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)

A. Kambadakone et al.: LI-RADS technical requirements

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

A. Kambadakone et al.: LI-RADS technical requirements

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

A. Kambadakone et al.: LI-RADS technical requirements

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-

A. Kambadakone et al.: LI-RADS technical requirements

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.

References 1. Wald C, Russo MW, Heimbach JK, et al. (2013) New OPTN/ UNOS policy for liver transplant allocation: standardization of

A. Kambadakone et al.: LI-RADS technical requirements

2. 3.

4. 5. 6.

7. 8.

9. 10. 11. 12.

13.

14. 15.

16.

17.

18.

19. 20.

21. 22.

liver imaging, diagnosis, classification, and reporting of hepatocellular carcinoma. Radiology 266(2):376–382 Bruix J, Sherman M (2011) American Association for the Study of Liver D. Management of hepatocellular carcinoma: an update. Hepatology 53(3):1020–1022 Kudo M, Matsui O, Izumi N, et al. (2014) JSH consensus-based clinical practice guidelines for the management of hepatocellular carcinoma: 2014 Update by the Liver Cancer Study Group of Japan. Liver Cancer. 3(3–4):458–468 Lee JM, Park JW, Choi BI (2014) 2014 KLCSG-NCC Korea Practice Guidelines for the management of hepatocellular carcinoma: HCC diagnostic algorithm. Dig Dis 32(6):764–777 Omata M, Lesmana LA, Tateishi R, et al. (2010) Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma. Hepatol Int 4(2):439–474 European Association For The Study Of The (2012) L, European Organisation For R, Treatment Of C. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56(4):908–943 Baron RL, Oliver JH, Dodd GD, et al. (1996) Hepatocellular carcinoma: evaluation with biphasic, contrast-enhanced, helical CT. Radiology 199(2):505–511 Lim JH, Kim CK, Lee WJ, et al. (2000) Detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic livers: accuracy of helical CT in transplant patients. AJR Am J Roentgenol 175(3):693–698 Kawata S, Murakami T, Kim T, et al. (2002) Multidetector CT: diagnostic impact of slice thickness on detection of hypervascular hepatocellular carcinoma. AJR Am J Roentgenol 179(1):61–66 Laghi A, Iannaccone R, Rossi P, et al. (2003) Hepatocellular carcinoma: detection with triple-phase multi-detector row helical CT in patients with chronic hepatitis. Radiology. 226(2):543–549 Murakami T, Kim T, Takamura M, et al. (2001) Hypervascular hepatocellular carcinoma: detection with double arterial phase multi-detector row helical CT. Radiology 218(3):763–767 Maetani YS, Ueda M, Haga H, et al. (2008) Hepatocellular carcinoma in patients undergoing living-donor liver transplantation. Accuracy of multidetector computed tomography by viewing images on digital monitors. Intervirology 51(Suppl 1):46–51 ACR–SPR practice parameter for the performance of computed tomography (CT) of the abdomen and computed tomography (CT) of the pelvis [Internet]. https://www.acr.org/~/media/ACR/ Documents/PGTS/guidelines/CT_Abdomen_Pelvis.pdf Weg N, Scheer MR, Gabor MP (1998) Liver lesions: improved detection with dual-detector-array CT and routine 2.5-mm thin collimation. Radiology. 209(2):417–426 Abdelmoumene A, Chevallier P, Chalaron M, et al. (2005) Detection of liver metastases under 2 cm: comparison of different acquisition protocols in four row multidetector-CT (MDCT). Eur Radiol 15(9):1881–1887 Basilico R, Filippone A, Ricciardi M, Iezzi A, Bonomo L (eds) (2000) Impact of slice thickness on the detection of liver lesions with multislice CT2000 2000/11//undefined. USA: Radiological Soc North Amer Haider MA, Amitai MM, Rappaport DC, et al. (2002) Multidetector row helical CT in preoperative assessment of small (£ 1.5 cm) liver metastases: is thinner collimation better? Radiology 225(1):137–142 Kopka L, Rodenwaldt J, Hamm BK (eds) (2000) Biphasic multislice helical CT of the liver: intraindividual comparison of different slice thickness for the detection and characterization of focal liver lesion. Easton: Radiological Soc North Amer Smith JT, Hawkins RM, Guthrie JA, et al. (2010) Effect of slice thickness on liver lesion detection and characterisation by multidetector CT. J Med Imaging Radiat Oncol 54(3):188–193 Hwang SH, Yu J-S, Chung J-J, Kim JH, Kim KW (2011) Diagnosing small hepatic cysts on multidetector CT: an additional merit of thinner coronal reformations. Korean J Radiol 12(3):341–350 Jaffe TA, Nelson RC, Johnson GA, et al. (2006) Optimization of multiplanar reformations from isotropic data sets acquired with 16-detector row helical CT scanner. Radiology 238(1):292–299 Marin D, Catalano C, De Filippis G, et al. (2009) Detection of hepatocellular carcinoma in patients with cirrhosis: added value of

23.

24. 25. 26.

27. 28.

29.

30.

31.

32. 33. 34.

35. 36. 37. 38. 39. 40. 41. 42. 43. 44.

45.

coronal reformations from isotropic voxels with 64-MDCT. AJR Am J Roentgenol 192(1):180–187 Sandrasegaran K, Rydberg J, Tann M, et al. (2007) Benefits of routine use of coronal and sagittal reformations in multi-slice CT examination of the abdomen and pelvis. Clin Radiol 62(4):340–347 Chang KJ, Kamel IR, Macura KJ, Bluemke DA (2008) 3.0-T MR imaging of the abdomen: comparison with 1.5 T1. RadioGraphics 28(7):1983–1998 Girometti R (2015) 3.0 Tesla magnetic resonance imaging: a new standard in liver imaging? World J Hepatol 7(15):1894 Schindera ST, Merkle EM, Dale BM, Delong DM, Nelson RC (2006) Abdominal magnetic resonance imaging at 3.0 T what is the ultimate gain in signal-to-noise ratio? Acad Radiol 13(10):1236–1243 Soher BJ, Dale BM, Merkle EM (2007) A review of MR physics: 3 T versus 1.5 T. Magn Reson Imaging Clin N Am 15(3):277–290 Kukuk GM, Gieseke J, Weber S, et al. (2011) Focal liver lesions at 3.0 T: lesion detectability and image quality with T2-weighted imaging by using conventional and dual-source parallel radiofrequency transmission. Radiology 259(2):421–428 Lee MH, Kim YK, Park MJ, et al. (2013) Gadoxetic acid-enhanced fat suppressed three-dimensional T1-weighted MRI using a multiecho Dixon technique at 3 tesla: emphasis on image quality and hepatocellular carcinoma detection. J Magn Reson Imaging 38(2):401–410 Ramalho M, Here´dia V, Tsurusaki M, Altun E, Semelka RC (2009) Quantitative and qualitative comparison of 1.5 and 3.0 Tesla MRI in patients with chronic liver diseases. J Magn Reson Imaging 29(4):869–879 Tsurusaki M, Semelka RC, Zapparoli M, et al. (2009) Quantitative and qualitative comparison of 3.0 T and 1.5 T MR imaging of the liver in patients with diffuse parenchymal liver disease. Eur J Radiol 72(2):314–320 Zapparoli M, Semelka RC, Altun E, et al. (2008) 3.0-T MRI evaluation of patients with chronic liver diseases: initial observations. Magn Reson Imaging 26(5):650–660 Reinig JW, Dwyer AJ, Miller DL, et al. (1989) Liver metastases: detection with MR imaging at 0.5 and 1.5 T. Radiology 170(1):149–153 Semelka RC, Simm FC, Recht M, et al. (1991) T1-weighted sequences for MR imaging of the liver: comparison of three techniques for single-breath, whole-volume acquisition at 1.0 and 1.5 T. Radiology 180(3):629–635 Campeau NG, Johnson CD, Felmlee JP, et al. (1995) MR imaging of the abdomen with a phased-array multicoil: prospective clinical evaluation. Radiology 195(3):769–776 Low RN (2007) Abdominal MRI advances in the detection of liver tumours and characterisation. Lancet Oncol 8(6):525–535 Schwartz LH, Panicek DM, Thomson E, et al. (1997) Comparison of phased-array and body coils for MR imaging of liver. Clin Radiol 52(10):745–749 Deshmane A, Gulani V, Griswold MA, Seiberlich N (2012) Parallel MR imaging. J Magn Reson Imaging 36(1):55–72 Keogan MT, Edelman RR (2001) Technologic advances in abdominal MR imaging. Radiology 220(2):310–320 Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P (1999) SENSE: sensitivity encoding for fast MRI. Magn Reson Med. 42(5):952–962 Hardy CJ, Giaquinto RO, Piel JE, et al. (2008) 128-channel body MRI with a flexible high-density receiver-coil array. J Magn Reson Imaging 28(5):1219–1225 Keil B, Wald LL (2013) Massively parallel MRI detector arrays. J Magn Reson 229:75–89 Zhang T, Grafendorfer T, Cheng JY, et al. (2016) A semiflexible 64-channel receive-only phased array for pediatric body MRI at 3T. Magn Reson Med 76(3):1015–1021 ACR–SAR–SPR practice parameter for the performance of magnetic resonance imaging (MRI) of the liver [Internet]. https:// www.acr.org/~/media/ACR/Documents/PGTS/guidelines/MRI_ Liver.pdf Choi BI, Cho JM, Han JK, Choi DS, Han MC (1996) Spiral CT for the detection of hepatocellular carcinomas:relative value of arterial- and late-phase scanning. Abdom Imaging 21(5):440–444

A. Kambadakone et al.: LI-RADS technical requirements

46. Furlan A, Marin D, Vanzulli A, et al. (1001) Hepatocellular carcinoma in cirrhotic patients at multidetector CT: hepatic venous phase versus delayed phase for the detection of tumour washout. Br J Radiol 2011(84):403–412 47. Iannaccone R, Laghi A, Catalano C, et al. (2005) Hepatocellular carcinoma: role of unenhanced and delayed phase multi-detector row helical CT in patients with cirrhosis. Radiology 234(2):460–467 48. Kim SK, Lim JH, Lee WJ, et al. (2002) Detection of hepatocellular carcinoma: comparison of dynamic three-phase computed tomography images and four-phase computed tomography images using multidetector row helical computed tomography. J Comput Assist Tomogr 26(5):691–698 49. Kim T, Murakami T, Hori M, et al. (2002) Small hypervascular hepatocellular carcinoma revealed by double arterial phase CT performed with single breath-hold scanning and automatic bolus tracking. AJR Am J Roentgenol 178(4):899–904 50. Kim T, Murakami T, Takahashi S, et al. (1999) Optimal phases of dynamic CT for detecting hepatocellular carcinoma: evaluation of unenhanced and triple-phase images. Abdom Imaging 24(5):473–480 51. Mitsuzaki K, Yamashita Y, Ogata I, et al. (1996) Multiple-phase helical CT of the liver for detecting small hepatomas in patients with liver cirrhosis: contrast-injection protocol and optimal timing. AJR Am J Roentgenol 167(3):753–757 52. Monzawa S, Ichikawa T, Nakajima H, et al. (2007) Dynamic CT for detecting small hepatocellular carcinoma: usefulness of delayed phase imaging. AJR Am J Roentgenol 188(1):147–153 53. Zhao H, Zhou K-R, Yan F-H (2003) Role of multiphase scans by multirow-detector helical CT in detecting small hepatocellular carcinoma. World J Gastroenterol 9(10):2198–2201 54. Rengo M, Caruso D, De Cecco CN, et al. (2012) High concentration (400 mgI/mL) versus low concentration (320 mgI/mL) iodinated contrast media in multi detector computed tomography of the liver: a randomized, single centre, non-inferiority study. Eur J Radiol 81(11):3096–3101 55. Ha¨nninen EL, Vogl TJ, Felfe R, et al. (2000) Detection of focal liver lesions at biphasic spiral CT: randomized double-blind study of the effect of iodine concentration in contrast materials. Radiology 216(2):403–409 56. Yagyu Y, Awai K, Inoue M, et al. (2005) MDCT of hypervascular hepatocellular carcinomas: a prospective study using contrast materials with different iodine concentrations. AJR Am J Roentgenol 184(5):1535–1540 57. Awai K, Kanematsu M, Kim T, et al. (2016) The optimal body size index with which to determine iodine dose for hepatic dynamic CT: a prospective multicenter study. Radiology 278(3):773–781 58. Brink JA, Heiken JP, Forman HP, et al. (1995) Hepatic spiral CT: reduction of dose of intravenous contrast material. Radiology 197(1):83–88 59. Yamashita Y, Komohara Y, Takahashi M, et al. (2000) Abdominal helical CT: evaluation of optimal doses of intravenous contrast material–a prospective randomized study. Radiology 216(3):718–723 60. Fujigai T, Kumano S, Okada M, et al. (2012) Optimal dose of contrast medium for depiction of hypervascular HCC on dynamic MDCT. Eur J Radiol 81(11):2978–2983 61. Heiken JP, Brink JA, Gaines MV, et al. (1995) Dynamic incremental CT: effect of volume and concentration of contrast material and patient weight on hepatic enhancement. Radiology 195(2):353–357 62. Ichikawa T, Motosugi U, Morisaka H, et al. (2012) Optimal iodine dose for 3-dimensional multidetector-row CT angiography of the liver. Eur J Radiol 81(9):2450–2455 63. Ichikawa T, Okada M, Kondo H, et al. (2013) Recommended iodine dose for multiphasic contrast-enhanced mutidetector-row computed tomography imaging of liver for assessing hypervascular hepatocellular carcinoma: multicenter prospective study in 77 general hospitals in Japan. Acad Radiol 20(9):1130–1136 64. Yanaga Y, Awai K, Nakaura T, et al. (2008) Optimal contrast dose for depiction of hypervascular hepatocellular carcinoma at dynamic CT using 64-MDCT. AJR Am J Roentgenol 190(4):1003–1009

65. Furuta A, Ito K, Fujita T, et al. (2004) Hepatic enhancement in multiphasic contrast-enhanced MDCT: comparison of high- and low-iodine-concentration contrast medium in same patients with chronic liver disease. AJR Am J Roentgenol 183(1):157–162 66. Vignaux O, Legmann P, Coste J, Hoeffel C, Bonnin A (1999) Cirrhotic liver enhancement on dual-phase helical CT: comparison with noncirrhotic livers in 146 patients. AJR Am J Roentgenol 173(5):1193–1197 67. Awai K, Takada K, Onishi H, Hori S (2002) Aortic and hepatic enhancement and tumor-to-liver contrast: analysis of the effect of different concentrations of contrast material at multi-detector row helical CT. Radiology 224(3):757–763 68. Bae KT, Heiken JP, Brink JA (1998) Aortic and hepatic peak enhancement at CT: effect of contrast medium injection rate– pharmacokinetic analysis and experimental porcine model. Radiology 206(2):455–464 69. Erturk SM, Ichikawa T, Sou H, et al. (2008) Effect of duration of contrast material injection on peak enhancement times and values of the aorta, main portal vein, and liver at dynamic MDCT with the dose of contrast medium tailored to patient weight. Clin Radiol 63(3):263–271 70. Ichikawa T, Erturk SM, Araki T (2006) Multiphasic contrastenhanced multidetector-row CT of liver: contrast-enhancement theory and practical scan protocol with a combination of fixed injection duration and patients’ body-weight-tailored dose of contrast material. Eur J Radiol 58(2):165–176 71. Itoh S, Ikeda M, Achiwa M, et al. (2004) Late-arterial and portalvenous phase imaging of the liver with a multislice CT scanner in patients without circulatory disturbances: automatic bolus tracking or empirical scan delay? Eur Radiol 14(9):1665–1673 72. Schima W, Hammerstingl R, Catalano C, et al. (2006) Quadruplephase MDCT of the liver in patients with suspected hepatocellular carcinoma: effect of contrast material flow rate. AJR Am J Roentgenol 186(6):1571–1579 73. Awai K, Hiraishi K, Hori S (2004) Effect of contrast material injection duration and rate on aortic peak time and peak enhancement at dynamic CT involving injection protocol with dose tailored to patient weight. Radiology 230(1):142–150 74. Awai K, Inoue M, Yagyu Y, et al. (2004) Moderate versus high concentration of contrast material for aortic and hepatic enhancement and tumor-to-liver contrast at multi-detector row CT. Radiology 233(3):682–688 75. Dorio PJ, Lee FT, Henseler KP, et al. (2003) Using a saline chaser to decrease contrast media in abdominal CT. AJR Am J Roentgenol 180(4):929–934 76. Schoellnast H, Tillich M, Deutschmann HA, et al. (2003) Abdominal multidetector row computed tomography: reduction of cost and contrast material dose using saline flush. J Comput Assist Tomogr 27(6):847–853 77. Schoellnast H, Tillich M, Deutschmann HA, et al. (2004) Improvement of parenchymal and vascular enhancement using saline flush and power injection for multiple-detector-row abdominal CT. Eur Radiol 14(4):659–664 78. Cortis K, Liotta R, Miraglia R, et al. (2016) Incorporating the hepatobiliary phase of gadobenate dimeglumine-enhanced MRI in the diagnosis of hepatocellular carcinoma: increasing the sensitivity without compromising specificity. Acta Radiol 57(8):923–931 79. Hope TA, Fowler KJ, Sirlin CB, et al. (2014) Hepatobiliary agents and their role in LI-RADS. Abdom Imaging 40(3):613–625 80. Kim YK, Lee JM, Kim CS (2004) Gadobenate dimeglumine-enhanced liver MR imaging: value of dynamic and delayed imaging for the characterization and detection of focal liver lesions. Eur Radiol 14(1):5–13 81. Pirovano G, Vanzulli A, Marti-Bonmati L, et al. (2000) Evaluation of the accuracy of gadobenate dimeglumine-enhanced MR imaging in the detection and characterization of focal liver lesions. Am J Roentgenol 175(4):1111–1120 82. Ringe KI, Husarik DB, Sirlin CB, Merkle EM (2010) Gadoxetate disodium-enhanced MRI of the liver: part 1, protocol optimization and lesion appearance in the noncirrhotic liver. AJR Am J Roentgenol 195(1):13–28

A. Kambadakone et al.: LI-RADS technical requirements

83. Vogl TJ, Ku¨mmel S, Hammerstingl R, et al. (1996) Liver tumors: comparison of MR imaging with Gd-EOB-DTPA and Gd-DTPA. Radiology 200(1):59–67 84. Carlos RC, Kim HM, Hussain HK (2003) Developing a prediction rule to assess hepatic malignancy in patients with cirrhosis. AJR Am J Roentgenol 180(4):893–900 85. Ito K, Honjo K, Fujita T, et al. (1996) Hepatic parenchymal hyperperfusion abnormalities detected with multisection dynamic MR imaging: appearance and interpretation. J Magn Reson Imaging 6(6):861–867 86. Khan AS, Hussain HK, Johnson TD, et al. (2010) Value of delayed hypointensity and delayed enhancing rim in magnetic resonance imaging diagnosis of small hepatocellular carcinoma in the cirrhotic liver. J Magn Reson Imaging 32(2):360–366 87. Kuwatsuru R, Kadoya M, Ohtomo K, et al. (2001) Comparison of gadobenate dimeglumine with gadopentetate dimeglumine for magnetic resonance imaging of liver tumors. Invest Radiol 36(11):632–641 88. Marrero JA, Hussain HK, Nghiem HV, et al. (2005) Improving the prediction of hepatocellular carcinoma in cirrhotic patients with an arterially-enhancing liver mass. Liver Transpl 11(3):281–289 89. Semelka RC, Helmberger TK (2001) Contrast agents for MR imaging of the liver. Radiology 218(1):27–38 90. Willatt JM, Hussain HK, Adusumilli S, Marrero JA (2008) MR imaging of hepatocellular carcinoma in the cirrhotic liver: challenges and controversies. Radiology 247(2):311–330 91. H-m Zhang (2006) Evaluation of Gd-BOPTA and Gd-DTPA in contrast-enhanced MR imaging of the liver. Zhonghua Zhong Liu Za Zhi 28(2):111–115 92. Francis IR, Cohan RH, McNulty NJ, et al. (2003) Multidetector CT of the liver and hepatic neoplasms: effect of multiphasic imaging on tumor conspicuity and vascular enhancement. AJR Am J Roentgenol 180(5):1217–1224 93. Sultana S, Awai K, Nakayama Y, et al. (2007) Hypervascular hepatocellular carcinomas: bolus tracking with a 40-detector CT scanner to time arterial phase imaging. Radiology 243(1):140–147 94. Sharma P, Kalb B, Kitajima HD, et al. (2011) Optimization of single injection liver arterial phase gadolinium enhanced MRI using bolus track real-time imaging. J Magn Reson Imaging 33(1):110–118 95. Mitchell DG, Palazzo J, Hann HW, et al. (1991) Hepatocellular tumors with high signal on T1-weighted MR images: chemical shift MR imaging and histologic correlation. J Comput Assist Tomogr 15(5):762–769 96. Jang H-J, Kim TK, Khalili K, et al. (2013) Characterization of 1-to 2-cm liver nodules detected on hcc surveillance ultrasound according to the criteria of the American Association for the Study of Liver Disease: is quadriphasic CT necessary? AJR Am J Roentgenol 201(2):314–321 97. Luke FE, Allen BC, Moshiri ST, et al. (2013) Multiphase multidetector row computed tomography in the setting of chronic liver disease and orthotopic liver transplantation: can a series be eliminated in order to reduce radiation dose? J Comput Assist Tomogr 37(3):408–414 98. An C, Park M-S, Kim D, et al. (2013) Added value of subtraction imaging in detecting arterial enhancement in small (< 3 cm) hepatic nodules on dynamic contrast-enhanced MRI in patients at high risk of hepatocellular carcinoma. Eur Radiol 23(4):924–930 99. Yu JS, Kim YH, Rofsky NM (2005) Dynamic subtraction magnetic resonance imaging of cirrhotic liver: assessment of high signal intensity lesions on nonenhanced T1-weighted images. J Comput Assist Tomogr 29(1):51–58 100. Bargellini I, Vignali C, Cioni R, et al. (2010) Hepatocellular carcinoma: ct for tumor response after transarterial chemoembolization in patients exceeding milan criteria—selection parameter for liver transplantation. Radiology 255(1):289–300 101. Bajpai S, Kambadakone A, Guimaraes AR, et al. (2015) Imageguided Treatment in the hepatobiliary system: role of imaging in treatment planning and posttreatment evaluation. Radiographics 35(5):1393–1418 102. Ichikawa T, Kitamura T, Nakajima H, et al. (2002) Hypervascular hepatocellular carcinoma: can double arterial phase imaging with

103.

104.

105.

106. 107. 108.

109.

110.

111.

112.

113.

114. 115. 116.

117.

118.

119.

120.

multidetector CT improve tumor depiction in the cirrhotic liver? AJR Am J Roentgenol 179(3):751–758 Mori K, Yoshioka H, Takahashi N, et al. (2005) Triple arterial phase dynamic MRI with sensitivity encoding for hypervascular hepatocellular carcinoma: comparison of the diagnostic accuracy among the early, middle, late, and whole triple arterial phase imaging. AJR Am J Roentgenol 184(1):63–69 Noguchi Y, Murakami T, Kim T, et al. (2002) Detection of hypervascular hepatocellular carcinoma by dynamic magnetic resonance imaging with double-echo chemical shift in-phase and opposed-phase gradient echo technique: comparison with dynamic helical computed tomography imaging with double arterial phase. J Comput Assist Tomogr 26(6):981–987 Oi H, Murakami T, Kim T, et al. (1996) Dynamic MR imaging and early-phase helical CT for detecting small intrahepatic metastases of hepatocellular carcinoma. AJR Am J Roentgenol 166(2):369–374 Shinmura R, Matsui O, Kobayashi S, et al. (2005) Cirrhotic nodules: association between MR imaging signal intensity and intranodular blood supply. Radiology 237(2):512–519 Yamashita Y, Hatanaka Y, Yamamoto H, et al. (1994) Differential diagnosis of focal liver lesions: role of spin-echo and contrast-enhanced dynamic MR imaging. Radiology 193(1):59–65 Yamashita Y, Mitsuzaki K, Yi T, et al. (1996) Small hepatocellular carcinoma in patients with chronic liver damage: prospective comparison of detection with dynamic MR imaging and helical CT of the whole liver. Radiology 200(1):79–84 Yoshioka H, Sato J, Takahashi N, et al. (2004) Dual double arterial phase dynamic MR imaging with sensitivity encoding (SENSE): which is better for diagnosing hypervascular hepatocellular carcinomas, in-phase or opposed-phase imaging? Magn Reson Imaging 22(3):361–367 Yoshioka H, Takahashi N, Yamaguchi M, et al. (2002) Double arterial phase dynamic MRI with sensitivity encoding (SENSE) for hypervascular hepatocellular carcinomas. J Magn Reson Imaging 16(3):259–266 Goshima S, Kanematsu M, Kondo H, et al. (2006) MDCT of the liver and hypervascular hepatocellular carcinomas: optimizing scan delays for bolus-tracking techniques of hepatic arterial and portal venous phases. AJR Am J Roentgenol 187(1):W25–W32 Huang J-S, Pan H-B, Chou C-P, et al. (2008) Optimizing scanning phases in detecting small (< 2 cm) hepatocellular carcinoma: whole-liver dynamic study with multidetector row CT. J Comput Assist Tomogr 32(3):341–346 Kagawa Y, Okada M, Yagyu Y, et al. (2013) Optimal scan timing of hepatic arterial-phase imaging of hypervascular hepatocellular carcinoma determined by multiphasic fast CT imaging technique. Acta Radiol 54(8):843–850 Kim M-J, Choi JY, Lim JS, et al. (2006) Optimal scan window for detection of hypervascular hepatocellular carcinomas during MDCT examination. AJR Am J Roentgenol 187(1):198–206 Adibi A, Shahbazi A (2014) Automatic bolus tracking versus fixed time-delay technique in biphasic multidetector computed tomography of the abdomen. Iran J Radiol 11(1):4617 Besa C, Kakite S, Cooper N, Facciuto M, Taouli B (2015) Comparison of gadoxetic acid and gadopentetate dimeglumineenhanced MRI for HCC detection: prospective crossover study at 3 T. Acta Radiol Open 4(2):2047981614561285 Zech CJ, Vos B, Nordell A, et al. (2009) Vascular enhancement in early dynamic liver MR imaging in an animal model: comparison of two injection regimen and two different doses Gd-EOB-DTPA (gadoxetic acid) with standard Gd-DTPA. Invest Radiol 44(6):305–310 Davenport MS, Viglianti BL, Al-Hawary MM, et al. (2013) Comparison of acute transient dyspnea after intravenous administration of gadoxetate disodium and gadobenate dimeglumine: effect on arterial phase image quality. Radiology 266(2):452–461 Motosugi U, Ichikawa T, Sou H, et al. (2009) Dilution method of gadolinium ethoxybenzyl diethylenetriaminepentaacetic acid (GdEOB-DTPA)-enhanced magnetic resonance imaging (MRI). J Magn Reson Imaging 30(4):849–854 Hope TA, Saranathan M, Petkovska I, et al. (2013) Improvement of gadoxetate arterial phase capture with a high spatio-temporal

A. Kambadakone et al.: LI-RADS technical requirements

121.

122.

123.

124. 125.

126. 127.

128. 129. 130. 131. 132. 133. 134.

135.

136.

137. 138. 139. 140. 141.

resolution multiphase three-dimensional SPGR-Dixon sequence. J Magn Reson Imaging 38(4):938–945 Yoon JH, Lee JM, Yu MH, Kim EJ, Han JK (2016) Triple arterial phase MR imaging with gadoxetic acid using a combination of contrast enhanced time robust angiography, keyhole, and viewsharing techniques and two-dimensional parallel imaging in comparison with conventional single arterial phase. Korean J Radiol 17(4):522–532 Ikram NS, Yee J, Weinstein S, et al. (2017) Multiple arterial phase MRI of arterial hypervascular hepatic lesions: improved arterial phase capture and lesion enhancement. Abdom Radiol 42(3):870–876 Pietryga JA, Burke LMB, Marin D, Jaffe TA, Bashir MR (2014) Respiratory motion artifact affecting hepatic arterial phase imaging with gadoxetate disodium: examination recovery with a multiple arterial phase acquisition. Radiology 271(2):426–434 Krinsky GA, Lee VS (2000) MR imaging of cirrhotic nodules. Abdom Imaging 25(5):471–482 Peterson MS, Baron RL, Murakami T (1996) Hepatic malignancies: usefulness of acquisition of multiple arterial and portal venous phase images at dynamic gadolinium-enhanced MR imaging. Radiology 201(2):337–345 Foley WD, Mallisee TA, Hohenwalter MD, et al. (2000) Multiphase hepatic CT with a multirow detector CT scanner. AJR Am J Roentgenol 175(3):679–685 Liu YI, Kamaya A, Jeffrey RB, Shin LK (2012) Multidetector computed tomography triphasic evaluation of the liver before transplantation: importance of equilibrium phase washout and morphology for characterizing hypervascular lesions. J Comput Assist Tomogr 36(2):213–219 Kormano M, Dean PB (1976) Extravascular contrast material: the major component of contrast enhancement. Radiology 121(2):379–382 Lim JH, Choi D, Kim SH, et al. (2002) Detection of hepatocellular carcinoma: value of adding delayed phase imaging to dualphase helical CT. AJR Am J Roentgenol 179(1):67–73 Niendorf E, Spilseth B, Wang X, Taylor A (2015) Contrast enhanced MRI in the diagnosis of HCC. Diagnostics 5(3):383–398 Karahan OI, Yikilmaz A, Isin S, Orhan S (2003) Characterization of hepatocellular carcinomas with triphasic CT and correlation with histopathologic findings. Acta Radiol 44(6):566–571 Liu YI, Shin LK, Jeffrey RB, Kamaya A (2013) Quantitatively defining washout in hepatocellular carcinoma. AJR Am J Roentgenol 200(1):84–89 Agnello F, Dioguardi Burgio M, Picone D, et al. (2016) Magnetic resonance imaging of the cirrhotic liver in the era of gadoxetic acid. World J Gastroenterol 22(1):103–111 Van Montfoort JE, Stieger B, Meijer DKF, et al. (1999) Hepatic uptake of the magnetic resonance imaging contrast agent gadoxetate by the organic anion transporting polypeptide Oatp1. J Pharmacol Exp Therap 290(1):153–157 Lee NK, Kim S, Kim GH, et al. (2012) Significance of the ‘‘Delayed hyperintense portal vein sign’’ in the hepatobiliary phase MRI obtained with Gd-EOB-DTPA. J Magn Reson Imaging 36(3):678–685 Fu G-L, Du Y, Zee C-S, et al. (2012) Gadobenate dimeglumineenhanced liver magnetic resonance imaging: value of hepatobiliary phase for the detection of focal liver lesions. J Comput Assist Tomogr 36(1):14–19 Van Beers BE, Pastor CM, Hussain HK (2012) Primovist, Eovist: what to expect? J Hepatol 57(2):421–429 EOVIST (Bayer HealthCare Pharmaceuticals Inc.): FDA Package Insert, Page 5. MedLibraryorg. Kirchin MA, Pirovano GP, Spinazzi A (1998) Gadobenate dimeglumine (Gd-BOPTA). An overview. Invest Radiol 33(11):798–809 Malone D, Zech CJ, Ayuso C, et al. (2008) Magnetic resonance imaging of the liver: consensus statement from the 1st International Primovist User Meeting. Eur Radiol Suppl 18(4):849–864 Tschirch FTC, Struwe A, Petrowsky H, et al. (2008) Contrastenhanced MR cholangiography with Gd-EOB-DTPA in patients with liver cirrhosis: visualization of the biliary ducts in comparison with patients with normal liver parenchyma. Eur Radiol 18(8):1577–1586

142. Cruite I, Schroeder M, Merkle EM, Sirlin CB (2010) Gadoxetate disodium-enhanced MRI of the liver: part 2, protocol optimization and lesion appearance in the cirrhotic liver. AJR Am J Roentgenol 195(1):29–41 143. Kobi M, Paroder V, Flusberg M, Rozenblit AM, Chernyak V (2017) Limitations of GD-EOB-DTPA-enhanced MRI: can clinical parameters predict suboptimal hepatobiliary phase? Clin Radiol 72(1):55–62 144. Bashir MR, Merkle EM (2011) Improved liver lesion conspicuity by increasing the flip angle during hepatocyte phase MR imaging. Eur Radiol 21(2):291–294 145. Frydrychowicz A, Nagle SK, D’Souza SL, Vigen KK, Reeder SB (2011) Optimized high-resolution contrast-enhanced hepatobiliary imaging at 3 tesla: a cross-over comparison of gadobenate dimeglumine and gadoxetic acid. J Magn Reson Imaging 34(3):585–594 146. Nagle SN, Busse RF, Brau AC, et al., editors. High-Resolution Free-Breathing 3D T1 Weighted Hepatobiliary Imaging Optimized for Gd-EOB-DTPA2009 2009. 147. Earls JP, Theise ND, Weinreb JC, et al. (1996) Dysplastic nodules and hepatocellular carcinoma: thin-section MR imaging of explanted cirrhotic livers with pathologic correlation. Radiology 201(1):207–214 148. Kelekis NL, Semelka RC, Woosley JT (1996) Malignant lesions of the liver with high signal intensity on T1-weighted MR images. J Magn Reson Imaging 6(2):291–294 149. Kelekis NL, Semelka RC, Worawattanakul S, et al. (1998) Hepatocellular carcinoma in North America: a multiinstitutional study of appearance on T1-weighted, T2-weighted, and serial gadolinium-enhanced gradient-echo images. AJR Am J Roentgenol 170(4):1005–1013 150. Matos AP, Velloni F, Ramalho M, et al. (2015) Focal liver lesions: practical magnetic resonance imaging approach. World J Hepatol 7(16):1987–2008 151. Ito K (2006) Hepatocellular carcinoma: conventional MRI findings including gadolinium-enhanced dynamic imaging. Eur J Radiol 58(2):186–199 152. Larson RE, Semelka RC, Bagley AS, et al. (1994) Hypervascular malignant liver lesions: comparison of various MR imaging pulse sequences and dynamic CT. Radiology 192(2):393–399 153. Low RN, Francis IR, Sigeti JS, Foo TK (1993) Abdominal MR imaging: comparison of T2-weighted fast and conventional spinecho, and contrast-enhanced fast multiplanar spoiled gradientrecalled imaging. Radiology 186(3):803–811 154. Yoshikawa T, Mitchell DG, Hirota S, et al. (2006) Focal liver lesions: breathhold gradient- and spin-echo T2-weighted imaging for detection and characterization. J Magn Reson Imaging 23(4):520–528 155. Miller FH, Hammond N, Siddiqi AJ, et al. (2010) Utility of diffusion-weighted MRI in distinguishing benign and malignant hepatic lesions. J Magn Reson Imaging 32(1):138–147 156. Inchingolo R, De Gaetano AM, Curione D, et al. (2015) Role of diffusion-weighted imaging, apparent diffusion coefficient and correlation with hepatobiliary phase findings in the differentiation of hepatocellular carcinoma from dysplastic nodules in cirrhotic liver. Eur Radiol 25(4):1087–1096 157. Park MJ, Kim YK, Lee MH (2013) Lee JHWJ. Validation of diagnostic criteria using gadoxetic acid-enhanced and diffusionweighted MR imaging for small hepatocellular carcinoma (£ 2.0 cm) in patients with hepatitis-induced liver cirrhosis. Acta Radiol 54(2):127–136 158. Park MJ, Kim YK, Lee MW, et al. (2012) Small hepatocellular carcinomas: improved sensitivity by combining gadoxetic acidenhanced and diffusion-weighted MR imaging patterns. Radiology 264(3):761–770 159. Piana G, Trinquart L, Meskine N, et al. (2011) New MR imaging criteria with a diffusion-weighted sequence for the diagnosis of hepatocellular carcinoma in chronic liver diseases. J Hepatol 55(1):126–132 160. Heo SH, Jeong YY, Shin SS, et al. (2010) Apparent diffusion coefficient value of diffusion-weighted imaging for hepatocellular carcinoma: correlation with the histologic differentiation and the expression of vascular endothelial growth factor. Korean J Radiol 11(3):295–303

A. Kambadakone et al.: LI-RADS technical requirements

161. Khatri G, Merrick L, Miller FH (2010) MR imaging of hepatocellular carcinoma. Magn Reson Imaging Clin N Am 18(3):421–450 162. Lim KS (2014) Diffusion-weighted MRI of hepatocellular carcinoma in cirrhosis. Clin Radiol 69(1):1–10 163. Ahn J-H, Yu J-S, Cho E-S, et al. (2016) Diffusion-weighted MRI of malignant versus benign portal vein thrombosis. Korean J Radiol 17(4):533–540 164. Catalano OA, Choy G, Zhu A, Hahn PF, Sahani DV (2010) Differentiation of malignant thrombus from bland thrombus of the portal vein in patients with hepatocellular carcinoma: application of diffusion-weighted MR imaging. Radiology 254(1):154–162 165. Sandrasegaran K, Tahir B, Nutakki K, et al. (2013) Usefulness of conventional MRI sequences and diffusion-weighted imaging in differentiating malignant from benign portal vein thrombus in cirrhotic patients. AJR Am J Roentgenol 201(6):1211–1219 166. Gourtsoyianni S, Papanikolaou N, Yarmenitis S, et al. (2008) Respiratory gated diffusion-weighted imaging of the liver: value of apparent diffusion coefficient measurements in the differentiation between most commonly encountered benign and malignant focal liver lesions. Eur Radiol 18(3):486–492 167. Koh D-M, Takahara T, Imai Y, Collins DJ (2007) Practical aspects of assessing tumors using clinical diffusion-weighted imaging in the body. Magn Reson Med Sci 6(4):211–224 168. Taouli B (2012) Diffusion-weighted MR imaging for liver lesion characterization: a critical look. Radiology 262(2):378–380 169. Schmid-Tannwald C, Oto A, Reiser MF, Zech CJ (2013) Diffusion-weighted MRI of the abdomen: current value in clinical routine. J Magn Reson Imaging 37(1):35–47 170. Kim S, Mannelli L, Hajdu CH, et al. (2010) Hepatocellular carcinoma: assessment of response to transarterial chemoembolization with image subtraction. J Magn Reson Imaging 31(2):348–355 171. Nakaura T, Awai K, Yanaga Y, et al. (2008) Detection of early enhancement of hypervascular hepatocellular carcinoma using single breath-hold 3D pixel shift dynamic subtraction MDCT. AJR Am J Roentgenol 190(1):W13–W18

172. Okumura E, Sanada S, Suzuki M, Takemura A, Matsui O (2011) Effectiveness of temporal and dynamic subtraction images of the liver for detection of small HCC on abdominal CT images: comparison of 3D nonlinear image-warping and 3D global-matching techniques. Radiol Phys Technol 4(2):109–120 173. Sec¸il M, Obuz F, Altay C, et al. (2008) The role of dynamic subtraction MRI in detection of hepatocellular carcinoma. Diagn Interv Radiol 14(4):200–204 174. Sundarakumar DK, Wilson GJ, Osman SF, Zaidi SF, Maki JH (2015) Evaluation of image registration in subtracted 3D dynamic contrast-enhanced MRI of treated hepatocellular carcinoma. AJR Am J Roentgenol 204(2):287–296 175. Winters SD, Jackson S, Armstrong GA, et al. (2012) Value of subtraction MRI in assessing treatment response following imageguided loco-regional therapies for hepatocellular carcinoma. Clin Radiol 67(7):649–655 176. Gupta RT, Brady CM, Lotz J, Boll DT, Merkle EM (2010) Dynamic MR imaging of the biliary system using hepatocyte-specific contrast agents. AJR Am J Roentgenol 195(2):405–413 177. Lee VS, Lavelle MT, Rofsky NM, et al. (2000) Hepatic MR imaging with a dynamic contrast-enhanced isotropic volumetric interpolated breath-hold examination: feasibility, reproducibility, and technical quality. Radiology 215(2):365–372 178. Rofsky NM, Lee VS, Laub G, et al. (1999) Abdominal MR imaging with a volumetric interpolated breath-hold examination. Radiology 212(3):876–884 179. Yu J-S, Rofsky NM (2003) Dynamic subtraction MR imaging of the liver: advantages and pitfalls. AJR Am J Roentgenol 180(5):1351–1357 180. Lee SR, Kilcoyne A, Kambadakone A, Arellano R (2016) Interventional oncology: pictorial review of post-ablation imaging of liver and renal tumors. Abdom Radiol 41(4):677–705