of interest, witha predefined size (10 mm in length and 5 mm in width), providedby the system [11,12].
Published studies showed high percentages of patients in whomliver stiffness (LS) could be evaluated by means of ARFI elastography[13–16], but no data are available regarding the factors associated
with the impossibility to obtain reliable LS measurements by meansof this elastographic technique.
The aim of this study was to assess the feasibility of ARFI elastog-raphy in a large cohort of subjects and to identify factors associated
S. Bota et al. / European Journal of Radiology 83 (2014) 268– 272 269
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. Subjects and methods
.1. Subjects
Our retrospective study included 1031 adult subjects with orithout chronic liver disease evaluated in our department betweenctober 2009 and December 2012. We included in our study:ealthy volunteers – defined as subjects without a history of hep-topathies, with a normal abdominal ultrasound, but additionalests as aminotransferases or viral markers were not performed;atients with chronic hepatitis B and C evaluated by means of ARFIlastography and liver biopsy (LB); patients diagnosed with liverirrhosis by means of clinical, biological, ultrasound, endoscopicnd/or laparoscopic criteria; patients with non-cirrhotic ascites –ncluding patients with demonstrated peritoneal carcinomatosis
ith histological proof, acute pancreatitis with ascites, which wasater resolved, or lymphatic ascites; and patients with focal liveresions in the absence chronic liver disease.
At the time of ARFI measurements, besides the epidemiologicalnd demographic data, the following serum biological parametersere determined in all subjects included in our study, with the
xception of healthy volunteers: aminotransferases, alkaline phos-hatase, gamma-glutamyl transpeptidase, total bilirubin, albumin,holinesterase, prothrombin time.
All subjects signed an informed consent; the study waspproved by the local Ethics Committee and was in accordance withhe Helsinki Declaration of 1975.
.2. ARFI elastography
ARFI was performed in all patients, in fasting condition, with aiemens Acuson S2000TM ultrasound system (Siemens AG, Erlan-en, Germany), software version 2.0, with a 4CI ultrasound probe.canning was performed between the ribs with the patient inupine position, in the Vth or VIIIth segment of the right liver lobe,–2 cm under the capsule, with minimal scanning pressure appliedy the operator, while the patients were asked to stop breathingor a moment, in order to minimize breathing motion. In every
atient, we aimed for 10 valid acquisitions in the same place ofhe right liver lobe, and a median value was calculated, the resulteing measured in m/s (Fig. 1). If the measurement was not valid,X.XX” was displayed on the screen (Fig. 2).
obese subject.
Even if the device’s manufacturer did not make any indica-tion regarding the quality of ARFI measurements, published studies[17,18] demonstrated that to have a better concordance of LS mea-surements by means of ARFI elastography with histological fibrosis,quality parameters should be used, similar with Transient Elastog-raphy (TE) measurements. The quality parameters that we usedwere: interquartile range interval (IQR = the difference between the75th percentile and the 25th percentile, essentially the range of themiddle 50% of the data) and success rate (SR = the ratio of valid shotsto the total number of shots).
Reliable ARFI measurements were defined as: median value of10 valid LS measurements with a SR ≥ 60% and an IQR < 30%. Fail-ure of ARFI measurements was defined as no valid measurementobtained after at least 10 shots, and a measurement was consid-ered as unreliable in the following situations: fewer than 10 validshots; or median of 10 valid measurements with SR < 60% and/orIQR ≥ 30%.
The operators who performed ARFI measurements were blindedto all patients’ clinical, serologic, and histological data.
2.3. Abdominal ultrasound
Abdominal ultrasound examination was performed in all sub-jects included in the study by using a Siemens Acuson S2000TM
ultrasound system (Siemens AG, Erlangen, Germany) with a 4CIultrasound probe. We recorded in all cases the liver structure, thepresence of focal liver lesions, the presence of ascites, and theantero-posterior diameter of the spleen.
2.4. Liver biopsy
Liver biopsy was performed echo-assisted in the same sessionwith ARFI measurements in patients with chronic hepatitis B and C,using Menghini type modified needles, 1.4 and 1.6 mm in diameter.
The LBs were assessed according to the Metavir score, by a seniorpathologist, blinded to the results of ARFI measurements and toall patients’ clinical, serologic, and histological data. Fibrosis wasstaged on a 0–4 scale: F0 – no fibrosis; F1 – portal fibrosis withoutsepta; F2 – portal fibrosis and few septa extending into lobules; F3
– numerous septa extending to adjacent portal tracts or terminalhepatic venules and F4 – cirrhosis..
270 S. Bota et al. / European Journal of Radiology 83 (2014) 268– 272
Table 1Main subjects’ characteristics. Numerical variables with normal distribution arepresented as mean value ± standard deviation, while variables with non-normaldistribution are presented as median values and range intervals.
Parameter
Age (years) 55 (18–86)Gender
Female n = 435 (42.2%)Male n = 596 (57.8%)
Body mass index – BMI (kg/m2) 25.3 (18.6–46.2)Etiology
Healthy volunteers n = 207 (20.1%)Chronic hepatitis B with LB n = 53 (5.1%)Chronic hepatitis C with LB n = 107 (10.4%)Liver cirrhosis n = 582 (56.5%)Non-cirrhotic ascites n = 49 (4.7%)Focal liver lesions without liver disease n = 33 (3.2%)
CirrhosisYes n = 604 (58.5%)No n = 427 (41.5%)
AscitesYes n = 301 (29.2%)No n = 730 (70.8%)
Focal liver lesionsYes n = 160 (15.5%)No n = 871 (84.5%)
Table 3Multivariate analysis of factors associated with failed and unreliable LS measure-ments by means of ARFI elastography.
Parameter Coefficient Standard error p value
Age 0.020 0.008 0.01Male gender −0.568 0.268 0.03
TUp
Cholinesterase (U/L) 3910 (600–15,590)Prothrombin time (%) 89.7 (15–124)
.5. Statistical analysis
The statistical analysis was performed using the MedCalc Soft-are, version 12.7.0 (MedCalc Program, Belgium). The distribution
f numerical variables was first tested by the Kolmogorov–Smirnovest. For numerical variables with normal distribution, the meanalue and standard deviation were presented, while for non-normalistribution median values and range intervals were presented. Dif-erences between numerical variables were analyzed by parametrict-test) or nonparametric tests (Mann–Whitney test) according tohe normal or non-normal distribution. Qualitative variables wereresented as numbers and percentages. Chi-square (�2) test (with
ates’ correction for continuity) was used for comparing propor-ions expressed as percentages (“n” designates the total numberf patients included in a particular subgroup). The influence ofemographic characteristics and biological data on the risk of failed
able 2nivariant analysis of factors associated with failed and unreliable LS measurements bresented as mean value ± standard deviation, while variables with non-normal distribut
Parameter Reliable measurements
Age (years) 55 (18–86)
GenderFemale n = 414 (43.1%)
Male n = 547 (56.9%)
BMI (kg/m2) 25.1 (16.4–46.2)
Presence of cirrhosis n = 560 (58.2%)
Presence of ascites n = 281 (29.2%)
Presence of focal liver lesions n = 147 (15.3%)
AST (U/L) 81 (15–731)
ALT (U/L) 54 (16–1330)
Alkaline phosphatase (U/L) 97 (16–1233)
GGTP (U/L) 71 (11–1983)
Total bilirubin (mg/dl) 1.4 (0.2–19)
Albumin (g/dl) 3.6 (1.4–6.4)
Cholinesterase (U/L) 4032 (600–15,590)
Prothrombin time (%) 89.7 (15–124)
BMI 0.162 0.024 <0.0001
and unreliable LS measurements by means of ARFI elastographywas assessed by comparing the reliable with failed and unreli-able measurements, firstly by univariant analysis. In the secondstep, the independent discriminative values of variables reach-ing statistic significance by univariant analysis were assessed bystepwise logistic regression analysis. Areas under receiver oper-ating characteristics (AUROC) curves were built to discriminatecut-off values associated with the risk factors for failed and unre-liable measurements. The optimal cut-off values were obtainedby using Youden index (sensibility + specificity − 1) from AUROCcurves analysis. 95% confidence intervals (CI) were calculated foreach predictive test and a p-value less than 0.05 was regarded assignificant for each statistic test.
3. Results
The main characteristics of the 1031 subjects included in thisstudy are presented in Table 1.
From the 1031 subjects, failure of LS measurements by means ofARFI elastography was observed in 4 subjects (0.3%) and unreliableLS measurements in 66 subjects (6.4%), so reliable LS measurementswere obtained in 961 subjects (93.3%).
In univariant analysis, older age, male gender and higher BMIwere associated with the risk of failed and unreliable measure-ments (Table 2).
All factors associated with the risk of failed and unreliable LSmeasurements by ARFI elastography in univariant analysis werealso independently associated with the impossibility to obtain reli-able measurements in multivariate analysis also (Table 3).
AUROC curves were built to discriminate cut-off values associ-ated with the risk factors for failed and unreliable LS measurementsby means of ARFI elastography. We found the following cut-off values as predictors of failed and unreliable measurements:age > 58 years (AUROC = 0.590, p = 0.003) and BMI > 27.7 kg/m2
(AUROC = 0.653, p = 0.0001). The relationships between failed andunreliable LS measurements by ARFI elastography and differentparameters are presented in Table 4.
y means of ARFI elastography. Numerical variables with normal distribution areion are presented as median values and range intervals.
The rate of reliable LS measurements by means of ARFIlastography was significantly higher in normal weight sub-ects (BMI = 18.5–24.9 kg/m2) as compared with overweightBMI = 25–29.9 kg/m2) and obese subjects (BMI ≥ 30 kg/m2): 97.3%s. 93.4%, p = 0.01 and 97.3% vs. 82.4%, p < 0.0001, respectively. Also,he rate of reliable ARFI measurements was significantly highern overweight as compared with obese patients: 93.4% vs. 82.4%,
= 0.0004.
. Discussion
The feasibility of elastographic methods for the non-invasivevaluation of liver fibrosis is very important, because in order to besed in daily clinical practice, a method should be able to properlyvaluate a large number of patients.
Large published studies in the field of TE demonstrated that reli-ble LS measurements, using the standard M-probe, are obtained in0–85% of cases [19,20]. Regarding ARFI elastography, because theanufacturer did not specify that quality criteria are needed forRFI measurements, only a few published studies used the qual-
ty criteria applied for TE [14–16,21,22]. But, recently publishedtudies [18] demonstrated the importance of quality parametersespecially IQR) for the correlation of LS measurements assessedy means of ARFI with histological fibrosis. The manufacturer rec-gnized the importance of these technical parameters and newoftware which automatically displays the value of the qualityriteria parameters was developed, similar with TE.
Until now, there are no studies that analyze the factors associ-ted with the impossibility to obtain reliable LS measurements byeans of ARFI elastography, our study being the first to perform a
etailed analysis of the factors associated with failed and unreliableRFI measurements in a large cohort of subjects.
The rate of reliable LS measurements obtained in our presenttudy was very good (93.3%), in line with the results of other pub-ished studies in field of ARFI elastography [14–16,21], and muchigher than in case of TE (using the standard M-probe) [19,20].
Similar with TE [19,20], older age and higher BMI were associ-ted with the impossibility to obtain reliable ARFI measurements.ut, unlike TE, in which age > 50 years and BMI > 30 kg/m2 weressociated with high ORs (3.5 and 10.5, respectively) for failednd unreliable TE measurements in Castéra et al. [19] study; and2.04 and 3.34, respectively), for age > 52 years and BMI > 30 kg/m2
n the study of Sirli et al. [20] study, in our present study theRs were much lower, only 0.49 for age > 58 years and 0.24 forMI ≥ 30 kg/m2. According to our results, these parameters havenly a limited influence in daily clinical practice. Thus, if in obeseatients reliable LS measurements by means of TE (standard M-robe) are obtained only in approximately 50% of patients [19,20];
n our present study reliable ARFI measurements were obtainedn 82.4% of cases. In our study the rate of reliable LS measure-
ents by means of ARFI elastography in obese patients was similarr higher than the one presented in studies which used the XL-
robe, designed specifically for overweight and obese subjects, forE [23,24].
In TE studies [19,20], female gender was associated with failednd unreliable LS measurements, but our study showed that in ARFI
adiology 83 (2014) 268– 272 271
elastography male gender was associated with the impossibilityto obtain reliable LS measurements. One explanation can be theolder age and higher BMI in our cohort of men as compared withwomen: 56 (19–84) years vs. 54 (18–86) years, p = 0.0003 and 25.9(19.2–45.2) kg/m2 vs. 24.2 (18.6–46.2) kg/m2, p < 0.0001, respec-tively. Also, the OR was small (0.58) meaning that this factor doesnot have a great importance in daily clinical practice, basically therate of reliable LS measurements by means of ARFI elastographybeing higher than 90% for both genders (95.1% in women and 91.7%in men, respectively).
Our study demonstrated that the presence of cirrhosis, of ascitesor of focal liver lesions did not influence the rate of reliable ARFImeasurements. This is an important finding, especially becauseTE cannot be performed if perihepatic ascites is present. Anotheradvantage of ARFI elastography as compared to TE is that the regionof interest is chosen under ultrasound examination, thus the exam-iner can be sure that the measurement is performed in normal liverparenchyma if focal liver lesions are present.
As expected, the aminotransferases, alkaline phosphatase,GGTP, total bilirubin, cholinesterase, serum albumin level andprothrombin index did not influence the rate of reliable LS measure-ments by means of ARFI elastography. But, according to publishedstudies [25–27] high aminotransferases level and cholestasis influ-ence the accuracy of ARFI elastography for the non-invasiveevaluation of liver fibrosis, these data being similar with thosepublished regarding TE [28–30].
We tried to analyze the four cases with failure of LS measure-ments by means of ARFI elastography, but being a retrospectivestudy not all the data were available. All four subjects were obese(two subjects with BMI between 30 and 35 kg/m2, one subject withBMI between 35.1 and 40 kg/m2 and one with BMI ≥ 40 kg/m2),three were cirrhotic patients (two of them with ascites) and onesubject was a healthy volunteer. In the ultrasound reports thereis a mention regarding the poor acoustic window in three, whilein one case (cirrhotic patient with ascites) it is reported thatthe patient had difficulties to stop breathing at the moment ofLS evaluation. The patient position for LS evaluation by meansof ARFI elastography was not changed in any of these fourcases.
The strong point of our study is the large number of subjects inwhich the feasibility of LS measurements by means of ARFI elasto-graphy was evaluated, but our research has also some limitations,such as the retrospective design and the inclusion of a hetero-geneous population: healthy volunteers; patients with chronichepatitis B and C evaluated by means of LB and ARFI elastogra-phy; cirrhotic patients diagnosed by means of clinical, biological,ultrasound, endoscopic and/or laparoscopic criteria; patients withnon-cirrhotic ascites; and subjects with focal liver lesions in theabsence of chronic liver disease.
In patients with liver tumors we presented only data regardingARFI measurements in the apparently healthy parenchyma sur-rounding the focal liver lesions, because the subject of the presentresearch was to assess the feasibility of ARFI elastography for LSevaluation. It should be specified that the evaluation of LS stiff-ness in a patients with liver tumors is very important. Thus, if theLS measurements suggest a severe fibrosis or liver cirrhosis, thefirst type of lesion that we should think about is a hepatocellularcarcinoma, but if the LS measurements suggest the absence of sig-nificant fibrosis we should think firstly to a benign liver lesion ifthe tumor is unique or to liver metastases if multiple tumors arepresent.
In conclusion, reliable LS measurements by means of ARFI elas-
tography were obtained in 93.3% of cases. Older age, higher BMIand male gender were associated with the risk of failed and unreli-able measurements, but their influence is limited as compared withTE.
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72 S. Bota et al. / European Journ
onflict of interest
Ioan Sporea is in the Advisory Bord of Siemens from November013. The authors have any conflict of interest.
cknowledgment
For the young researchers grant “Utilitatea metodelor elas-ografice de tip shear-waves în evaluarea pacientilor cu cirozaepatica” awarded by the “Victor Babes ” University of Medicinend Pharmacy Timis oara, Romania.
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