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 Table of Contents  
REVIEW ARTICLE
Year : 2021  |  Volume : 23  |  Issue : 2  |  Page : 117-123

Acoustic radiation force impulse (ARFI) in the evaluation of liver fibrosis in chronic liver disease: Where do we stand today?


1 Consultant Radiologist, Department of Imaging, Breach Candy Hospital Trust, Mumbai, Maharashtra, India
2 Gastroenterology Division, Department of Medicine, INHS Asvini, Mumbai, Maharashtra, India

Date of Submission02-Jan-2021
Date of Decision14-May-2021
Date of Acceptance26-May-2021
Date of Web Publication07-Oct-2021

Correspondence Address:
Dr. Surg Cdr Pradipta C Hande
Consultant Radiologist, Breach Candy Hospital Trust, Mumbai, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jmms.jmms_2_21

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  Abstract 


Chronic liver disease (CLD) is common in clinical practice, and the estimation of liver fibrosis (FIB) is crucial for the treatment of these patients. Liver elastography is more widely used in the evaluation of hepatic steatosis and FIB. Acoustic radiation force impulse (ARFIs) are an imaging technique which is available on ultrasonography machines to indicate tissue stiffness of various organs as it correlates with tissue elasticity. Various etiologies can cause moderate-to-severe hepatic FIB which can lead to altered liver function with structural and biochemical abnormalities which eventually result in liver failure. Commercially available ultrasound machines with incorporated ability for shear-wave (SW) technology and available software systems can perform ARFI. Usually, curved array 3.5–4 MHz transducers are used for obtaining SW velocities. We aim to review the clinical applications of ARFI as a noninvasive method using SW velocity measurements to assess the severity of liver FIB in liver parenchymal diseases. In this article, we have discussed the efficacy of quantitative assessment to evaluate the severity of liver disease which has a direct impact on the management and outcome of CLD.

Keywords: Acoustic radiation force impulses, liver elastography, liver stiffness, shear wave


How to cite this article:
Hande PC, Hande V. Acoustic radiation force impulse (ARFI) in the evaluation of liver fibrosis in chronic liver disease: Where do we stand today?. J Mar Med Soc 2021;23:117-23

How to cite this URL:
Hande PC, Hande V. Acoustic radiation force impulse (ARFI) in the evaluation of liver fibrosis in chronic liver disease: Where do we stand today?. J Mar Med Soc [serial online] 2021 [cited 2021 Dec 3];23:117-23. Available from: https://www.marinemedicalsociety.in/text.asp?2021/23/2/117/327561




  Introduction Top


Liver fibrosis (FIB) is the common outcome of chronic inflammatory processes due to multiple etiologies causing pathophysiological responses that can result in cirrhosis. Disruption and remodelling of normal architectural anatomy and accumulation of collagen in severe FIB in chronic liver disease can cause portal hypertension. It is imperative that the early diagnosis and assessment of severity of FIB should be done for adequate and timely treatment of liver disease and prevent irreversible changes which can lead to cirrhosis of the liver. Acoustic radiation force impulses (ARFI) elastography is currently a noninvasive easily available technique using ultrasonography (USG) to evaluate the tissue elasticity of the liver, thereby indicative of the extent of FIB. Vibration-controlled transient elastography (TE) known popularly as FibroScan, when available is a known method for the assessment of liver stiffness[1] measured in kilo-Pascal (kPa). The accuracy of the values is unreliable in extensive steatosis, in obese subjects and ascites.[2],[3]

Liver biopsy with histopathology is the accepted gold standard for the assessment of liver FIB.[4],[5],[6] However, it is an invasive procedure with its complications and also variable reports due to sampling errors and interobserver variability can be a limitation.[7],[8] Furthermore, it cannot be used repeatedly for monitoring and close follow-up unless indicated. The reliability of biochemical serum markers alone has been questioned for early FIB.

Physical principles

ARFI technology uses tissue strain imaging to assess tissue stiffness. Shear waves (SWs) are generated inside a region of interest (ROI) usually of a fixed size (10 mm × 5 mm) on a conventional gray scale ultrasound (US) image in commercially available US machines. Short duration, focused acoustic-push impulse which travel along the main US beam excite the target tissue and create shear stresses which depends on the intensity, frequency, and the nature of the tissue that attenuates (due to absorption) the incident wave.[9] This results in SW that propagate perpendicular to the incident US beam, moving away from the main excitation [Figure 1]. The SW is proportional to the density and shear modulus which in turn is related to the elasticity or stiffness of the interrogated tissue.[9],[10] The peak displacement amplitude is inversely proportional to the elasticity of the tissue. That means softer tissues tend to move farther than stiffer tissue and takes longer to reach the peak displacement and thus recover slower.[10],[11] Tissue response is obtained, time-to-peak displacement and recovery times are monitored and tracked which gives the quantitative estimation of the stiffness of the tissue/organ.[9],[10],[12] Shear-wave propagation velocity is proportional to the square root of tissue elasticity and SW velocity (SWV) measured is expressed in m/s.[13] The tissue stiffness can be evaluated as velocities can be converted and expressed in kPa by multiplying it by a calculated conversion factor which is specified by the manufacturer for each machine.
Figure 1: Acoustic radiation force impulses principle: Transducer generates ultrasound push pulses into the liver (thick arrow) which results in shear waves as it travels through the tissue. Region of interest box placed at a given depth can detect the shear wave as shown, converted into velocity and is a function of the elasticity of the tissue which is indicative of the stiffness of the parenchyma

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  Technique of Performing Acoustic Radiation Force Impulses Elastography Top


ARFI is usually performed with the patient lying in the decubitus position using intercostal window to scan the right lobe of the liver. The examination should be preferably done on an empty stomach applying minimal pressure while scanning with advice to hold the breath.[14] A depth of at least 2–3 cm below the liver capsule is chosen to standardize the examination. The left lobe being close to the heart causes excessive tissue motion by the cardiac pulsations which may disrupt the SWs, and the readings may be variable.[10] The ROI are more superficial, closer to the liver capsule. ROI placement should be as vertical as possible for acquisition of SWV measurements at any particular depth. It is recommended that at least 4 acquisitions of ARFI be performed at varying depths for each segment from the right lobe (segments 5, 6, 7, and 8) for a patient [Figure 2]. The mean SWV and SD values are calculated for reliable measurements for liver stiffness and are reported in a standard format.
Figure 2: (a-d) Shear wave velocity values are increased using acoustic radiation force impulses with acquisitions from varying depths for each segment from the right lobe. (e) Increased liver span is noted suggestive of mild hepatomegaly (f) Portal vein is prominent (12.4mm) in diameter at the porta

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The SWV propagating through the tissues is strongly influenced by the anatomical and physiological factors which can give variable results as also the geometry and anisotropy of the organs.[10] The most relevant intrinsic factor is the wavelength: If lower transmitting frequencies are used, lower frequency pulses are generated, which in turn exert greater acoustic pressure, resulting in faster travelling SWs. The depth is important as significantly lower SWV values were obtained in the deeper portion of the right lobe of the liver in healthy volunteers.[15],[16] The more parallel the ROI is oriented to the main US beam, the higher the SWV results are in a given target organ. In clinical practice, it is important to remember that these variable factors may result in miscalculations and can give erroneous results.


  Discussion Top


The prevalence of chronic liver disease (CLD) is increasing worldwide as also in Asia due to the growing prevalence of nonalcoholic fatty liver disease (NAFLD), alcoholic CLD, and hepatitis B virus, hepatitis C virus (HCV) infection.[17],[18] Diabetes, obesity, and metabolic syndrome also contribute in the increasing population of NAFLD in the Asian–Pacific region.[19] In practice, the degree of liver FIB is an important factor that affects the treatment and prognosis of patients with chronic hepatitis. The use of USG-based elastography can help in the direct and indirect quantification of liver stiffness.[20] In the recent years, several prospective observational studies have published the utility of ARFI for evaluated of liver FIB with biopsy results. The main advantage of ARFI elastography is that it is available on commercially available USG machines. Initial sonography of the liver is important as it gives a baseline assessment of size, margins, and echotexture as also the echogenicity of the liver. Real-time gray scale USG can be performed for the evaluation of hepatic echotexture, whether it is homogeneously increased echogenicity that is suggestive of diffuse fatty infiltration. Focal fat sparing may be seen as focal areas relatively hypoechoic to the surrounding “brighter” parenchyma and usually have geographic margins. These can be detected commonly and need to be differentiated from focal liver lesions which may need to be investigated further. In the same way, if there are patchy areas of increased echogenicity within the liver parenchyma, they may be suggestive of inhomogeneous fatty infiltration which is also not an uncommon finding.

USG can also assess coarse or heterogeneous echotexture. It must be remembered that the value of liver USG and ARFI is not only to assess FIB but as also to indicate cirrhosis and detect the more sinister hepatocellular carcinoma as early as possible. This is where ARFI scores in clinical practice since the ROI can be placed in specific suspicious areas chosen on conventional sonographic images and SWV can be acquired. Histologic activity index was assessed on liver biopsy which has been accepted as the standard using METAVIR scoring system for staging of FIB: F0-no FIB; F1-periportal FIB; F2-Fibrous septa going away from portal areas; F3-bridging FIB; F4-cirrhosis.[21] Several meta-analyses assessed that the measurement of liver stiffness in CLD with TE significantly correlated with degree of FIB on pathology for stages F ≥2.[22],[23],[24] As for its diagnostic performance, many published studies report high accuracy of ARFI in chronic viral and alcoholic liver disease.[22],[25],[26],[27] Meta-analysis study by Bota et al. concluded ARFI elastography gives reliable measurements with similar predictive values to TE for significant FIB and cirrhosis.[2] They proposed cutoff values to predict significant liver FIB and compensated liver cirrhosis.[28] SWV measured by ARFI elastography demonstrated reliable results for estimating liver FIB, even in the presence of steatosis and ascites.[28],[29],[30],[31] ARFI values have been correlated with Aspartate Amino Transferase to Platelet Ratio Index (APRI) values in some studies.

The pooled meta-analysis by Friedrich-Rust et al. suggested ARFI cutoff values for various histological stages of liver FIB.[22] F2 was defined as significant FIB with ARFI values of 1.34 m/s, F 3 as severe FIB with 1.55 m/s and F 4 as cirrhosis with 1.80 m/s, respectively. These cutoff values were compared with the results in a study of 70 patients by Yap et al.[6] Amrapurkar et al.[32] reported in a prospective observational study in 171 patients that mean ARFI was significantly higher (P = 0.001) and had a good predictive value for the diagnosis in Stage 3–4 FIB with 95% confidence interval of 1.31–3.67. However, they found no statistical difference (P = 0.77) in ARFI score between Stage 0 and 1–2 FIB.[32] However, it failed to correlate with lesser degree of FIB. These observations were similar to a study by Yap et al. which assessed ARFI in CLD and showed strong correlation of ARFI values with higher FIB scores.[6] A study in 55 consecutive patients of CLD by Takahashi et al. found that ARFI measurements correlated with histological FIB with confidence (P < 0.0001) in Stage 4 FIB.[30] This was also reported by Haque et al. that ARFI was more accurate for severe FIB and cirrhosis of varying etiologies.[33]

ARFI values are seen to be significantly increased in cholestasis which is suggestive of increased stiffness. Studies have reported reduced specificity for TE in patients with cholestasis, increased serum bilirubin and Alanine transaminase (ALT) levels, obesity with body mass index (BMI) >25 kg/m2 and severe steatosis.[34],[35]

Several studies have been published that have compared ARFI with other noninvasive techniques such as TE.[36] The USG transducer can be placed even in smaller intercostal spaces and even in moderately over weight patients as it requires that the liver is visualized enough so that the ROI can be placed in the hepatic parenchyma (within the maximum depth specified), while with TE the liver must not be more than 25 mm from the skin.[3] Pfeifer et al. reported in a study that patients with raised bilirubin, γGT and increased ALP showed evidence of cholestasis on routine USG also had high SWV on ARFI >1.8 m/s with a mean of 2.91 m/s ± 0.89 m/s with no clinical evidence or signs of cirrhosis.[37] In patients with total bilirubin levels >10 mg/dl, mean ARFI values were higher in the every stage of liver FIB (Stages 1–4). SWV with ARFI did not show significant difference in the study for patients with BMI >25 kg/m2 or ≤25 kg/m2.[32]

Chronic alcohol consumption can result in hepatic steatosis, alcoholic steatohepatitis, steato-FIB, and finally to alcoholic cirrhosis. Laboratory biochemical indices such as aspartate transaminase (AST): ALT ratio >1, APRI (AST-platelet ratio index), and FIB-4 indices are used to monitor the stages of liver FIB in alcoholic liver disease.[38] The US elastography methods have an advantage over serology tests because the results are obtained immediately and cuts out the waiting for laboratory results.

ARFI values correlated well with liver stiffness in all stages of FIB when serum bilirubin was <10 mg/dl, ALT <300 IU/L and patients did not have ascites.[32] Pooled meta-analysis by Bota et al.[39] have shown that mean SWV measurements by ARFI were significantly higher in cirrhotics with ascites than in those with noncirrhotic ascites: 3.04 ± 0.70 versus 1.45 ± 0.59 m/s (P < 0.001). Mean SWV was seen to be higher in patients with ascites; however, the difference was statistically not significant as compared to those without ascites[32] and showed ARFI values were more reliable than TE in patients with ascites. Since USG of the liver can be done in more than one plane, the ROI can be placed appropriately and ARFI is thus less sensitive to the presence of ascites and to obesity as compared with TE.[10]

Even while TE correlates with FIB on liver biopsy, it is reliable in identifying stages F >2.[23],[24] In the diagnosis of F >2, ARFI showed 74% summary sensitivity and 83% summary specificity and in F = 4 these reach up to 87%.[2] The available cutoff values of SW velocities were validated by a study which showed liver stiffness with ARFI has an independent diagnostic ability to perform with AUROC of 0.98 for cirrhosis.[38] A study on ARFI of liver as a screening tool for liver FIB in alcoholic liver disease showed ARFI cutoff values of 1.51 m/s (F >3) and 1.87 m/s (F = 4).[38] Rizzo et al.[40] compared TE and ARFI for noninvasive staging of liver FIB in patients with chronic Hepatitis C and Leung et al.[41] showed comparable results by both methods for quantitative elastography for liver stiffness in Hepatitis B carriers as was reported in other studies by Doherty et al.[42] and Jaffer et al.[43] Friedrich-Rust et al.[44] and Gerber et al.[45] assessed liver FIB in NAFLD and CLD by ARFI and TE methods and reported no significant difference in the values, respectively.

ARFI is a reliable noninvasive assessment in which low SWV allows exclusion of cirrhosis. It is important to understand that SWV values measured by ARFI need to be interpreted as normal or abnormal within a given range. The common measures of statistical dispersion are used effectively for this. Interquartile range which includes 50% of the measurements, excludes extreme values is the difference between the upper and lower quartiles. Standard deviation (SD) shows how much variation there is from the mean (i. e. mean ± SD includes 68.27% of the measurements) of the entire range of values. Studies have emphasized the importance of establishing a quality parameter to make values more reliable. Goertz et al.[46] reported the diagnostic accuracy of ARFI can be improved by applying a maximum SD of 30% of the mean ARFI as a quality parameter for the classification of hepatic FIB. Higher SD may be due to inhomogeneous morphology of the liver parenchyma which is common with changes in hepatic FIB. SWV values with high SD values can be falsely interpreted as extensive or severe FIB and leads to overstaging. The SD should be reflected clearly in the report to make it reliable.

In CLD, prognosis and treatment are related to the stage of hepatic FIB. It is accepted that histopathologic examination is the gold standard to diagnose and confirm liver steatosis, FIB, and cirrhosis. Liver biopsy as the standard method is not only an invasive procedure with known complications but also it has observer variability as is limited by potential sampling errors and needs proper patient selection and preparation.[1],[8]

AASLD (American Association of Study of Liver Diseases) recent guidelines recommend a specimen length of 20 mm, (or better 25 mm) at least 11 portal tracts.[4] This may require more needle passes to meet these criteria[22],[47] which can result in higher risk of procedure-related complications, especially in patients with deranged blood coagulation profiles. Furthermore, liver FIB is a sequential and continuous process, and the staging of liver FIB should be evaluated frequently. In contrast to liver biopsy, ARFI imaging is not invasive and can be repeated many times in the same patient.[3]

The accuracy of ARFI in the prediction of complications of CLD is more controversial. TE has been found to be less sensitive in obese patients with high BMI and in the presence ascites. A study in patients with cirrhosis for portal hypertension and esophageal varices using TE and ARFI by Salzl et al.[48] reported that TE was not reliable for liver stiffness in 22 (25%) patients and ARFI in 1 (1%) patient, due to ascites or obesity. Sensitivity and specificity for ARFI (AUC 0.855) were higher (71.4% and 87.5%, respectively) as compared to other methods.

Some studies have included the value of elastography in predicting high grade from low grade varices in portal hypertension. TE can predict clinically significant portal hypertension; however, it has low specificity to determine esophageal varices. Morishita et al.[49] found ARFI value increased significantly higher in patients with HCV cirrhosis with high risk esophageal varices (P < 0.001) than that for low-risk varices (P < 0.001). Noninvasive methods for diagnosing esophageal varices in cirrhotic patients are required to avoid unnecessary invasive screening endoscopic examinations. In another study, liver ARFI could not correlate with size of varices but splenic ARFI could differentiate between the presence and absence of varices.[32]

ARFI elastography can be used as a screening tool in asymptomatic patients with suspected liver cirrhosis when biochemical tests reveal an abnormality or altered biochemical indices (e.g., APRI and FIB-4).[38] ARFI elastography of the liver can significantly reduce the need for liver biopsy.[1] Liver biopsy is not suitable for repeated evaluations as it is invasive and may cause major complications (0.3%–0.5%).[3]

Fierbinteanu-Braticevici et al.[50] demonstrated that ARFI can predict F3 and F4 stage FIB better. The optimal cutoff value to identify FIB stage F3 or higher was 1.54 m/s, with sensitivity and specificity of 97% and 100%, respectively. The optimal cutoff value in predicting cirrhosis (stage F4) was 1.94 m/s with sensitivity of 100% and specificity of 98.1%. ARFI as TE can help in confirm the diagnosis of cirrhosis[51] with ARFI values >2.6 m/s and TE liver stiffness >14kPa suggest cirrhosis.[1] TE values >21kPa is associated with portal hypertension and its complications[52] and esophageal varices are unlikely if hepatic stiffness is <19.5kPa.[53]

Limitations and pitfalls

ARFI could not differentiate between Stage 0 and early FIB. ARFI values were not reliable in patients with bilirubin >10 mg/dl as also in severely decompensated liver function ALT >300 IU/L. ARFI could not correlate with size of varices, but splenic ARFI could differentiate between the presence and absence of varices.[32] Liver stiffness values are over-estimated in postprandial state, active hepatic inflammation cholestasis, and right heart failure.[1] SW velocities in the left lobe of the liver were found unreliable due to the effect of cardiac pulsations degrading the quality of SW in studies.[54],[55]

Standard cutoff values of SW velocities by ARFI are variable [Table 1].[63] It is difficult for the objective comparison of cutoff values in varied clinical settings and across different US systems produced by different manufacturers. The normal cutoff values must also be adapted from time to time in relation to the clinical and technical settings.[3] Furthermore, the technique of ARFI elastography needs to be standardized with uniform protocols and reporting formats.
Table 1: Mean shear wave velocities values using acoustic radiation force impulse in various studies

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  Conclusion Top


In conclusion, ARFI elastography is a relatively widely available, noninvasive radiological technique which can be used in conjunction with biochemical indices, for assessment of liver stiffness. SWV values by ARFI have a high diagnostic value for significant (F ≥ 2) and severe (F ≥ 3) hepatic FIB and cirrhosis. Various studies have shown that ARFI has an advantage over TE in patients with ascites and in patients with high BMI.

ARFI elastography is a reliable noninvasive method that can be repeated frequently for patients of CLD on follow-up who can be monitored closely to predict advancing FIB and can significantly reduce the need for repeated liver biopsy.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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