Semana 1-Paper, Ultrasound Liver
Semana 1-Paper, Ultrasound Liver
Semana 1-Paper, Ultrasound Liver
This multidisciplinary update of the Society of Radiologists in Ultrasound consensus statement on liver elastography incorporates the
large volume of new information available in the literature since the initial publication. The recommended procedure for acquiring
stiffness measurements is reviewed. There has been substantial improvement in the acoustic radiation force impulse (ARFI)
technology—most notably the addition of a quality assessment of the shear wave propagation. Due to the efforts of the
Quantitative Imaging Biomarkers Alliance, or QIBA, the variability of liver stiffness measurements between systems had decreased.
There are now effective treatments for hepatitis B and hepatitis C, and follow-up after effective treatment should be based on the
use of the delta change of the value obtained at viral eradication or suppression. Because the detection of compensated advanced
chronic liver disease (cACLD) is very important, the new guidelines are made based on the probability of cACLD for given stiffness
values. The panel recommends a vendor-neutral rule of four for interpretation for ARFI techniques. This new method simplifies
interpretation of liver stiffness results and is more clinically relevant.
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Update to the Society of Radiologists in Ultrasound Liver Elastography Consensus Statement
Table 1: Recommendations for Performing Liver Stiffness Measurements with the ARFI Technique
Recommendations
1. Patients should fast at least 4 hours before the examination
2. Measurement should be taken at an intercostal space with the patient in the supine or slight lateral decubitus (30°) position with right
arm in extension
3. Measurements should be taken at neutral breathing during a breath hold
4. Measurement should be taken at least 15–20 mm below liver capsule in pSWE
5. The 2D SWE region of interest can be positioned closer to the liver capsule, if reverberation artifacts are avoided; however, the measure-
ment box should be positioned at least 15–20 mm below the liver capsule
6. Results can be reported in meters per second or in kilopascals
7. In most systems, the maximum ARFI push pulse is at 4–4.5 cm from the transducer, which is the optimal location for obtaining mea-
surements. In most systems, the ARFI push pulse is attenuated by 6–7 cm, limiting adequate shear wave generation
8. Major potential confounding factors include liver severe inflammation indicated by AST and/or ALT elevation greater than five times
upper normal limits, obstructive cholestasis, liver congestion, acute hepatitis, and infiltrative liver disease (these all lead to overestimation
of the stage of fibrosis)
9. Ten measurements should be obtained with pSWE, and the final result should be expressed as the median together with the IQR/M
10. Fewer than 10 measurements with pSWE can be obtained (at least five); however, the IQR/M should be within the recommended range
11. For 2D SWE, five measurements should be obtained when the manufacturer’s quality criteria are available, and the final result should be
expressed as the median together with the IQR/M
12. The most important reliability criterion is an IQR/M of 30% of the 10 measurements (pSWE) or five measurements (2D SWE) for
kilopascals and 15% for measurements in velocity (in meters per second)
13. Adequate B-mode liver imaging is a prerequisite for point and 2D SWE as shear waves are tracked with B-mode
Note.—ALT = alanine aminotransferase, ARFI = acoustic radiation force impulse, AST = aspartate aminotransaminase, IQR/M = inter-
quartile range–to-median ratio, pSWE = point SWE, SWE = shear-wave elastography, 2D = two-dimensional.
Figure 1: (a) Image obtained with point shear-wave elastography (pSWE) system (ElastPQ; Philips, Bothell, Wash). A standard deviation (Std) of 30% or less of the
mean value is indicative of an acquisition of good quality. In this case, the standard deviation is 1.06/9.90 or 10.7%. When the signal-to-noise ratio of an acquisition is
very low, the mean value is not shown. (b) Image obtained with pSWE (SWM; Hitachi, Tokyo, Japan). “VsN” is a reliability index that indicates the percentage of effec-
tive push-track sequences. When the signal-to-noise ratio of an acquisition is very low, the mean value is not shown. A good acquisition has a VsN of at least 50%. In this
case, the VsN measurements are all above 66%. (c) Image obtained with pSWE (VTQ; Siemens, Mountain View, Calif). The system automatically filters out the measure-
ments that are not good. In these cases, the numeric value of shear-wave speed is replaced by an “XXX” sequence. (d) Images obtained with two-dimensional (2D)
shear-wave elastography (SWE) (EQI, Philips). The color-coded confidence map (left) is an evaluation of the quality of the acquired signals. The confidence threshold
(CT) is set at 60%: Areas of low quality (red) are filtered out and left blank on the color-coded image of liver stiffness assessment (right); the yellow color on the confidence
map is a warning, that is, it indicates that the acquisition in that area is not the highest quality (Fig 1 continues).
for the staging of liver fibrosis with vibration-controlled transient For other causes such as alcoholic hepatitis, primary biliary
elastography, the consensus panel proposes a vendor-neutral “rule cirrhosis, Wilson disease, autoimmune hepatitis, sclerosing chol-
of four” (5, 9, 13, 17 kPa) for the ARFI techniques for viral etiolo- angitis, and drug-induced liver disease, there is insufficient data
gies and NAFLD: Liver stiffness of 5 kPa (1.3 m/sec) or less has to make a conclusion.
high probability of being normal; liver stiffness less than 9 kPa (1.7 Table 2 summarizes these cut-off value recommendations and
m/sec), in the absence of other known clinical signs, rules out cA- provides them in both kilopascals and meters per second. For
CLD; values between 9 kPa (1.7 m/sec) and 13 kPa (2.1 m/sec) are those who would like a value to rule out significant fibrosis, most
suggestive of cACLD but may need further test for confirmation; studies that used ARFI (pSWE and 2D SWE) suggest that a liver
and values greater than 13 kPa (2.1 m/sec) are highly suggestive of stiffness value of less than 7 kPa (1.5 m/sec) can help rule out
cACLD. There is a probability of CSPH with liver stiffness values significant fibrosis.
greater than 17 kPa (2.4 m/sec), but additional patient testing may With vibration-controlled transient elastography, the ala-
be required. In some patients with NAFLD, the cut-off values for nine aminotransferase–adapted cut-off values of liver stiffness
cACLD may be lower and follow-up or additional testing in those reportedly improved the staging of liver fibrosis in patients
with values between 7 and 9 kPa is recommended. with chronic hepatitis B in a single study (36). The consensus
Figure 1 (continued): (e) Images obtained with 2D SWE (STE; Mindray, Shen-
zhen, China). Two quality criteria are provided: the motion stability (M-STB) index,
which is indicated by stars (with the highest stability shown with five green stars), and
the reliability (RLB) map, which goes from purple to green—with the latter indicating
the highest reliability. The stars are an indicator of motion during the acquisition. When
there are fewer than four stars, there is significant motion during the acquisition and
that frame should not be used for liver stiffness measurement. (f) Images obtained
with 2D SWE (Aplio; Canon, Tochigi, Japan). The system filters out values with a low
signal-to-noise ratio, and these areas are left blank. The proprietary quality parameter
is the propagation map (right). A proper propagation map is displayed with parallel
lines, with the intervals between the lines constant. The propagation map is used to
guide placement of the measurement box. Image on left is velocity map. (g) Images
obtained with 2D SWE (SSI; SuperSonic, Aix-en-Provence, France). Values with a
low signal-to-noise ratio are filtered out. The stability index (SI) is an indicator of tem-
poral stability, and it is displayed while positioning the measurement box (Q-Box). An
acquisition of good quality should have a stability index greater than 90%. Top image
is velocity map, and bottom image is B-mode image.
Table 2: Recommendation for Interpretation of Liver Stiffness Values Obtained with ARFI Techniques in Patients with Viral Hepa-
titis and NAFLD
panel therefore does not recommend alanine aminotransfer- (1,3,5). These conditions include, but are not limited to, acute
ase–adapted cut-offs until additional publications confirm its hepatitis, liver inflammation, transaminitis flares with ala-
usefulness. The updated World Federation of Ultrasound in nine aminotransferase value more than five times the up-
Medicine and Biology guidelines provide a detailed review of per limit of normal, obstructive cholestasis, hepatic con-
the literature for several of the causes that progress to chronic gestion, and infiltrative liver diseases such as amyloidosis,
liver disease and associated confounding factors (3). lymphoma, or extramedullary hematopoiesis. Other factors
may also affect liver stiffness measurement, such as post-
Confounding Factors prandial hyperemia or intense physical exercise. In all these
There are several clinical conditions in which an increase conditions, however, stiffness values within the normal
of liver stiffness unrelated to liver fibrosis can be observed range exclude significant liver fibrosis.
Table 3: Recommendations for Performing Spleen Stiffness Measurements with the ARFI Technique
Recommendations
1. Patients should fast at least 4 hours before the examination (56)
2. Measurement should be taken at an intercostal space with the patient in supine position with left arm in extension
3. Measurements should be taken during breath hold at neutral breathing (57)
4. Measurement should be taken at least 15 mm below spleen capsule with pSWE and reverberation artifacts avoided with 2D SWE. The
region of interest should be placed perpendicular to the splenic surface
5. Results can be reported in meters per second or kilopascals
6. In most systems, the maximum ARFI push pulse is at 4–4.5 cm from the transducer, which is the optimal location for obtaining mea-
surements. In most systems, the ARFI push pulse is attenuated by 6–7 cm, limiting adequate shear wave generation
7. Ten measurements should be obtained with pSWE, and the final result should be expressed as the median together with the IQR/M
8. For 2D SWE, five measurements should be obtained, and the final result should be expressed as the median together with the IQR/M
9. The most important reliability criteria is a IQR/M of 30% of the recommended measurements for kilopascals and 15% for meters
per second
Note.—ARFI = acoustic radiation force impulse, IQR/M = interquartile range–to-median ratio, pSWE = point SWE, SWE = shear-wave
elastography, 2D = two-dimensional.
of liver stiffness values over time should be used instead of the ab-
solute values (37–40,42). Thus, every patient becomes his or her
own control. Because there is an approximately 10% variability of
the measurements within a vendor and between vendors (29,30),
a clinically significant change should be considered when the delta
change is greater than 10%. The panel recommends using the
same equipment for follow-up studies. In patients with chronic vi-
ral hepatitis who are successfully treated, the baseline liver stiffness
should be that obtained after viral eradication or suppression. Ap-
plying this rule, liver stiffness assessment can be suitable for evalu-
ating all clinical conditions leading to an increase of liver stiffness,
independent of the disease etiology including nonfibrotic causes of
liver stiffness increase, such as congestive heart failure.
Spleen Stiffness
It has been reported that liver stiffness correlates with the se-
verity of liver fibrosis up to the threshold of CSPH, defined as
Figure 2: Image obtained with two-dimensional (2D) shear-wave elastogra- an increase in hepatic venous pressure gradient greater than
phy (SWE) demonstrates area of increased stiffness (red and teal, arrows) due to 10 mm Hg (43). In patients with CSPH, the strength of the
reverberation artifact. The reverberation artifact occurs below the liver capsule in correlation between liver stiffness and fibrosis decreases, prob-
both point SWE (pSWE) and 2D SWE. In pSWE, the artifact is not seen; therefore, ably due to an increasing role played by extrahepatic factors,
it is important to obtain measurements at least 1.5 cm below the liver capsule to
avoid the artifact. This area should be avoided when placing the measurement
mainly the increase in portal venous inflow, as portal hyperten-
box for liver stiffness measurements. sion progresses (10,44). The acquisition technique is the same
as that for liver, except the measurements are taken between the
left ribs with the patient in a supine or slight right lateral posi-
Follow-up tion. It is the opinion of the expert panel that adequate studies
In patients with chronic hepatitis B virus or hepatitis C virus have not been performed to provide cut-off values at this time.
who have been successfully treated with antiviral drugs, the A review of the existing literature is provided below. In patients
cut-offs obtained in viremic patients should not be used be- with chronic liver disease, splenic measurements should only
cause a rapid decline of stiffness values has been observed in be taken in patients with cACLD as significant portal pressures
these patients, likely due to the decrease of liver inflammation are not expected at lower levels of fibrosis.
(3,5). When liver cirrhosis is evident with B-mode findings, CSPH is predictive of the development of complications of
elastography should not be used to rule out the disease because cirrhosis, including variceal rupture and death. However, it is
a value in the low range of liver stiffness may only indicate a also present in about 50%–60% of patients with compensated
successful response to antiviral treatment. cirrhosis without gastroesophageal varices (12,45). It appears
On the basis of results of both prospective and retrospective that spleen stiffness shows better correlation with portal pressure
studies with more than 1000 patients (37–41), the delta change than does liver stiffness (46). Portal hypertension leads to splenic
Figure 3: (a) Artifacts occur around large blood vessels and bile ducts. These artifacts are not seen in point shear-wave elastog-
raphy (SWE), and therefore measurements should be obtained at least 5 mm from these structures. In two-dimensional SWE, these
artifacts can be identified and avoided. Image on right is velocity map, and image on left is quality map. Arrows indicate artifacts.
Depending on the vendor, artifacts may not be color-coded or appear as areas of increased stiffness (teal). These areas should be
avoided when placing the measurement box. (b) Shear-wave propagation occurs in all directions perpendicular to the acoustic
radiation force impulse (ARFI) pulse. Therefore, artifacts from a blood vessel just out of the image plane can also produce artifacts.
Velocity image (right) shows artifacts in teal (white arrows). These artifacts are most likely from vessels just out of the image plane. The
measurement box should not include these areas. Black arrows point to teal areas at the deep part of the image. These are artifacts
from the ARFI pulse strength decreased due to attenuation, leading to weak shear waves that make it difficult to obtain accurate esti-
mates of shear-wave speed. Note that the quality map (left) in this case suggests high quality throughout the field of view. The quality
map does not identify all artifacts, and both the quality map and velocity map should be evaluated for artifacts.
congestion, increasing splenic stiffness. In fact, portal hyperten- However, there are differences in cut-off values between studies,
sion may cause splenic fibrosis (47). and the level of evidence is still too low to recommend spleen stiff-
In healthy individuals, the spleen is stiffer than the liver. Several ness in the diagnostic work-up of patients with cirrhosis.
studies, most of which were performed with vibration-controlled For ARFI-based techniques, limited studies suggest that
transient elastography, have shown that, in patients with portal abdominal wall thickness and splenic longitudinal diam-
hypertension, spleen stiffness is more reliable than liver stiffness eter are independent predictors of successful spleen stiffness
for assessing the risk of CSPH and esophageal varices (46,48–50). measurement (51,52). The feasibility of performing spleen
Figure 4: Images from two-dimensional shear-wave elastography. Image on left is confidence map, and image on right is veloc-
ity map. When the acoustic radiation force impulse pulse is not perpendicular to the liver capsule, artifacts occur. In this case, the liver
capsule (dashed white line) is not parallel to the transducer (solid white line) or the field-of-view box (red line). The heterogeneous
stiffness measurements in the field of view are due to artifacts occurring because the three lines are not parallel.
Protocol for acquisition: As reported in Table 1, the most important criterion is IQR/M 30% for values in kilopascals and 15% for values
in meters per second. In pediatric patients, the same protocol must be used
Protocol for 2D SWE acquisition in children who are unable to hold their breath: The consensus panel suggests recording a 2D SWE cine
loop for up to 30 seconds if real-time 2D SWE is available, reviewing it, and choosing the image that demonstrates the most stable pattern
for the stiffness measurement. No more than one image should be chosen in each recorded cine loop
Cut-off values: “rule of four” (5, 9, 13, 17 kPa) for the ARFI techniques for viral causes and NAFLD (Table 2)
NAFLD and rare diseases in pediatric patients: The number of published pediatric studies of NAFLD remains low, and the cutoff values for
staging liver fibrosis varies between studies. It is expert opinion that each patient becomes his or her own control, using the stiffness delta
changes over time to evaluate the efficacy of the treatment or the progression of disease—remembering that the measurement reflects stiff-
ness and not fibrosis
Follow-up: The use the delta changes of LS values over time should be used instead of the absolute values. In patients with chronic viral
hepatitis who are successfully treated, the baseline LS stiffness should be that obtained after viral eradication or suppression. A clinically
significant change should be considered when the delta change is greater than 10%. Applying this rule, LS assessment can be suitable for
evaluating all clinical conditions leading to an increase of LS, independent of the disease cause including nonfibrotic causes of LS increase
(eg, congestive heart failure)
Spleen stiffness: It appears that spleen stiffness is better correlated with portal pressure than LS. However, there are differences in cut-off values
between studies and the level of evidence is still low to recommend spleen stiffness in the diagnostic work-up of patients with cirrhosis
Reporting: The report should include the system vendor name, the SWE technique (pSWE or 2D SWE), the probe used, the number of
acquisitions, the IQR/M, and conclusions (Fig 5)
Note.—ARFI = acoustic radiation force impulse, IQR/M = interquartile range–to-median ratio, LS = liver stiffness, NAFLD = non-alcohol-
ic fatty liver disease, pSWE = point SWE, SWE = shear-wave elastography, 2D = two-dimensional.
Pediatric Patients The mean normal shear-wave velocity value ranges from 1.07
The use of a noninvasive technique for staging liver fibrosis is of to 1.16 m/sec (66–68).
great interest because it may avoid liver biopsy, which, in addi- For liver disease associated with cystic fibrosis, autoimmune
tion to its well-known complications, is particularly stressful for hepatitis, biliary atresia and the Kasai procedure, or congeni-
pediatric patients. In the pediatric age group, NAFLD is the most tal heart disease with Fontan surgery or even NAFLD or viral
common cause of chronic liver disease. A 2015 meta-analysis hepatitis, it is expert opinion that each patient becomes his or
(62) determined that the pooled mean prevalence of NAFLD in her own control, using the stiffness delta changes over time to
the United States was 7.6% in the general U.S. pediatric popula- evaluate the efficacy of the treatment or the progression of dis-
tion and that it reached 34.2% in obese children. In one study of ease—remembering that the measurement reflects stiffness and
347 children suspected of having NAFLD who were identified not fibrosis. Results must always be interpreted considering
through screening in primary care and referral to pediatric gas- transaminase values and clinical condition.
troenterology, advanced fibrosis was present in 17% of 193 chil-
dren diagnosed with NAFLD at liver biopsy. Conversely, in 242 Steatosis Assessment
consecutive adolescents undergoing bariatric surgery, the preva- Liver fat content has also been evaluated by using US-based
lence of NAFLD was 58.8%, and 6% of the cohort had definite methods. Several studies have demonstrated proof of concept.
nonalcoholic steatohepatitis. Fibrosis was mild: 81% had none, Although there is insufficient evidence at this time to provide
while 18% had stage 1 or 2 fibrosis (63,64). recommendations regarding the use of US-based methods in
The use of noninvasive techniques in this population is par- this setting, early work suggests that these methods will be
ticularly appealing. However, the number of published pediatric clinically useful (69–73).
studies of NAFLD to date remains low and the cut-off values for
staging liver fibrosis vary between studies (65). Artifacts
For liver stiffness assessment, the procedure used for adults Artifacts are common in ARFI-based techniques and can sig-
should be adopted. In children who are unable to hold their nificantly change the liver stiffness value. It is important to
breath, the consensus panel suggests recording a 2D SWE cine recognize and avoid these artifacts (eg, liver capsule reverbera-
loop for up to 30 seconds if real-time 2D SWE is available, tion artifact [Fig 2], ARFI push artifacts, artifacts from blood
reviewing it, and choosing the image demonstrating the most vessels [Fig 3], and the artifact that occurs when the transducer
stable pattern for the stiffness measurement. No more than one is not parallel to the liver capsule [Fig 4]). Most systems now
image should be chosen in each recorded cine loop. have a confidence map or quality map that helps identify most
For ARFI-based techniques, most published studies have artifacts. However, none of the confidence maps or quality
shown that age has no significant influence on liver stiffness maps depict all artifacts and knowledge of artifacts is crucial
values (66–68). However, there is not enough literature at this for obtaining accurate liver stiffness values. Although a detailed
time for the panel to recommend the rule of four for NAFLD in discussion of artifacts is beyond the scope of this article, it is
pediatric patients. available elsewhere (74–77).
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