Intrabiliary Growth of Colorectal Liver Metastasis: Spectrum of Imaging Findings and Implications for Surgical Management

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1 Gastrointestinal Imaging Pictorial Essay Peungjesada et al. Gastrointestinal Imaging Pictorial Essay Silanath Peungjesada 1 Thomas. loia 2 Harmeet Kaur 1 Leonardo Marcal 1 Haesun Choi 1 Jean-Nicolas Vauthey 2 Evelyne M. Loyer 1 Peungjesada S, loia T, Kaur H, et al. Keywords: biliary invasion, colorectal liver metastasis, CT DOI: /JR Received June 27, 2012; accepted after revision March 4, Department of Diagnostic Radiology, University of Texas M. D. nderson Cancer Center, 1400 Pressler St, Unit 1473, Houston, TX ddress correspondence to E. M. Loyer (eloyer@mdanderson.org). 2 Department of Surgical Oncology, University of Texas M. D. nderson Cancer Center, Houston, TX. CME/SM This article is available for CME/SM credit. WE This is a web exclusive article. JR 2013; 201:W582 W X/13/2014 W582 merican Roentgen Ray Society Intrabiliary Growth of Colorectal Liver Metastasis: Spectrum of Imaging Findings and Implications for Surgical Management OJECTIVE. The propensity for colorectal liver metastasis to invade the biliary tree is increasingly recognized, placing particular emphasis on the risk of postoperative recurrence. This article illustrates the spectrum of imaging findings when colorectal metastasis invades the biliary tree. CONCLUSION. Knowledge of the imaging features of intrabiliary invasion by colorectal liver metastasis improves the quality of preoperative staging and is crucial in an era in which nonanatomic wedge resection and radiofrequency ablation are routinely performed. I nvasion of the bile ducts by colorectal liver metastasis is a pattern of dissemination that has been discussed predominantly in the surgical and pathologic literature. Identification of this growth pattern on cross-sectional imaging is critical to preoperative staging [1 3]. Over the past decade, the rate of hepatic resection of colorectal liver metastasis has increased, and long-term survival rates have improved. These results are due to advances in chemotherapy and surgical techniques combined with high-quality imaging for treatment planning. Unrecognized bile duct involvement of colorectal liver metastasis increases the likelihood of incomplete tumor clearance because the true extent of the disease is underestimated [1 4]. In addition, the propensity for biliary invasion by colorectal liver metastasis may lead to unanticipated postoperative recurrences that are confined to the biliary tree [1]. Finally, biliary invasion by colorectal liver metastasis may be misleading because it can mimic primary biliary neoplasia [5, 6]. The purpose of this article is to present the spectrum of CT findings of biliary involvement of metastatic colorectal liver metastasis and the unique patterns of recurrence after hepatic resection in the presence of unrecognized biliary invasion. Liver metastases are rarely associated with bile duct dilatation. However, Jhaveri et al. [7] showed that, in a cohort of 297 patients, the incidence of biliary dilatation with colorectal liver metastasis was 16.5%, whereas that with other tumor types was only 3.0%. Okano et al. [8] showed that, in a cohort of 149 patients, macroscopic tumoral invasion of the bile ducts occurred in 12% of patients and microscopic invasion occurred in 29% of patients. These data suggest that biliary involvement by colorectal liver metastasis is underrecognized. ile duct invasion by colorectal liver metastasis can be secondary to intraductal tumor growth, as seen with papillary cholangiocarcinoma and hepatocellular carcinoma, or to perineural or peribiliary infiltration, as seen with hilar cholangiocarcinoma. In colorectal liver metastasis, tumor cells spread along intact basement membranes and replace the nonneoplastic ductal epithelium with formation of papillary projections in the larger ducts, mimicking papillary cholangiocarcinoma [2, 9, 10]. Macroscopic biliary invasion can be detected on cross-sectional images [4 6, 8]. Involved ducts are dilated, are of soft-tissue attenuation, and may be seen upstream or downstream from the neoplastic mass. Fine punctate calcifications may be present within the intraductal component of the tumor at the time of diagnosis [5]. ile ducts that are obstructed without intraductal invasion are of water attenuation and always located upstream of the obstruction (Fig. 1). iliary invasion can affect intrahepatic or extrahepatic bile ducts. For practical purposes, we have classified biliary involvement of colorectal liver metastasis anatomically into two categories: peripheral (involvement of second-order and smaller bile ducts) and central (involvement of the first-order and extrahepatic bile ducts).these two types of W582 JR:201, October 2013

2 involvement are distinct in their clinical presentations, diagnostic challenges, recurrence patterns, and management. Imaging Technique t our institution, patients with hepatic colorectal metastasis are evaluated routinely with single-phase helical CT obtained during the portal phase (4-, 16-, or 64-MDCT Light- Speed, GE Healthcare). Most patients who are eligible for resection undergo a multiphasic liver protocol. Optimally, the liver protocol should be performed before neoadjuvant chemotherapy at a time when metastases are most obvious and the risk of missing them is lower. lthough the diagnosis of biliary invasion does not require a liver protocol, a subtle invasion, such as small parenchymal metastasis, is easier to identify on a multiphasic study. This technique is supported by the very rare detection in our surgeons experience of additional disease at intraoperative sonography or palpation. The arterial phase provides an exquisite depiction of the vascular anatomy, which is important to surgical planning. liver protocol includes an unenhanced evaluation of the liver followed by a late arterial phase, portal phase, and delayed phase. Scanning is performed at 30 seconds, 60 seconds, and approximately 3 minutes after the start of injection. The injection rate is 3 5 ml/s. Image reconstruction thicknesses used for diagnostic interpretation are 2.5 and 5 mm for multiphasic techniques and 5 mm for single-phase techniques. lthough a highquality single portal phase study is sufficient in many cases, in our experience, the liver protocol improves the detection and characterization of small lesions, allowing optimal surgical planning. Peripheral iliary Involvement Preoperative Diagnosis The radiographic spectrum of peripheral biliary involvement ranges from cases in which a neoplastic mass is the dominant lesion to cases in which biliary dilatation is the main observation and the neoplastic mass is very small or, rarely, radiographically absent. ecause of its peripheral location, the biliary invasion is clinically silent. Regardless of the relative extent of ductal involvement, the association of a mass with an abnormal bile duct or ducts, particularly downstream from the mass, should lead one to consider the possibility of biliary invasion. Frequently encountered patterns of peripheral biliary involvement are discussed in this section. Metastasis with obvious ductal invasion Most often, a parenchymal metastasis is associated with one or more dilated bile ducts (Figs. 2 and 3). The dilated ducts can be seen upstream or downstream from the metastasis and vary in length. The metastasis may be small or large. Metastasis with subtle ductal invasion Colorectal liver metastasis may invade a short segment of a peripheral duct (Figs. 4 and 5). In some cases, biliary invasion is detected only by recognizing that a nodule that persists from one slice to the next is, in reality, the cross-section of a dilated duct usually seen along the corresponding opacified portal venule (Fig. 6). Subtle peripheral bile duct invasion is easily overlooked in the absence of high-quality imaging technique combined with careful review of orthogonal planes. Peripheral bile duct invasion without an obvious parenchymal metastasis hepatic mass may be very small and not definable on imaging, with radiographic findings suggesting that involvement is limited to the biliary tree. This appears as a linear area of soft-tissue attenuation occasionally seen as a branching structure simulating a small portal thrombus (Figs. 7 and 8). The risk of confusing biliary obstruction with portal thrombus is compounded by the fact that both are associated with increased arterial perfusion [10]. In such cases, a diagnosis of metastasis may not be considered because of the absence of a soft-tissue mass. The important point here is that the focal area of increased arterial flow should not be systematically dismissed and assumed to result from a small bland thrombus, which is a relatively common event, particularly after laparotomy. Visualization of an opacified venule paired with the dilated duct helps in the differential diagnosis. Tumor thrombi do occur in colorectal liver metastasis but are exceedingly rare. Linear or punctate calcification indicative of intrabiliary metastasis Colorectal liver metastases are frequently calcified. Likewise, biliary extension may appear as subtle calcifications distributed in a linear pattern best seen on unenhanced images (Fig. 9). Patterns of Recurrence and Management The hallmark and risk of bile duct involvement by colorectal liver metastasis is that the tumors can grow longitudinally, extending beyond the confines of the main parenchymal neoplastic mass. In nonanatomic wedge resection, the surgical margin may be too narrow to encompass the involved duct or ducts. Consequently, the presence of peripheral biliary invasion contraindicates nonanatomic wedge resections and favors formal anatomic left or right hepatic resection. The risk of insufficient margin must also be considered when performing radiofrequency ablation. In cases in which intrabiliary invasion is not preoperatively recognized, resection or ablation can be incomplete and expose the patient to the risk of local recurrence in the liver remnant (Figs. 5 and 6). Central iliary Involvement Preoperative Diagnosis Colorectal liver metastasis that invades first-order bile ducts and extrahepatic ducts may create a central biliary obstruction that results in jaundice. Diagnosis of metastasis to the central bile ducts may be difficult when the history of colorectal liver metastasis is remote and an intrahepatic mass is not present. In such cases, the clinical and radiographic pattern can mimic that of papillary cholangiocarcinomas, and diagnosis relies on clinical history and pathologic analysis [5, 6]. Frequently encountered patterns of central biliary involvement are discussed in this section. Central bile duct invasion with intrahepatic metastasis Involvement of the firstorder bile ducts and extrahepatic ducts by colorectal liver metastasis can be a consequence of contiguous downstream involvement of the biliary tree by peripherally located tumors (Fig. 10). Central bile duct invasion without obvious intrahepatic metastasis Colorectal liver metastasis can involve the first-order bile ducts without obvious parenchymal metastasis: in such cases, the disease appears to be limited to the bile ducts. The main barrier to diagnosis of this presentation is the risk of confusion of the metastasis with a primary bile duct malignancy, particularly because the metastasis may develop several years after resection of the primary tumor [2] (Figs. 9 and 11). Sometimes, a very small liver metastasis near the biliary hilum can invade the first-order bile duct and be difficult to detect because of its size (Fig. 12). Patterns of Recurrence and Management fter resection, patients with central biliary involvement may have isolated intrabiliary recurrences. iliary recurrence may precede the development of parenchymal metastasis (Figs. 12 and 13). With central biliary obstruction, the consideration is for an extrahepatic bile duct resection with the JR:201, October 2013 W583

3 Peungjesada et al. need for bilioenteric reconstruction, which is otherwise rare in the surgical management of colorectal liver metastases. Without proper recognition of the presence and extent of biliary invasion, noncurative resections are likely to be performed with adverse shortand long-term outcomes for the patient. Conclusion The propensity for colorectal liver metastasis to invade the bile ducts is now well recognized. Various patterns of radiologic presentation are described here. Recognition of these patterns can improve surgical treatment planning and lower the risk of local recurrence. The use of high-resolution studies performed before neoadjuvant chemotherapy is crucial because biliary invasion of colorectal liver metastasis may be subtle or concealed by the response to chemotherapy. References 1. Povoski SP, Klimstra DS, rown KT, et al. Recognition of intrabiliary hepatic metastases from colorectal adenocarcinoma. HP Surg 2000; 11: ; discussion, Riopel M, Klimstra DS, Godellas CV, lumgart LH, Westra WH. Intrabiliary growth of metastatic colonic adenocarcinoma: a pattern of intrahepatic spread easily confused with primary neoplasia of the biliary tract. m J Surg Pathol 1997; 21: Okano K, Yamamoto J, Moriya Y, et al. Macroscopic intrabiliary growth of liver metastases from colorectal cancer. Surgery 1999; 126: Jinzaki M, Tanimoto, Suzuki K, et al. Liver metastases from colon cancer with intra-bile duct tumor growth: radiologic features. J Comput ssist Tomogr 1997; 21: Lee YJ, Kim SH, Lee JY, et al. Differential CT features of intraductal biliary metastasis and dou- ble primary intraductal polypoid cholangiocarcinoma in patients with a history of extrabiliary malignancy. JR 2009; 193: Wenzel DJ, Gaede JT, Wenzel LR. Intrabiliary colonic metastasis mimicking primary biliary neoplasia. JR 2003; 180: Jhaveri KS, Halankar J, guirre D, et al. Intrahepatic bile duct dilatation due to liver metastases from colorectal carcinoma. JR 2009; 193: Okano K, Yamamoto J, Okabayashi T, et al. CT imaging of intrabiliary growth of colorectal liver metastases: a comparison of pathological findings of resected specimens. r J Radiol 2002; 75: Muramatsu Y, Takayasu K, Furukawa Y, et al. Hepatic tumor invasion of bile ducts: wedge-shaped sign on MR images. Radiology 1997; 205: Yamamoto J, Sugihara K, Kosuge T, et al. Pathologic support for limited hepatectomy in the treatment of liver metastases from colorectal cancer. nn Surg 1995; 221:74 78 Fig. 1 Two different patients with biliary obstruction, one with and one without tumor involvement of bile duct., 50-year-old man with colorectal liver metastasis. Portal phase contrast-enhanced CT shows downstream tumoral infiltration in segment III bile duct. ile duct (black arrow) is dilated and of soft-tissue attenuation. Large metastasis is seen in right liver. Note opacified segment III portal vein (white arrow) accompanying dilated duct., 64-year-old woman with colorectal liver metastasis. Portal phase contrast-enhanced CT shows metastasis in segment IVa, infiltration of hilar fissure with obstruction, and upstream dilatation of right hepatic bile duct. ile duct (arrow) is of water attenuation and is filled with bile. W584 JR:201, October 2013

4 Fig year-old man 9 months after right hemicolectomy for T3N1 colon carcinoma. Contrast-enhanced CT image in portal phase shows metastasis in segment VIII and downstream infiltration of bile duct (arrow). ttenuation of duct and metastasis are identical and consistent with tumor extension in bile duct. Fig year-old man 7 years after right hemicolectomy for carcinoma. Contrast-enhanced CT image in portal phase shows small metastasis (arrowhead) in segment IVa. Dilated bile ducts (arrows) are filled with soft tissue, consistent with tumoral invasion. Fig year-old man 3 years after sigmoid resection for T3N0 sigmoid carcinoma., Portal phase contrast-enhanced CT image obtained before wedge resection shows metastasis in segment VI (arrowhead) and very subtle bile duct invasion (arrow)., Portal phase contrast-enhanced CT image was obtained 2.5 years after wedge resection of segment VI tumor. Note surgical bed limited by surgical sutures (asterisk). Small nodule at surgical margin (arrowhead) is consistent with recurrence. Recurrent tumor (arrow) has retained propensity for intrabiliary growth. Fig year-old man with colorectal liver metastasis. Serial studies illustrate local recurrence after resection. and, Portal phase contrast-enhanced CT scans obtained before left hepatectomy show small metastasis at margin between segments IVa and VIII (arrow, ) with upstream tumoral extension in segment VIII duct (arrow, ). C, Portal phase contrast-enhanced CT scan obtained 5 months after left hepatectomy shows that small dilated bile duct in segment VIII (large arrow) has not been resected. Note surgical sutures (small arrow). (Fig. 5 continues on next page) C JR:201, October 2013 W585

5 Peungjesada et al. Fig. 5 (continued) 62-year-old man with colorectal liver metastasis. Serial studies illustrate local recurrence after resection. D, Portal phase contrast-enhanced CT scan obtained 3 years after left hepatectomy reveals progression of tumor at margin of resection (large arrow). Note surgical sutures demarcating surgical margin (small arrow). Fig year-old woman with colorectal liver metastasis., Contrast-enhanced CT image in portal phase shows metastasis in segment VI (arrowhead) with small nodule (arrow) adjacent to dominant mass., Coronal reconstruction image shows that small nodule on axial images corresponds to bile duct dilated by tumor (arrow), upstream from parenchymal metastasis (arrowhead). Fig year-old woman with colorectal liver metastasis 2 years after left hemicolectomy. Images illustrate value of arterial imaging., Contrast-enhanced CT image in arterial phase shows linear hypoattenuating structure in segment II (arrow), compatible with obstructed bile duct and surrounding secondary hyperemia. This pattern mimics peripheral portal thrombus. Note metastasis in segment I (arrowhead). Surgical resection confirmed metastases in segments I and II., Contrast-enhanced CT image in portal phase confirms transient nature of arterial phase hyperemia. Note linear hypoattenuating structure in segment II (arrow) and metastasis in segment I (arrowhead). D W586 JR:201, October 2013

6 D Fig year-old man with synchronous colorectal liver metastasis. Serial studies illustrate response to neoadjuvant chemotherapy followed by recurrence after right hepatectomy., Portal phase contrast-enhanced CT image obtained before neoadjuvant chemotherapy shows biliary metastasis in segment III (arrow) and hepatic parenchymal metastases in segments IVa and VI (asterisks)., Portal phase contrast-enhanced CT image obtained after 14 cycles of neoadjuvant chemotherapy shows response with decrease in size of metastases in segment IVa and VI (asterisks) and resolution of biliary metastasis in segment III (oval). C, Portal phase contrast-enhanced CT image obtained 10 months after extended right hepatectomy shows recurrent biliary metastasis in segment III (arrow). D, PET/CT image obtained 10 months after extended right hepatectomy shows uptake in segment III (arrow); recurrent biliary metastasis was confirmed as diagnosis. Fig year-old woman, 5 years after low anterior resection for rectosigmoid carcinoma, with increasing levels of carcinoembryonic antigen and elevated liver function enzymes. iopsy-proven colorectal liver metastasis was found in segment VI., Portal phase contrast-enhanced CT image before chemotherapy shows tumoral invasion of segment VI bile duct (arrows) extending to hilum of liver. Parenchymal metastasis (not shown) was present in segment VI. Calcifications (arrowheads) are seen within biliary tree., Oblique coronal reconstruction image from unenhanced CT after neoadjuvant chemotherapy shows linear calcification corresponding to treated tumor in segment VI (arrow). Treated parenchymal metastasis more caudally also shows calcifications (arrowhead). Calcifications that are dispersed within tumor before treatment become more conspicuous as size of tumor decreases. Fig year-old man 5 years after low anterior resection for T3N0 rectal carcinoma., Portal phase contrast-enhanced CT image with oblique reconstruction shows tumor (asterisk) in segment VIII with extension into right hepatic duct (black arrow). Tumor is reaching bifurcation. Common hepatic and common bile ducts are normal, of smaller caliber than right hepatic duct, and of water attenuation (white arrow)., PET/CT image shows 18 F-FDG uptake by tumor in segment VIII and invaded right hepatic duct. C JR:201, October 2013 W587

7 Peungjesada et al. Fig year-old man 5 years after total colectomy for T3N0 carcinoma, 4 months after cholecystectomy for right upper quadrant pain and decreased gallbladder ejection fraction., ERCP image obtained because of persistent right upper quadrant pain and elevated liver enzyme levels after cholecystectomy shows obstruction of right hepatic duct (arrowhead); brushing revealed malignant epithelial cells., Portal phase contrast-enhanced CT image shows segment VIII dilated by tumor (black arrow) with downstream extension into right hepatic duct. Segment VII bile duct is dilated and of water attenuation (white arrow) but not invaded by tumor. Right hepatectomy confirmed intrabiliary metastasis. D Fig year-old woman 2.5 years after total colectomy for T3N0 for colon carcinomas. Serial CT scans show biliary metastasis, surgical treatment, and postoperative tumor recurrence. Patient underwent left hepatectomy, resection of left hepatic duct, and Roux-en-Y hepaticojejunostomy for segment IV colorectal liver metastasis invading left hepatic duct. and, Contrast-enhanced CT scans were obtained before left hepatectomy. Portal phase contrast-enhanced CT scan () shows small metastasis in segment IV (arrow) and biliary obstruction of left hepatic lobe. Slightly more cranial image () shows tumoral extension into left hepatic duct (arrow) responsible for upstream obstruction and dilatation of biliary tree in left hepatic lobe. C, Portal phase contrast-enhanced CT scan obtained 8 months after left hepatectomy and Roux-en-Y reconstruction shows normal common bile duct (arrow). D, Portal phase contrast-enhanced CT scan obtained 2 years after left hepatectomy shows new common bile dilatation with intraluminal mass (arrow), consistent with recurrent biliary metastasis. E, Portal phase contrast-enhanced CT scan obtained 3 years after left hepatectomy shows progression of intraductal tumor. Duct is markedly enlarged and distended by tumor (arrow). E C W588 JR:201, October 2013

8 FOR YOUR INFORMTION This article is available for CME/SM credit. To access the exam for this article, follow the prompts. Fig year-old man 8 years after colectomy for stage III colon carcinoma and 2.5 years after left hepatectomy, resection of common bile duct, and hepaticojejunostomy for segment IVb and II colorectal liver metastasis with invasion of left hepatic duct and common bile duct., Portal phase contrast-enhanced CT scan shows dilatation of remaining distal common bile duct (arrow). Ductal lumen is of fluid attenuation at this level., Contrast-enhanced CT scan at more caudal level than in shows soft-tissue mass in distal common bile duct (arrow). This was biopsy-proven carcinoma compatible with colorectal liver metastasis. JR:201, October 2013 W589