ª Springer Science+Business Media, LLC 2017
Abdominal Radiology
Abdom Radiol (2017) DOI: 10.1007/s00261-017-1325-y
LI-RADS technical requirements for CT, MRI, and contrast-enhanced ultrasound Avinash Kambadakone ,1 Alice Fung,2 Rajan Gupta,3 Thomas Hope,4 Kathryn Fowler,5 Andrej Lyshchik,6 Karthik Ganesan,7 Vahid Yaghmai,8 Alexander Guimaraes,2 Dushyant Sahani,1 Frank Miller8 1
Department of Radiology, Massachusetts General Hospital, Harvard Medical School, 55 Fruit Street, White 270, Boston, MA 02114, USA 2 Department of Diagnostic Radiology, Oregon Health and Science University, Portland, OR, USA 3 Department of Radiology, Duke University School of Medicine, Durham, NC, USA 4 Department of Radiology, University of California San Francisco, San Francisco, CA, USA 5 Department of Radiology, Washington University School of Medicine, St Louis, MO, USA 6 Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, PA, USA 7 Department of Radiology, Sir HN Reliance Foundation Hospital and Research Centre, Mumbai, India 8 Department of Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
Abstract Accurate detection and characterization of liver observations to enable HCC diagnosis and staging using LIRADS requires a technically adequate imaging exam. To help achieve this objective, LI-RADS has proposed technical requirements for CT, MR, and contrast-enhanced ultrasound of liver. This article reviews the technical requirements for liver imaging, including the description of minimum acceptable technical standards, such as the scanner hardware requirements, recommended dynamic imaging phases, and common technical challenges of liver imaging. Key words: HCC—LI-RADS—CT—MRI—CEUS
Liver Imaging-Reporting and Data System (LI-RADS) aims to develop a standardized reporting and data collection system, along with minimum acceptable technical parameters for CT, MR, and contrast-enhanced ultrasound (CEUS) imaging of the liver in patients undergoing HCC surveillance. LI-RADS provides definitions and descriptions for the various contrast-enhanced phases which enable a confident diagnosis and staging of HCC
Correspondence to: Avinash Kambadakone; email: akambadakone@ mgh.harvard.edu
and monitoring treatment response using CT, MRI with extracellular agents (ECA), or MRI with hepatobiliary agents (HBA). While the imaging descriptors for the diagnosis of HCC are established and widely utilized in various US and international HCC diagnostic algorithms, the technical requirements for CT, MRI, and CEUS are not yet well defined [1–6]. The availability of a wide range of scanner options and technical parameters renders the goal of developing these technical standards complex and challenging. The Technique Working Group of LI-RADS proposes minimal technical requirements for the performance of CT, MR, and CEUS in order to achieve the delicate balance of wide acceptability as well as diagnostically optimal imaging. The recommendations for technical requirements are mostly evidence-based; however, when high-grade, robust evidence is lacking, consensus expert opinion is considered. The purpose of this review is to discuss the technical recommendations by LI-RADS for optimal liver imaging and the common technical challenges.
Technical specifications for CT Scanner configuration Liver Imaging-Reporting and Data System recommends multi-detector row CT (MDCT) scanner technology with a minimum of 8-detector row for multiphasic examination of the liver (Table 1) [1]. Single-slice CT scanner technology allows liver imaging in the portal venous
A. Kambadakone et al.: LI-RADS technical requirements Table 1. LI-RADS v2017 technical recommendations for CT compared to OPTN Policy 3.6.4.4 Feature Scanner type Detector type Axial reconstructed slice thickness Multi-planar reformations Pre-contrast imaging Dynamic contrast-enhanced phases
Dynamic phases (timing) Contrast considerations
LI-RADS v2017 Multi-detector row scanner Minimum of 8-detector rows £ 5 mm Multi-planar reformations are suggested. Thinner slices with section thickness £ 3 mm are suggested Suggested for initial diagnosis Required for patients treated with locoregional therapy Arterial phase* Portal venous phase Delayed phase Bolus tracking or fixed timed delay is suggested ‡ 300 mgI/mL for a dose of 1.5–2.5 mL/ kg body weight Injection rate of ‡ 3 mL/sec Saline chaser bolus (30–40 mL) with same injection rate Power injector
OPTN recommendations Multi-detector row scanner Minimum of eight-detector rows Minimum of 5 mm No recommendations No recommendations Late arterial phase Portal venous phase Delayed phase (> 120 s after initial injection of contrast) Bolus tracking or timing bolus recommended for accurate timing Minimum of 300 mgI/Ml or higher for a dose of 1.5 mL/kg body weight Minimum injection rate of 3 mL/sec, better, 4–6 mL/sec Saline flush Power injector
IVCM intravenous contrast media * Late arterial phase strongly preferred over early arterial phase
phase, but has limited ability to scan the liver in multiple phases due to slower scan speed and longer acquisition time. Multiphasic liver imaging with single-slice CT scanners has lower sensitivity for detection of focal hepatic lesions, such as dysplastic nodules and HCC, especially lesions < 2 cm [7, 8]. MDCT is superior to singleslice CT, offering advantages such as reduced gantry rotation time and the ability to obtain thinner axial slices. Reduced gantry rotation time allows shorter scan duration, enabling the entire upper abdomen to be scanned during a single comfortable breath hold and permits precise timing of the contrast bolus for optimal acquisition of different hepatic enhancement phases. Faster scan acquisition also reduces motion artifacts, which is particularly crucial for critically ill patients and those with ascites. Thinner, sub-millimeter sections obtained with MDCT scanners result in improved z-axis spatial resolution, reduced partial volume averaging artifacts, and enhanced detection of small lesions. These improvements have contributed to improved tumor detection rates on multiphasic liver imaging with MDCT to be within acceptable range of 90% [9–11]. Increasing the number of detector rows allows acquisition of thinner sections along the z-axis, facilitating the generation of isotropic datasets and reconstruction of multi-planar reformations with sub-millimeter resolution in any desired plane. This, in turn, improves HCC detection, especially small lesions. For example, four-detector row MDCT has an overall sensitivity of 73% for HCC, with the detection rate for lesions < 1 cm below 50%, whereas eight-detector row MDCT has sensitivity of 87% and positive predictive value of 96% for HCC detection in patients undergoing living donor liver transplantation [9–12].
Axial slice thickness Multiphasic CT of the liver with reconstructed axial slice thickness of £ 5 mm is considered the minimum acceptable standard for liver imaging [13]. Reconstructed slice thickness ‡ 6 mm results in signal averaging and contributes to partial volume artifacts, potentially leading to decreased sensitivity for detection of small HCC [9, 14]. Axial slice thickness of £ 5 mm allows the depiction of the smallest resolvable observations as well as provides detailed demonstration of segmental and vascular anatomy of the liver for treatment planning. Thinner sections (< 5 mm) are desirable for improved detection of small lesions and for enhanced quality of multi-planar reformations [9, 15–19].
Multi-planar reformations Multi-planar reformations in the coronal or sagittal planes allow for greater accuracy and confidence in the interpretation of abdomen-pelvic CT scans [14, 20–23]. In patients with cirrhosis, thinner isotropic coronal reformatted images in combination with axial images enhance reader confidence for evaluation of HCC [22]. Multi-planar reformations also permit confident diagnosis of sub-centimeter hepatic cysts that are poorly characterized on axial images [20, 22]. Multi-planar reformations may be helpful to differentiate HCC from other benign entities, such as arterio-portal shunts and perfusion alterations. These entities can have a mass-like configuration on axial scans, and coronal or sagittal planes may more obviously demonstrate the typical wedge-shaped morphology with preserved hepatic and vascular architecture (Fig. 1) [22]. Multi-planar refor-
A. Kambadakone et al.: LI-RADS technical requirements
Fig. 1. Multi-planar reformations. A Axial contrast-enhanced CT image shows an arterially enhancing observation in the dome of liver (arrow). B Coronal and C sagittal reformatted CT images depict the peripheral wedge-shaped nat-
ure of the observation (arrow) helping to characterize the observation as perfusion alteration. Additionally, undistorted vessels coursing through the observation can be seen on the axial and coronal reformatted images.
mations also enhance the assessment of liver observations which are anatomically difficult to evaluate on axial images such as the hepatic dome and inferior tip, particularly in the cirrhotic liver. According to LI-RADS, when the observation margins are more clearly depicted on the multi-planar reformations, they can be used to measure the observation size [22]. Multi-planar reformations with thinner slices could potentially impede the ability to detect smaller lesions due to increased image noise. Hence, a section thickness of 3 mm for multiplanar reformatted images has been reported to provide an optimal balance between improved resolution and higher image noise [22].
standard of care for liver imaging (Table 2) [1, 24]. Higher field strengths magnets (1.5 T or higher) are preferred as they not only allow reliable scanning of the liver in multiple phases (temporal resolution), but also provide a higher spatial and contrast resolution to enable assessment of small hepatic lesions [25–27]. The accuracy for diagnosis and staging of HCC using a 1.5 T MR is comparable to 3.0 T MR with improved dynamic contrast-enhanced image acquisition at 3.0 T [25, 28–32]. There is a paucity of data on the performance of liver MRI at lower field strengths (£ 1 T) [33, 34]. Generally, liver MRI performed at lower field strengths (£ 1 T) has inferior signal-to-noise ratio and image quality [34]. Most of the data for liver MRI at lower field strengths have been for non-contrast examinations which make comparison to higher field strength magnets (1.5 T or higher) difficult. Thus, the strength of the evidence lies in the extensive utilization of 1.5 and 3.0 T MR scanners worldwide for liver imaging [1].
Technical specifications for MR Scanner configuration MR imaging of the liver is typically performed on 1.5 Tesla (T) MR scanners which is an acceptable minimal
A. Kambadakone et al.: LI-RADS technical requirements Table 2. LI-RADS v2017 technical recommendations for MRI compared to OPTN Policy 3.6.4.4 LI-RADS v2017
OPTN recommendations
Contrast MR scanner Coil type Minimum sequences
ECA and HBA 1.5 Tesla or greater Phased array multichannel torso coil Unenhanced T1-weighted OP and IP imaging T2-weighted imaging (Fat suppression optional) Multiphase T1-weighted imaging Pre-contrast imaging Arterial phase* Portal venous phase Delayed phase (or Transitional phase)**
Diffusion-weighted imaging Multi-planar acquisitions Subtraction images Slice thickness
Suggested Suggested Suggested £ 8 mm and inter-slice gap of £ 2 mm for 2D sequences £ 5 mm for dynamic contrast-enhanced series (3D preferable) Bolus tracking or fixed timed delay is suggested
ECA 1.5 Tesla or greater Phased array multichannel torso coil T1-weighted OP and IP imaging T2-weighted imaging (with and without fat saturation) Dynamic post-gadolinium T1-weighted gradient echo sequence (3D preferable) Pre-contrast T1-weighted Late arterial phase Portal venous phase Delayed phase (> 120 s after initial injection of contrast) No recommendations No recommendations No recommendations 5 mm or less for dynamic series, 8 mm or less for other imaging
Feature
Dynamic phase timing
Bolus tracking or timing bolus recommended for accurate timing
HBA hepatobiliary agents, ECA extracellular agents, IP in-phase, OP out-of-phase imaging * Late arterial phase is strongly preferred over early arterial phase ** Delayed phase applies to MRI with extracellular agents and to MRI with extracellular agents with modest hepatocellular uptake (e.g., gadobenate dimeglumine). The term does not apply to MRI with HBA with strong hepatocellular uptake (e.g., gadoxetic acid), for which the term transitional phase is preferred
Type of Coil Phased array multichannel torso coils are required for multiphasic MR examination of the liver (Table 1). Torso phased array coil is constituted by a phased array of multiple surface coils designed for whole volume imaging. Because the phased array coil design improves the signal-to-noise ratio (SNR) and spatial resolution as compared to a body coil, the detection of liver lesions on a 1.5 T MRI is improved with faster acquisition times [35–37]. Phased array coils with specific coil element configurations are capable of parallel imaging which permits considerable reduction in scan time and, therefore, potential for improved temporal resolution [38–40]. High-density surface coils with increasing numbers of elements are desirable, and most modern, state-of-the-art MRI scanners have at least 4-channel and up to 32-channel phased array coils. Higher number of receiver channels in the coil enables higher acceleration factors for parallel imaging and improved SNR [41–43]. Enhanced temporal resolution from parallel imaging enables dynamic multiphasic image acquisition which is required for hepatic lesion characterization and should be used for liver imaging [1].
Axial slice thickness The impact of slice thickness on detection sensitivity for dynamic multiphasic MRI of the liver has not been extensively studied. Thicker slices may have decreased
sensitivity for the detection of small HCC [9, 14]. Thinner slices of < 5 mm have the limitations of increased scan and interpretation time, false positives, and decreased SNR [9, 15–19]. For 2D sequences such as T2-weighted and diffusion-weighted sequences, a slice thickness of £ 8 mm and an inter-slice gap of £ 2 mm are suitable for accurate diagnosis and staging of HCC [1, 44]. Contrastenhanced images should be acquired using a 3-D acquisition, and the slice thickness should be £ 5 mm to achieve high spatial resolution [1, 44]. Technical requirements: contrast-enhanced phases Dynamic contrast-enhanced imaging of the liver in multiple phases is essential to allow diagnosis of a wide range of liver observations. The dual vascular supply of liver (portal venous system, 75% and hepatic arterial system, 25%) results in sequential opacification of the hepatic arteries, followed by the portal veins and the hepatic veins after administration of intravenous contrast. Multiphasic dynamic CT or MRI scanning of the liver is required for the imaging diagnosis of HCC as it allows the depiction of LI-RADS major features such as ‘‘arterial phase hyperenhancement,’’ ‘‘washout appearance,’’ and ‘‘capsule’’ [7, 10, 45–53]. The following sections describe in detail the technical definitions of various contrast-enhanced phases essential for identification of the LI-RADS major features as well as the technical parameters required to achieve these phases (Table 1).
A. Kambadakone et al.: LI-RADS technical requirements
Contrast media considerations: CT. During multiphasic liver CT, the total iodine dose and the rate of delivery of iodinated contrast medium play a vital role in hepatic arterial opacification, enhancement of the liver parenchyma, and detection of hypervascular HCC. While arterial enhancement and detection of hypervascular focal hepatic lesions are mainly dependent on flow rate, hepatic parenchymal enhancement is mainly dependent on total iodine dose [54]. A wide range of intravenous (IV) contrast media (CM) with varying iodine concentrations are available (240–400 mgI/mL). With adjustment of contrast volume, any contrast concentration may be used to administer the optimal iodine dose. For a given contrast dose and injection protocol, lower concentration CM (300–320 mgI/mL) show lower degrees of tumor enhancement and detectability in the late arterial phase than CM with higher concentrations (350–400 mgI/mL) [55, 56]. Moderate or higher iodinated CM concentrations (350 mgI/mL or higher) are desirable for improved detection of hypervascular HCC and enhanced quality of CT scans [55–59]. Contrast dose may be further optimized by using body indices. Although the most suitable body index to determine contrast dose is debatable, weight-based iodine-dosing system have been advocated [57, 58]. The optimal dose of iodinated CM for liver imaging is reported to range between 521 and 647 mg I/kg to generate hepatic parenchymal enhancement of at least 50 Hounsfield Units (HU) which provides superior hepatic imaging quality [60–64]. Higher iodine concentration is preferred in patients with decreased cardiac output, obesity, cirrhosis, or portal vein thrombosis as these co-morbidities result in decreased liver perfusion [65, 66]. In patients with cirrhosis, the use of higher iodine concentration leads to improved lesion to liver contrast and higher average hepatic parenchymal attenuation in the portal venous phase [11, 67]. Higher injection rates (> 2 mL/s) help to increase the magnitude of arterial enhancement and increase the temporal separation of the arterial and portal venous phases [68]. Injection rates > 3 mL/s improve sensitivity for detection of hypervascular HCC, especially for small lesions [69–72]. For optimal dynamic multiphasic CT of the liver, IVCM concentration of 300 mgI/mL or greater with a volume resulting in a dose of 1.5–2.5 mL/kg body weight and an injection rate of 3 mL/sec or higher is
recommended [69–74]. The CM bolus should ideally be followed by a saline chaser bolus (30–40 mL) at the same injection rate to permit efficient CM utilization and improve the degree of contrast enhancement by pushing the residual contrast in the injection tubing and peripheral veins [75–77]. Contrast media considerations: MRI. Dynamic contrast-enhanced (DCE) MRI of the liver can be performed with gadolinium-based extracellular contrast agents (ECA) or hepatobiliary contrast agents (HBA). ECAs are administered intravenously at a dose of 0.1 mmol/kg and are excreted primarily through glomerular filtration. HBAs include gadoxetate disodium (Gd-EOB-DTPA) and gadobenate dimeglumine (Gd-BOPTA) and have both extracellular and hepatobiliary phases with a portion of the administered dose taken up by hepatocytes and excreted into the biliary system. MRI with HBAs not only depicts enhancement characteristics on arterial and portal venous phases similar to that seen with MRI with ECAs, but also provides information in regards to the presence of functioning hepatocytes during the hepatobiliary phase (HBP) (Table 3). This combination of findings improves detection of HCCs [78–80]. Gadoxetate disodium at a dose of 0.025 mmol/kg and gadobenate dimeglumine at a dose of 0.1 mmol/kg provide optimal enhancement characteristics of the liver and focal liver lesions in the dynamic phases and HBP [81–83]. The contrast efficacy and enhancement characteristics of gadobenate dimeglumine are comparable to ECAs for early dynamic imaging, including the delayed phase [84– 91]. Studies of liver MRI with gadobenate dimeglumine and gadoxetate disodium in patients with HCC, cholangiocarcinoma, and metastases have shown comparable contrast enhancement characteristics in the dynamic phases although delayed phase gadoxetate imaging can be confounded by early hepatobiliary excretion [87, 91]. Dynamic phase timing Accurate timing of image acquisition during the various dynamic phases is critical to enable precise determination of liver lesion characteristics and enhancement properties. The optimal scan window for the late hepatic arte-
Table 3. LI-RADS v2017 dynamic contrast enhanced phases for MR imaging with ECA and HBA Contrast agent Required images
Suggested Images
Extracellular agents Gadobenate dimeglumine Multiphase T1-weighted imaging Pre-contrast imaging Arterial phase* Portal venous phase Delayed phase (> 2 min after injection) 1–3 h hepatobiliary phase with gadobenate
* Late arterial phase is strongly preferred over early arterial phase
Gadoxetate disodium Multiphase T1-weighted imaging Pre-contrast imaging Arterial phase* Portal venous phase Transitional phase (2–5 min after injection) Hepatobiliary phase (15–20 min after injection)
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rial and portal venous phases is dependent on the scan and contrast parameters, specifically, contrast injection and volume, and the level and degree of aortic enhancement used for triggering. Bolus tracking and test bolus methods are the most commonly used tools to establish aortic enhancement. Bolus tracking is preferable due to the need for lower CM volume, reduced examination times, and more optimal timing instead of the test bolus method which can decrease the conspicuity of a hepatic lesion [92, 93]. With bolus tracking, once a certain degree of aortic enhancement is reached, a set time delay occurs prior to the acquisition of the hepatic arterial phase. A power injector should be used for dynamic phase timing. While the bolus tracking method is desirable to precisely time the acquisition of various dynamic phases, this technology might not be widely available. Additionally, studies have shown that optimal timing of the arterial phase can be achieved empirically without bolus tracking or test bolus methods if the CM dose is weight-based and the CM is administered over a consistent duration, especially for patients < 70 years of age without cardiovascular disease [69, 71, 73, 94]. As such, in patients without circulatory disturbances, precise timing can be accomplished by using an empirically determined fixed time delay from the start of contrast injection. This technique provides a similar degree of enhancement of the liver, aorta, portal vein, and optimal lesion to liver conspicuity in comparison to bolus tracking methods [71]. However, in the presence of large amount of ascites, venous thrombosis, or cardiovascular co-morbidities, bolus tracking is a suitable option.
Vascular phases Pre-contrast imaging Images acquired before IVCM administration serve to determine the intrinsic CT attenuation or T1 intensity of observations relative to background hepatic parenchyma and act as a baseline to determine imaging findings after contrast enhancement [89, 90, 95]. Pre-contrast imaging additionally provides information on the presence and distribution of fat, iron, calcification, blood products, and iodized oil [89, 90, 95]. While pre-contrast CT imaging may contribute to LI-RADS categorization, the incremental benefit often is low, and the addition of these images increases radiation exposure. The risk–benefit of pre-contrast CT imaging is not established, and LIRADS suggests, but does not mandate, unenhanced CT image acquisition for initial diagnosis of HCC and staging [50, 96, 97]. For liver MRI, however, pre-contrast imaging is required to facilitate determination of enhancement characteristics. For observations that exhibit inherent T1 hyperintensity, subtraction imaging may help in the assessment of arterial phase hyperenhancement [89, 90, 98, 99]. For imaging performed after locoregional therapies for HCC, particularly tran-
scatheter arterial chemoembolization (TACE) with iodized oil, pre-contrast CT imaging is necessary to detect tumor uptake of the embolic material and to differentiate between areas of tumor enhancement versus iodized oil deposits [100]. In patients who have undergone other locoregional therapies such as thermal ablation or selective internal radiation therapy (SIRT), pre-contrast imaging is required for both CT and MRI to assess the treatment zone which is often heterogeneous due to the presence of edema, hemorrhage, and/or necrosis [101].
Late hepatic arterial phase In liver imaging, the arterial phase refers to the hepatic arterial phase unless otherwise specified and corresponds to the phase of contrast enhancement in which the hepatic artery and branches are fully enhanced and the hepatic veins are not enhanced by antegrade flow (Fig. 2). The hepatic arterial phase may be sub-classified into early and late hepatic arterial phases. The late hepatic arterial phase is characterized by fully enhanced portal veins, while the portal veins are unenhanced on the early arterial phase [10, 53, 89, 92]. The late arterial phase is strongly preferred for HCC diagnosis and staging because HCC enhancement is usually greater in the late than in the early arterial phase. In addition, some HCCs show hyperenhancement only in the late arterial phase [10, 48, 53, 88, 89, 102–110]. For these reasons, arterial phase acquisition, preferably in the late arterial phase, is required for liver CT and MRI with ECA and HBA. For optimal image acquisition in the late arterial phase on CT, precise scan timing after contrast injection is essential. The literature includes various reports of ideal time delay between aortic enhancement and appropriate hepatic arterial phase imaging; however, the exam parameters used in these studies vary widely, including the aortic level used for enhancement evaluation, the threshold of aortic enhancement for triggering, the rate and volume of contrast injected, and the number of detector rows of the CTs used [93, 111–114]. Common sites for the aortic level used for enhancement evaluation include the level of L1, celiac axis, and the diaphragmatic hiatus. The threshold of aortic enhancement for triggering ranges between 100 and 150 HU. These variables, thus, result in a wide range of optimal scan delays of 10–30 s after aortic threshold enhancement for the late arterial phase acquisition [46, 71, 93, 111–114]. Using the bolus tracking method, a scan delay of 15–30 s after aortic threshold enhancement of 100–150 HU is suggested for late hepatic arterial phase acquisition. Using a fixed timing delay with an injection rate of 3–5 mL/sec, scanning can be performed at 35–45 s after the start of contrast injection [71, 115]. However, as discussed earlier, the timing of arterial-phase imaging using a fixed time delay can be inaccurate in patients with circulatory
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Fig. 2. Dynamic contrast-enhanced phases on CT and MRI. Axial contrast-enhanced A CT and B MR image depicting late arterial phase with enhancement of aorta, hepatic artery branches (thin white arrow), and intrahepatic portal vein branches (thick white arrow) without enhancement of hepatic veins. Axial contrast-enhanced C CT and D depicting portal venous phase with peak enhancement of liver parenchyma as
well as strong enhancement of portal vein branches and enhancement of hepatic veins (thick black arrow) by antegrade flow. Axial contrast-enhanced E CT and F MR image demonstrating the delayed phase image obtained at 150 s with comparable enhancement of the portal and hepatic veins and of the liver parenchyma which is less than in the portal and venous phase.
disturbances and not recommended in these patients [71, 94]. The late arterial phase acquisition on MR provides suitable enhancement characteristics for liver and focal lesions, including lesion conspicuity and detection of arterial hyperenhancement [87, 89, 91, 116]. The arterial phase acquisition with gadoxetate disodium is technically
challenging and may be suboptimal. The main challenge to the acquisition of a good-quality arterial phase is the volume of the gadoxetate disodium bolus. A contrast bolus of 10 mL (FDA-approved dose) injected at a rate of 2 mL/s may result in temporal mismatch since the data acquisition for a high-resolution arterial acquisition can last for about 20 s. This temporal mismatch can not
A. Kambadakone et al.: LI-RADS technical requirements
only result in truncation artifacts but also make adequate timing even more critical because the filling of the center of k space must coincide with the bolus arrival in the main portal vein in order to achieve a late arterial phase [117]. Another challenge is the respiratory motion artifact affecting hepatic arterial phase described in patients who experience transient severe motion (TSM) in association with IV bolus injection of gadoxetate disodium degrading the quality of arterial phase images [118]. In order to compensate for the smaller contrast volume, either the scan time is shortened or the contrast bolus is stretched by using a lower injection rate, such as 1 mL/s [117, 119]. Another approach to compensate for temporal mismatch is to acquire several (generally 2 or 3) consecutive arterial phases, each with a slightly lower spatial resolution than the other dynamic sequences [120, 121]. Multiple arterial acquisition techniques may not only increase the probability of capturing an adequately timed late arterial phase, but can also reduce the effect of motion artifacts that can, otherwise, impair the quality of arterial datasets [122, 123].
Portal venous phase The portal venous phase demonstrates full and maximal enhancement of the portal veins, enhancement of hepatic veins by antegrade flow, and peak enhancement of the hepatic parenchyma. Portal venous phase is required for multiphasic liver imaging with CT and MRI since this phase is essential for the demonstration of hypo-enhancement of liver observations relative to the liver parenchyma known as ‘‘washout appearance,’’ a LIRADS major feature [86, 88–90, 124, 125]. The portal venous phase contrast efficacy and enhancement characteristics of HBAs are comparable to ECA, thereby enabling accurate evaluation of washout appearance [86, 88–90, 116, 124, 125]. For CT, multiple studies agree that a 45–55 s delay after aortic threshold enhancement (50–120 HU) using a bolus tracking method results in optimal portal venous phase imaging of the liver with satisfactory hepatic parenchymal enhancement [46, 111]. When using fixed timing delay, imaging 60–75 s after the start of injection yields optimal portal venous phase based on an injection rate of 3–5 mL/sec [52, 92, 112, 126, 127]. If injection duration is used with a weightbased dose of contrast, optimal portal venous imaging time is estimated by adding injection duration plus 30 s [70].
Delayed phase The delayed phase is performed after the portal venous phase and demonstrates decreased, but persistent, enhancement of the portal and hepatic veins and the hepatic parenchyma when compared to the portal venous phase. For post-contrast images acquired after portal
venous phase, it is important to be cognizant of the salient differences in the terminology and enhancement characteristics of liver and hepatic vasculature depending on the contrast agents used. The term ‘‘delayed phase’’ applies to multiphasic liver CT, MRI with ECA ,and liver MR performed with gadobenate dimeglumine. Delayed phase imaging improves HCC detection and characterization, particularly for small lesions [46, 47, 50–52, 96]. Because the washout appearance of some HCC is better depicted on delayed phase, a combination of both the portal venous phase and delayed phase is superior to the use of the portal venous phase alone [46, 47, 50–52, 85, 86, 88, 96, 124]. For these reasons, the delayed phase is required for multiphasic CT and MRI of the liver [46, 47, 50–52, 84–86, 88, 96, 124]. During multiphasic liver imaging, a state of equilibrium between the vascular space and the interstitial space occurs within 2–5 min after IVCM injection [128]. Studies validating the use of delayed phase imaging employ various scan delays with most of the studies advocating scanning between 3 and 5 min after contrast injection [46, 47, 52, 127, 129]. Studies demonstrate that at 120 s after injection initiation, hypervascular tumors are almost always hypoattenuating/hypointense to the background liver [112, 130]. Additionally, the liver to tumor contrast is almost constant between 120 and 190 s for both hypervascular and hypovascular HCCs [112]. Therefore, for delayed phase acquisition, scan timing of > 120 s after start of injection is suggested, preferably with a scan delay of 3–5 min [46–48, 50, 52, 96, 97, 131, 132].
Transitional phase The transitional phase refers to post-contrast images acquired after the portal venous phase and before the HBP when performing liver MRI with HBA exhibiting strong hepatocellular uptake such as gadoxetate disodium (Fig. 3). During this phase, the portal and hepatic veins demonstrate persistent, but decreasing enhancement, to a lesser degree than during the portal venous phase, and the liver parenchyma continues to increase in enhancement. Due to the progressive enhancement of hepatic parenchyma following the portal venous phase, the transitional phase with gadoxetate disodium is not analogous to the equilibrium or delayed phase seen in MRI with ECA [133]. While in the delayed phase, the ECAs are equally distributed among the intravascular and extravascular–extracellular compartments, gadoxetate disodium, on the other hand, is distributed among four compartments within the liver, namely the intravascular space, extracellular–extravascular space, intracellular– hepatocyte space, and biliary ductal system [82, 134]. In MR examinations with ECAs, portal venous phase and delayed phase together are superior to portal venous
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Fig. 3. Hepatobiliary phase in a 65-year-old man with cirrhosis. Axial post-gadoxetate disodium MR images in the A arterial and B portal venous phase resemble the enhancement characteristics of MR images with ECA. Axial image in the C transitional phase demonstrates decreasing enhancement of the portal and hepatic veins while the liver
parenchyma continues to increase in enhancement. Axial image in the D hepatobiliary phase depicts the liver parenchyma which is characteristically hyperintense relative to hepatic vasculature and spleen along with contrast excretion into biliary system (arrow).
phase alone for depiction of tumor washout as the washout appearance is better depicted on the delayed phase in some HCCs [85, 86, 88, 124]. For these reasons, with gadoxetate disodium, hypointense signal within an observation during transitional phase is not analogous to true washout, but may actually represent a combination of several enhancement features such as progressive hepatic enhancement, true washout by the observation, and lack of hepatobiliary uptake of contrast by the observation. Transitional phase acquisition with gadoxetate disodium may provide ancillary features favoring malignancy for characterization of focal observations such as ‘‘hepatobiliary phase hypointensity,’’ and, therefore, transitional phase imaging is required for
multiphasic liver MRI performed with gadoxetate disodium [85, 86, 89, 90, 124].
Hepatobiliary phase The hepatobiliary phase (HBP) refers to images obtained after the ‘‘delayed’’ or ‘‘transitional’’ phase in MRI scans performed with HBAs. In the HBP images, the hepatic parenchyma is characteristically hyperintense relative to the hepatic vasculature and the spleen and demonstrates contrast excretion into the biliary system. Enhancement of the hepatic parenchyma during the HBP should be considered suboptimal if the hepatic parenchyma is not unequivocally hyperintense relative to hepatic vascula-
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ture [79, 135]. In general, a combination of dynamic phase with HBP imaging allows improved detection of HCCs, enabling diagnosis of HCCs that do not show washout on earlier dynamic phase imaging [78, 80, 136]. Approximately 50% of administered dose of gadoxetate disodium is excreted via the biliary system and the excretion into the biliary canaliculi can be seen as early as 5 min after contrast administration [82, 83, 137]. In patients with normal liver function, HBP imaging can usually be performed within 15–20 min after gadoxetate disodium injection [138–140]. In contrast, approximately 2% to 5% of the administered dose of gadobenate dimeglumine is excreted via the biliary system [136]. In view of a lower excretion fraction for gadobenate, the hepatobiliary contrast enhancement is most prominent after a delay of 60–120 min, and typically a delay of 60 min consistently provides high-quality hepatobiliary phase imaging [139]. In patients with cirrhosis and severe hepatic dysfunction, HBA excretion by hepatocytes is diminished and delayed, and optimal timing of hepatobiliary phase imaging can be difficult [141]. For such patients, HBP imaging performed at 30 min or more after gadoxetate disodium injection may improve parenchymal enhancement, and patients with severe hepatocyte dysfunction may require HBP imaging as late as 60 min [142]. Similarly, in patients with cirrhosis and severe hepatic dysfunction, hepatobiliary phase imaging performed at 2–3 h after gadobenate may improve parenchymal enhancement [80]. In patients with chronic liver disease, total bilirubin levels ‡ 4.3 mg/dL and direct bilirubin levels ‡ 1.3 mg/dL provide optimal cut-off values for predicting suboptimal HBP and therefore liver MRI with HBAs could be potentially avoided in these patients [143]. Due to increased intrinsic T1 shortening in the liver parenchyma during the HBP, the use of a higher flip angle during the HBP improves T1 contrast. Generally, the flip angle for dynamic sequences ranges from 10 to 15, increasing the flip angle between 35 and 45 on 1.5 T MRI and 25 and 30 on 3T MRI allows improved T1 contrast [144–146].
Chemical shift imaging Unenhanced T1-weighted out-of-phase (OP) and inphase (IP) imaging allows for the detection of intralesional fat and iron and is necessary for the depiction of certain LI-RADS ancillary features (Fig. 4) [95, 147– 149]. IP and OP imaging should be acquired using a dual-echo technique rather than as separate single-echo acquisitions to ensure image co-registration across echoes. While using the dual-echo technique, OP images must be obtained before IP images using a lower echo time (TE) to allow fat and iron differentiation. When OP images are acquired first, signal loss on OP images relative to the IP images is due to the presence of fat, while
signal loss on the IP images relative to the OP images is related to T2* decay, suggesting iron content. However, when the IP images are acquired first at a lower TE, signal loss on the OP images may be due to either fat content or T2* decay.
T2-weighted Imaging T2-weighted imaging remains an important component in liver imaging, providing information about the presence of fluid, fibrosis, and ferromagnetic substances within tissues [150]. T2-weighted imaging improves distinction between solid and non-solid lesions and is necessary for the assessment of a number of ancillary LIRADS features (Fig. 5) [89, 124, 151–153]. For liver MRI, single-shot (SSFSE/HASTE), or multiecho techniques (FSE/TSE) may be performed with or without fat suppression to enable axial and coronal T2-weighted imaging. The T2-weighted images can be acquired using breath-hold or free-breathing techniques [154]. In order to minimize respiratory motion artifacts when using a free-breathing technique, respiratory compensation/respiratory triggering or multiple signal averages should be used [44]. Radial k-space filling techniques decrease the impact of motion on image quality [44]. For T2-weighted imaging, slice thickness of 8 mm and an inter-slice gap of 2 mm may be used although 5 mm thickness is optimal [44].
Diffusion-weighted imaging Diffusion-weighted imaging (DWI) measures tissue diffusivity and demonstrates tumor cellularity. DWI allows improved detection and characterization of focal observations within the liver, permitting differentiation of cysts from solid masses [155]. Combining hyperintensity at DWI to dynamic multiphasic MRI with ECA and HBA has been reported to improve detection and characterization of HCC in patients with chronic liver disease, in particular for tumors < 2 cm (Fig. 6) [156–159]. However, not all HCCs demonstrate restricted diffusion, and the background micro-architecture of the cirrhotic liver shows restricted diffusivity due to the presence of fibrotic tissue, which can influence the conspicuity of HCC at DWI. Accurate determination of histopathological grading of HCC is also challenging with DWI due to considerable overlap of the ADC values and the reduced ADC of the background cirrhotic liver [155, 160– 162]. In patients with HCC presenting with venous thrombus, the benefit of DWI signal characteristics and ADC values in differentiating tumor thrombus from bland thrombus is debatable [163–165]. Additionally, DWI is currently not as robust or widely available as other MRI sequences. Therefore, DWI is considered an optional complementary sequence to dynamic contrastenhanced MRI with ECA or HBA for diagnosis of HCC [166–168]. When acquired, a single-shot echo planar
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Fig. 4. T1-weighted out-of-phase (OP) and in-phase (IP) Imaging. A Axial T1-weighted OP and B IP images demonstrate two masses (thin and thick arrow) in right lobe of liver. Smaller mass measuring 2.4 cm (thin arrow) demonstrates loss of signal on OP images relative to IP images suggesting
intralesional fat. C Late arterial phase and D portal venous phase images show arterial phase hyperenhancement and portal venous phase washout appearance, respectively, of both masses (larger mass measuring 7.2 cm) compatible with diagnosis of HCC (LR-5).
imaging (SS-EPI) sequence with at least two b values (including b = 0–50 and b = 400–1000 s/mm2) should be employed. Using higher b values improves specificity by distinguishing HCC from benign cirrhotic nodules and arterially enhancing pseudolesions for which DWI can be especially useful [162]. To obviate the effect of motion, DWI can be acquired using breath-hold or freebreathing, respiratory-gated techniques, or multiple signal averages [44]. Free-breathing sequences allow acquisition of a higher number of b values, provide higher signal-to-noise ratio, and thinner sections com-
pared to breath-hold sequences, but at the cost of longer acquisition time and motion artifacts [169].
Subtraction imaging Generation of post-processed images by subtraction of pre-contrast from dynamic contrast-enhanced images improves detection of HCC both on CT and MRI [98, 99, 170–175]. Subtraction images are particularly helpful for qualitative determination of arterial hyperenhancement for observations that are inherently T1 hyperintense on MRI (attributed to deposition of fat,
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Fig. 5. T2-weighted imaging. Axial T2-weighted image depicts a right lobe 1.9 cm HCC (arrow) with moderate hyperintense signal on T2-weighted imaging. Mild-moderate T2 hyperintensity is an ancillary feature in LI-RADSÒ v2017.
hemorrhage, glycoprotein, or copper). Using a combination of subtraction and standard images improves detection of hypervascular HCCs including HCCs < 3 cm [98, 173]. Subtraction images generated using portal venous phase and delayed phase can also be used for improved recognition of ‘‘washout appearance’’ or ‘‘capsule’’ feature. Subtraction images can usually be obtained at the scanner console by automatic subtraction of the pre-contrast T1-weighted images from the dynamic T1-weighted images (Fig. 7) [90, 98, 99, 173, 176– 179]. For subtractions to be valid, the unenhanced and contrast-enhanced MR images must be acquired with a
Fig. 6. Diffusion-weighted Imaging. A Axial DWI image (b = 500 s/mm2) and B ADC map depicts a 2.1-cm mass (diagnosis: HCC) which demonstrates diffusion restriction
similar technique and be properly registered [99, 173]. Misregistration between unenhanced and enhanced images can be a source of artifacts and results in falsepositive diagnosis, particularly for nodules at the periphery and dome of liver [99, 173]. Improved co-registration for generation of optimal subtraction images can be facilitated by appropriate patient education prior to scanning and performing image acquisition by breath holding at end expiration [170]. Subtraction images are particularly useful in patients undergoing locoregional therapies for HCC, including thermal ablation and transarterial embolization treatment methods. The assessment of treatment response at the site of ablation or after TACE is rendered challenging due to the presence of post-treatment effects, such as edema, hemorrhage, and necrosis [101, 180]. Use of subtraction images allows accurate assessment of tumor necrosis after locoregional therapies particularly by enabling improved detection of arterial hyperenhancement of residual/recurrent tumors and enhancing reader confidence [170, 175].
Technical considerations for CEUS Ultrasound equipment Ultrasound scanners equipped with appropriate software and hardware packages for contrast-specific imaging should be used. To minimize the disruption of the microbubble contrast agent, CEUS imaging is performed at low acoustic pressures with mechanical index (MI) ranging from 0.05 to 0.3. For comparison, routine ultrasound B-mode imaging is routinely performed with
seen as increased signal on b500 image and dark on ADC map (arrow), an ancillary feature in LI-RADSÒ v2017.
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Fig. 7. Subtraction imaging. A Axial T1-weighted image demonstrates a 2.3-cm hyperintense nodule (arrow) in the dome of liver. The dynamic B arterial phase and C portal venous phase images demonstrate equivocal arterial phase hyperenhancement and portal venous phase washout appearance, respectively, due to intrinsic T1 hyperintensity of
nodule. D and E Subtraction images obtained for the corresponding arterial phase (B–A) and portal venous phase images (C–A) show improved depiction of arterial phase hyperenhancement and portal venous phase washout appearance.
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MI greater than 1, which would be detrimental for ultrasound contrast agents.
Contrast agents Contrast dosing should be based on the manufacturer’s guidelines. The contrast dose is generally 1.2–2.4 mL for sulfur hexafluoride lipid-type A microspheres, and 0.2 mL for Perflutren Lipid Microspheres, both of which may be repeated as necessary to a maximum dose which is weight related. The enhancement may be affected by the patient’s weight, scanner sensitivity to the contrast and transducer frequency. Contrast bolus is delivered over 2–3 s and immediately be followed by a 5–10 mL normal saline flush delivered at the rate of approximately 2 mL/sec.
Scanning technique In general, CEUS is a focused examination to evaluate one or a few observations and not suitable for staging the entire liver. Imaging should be performed in a dual screen format showing a low MI B-mode image alongside the contrast-only display to provide anatomic guidance and to ensure that the target lesion is kept within the field of view during CEUS. Baseline US imaging Patients first undergo baseline ultrasound (US) imaging to identify the observation/nodule and select the appropriate acoustic window for contrast-enhanced ultrasound (CEUS). B-mode measurements and sweeps of the nodule in the transverse and sagittal planes should be acquired. Following baseline imaging, patients undergo CEUS examination of the observation/nodule. CEUS imaging The real-time imaging benefits of CEUS should be utilized for accurate characterization of observation/nodules. Continuous insonation of large portions of highly vascular tissues (i.e., liver) may result in excessive destruction of microbubble contrast agent and substantial decrease in levels of contrast enhancement in late phases. To maximize benefits of real-time CEUS imaging and to preserve enough microbubbles to allow late contrast washout detection, we recommend the following imaging strategy: Continuous focused imaging of the nodule/observation should be performed for the first 60 s to capture peak arterial phase enhancement, characterize arterial phase hyperenhancement, and determine if early washout is present. If early washout is present, its onset should be recorded in seconds. After that, images are acquired intermittently every 30 s to avoid excessive bubble destruction while permitting the detection of late
washout and the characterization of washout degree. Intermittent imaging should be performed until there is an unequivocal clearance of microbubbles from the circulation (at least 4–6 min after injection) to detect mild and late washout, a major feature for LR-5 categorization (Please refer to the review article focused on CEUS LI-RADS for detailed discussion). One limitation of CEUS is the inability to image the entire liver in the arterial phase since only a part of the organ, usually with abnormality visible on pre-contrast B-mode, can be imaged with a single injection. This limitation could potentially be addressed by careful scanning of the entire liver in the delayed phases to detect additional focal areas of late washout as focal hypoenhancing regions in the liver that can be further evaluated in the arterial phase with repeat UCA injections. If the area of washout is associated with a solid nodule visible on B-mode imaging, this nodule could be further characterized in the arterial phase with repeat UCA injections.
Conclusion LI-RADS attempts to standardize the description of radiologic observations of liver pathology and is relevant only if consistent hepatic imaging protocols are used. The LI-RADS Technique Working Group presents protocol and hardware specifications based on evidence or best practices guidelines. Adherence to these recommendations helps guide hepatic imaging. In this way, LIRADS may be used for confident data collection and clear communication among radiologists and other clinicians worldwide to further patient care. Compliance with ethical standards Funding There is no source of funding for this project/review article. The author identifying information is on the title page that is separate from the manuscript. Conflict of interest Avinash Kambadakone declares he has no conflict of interest. Alice Fung declares she has no conflict of interest. Rajan Gupta declares he has no conflict of interest related to this project. Disclosures are: Consultant and Speakers Bureau—Bayer Pharma AG, Consultant—Invivo Corp, Consultant—Halyard Health. Thomas Hope declares he has no conflict of interest related to this project. Disclosures are: Research funding from GE. Kathryn Fowler declares she has no conflict of interest. Andrej Lyshchik declares he has no conflict of interest. Karthik Ganesan declares he has no conflict of interest. Vahid Yaghmai declares he has no conflict of interest. Alexander Guimaraes declares he has no conflict of interest Dushyant Sahani declares he has no conflict of interest related to this project. Disclosures are: Royalties from Elsevier and Research Grant from GE healthcare. Frank Miller declares he has no conflict of interest related to this project. Disclosures are: Research Grant from Siemens (No funds associated). Ethical approval This article does not contain any studies with human participants or animals performed by any of the authors.
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