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1 Gastrointestinal Imaging Original Research Jang et al. Multiphase CT in HCC Gastrointestinal Imaging Original Research Hyun-Jung Jang 1 Tae Kyoung Kim 1 Korosh Khalili 1 Leyla Yazdi 1 Ravi Menezes 1 Seong Ho Park 2 Morris Sherman 3 Jang HJ, Kim TK, Khalili K, et al. Keywords: cirrhosis, hepatocellular carcinoma (HCC), multiphasic CT, practice guidelines DOI: /AJR Received June 3, 2012; accepted after revision September 26, Department of Medical Imaging, University of Toronto, Toronto General Hospital, 585 University Ave, Toronto, ON M5G 2N2, Canada. Address correspondence to H. J. Jang (hyun-jung.jang@uhn.ca). 2 Department of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea. 3 Department of Gastroenterology, University of Toronto, Toronto General Hospital, Toronto, ON, Canada. AJR 2013; 201: X/13/ American Roentgen Ray Society 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? OBJECTIVE. The purpose of this study was to identify the essential number of phases from multiphasic CT for 1- to 2-cm hepatocellular carcinoma (HCC) on surveillance ultrasound and to compare the results with the American Association for the Study of Liver Disease (AASLD) standard (arterial phase hypervascularity and portal venous phase [PVP] or delayed phase hypovascularity). MATERIALS AND METHODS. The study included 110 newly detected nodules (1 2 cm; 36 HCC, 74 benign) in 96 patients detected in an HCC surveillance program. Three radiologists prospectively evaluated the attenuation of each nodule relative to the liver on each phase of quadriphasic CT. Univariate and multivariate logistic regression analyses were used to identify parameters associated with HCC. Multiple combinations of phases were compared with the AASLD standard. RESULTS. Only arterial phase hypervascularity and delayed phase hypovascularity were significantly associated with HCC both on univariate (odds ratio, arterial phase 7.51 [95% CI, ]; delayed phase, 2.80 [ ]) and multivariate analyses (arterial phase, [ ]; delayed phase, 4.39 [ ]). The combination of arterial phase and delayed phase yielded the highest specificity (99%) and sensitivity (57%). There was no significant difference between AASLD standard (sensitivity, 57%; specificity, 98%) versus biphasic (arterial phase hypervascularity and delayed phase hypovascularity: sensitivity, 57%; p = 1 and specificity, 99%; p = 0.32), triphasic (arterial phase hypervascularity and unenhanced or PVP hypovascularity: sensitivity, 53%; p = and specificity, 97%; p = 0.32), or quadriphasic combination (arterial phase hypervascularity and unenhanced, PVP or delayed phase hypovascularity: sensitivity, 57%; specificity, 97%), whereas the sensitivity of biphasic arterial phase and PVP was significantly lower (39% vs 57%, p = 0.022). CONCLUSION. For diagnosing 1- to 2-cm HCC detected on surveillance ultrasound, arterial phase and delayed phase are two essential phases, providing higher sensitivity than the combination of arterial phase and PVP, and equal performance with triphasic and quadriphasic combinations. The biphasic combination of arterial phase and delayed phase may replace quadriphasic CT recommended by AASLD. N oninvasive diagnosis of typical hepatocellular carcinoma (HCC) on the basis of imaging without biopsy has become a routine practice in many institutions [1 6]. This approach requires diagnostic criteria and imaging protocols that provide high specificity and reasonable sensitivity for diagnosing HCC [3, 4, 6]. Arterial hypervascularity is an essential feature of HCC. The depiction of washout is also crucial because most small arterial-enhancing foci with no washout on CT are not HCC and many of them are benign vascular shunting in liver cirrhosis [7 9]. The practice guidelines of the American Association for the Study of Liver Disease (AASLD) [3] define typical HCC as a nodule with arterial hypervascularity and washout in the later phases negative enhancement compared with the liver parenchyma. Imaging is an integral part of the practice guidelines of AASLD, which suggest aggressive workup and treatment of small nodules 1 cm or larger in patients at risk for developing HCC. Because of frequent overlapping features between benign nodules and HCC, the previous guidelines suggested the diagnosis of HCC for all 1- to 2-cm nodules requires coincidental findings on two dynamic contrast-enhanced studies [2]. Be- 314 AJR:201, August 2013

2 Multiphase CT in HCC cause the recent data show that typical HCC can be diagnosed by a single dynamic study with high specificity even for small (1 2 cm) nodules [5], the updated guidelines allow a definitive imaging diagnosis of all nodules 1 cm or larger if the nodule shows a typical appearance on a single dynamic study [3]. It is crucial to standardize the CT protocol to properly document the existence of HCC noninvasively because all atypical lesions should undergo invasive biopsy or resourceintensive follow-up [2, 5]. When multiphasic studies became available with the advent of helical CT, many studies proved the critical value of the arterial phase in addition to the conventional portal venous phase (PVP) for the detection of hypervascular HCC [10, 11], and a biphasic combination of arterial phase and PVP became the standard. Later, several studies investigated the additional value of unenhanced or delayed phase to the standard biphasic protocol. Unenhanced CT has been reported to be ineffective [12, 13], whereas several studies have found delayed phase a valuable addition in the diagnosis of HCC [13 16], although some have reported the opposite [17]. Currently, the CT protocol for this indication is variable and the standard protocol based on worldwide consensus is not established. Nodules detected on surveillance ultrasound for 32-month period 378 nodules in 271 patients 1- to 2-cm nodules on surveillance ultrasound 200 nodules in 161 patients CT performed 177 nodules in 144 patients 1- to 2-cm nodules on quadriphasic CT 130 nodules in 110 patients Final study population 110 nodules in 96 patients The updated AASLD guidelines recommend quadriphasic CT, a combination of unenhanced, arterial phase, PVP, and delayed phase, as a mandatory standard protocol [3]. This recommendation needs to be validated by a new study based on systematic implementation of the guideline for several reasons. First, the CT protocol derives from expert opinion rather than the systematic analysis of data, with the assumption that the inclusion of all four phases would achieve better performance than the combination of fewer phases. However, additional ionizing radiation due to multiphasic CT should be taken into account because the patients undergoing HCC surveillance are likely to have more follow-up CT studies for their nodule than patients on a transplantation list or in an advanced stage of HCC. Second, the performance of CT protocols needs to be newly assessed because previous studies comparing various combinations of multiphasic CT used their own arbitrary diagnostic criteria for HCC, including nonhypervascular or no washout HCC [12 15, 17]. Furthermore, prior studies retrospectively selected patients either with a suspected HCC from a CT database or with confirmed HCC from a pathology database. These studies may not be applicable to the current practice guidelines for CT not performed 23 nodules in 17 patients Typical hemangioma in contrast-enhanced ultrasound or MRI (n = 20) in 15 patients CT IV contrast agent contraindicated (n = 3) in two patients Typical hemangioma on CT (n = 24) in 19 patients Incomplete four phases (n = 23) in 15 patients No confirmation of diagnosis Less than 18 months of follow-up (n = 15) in 11 patients Local ablation therapy with no histologic confirmation or recurrence (n = 5) in three patients surveillance [13 16]. Third, the appearance on unenhanced CT is not defined in the diagnostic criteria in the AASLD practice guidelines, yet it is included in the protocol. The purpose of this study was to identify the essential number of phases from multiphasic CT for diagnosing small (1 2 cm) HCC found on surveillance ultrasound and to compare it with AASLD practice guidelines by measuring the performance of each phase and various combinations. Materials and Methods Subjects The research ethics board of our institution approved this retrospective analysis of a prospective clinical cohort of the HCC surveillance program on the basis of systematic implementation of the AASLD practice guidelines published in 2005 [2] in a single tertiary care center. Informed consent was waived because the surveillance protocol was formally accepted as a standard practice in our institution. According to the protocol, all nodules measuring 1 2 cm detected on ultrasound surveillance for HCC in our institution were prospectively further investigated with CT as well as MRI and contrast-enhanced ultrasound. All detected nodules were treated or followed up with imaging prospectively depending on the diagnosis. Benign nodules (74/110, 67%) 74 nodules in 66 patients Histopathology (n = 16) No growth 18 months (n = 58) HCC (36/110, 33%) 36 nodules in 30 patients Histopathology (n = 23) Interval growth (n = 11) Recurrence after local treatment (n = 2) Fig. 1 Flowchart shows study population. HCC = hepatocellular carcinoma. AJR:201, August

3 Jang et al. The inclusion criteria for nodules were as follows: detected on HCC surveillance ultrasound in our institution; 1 2 cm in size; further evaluated with standardized quadriphasic CT; other than typical hemangioma on imaging; and final diagnosis confirmed by histopathology or follow-up imaging at a minimum of 18 months. For a 32-month period between January 2006 and August 2008, 378 new nodules in 271 patients were detected by surveillance ultrasound that was performed for patients at risk for developing HCC. There were 200 nodules measuring 1 2 cm in 161 patients. After excluding 90 nodules in 65 patients that did not meet the inclusion criteria (Fig. 1), a total of 110 nodules in 96 patients (1.1 nodules per patient) finally made up our study population. The patient population included 56 men and 40 women with a mean age of 58 years (age range, years). The causes of liver disease were hepatitis B (n = 53), hepatitis C (n = 30), nonalcoholic steatohepatitis (n = 5), autoimmune hepatitis (n = 4), or others (n = 4). Most of the patients had Child-Pugh class A disease (n = 91, 95%) and the remaining patients had Child-Pugh class B (n = 5, 5%). Reference Standard A nodule was considered malignant if there was histologic proof, growth on follow-up imaging by at least 30% in diameter of the nodule at detection, or recurrence or metastasis after local ablation therapy performed within 6 months after CT. A nodule was considered nonmalignant if there was histologic proof or stability on followup imaging for a minimum of 18 months. Followup imaging was performed every 3 months for 18 months and every 6 months thereafter. CT Technique All imaging was performed using a 64-MDCT scanner (Aquilion 64, Toshiba Medical Systems). Scanning parameters were 120 kvp, approximately mas adjusted according to patient size (minimum 80 to maximum 440 mas [Sure Exposure, Toshiba Medical Systems), 0.5-mm section collimation, and pitch factor of during a single breath-hold volumetric acquisition. Images were obtained in a craniocaudal direction and reconstructed with 5-mm slice thickness and 2.5-mm intervals. Nonionic isosmolar iodinated contrast material (iodixanol, Visipaque 320, GE Healthcare) at 2 ml/kg with a maximum dose of 180 ml was injected through the antecubital vein at a rate of 5 ml/s. Using a bolus tracking system (Sure Start, Toshiba Medical Systems) with a trigger of the aorta reaching 100 HU, a four-phase scan was obtained with unenhanced, arterial phase (20 seconds after the trigger), PVP (60 seconds after the trigger), and delayed phase (180 seconds after the start of contrast injection) images. Image Analysis The relative attenuation of a nodule to the hepatic parenchyma on each phase of quadriphasic CT was determined prospectively by three abdominal radiologists who had 9 14 years of experience in abdominal imaging by consensus. Because this prospective analysis was part of our clinical protocol, the readers were not blinded to the patient s clinical information. The readers were allowed to change the window level and width of the CT images and also allowed to compare each phase for accurate localization of a nodule. When there was mixed attenuation within a nodule on arterial phase, partial hyperattenuation within a nodule was regarded as a positive finding. Likewise, partial hypoattenuation within a nodule was regarded as a positive finding on unenhanced, PVP, or delayed phase. Statistical Analysis Based on the definition in the AASLD practice guidelines of typical HCC hypervascularity in arterial phase and washout in PVP or delayed phase a positive finding for HCC on each phase in this study was hyperattenuation relative to parenchyma (hereafter referred to as hypervascularity ) on arterial phase and hypoattenuation relative to parenchyma (hereafter referred to as hypovascularity ) on unenhanced, PVP, or delayed phase. Univariate logistic regression analysis was used to identify which of the individual CT findings was predictive of malignancy. Odds ratios (ORs) with CIs were calculated for each variable; significance was defined as p < Because of the limited sample size, we decided to use a parsimonious approach to multivariate logistic regression analysis [18]. As a result, the only variables that were considered for inclusion in the multivariate model were those found to be significantly associated with outcome in univariate analysis. Generalized estimating equations were used for all logistic regression analyses to adjust for the correlation between multiple nodules within a patient [19]. Sensitivity, specificity, and corresponding 95% CI of each combination were calculated for the diagnosis of HCC, again adjusted for within-patient clustering. The sensitivity and specificity of each combination were also compared with those of the AASLD guidelines (arterial phase hypervascularity and washout TABLE 1: Univariate and Multivariate Analyses of Association Between CT Findings and Final Diagnosis CT Finding Malignant (n = 36) Nonmalignant (n = 74) Univariate Analysis Multivariate Analysis OR 95% CI p OR 95% CI p Unenhanced Hypoattenuation 25 (69) 23 (31) Iso- or hyperattenuation 11 (31) 51 (69) 1.00 Arterial phase Hyperattenuation 23 (64) 12 (16) < < Iso- or hypoattenuation 13 (36) 62 (84) PVP Hypoattenuation 23 (64) 33 (45) Iso- or hyperattenuation 13 (36) 41 (55) 1.00 Delayed phase Hypoattenuation 30 (83) 34 (46) Iso- or hyperattenuation 6 (17) 40 (54) Note Data in parentheses are percentages. All odds ratios (ORs), 95% CIs, and p values adjusted for clustering effect. Attenuation is relative to parenchyma. PVP = portal venous phase. 316 AJR:201, August 2013

4 Multiphase CT in HCC TABLE 2: Combinations of the Four CT Findings of Interest by Final Diagnosis No. of Positive CT Findings Combination of CT Findings Unenhanced (Hypoattenuation) in PVP or delayed phase) using an extension of the McNemar test for clustered data (%CLUSTPRO macro, Lieber ML and Ashley C, Cleveland Clinic Foundation). A p value of less than 0.05 was considered to indicate a significant difference. Analyses were performed using statistical software (SAS, version 9.2, SAS Institute and SPSS Statistics 17.0; SPSS for Windows 2008). Results Thirty-six nodules (36/110, 33%) in 30 patients fulfilled the malignant criteria by histology (n = 23, one by resection and 22 by 18-gauge core biopsy), growth (n = 11), or recurrence after local ablation therapy (n = 2). The histologic differentiation of 23 HCCs included six well-differentiated, one wellto-moderately differentiated, 15 moderately differentiated, and one poorly differentiated. The remaining 74 of 110 (67%) nodules in 66 patients fulfilled the nonmalignant criteria by histology (n = 16) or stability for a minimum of 18 months (n = 58; months; mean, 38 months; median, 36 months). Arterial Phase (Hyperattenuation) CT Findings Portal Venous Phase (Hypoattenuation) Univariate and Multivariate Logistic Regression Analysis Table 1 summarizes the frequency of positive findings for HCC (hypervascularity for arterial phase and hypovascularity for unenhanced, PVP, and delayed phases) on each phase. The majority (62/75, 83%) of nonhypervascular (iso- or hypoattenuating) nodules in the arterial phase were benign. A higher proportion of HCC showed hypovascularity (washout) in the delayed phase (30/36, 83%) than in the PVP (23/36, 64%). Univariate logistic regression analysis indicated that only arterial phase hypervascularity (adjusted odds ratio, 7.51; 95% CI, ; p < 0.001) and delayed phase hypovascularity (2.80, , p = 0.025) were significantly associated with HCC. There was insufficient evidence of an association for the remaining two CT findings (unenhanced, PVP). Multivariate logistic regression analysis showed that arterial phase hypervascularity (11.30, , p < 0.001) and delayed phase hypovascularity (4.39, , p = 0.026) were independent factors significantly associated with HCC. Combination of Findings Table 2 shows combinations of the four CT findings compared with final diagnoses. Among the 23 hypervascular HCCs in the arterial phase, 21 of 23 (91%) showed washout in the PVP 14 of 21 (67%) and in the delayed phase 21 of 21 (100%). Seven HCCs No. of Nodules Delayed Phase (Hypoattenuation) Benign Malignant Total 4 Combination 1 a Yes Yes Yes Yes Combination 2 a Yes Yes Yes No Combination 3 a Yes Yes No Yes Combination 4 Yes No Yes Yes Combination 5 a No Yes Yes Yes Combination 6 Yes Yes No No Combination 7 Yes No Yes No Combination 8 Yes No No Yes Combination 9 a No Yes Yes No Combination 10 a No Yes No Yes Combination 11 No No Yes Yes Combination 12 Yes No No No Combination 13 No Yes No No Combination 14 No No Yes No Combination 15 No No No Yes Combination 16 No No No No a Nodules that meet the American Association for the Study of Liver Disease criteria for hepatocellular carcinoma. showed washout only in the delayed phase, but none of HCCs showed washout only in the PVP. Therefore, seven HCCs (7/36, 19%) could be additionally diagnosed as HCC by AASLD criteria with combinations including delayed phase (Fig. 2) compared with arterial phase and PVP only. Nonhypervascular HCCs (13/36, 36%) were scattered in a variety of combinations in the different phases with considerable overlap with benign nodules. Of these 13 nonhypervascular HCCs, three (36, 8%) showed no positive findings on any of the four phases. Twenty-three of the 110 nodules (21%) met AASLD diagnostic criteria (combinations 1, 2, 3, 5, 9, and 10 in Table 2) and 21 of those 23 (91%) were HCCs. The two falsepositive nodules were both focal nodular hyperplasia (1.6 and 1.0 cm, respectively) in the same patient. The 1.6-cm nodule proven by biopsy showed washout in the PVP but not in delayed phase and the other 1-cm nodule that had been stable for 25 months showed washout in the delayed phase only. The most frequently observed findings in the 74 benign nodules were no positive findings on any of the four phases: iso- or hypovascular in the arterial phase, iso- or hypervascular in unenhanced phase, PVP, and delayed phase (26/74, 35%). Of 12 arterial phase hy- AJR:201, August

5 Jang et al. Fig year-old man with hepatitis B detected on surveillance ultrasound. A D, Quadriphasic CT images show 1.8-cm hepatic nodule. There is ill-defined hypervascular lesion (arrow) on arterial phase (B) not seen on unenhanced (A) or portal venous phase (C) images. On 3-minute delayed phase image (D), nodule clearly shows washout (arrow) and can be diagnosed as hepatocellular carcinoma (HCC) with biphasic combination of arterial and delayed phases. Nodule would be indeterminate in combinations without delayed phase. Diagnosis of HCC was confirmed by biopsy at time of radiofrequency ablation. pervascular nodules with no washout, 10 nodules (83%) were benign. All 11 nodules that were nonhypervascular in the arterial phase and hypovascular in the unenhanced, PVP, and delayed phases were benign. The positive and negative predictive values of each combination of imaging findings were not calculated because the number of nodules in each combination was too small for those values to be considered meaningful. Comparison of the Performance of Key Combinations of Phases The diagnostic performance of key combinations of phases is summarized in Table 3, along with how the sensitivity and specificity of each combination compared with those of the AASLD standard (arterial phase hypervascularity and PVP or delayed phase hypovascularity). Compared with the standard (sensitivity, 57% and specificity, 98%), the biphasic combination of arterial phase and PVP was found to have significantly lower sensitivity (39%, p = 0.022) while maintaining a similar specificity (99%, p = 0.32). The biphasic combination of arterial phase and delayed phase, which involved the two phases found to be the best predictors of outcome, yielded the highest sensitivity (57%) and specificity (99%) with no significant difference compared with the AASLD standard (sensitivity, 57%, p = 1.00; specificity, 98%, p = 0.32). The addition of unenhanced (triphasic of unenhanced, arterial phase, and PVP or quadriphasic of unenhanced, arterial phase, PVP and delayed phase) did not result in an appreciable difference in either the sensitivity (triphasic: 53%, p = 0.325; quadriphasic: 57%, p = 1) or the specificity (triphasic: 97%, p = 0.32; quadriphasic: 97%, p = 0.32) compared with the standard. Discussion There has been a recent shift of the practice strategy toward noninvasive diagnosis of typical HCC on the basis of clinicoradiologic findings alone without histopathologic proof. The AASLD guidelines define the appearances of typical HCC as hypervascularity in the arterial phase and washout in the PVP or A C delayed phase [2, 3]. Previous studies comparing various combinations of multiphasic CT generally measured the protocol that best showed the nodules, both typical and atypical, that were later confirmed as HCC [12 15, 17]. Under the current guidelines, atypical lesions on imaging require a second dynamic study or biopsy [3]. Therefore, the performance of various CT protocols needs to be newly assessed. The updated AASLD guidelines have expanded the application of noninvasive diagnosis of HCC to all typical nodules 1 cm or larger on a single dynamic imaging study and recommend quadriphasic MDCT as a standard technical requirement [3]. Currently, the CT protocol for this indication is variable with no worldwide consensus. Especially in the surveillance setting, it is crucial to standardize the CT protocol to properly document typical HCC noninvasively because all atypical lesions should undergo invasive biopsy or a second dynamic imaging study, and inconclusive results will have to undergo resource-intensive follow-up [2, 5]. Another consideration B D 318 AJR:201, August 2013

6 Multiphase CT in HCC TABLE 3: Diagnostic Performance of Key Combinations of CT Findings Diagnostic Criteria True-Positive False-Negative False-Positive True-Negative Sensitivity (%) a p b Sensitivity (%) a p b Biphasic (arterial phase hyperattenuation (24 56) (91 100) PVP hypoattenuation) Biphasic (arterial phase hyperattenuation (40 73) (91 100) delayed phase hypoattenuation) Triphasic (arterial phase hyperattenuation (40 73) 98 (89 100) PVP or delayed phase hypoattenuation) c Triphasic (arterial phase hyperattenuation (36 69) (90 99) PVP or unenhanced hypoattenuation) Quadriphasic (arterial phase hyperattenuation + PVP or delayed phase or unenhanced hypoattenuation) (40 73) (88 99) Note Data in parentheses are 95% CI. PVP = portal venous phase. a Adjusted for within-patient clustering. b Comparisons of sensitivity and specificity are versus the American Association for the Study of Liver Disease (AASLD) standard and are adjusted for intracluster correlation. The %CLUSTPRO macro (Lieber ML, Ashley C, Cleveland Clinic Foundation), an extension of the McNemar test for clustered data, was used for these formal comparisons. c The AASLD diagnostic criteria for HCC. should be given to the increased radiation exposure to patients undergoing quadriphasic CT compared with biphasic or triphasic CT. The AASLD recommendation, however, is based on expert opinion rather than systematic analysis of data. Our study can serve to provide the data of a homogeneous indication prospective enrollment of all 1- to 2-cm nodules detected on surveillance imaging on the basis of systematic implementation of the AASLD practice guidelines. Our statistical analysis clearly showed that arterial phase and delayed phase were the essential components of multiphasic CT for diagnosing small HCCs detected on surveillance ultrasound and additional unenhanced, PVP, or both did not improve the capability of CT. The radiation issue should be an important consideration for a surveillance population, the majority of whom had Child- Pugh class A disease in our study. Given that the starting age of surveillance can be as early as 40 years for otherwise healthy Asian men who are hepatitis B carriers, this group is likely to have more follow-up CT studies for any detected nodules for a longer period than pretransplantation patients with endstage liver diseases. There are ongoing endeavors to minimize radiation dose without compromising diagnostic ability by using new CT features such as low-kilovoltage imaging or new reconstruction algorithms. With supporting data, minimizing the number of phases for the proper indication can be the most direct way of reducing radiation. We believe the unenhanced phase can be removed from the CT protocol. We also suggest that at least followup studies for the nodule be performed with biphasic imaging consisting of the arterial phase and delayed phase. Vascular invasion or minute metastases are not observed in early small ( 2 cm) HCCs with atypical vascularity because of the presence of portal tracts as well as incompletely developed neoplastic arteries [20, 21]. However, until further validated by a large series, triphasic CT consisting of the arterial phase, PVP, and delayed phase may be performed for the initial scan because PVP is believed to be the optimal phase for the general evaluation of the abdomen and could serve as a baseline and a future road map of portal venous branches. We do not believe that our results can be generalized for other indications, such as pretransplantation patients who have end-stage liver cirrhosis or for therapeutic monitoring after locoregional therapy. Several studies have reported that delayed phase is a valuable addition in the diagnosis of HCC. A study by Lim et al. [14] with single-detector CT for preoperative evaluation of HCC showed significantly increased sensitivity for the detection of HCC, especially for small lesions (< 2 cm), by 9% (70% vs 61%) with additional delayed phase as compared with biphasic (arterial phase and PVP) CT, while the specificity remained the same. A study by Iannaccone et al. [13] found the biphasic combination of arterial phase and PVP had sensitivity of 89% and specificity of 98% for the detection of HCCs, and the addition of unenhanced phase showed no improvement but the addition of delayed phase increased the sensitivity to 93% while maintaining the specificity at 97%. Whereas other studies assessed additional benefit of delayed phase to the biphasic arterial phase and PVP combination as a standard, Monzawa et al. [15] compared the combinations of arterial phase and PVP, arterial phase and delayed phase, and all three phases (arterial phase, PVP, and delayed phase) of single helical CT for the detection of small ( 2 cm) HCCs. In that study, the combination of all three phases showed the best performance, followed by the combination of arterial phase and delayed phase, whereas our study showed no improvement in either sensitivity or specificity with additional PVP compared with a combination of arterial phase and delayed phase. Several aspects make the previous data [13 15] difficult to directly apply to the current surveillance algorithm. First, individual studies used different arbitrary diagnostic criteria for HCC. Those included any hypoattenuating nodule larger than 1 cm or 2 cm, delayed capsular enhancement regardless of the appearance on other phases, arterial phase hypervascularity with no washout, or mosaic appearance on PVP or delayed phase. Thus, the role of delayed phase was greater on additional detection of nonhypervascular HCC that was seen only as hypoattenuating lesions on delayed phase, which would be categorized as indeterminate by the current AASLD criteria. Second, these studies retrospectively selected patients either with suspected HCC from a CT database or with confirmed HCC from a pathology database, which would not reflect the clinical practice from surveillance to diagnosis. Third, the follow-up period was generally 6 12 months, which is not sufficient to verify the absence of HCC for small nodules. AJR:201, August

7 Jang et al. Arterial phase hypervascularity is a crux of HCC diagnosis. Washout is also recognized as one of two key features for the diagnosis of HCC in the AASLD guidelines because small arterial enhancing lesions with no washout on CT are frequently benign [8, 9]. In our study, 10 of 12 (83%) arterial phase hypervascular nodules with no washout were benign. Seven of 23 (30%) hypervascular HCCs showed no washout on PVP but washout on delayed phase. Therefore, seven of 36 (19%) HCCs could be additionally diagnosed as HCC attributed to delayed phase findings. None of 23 hypervascular HCCs showed washout on PVP only. Therefore, the omission of PVP would not miss the diagnosis of typical HCC. In a recent study by Luca et al. [16] using quadriphasic MDCT in cirrhotic candidates for liver transplantation, the pattern of hypervascularity without washout on CT showed only 21% sensitivity and 17% specificity for diagnosing HCC. Of 59 hypervascular HCCs with washout, 64% (38/59) showed washout only on delayed phase whereas only 5% (3/59) showed washout only on PVP. Most of the study patients with HCC (42 of 57, 74%), however, underwent pretransplantation transcatheter chemoembolization therapy, which could have affected the enhancement of the liver and nodules. Although the degree of liver cirrhosis of their group was likely worse than our surveillance patient group, the results of Luca et al. also support the importance of washout, which is much more frequently seen in the delayed phase than in the PVP. The reason for the late washout tendency of HCC is not clearly understood. Possible explanations suggested by previous researchers [14, 15] are relatively poor portal phase enhancement of the cirrhotic parenchyma due to portal hypertension and little interstitial retention of contrast material within highly cellular HCC compared with the liver parenchyma in the equilibrium phase. However, the tendency of late washout of HCC is also well recognized on ultrasound using a microbubble contrast agent that is purely intravascular with no interstitial retention [22]. There are a few limitations to this study. First, not all HCCs (23/36, 64%) and only 16 of 74 (22%) benign nodules in our study were confirmed by histopathology. However, all the remaining malignant lesions were confirmed by means of unequivocal interval growth or recurrence after locoregional therapy. Even between expert pathologists, significant variation has been documented [23] as to the dividing line between dysplastic nodules and HCC in the biopsy specimen, especially for small lesions as in our study. Therefore, we cannot exclude a small possibility of including dysplastic nodule for two well-differentiated HCCs confirmed by biopsy with no recurrence after local treatment. Conversely for benign nodules, we believe our long-term follow-up period (18 60 months; mean, 38 months; median, 36 months) should be sufficient to confirm and might be better to reflect the true biologic behavior of the nodules, given such difficulty in accurate pathologic diagnosis of small hepatocellular nodules from a biopsy specimen. Second, because the images were read prospectively by three experienced radiologists in consensus as part of our clinical protocol, we did not assess the interobserver variability. Moreover, the interpretation of one phase was not blinded at the interpretation of another phase, and the phases might have been potentially influenced by one another. However, because the readers only determined the attenuation of a specific nodule relative to the parenchyma on each phase, the subjectivity and variability would be minimal. Third, there might be a potential bias from the exclusion of 20 nodules without confirmatory diagnosis. In conclusion, for diagnosing 1- to 2-cm HCCs with multiphasic CT in an HCC surveillance group, arterial phase hypervascularity and delayed phase hypovascularity are the two essential findings significantly associated with the diagnosis of HCC according to the AASLD criteria, and the biphasic combination of arterial phase and delayed phase showed the best sensitivity and specificity. Performing all four phases as a mandatory standard protocol should be reconsidered because additional unenhanced, PVP, or both did not improve the capability of CT for this indication. Using these two essential phases only may reduce the radiation dose for these patients who are likely to undergo multiple follow-up imaging studies. References 1. Bruix J, Sherman M, Llovet JM, et al.; European Association for the Study of the Liver. Clinical management of hepatocellular carcinoma: conclusions of the Barcelona-2000 EASL conference. J Hepatol 2001; 35: Bruix J, Sherman M. 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