September 2009, VOLUME 193
NUMBER 3

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September 2009, Volume 193, Number 3

Gastrointestinal Imaging

Original Research

Intrahepatic Bile Duct Dilatation Due to Liver Metastases From Colorectal Carcinoma

+ Affiliations:
1Abdominal Imaging Division, Department of Medical Imaging, University of Toronto, University Health Network and Mount Sinai Hospital, 610 University Ave., 3-957, Toronto, ON M5G 2M9, Canada.

2Department of Medical Imaging, Fundacion Santa Fe de Bogota, University Hospital Calle, Bogota, Colombia.

3Department of Biostatistics, University Health Network, Toronto, ON, Canada.

4Department of Pathology, University Health Network, The Toronto General Hospital, Toronto, ON, Canada.

Citation: American Journal of Roentgenology. 2009;193: 752-756. 10.2214/AJR.08.2182

ABSTRACT
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OBJECTIVE. The objective of our study was to assess the association between colorectal liver metastases and intrahepatic bile duct dilatation and compare its frequency with the frequency of intrahepatic bile duct dilatation in other common noncolorectal metastases and hepatocellular carcinoma (HCC).

MATERIALS AND METHODS. A retrospective review of the radiology database was performed to obtain the records of patients who underwent CT for staging of histologically proven colorectal carcinoma (n = 1,000), noncolorectal carcinomas (n = 1,000), and HCC (n = 226). The CT scans of the 2,226 patients were reviewed for the presence of liver metastases and masses, the presence of intrahepatic bile duct dilatation directly related to the masses, the size of the largest lesion, and the associated caliber of the dilated intrahepatic bile duct.

RESULTS. Of the 297 patients with colorectal liver metastases, 49 (16.5%) had intrahepatic bile duct dilatation, whereas of the 263 patients with noncolorectal liver metastases, only eight (3%) had dilated ducts. Thirteen (5.7%) of the 226 patients with HCC had intrahepatic bile duct dilatation. Intrahepatic bile duct dilatation was present in significantly more patients with colorectal liver metastases (p < 0.05) than those with noncolorectal and HCC metastases. The mean sizes of the lesions and mean caliber of the dilated bile duct from colorectal metastases, noncolorectal metastases, and HCC were 5.3, 3.9, and 5.6 cm, respectively, and 5.1, 4.6, and 4.8 mm, respectively. Overall lesion size irrespective of diagnosis had no significant correlation with the probability of bile duct dilatation (p = 0.16; odds ratio = 1.08; 95% CI, 0.97–1.20). Lesion size also did not have a significantly different effect on the probability of dilatation for the three diagnoses (p = 0.71). The caliber of bile duct dilatation did not significantly differ among the three groups of patients by diagnosis (p = 0.70).

CONCLUSION. Colorectal liver metastases have a significantly higher tendency to cause intrahepatic bile duct dilatation than noncolorectal metastases and HCC due to the characteristic features, such as cholangiocarcinoma, of intrabiliary growth. This association has important diagnostic, surgical, and prognostic implications that make it necessary to highlight this finding while communicating with clinical colleagues.

Keywords: bile duct dilatation, colorectal cancer, CT, hepatocellular carcinoma, liver cancer, liver metastases

Introduction
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Cholangiocarcinoma [14] and occasionally hepatocellular carcinoma (HCC) [58] are accompanied by dilatation of the intrahepatic bile ducts. However, intrahepatic biliary dilatation is not widely associated with metastatic liver disease. We have frequently observed intrahepatic biliary duct dilatation from colorectal liver metastases in our subspecialized abdominal imaging practice. This feature has been reported in the surgical pathology literature [9, 10] and occasionally in the radiology literature [11, 12]; however, this specific association does not appear to be a well-recognized fact among radiologists even among those in subspecialized practice. To our knowledge, no studies have directly compared the frequency of this association in colorectal liver metastases versus noncolorectal metastases and HCC.

Herein we describe our study of the direct causal relationship between colorectal liver metastases and intrahepatic biliary dilatation and compare its frequency with that in other common noncolorectal metastases and HCC. We also discuss the diagnostic issues related to identifying this imaging finding as well as the surgical and prognostic implications thereof.

Materials and Methods
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Study Patients

This study received approval from the institutional research ethics board, and the need for patient consent was waived. We performed a retrospective review of the radiology reports database from January 2005 to July 2008 using keyword searches such as CT, staging, carcinoma, colon and rectal carcinoma, and liver metastasis and HCC to obtain consecutive patients who had histologically proven malignancy and had undergone CT for staging evaluation. In this search we obtained and assessed the records of a cohort of 1,000 patients with known colorectal carcinoma and of another cohort of 1,000 patients with noncolorectal carcinoma including primary malignancies such as breast, lung, pancreas, stomach, endometrium, cervix, and head and neck carcinomas and melanoma. To match the former two cohorts, 226 consecutive patients undergoing staging workup for known HCC were included. This number was arrived at randomly during the time period of the retrospective review by identifying patients who had undergone CT for known or suspected HCC because other imaging tests such as sonography had identified a liver mass and CT had been performed for confirmation or as part of pretreatment staging.

In patients with liver metastases who had not undergone surgical resection or biopsy of the liver mass, the follow-up CT scans obtained after treatment by chemotherapy or radiation therapy were also reviewed to confirm that the lesions being assessed in the study were indeed metastatic disease based on interval response or progression. The follow-up CT scans were obtained 6 weeks–6 months after treatment and were requested by surgeons or medical oncologists.

CT

The CT examinations were performed on a 64-MDCT scanner (Aquilion 64, Toshiba Medical Systems) using a 64 × 0.5 mm detector. Images were displayed in the axial plane using a slice thickness of 5.0 mm reconstructed every 2.5 mm and in the coronal plane reconstructed every 3 mm. The technical parameters included the following: 120 kVp, automatic exposure control, tube rotation time of 0.5 second, and SD of noise of 15. Each patient was injected with 100–150 mL of 270 mg I/mL iodixanol (Visipaque 270, GE Healthcare) at a rate of 2–3 mL/s. Images were obtained 70 seconds after the beginning of IV contrast administration.

Image Interpretation

All CT studies were assessed randomly by two subspecialty abdominal radiologists in consensus without knowledge of clinical information. CT images were reviewed to assess for the presence of a liver mass or metastasis, the presence of intrahepatic biliary duct dilatation directly related to a mass, the size of the largest mass causing intrahepatic biliary duct dilatation if multiple lesions were present in the same patient, and the caliber of the associated dilated intrahepatic bile duct. A positively dilated intrahepatic biliary duct was defined as a clear, hypodense tubular structure seen accompanying a contrast-opacified portal venous branch focally in the liver peripheral to the accompanying liver mass.

figure
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Fig. 1 Bar chart displays distribution of number of patients with intrahepatic biliary duct dilatation (IHBD) related to liver lesion according to diagnostic cohort group. HCC = hepatic cellular carcinoma.

Statistical Analysis

A Pearson's chi-square test was performed to assess whether the prevalence of intrahepatic biliary duct dilatation in patients with colorectal liver metastases significantly differed from that in patients with noncolorectal metastases or HCC. The impact of lesion size on the prevalence of intrahepatic biliary duct dilatation was assessed overall and within each of the three diagnostic categories using logistic regression and expressed as odds ratios (ORs) and associated 95% CIs. The relationship between the degree of intrahepatic biliary duct dilatation and diagnostic group was analyzed using the analysis of variance. A p value of less than 0.05 was considered significant for all tests.

Results
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Study Patients

There were 297 patients with liver metastases from colorectal carcinoma: 199 men and 98 women (male-to-female ratio = 2.03) who ranged in age from 41 to 89 years (median age, 69 years). Also included in the study were 263 patients with liver metastases from a noncolorectal primary malignancy (breast, n = 62; lung, n = 38; ovary, n = 20; prostate, n = 16; pancreas, n = 14; esophagus, n = 12; melanoma, n = 12; carcinoid, n = 11; gallbladder, n = 11; renal, n = 10; uterus, n = 7; urinary bladder, n = 6; lymphoma, n = 5; cervix, n = 5; neuroendocrine, n = 5; nasopharynx, n = 5; gastrointestinal stromal tumor, n = 4; unknown, n = 4; ampullary, n = 3; stomach, n = 3; sarcoma, n = 3; testis, n = 3; appendix, n = 2; small intestine, n = 1; thyroid, n = 1). This group was composed of 128 men and 135 women (male-to-female ratio = 0.95; age range, 43–90 years; median age, 67 years). Finally, 226 patients with HCC, 147 men and 79 women (male-to-female ratio = 1.86) ranging in age from 42 to 91 years (median age, 65 years), were included.

Prevalence of Intrahepatic Biliary Duct Dilatation

In the group of 1,000 patients with colorectal carcinoma, 297 had liver metastases on CT examinations (Fig. 1). Of these 297 patients with colorectal liver metastases, intrahepatic biliary duct dilatation (Fig. 2) directly related to the metastatic lesion was observed in at least one or more of the metastatic lesions in 49 patients (16.5%). Of the 1,000 patients with noncolorectal malignancies, liver metastases were seen in 263 patients. Eight (3%) of the 263 patients with liver metastases had intrahepatic biliary duct dilatation (primary cancer: breast, n = 2; lung, n = 2; lymphoma, n = 1; melanoma, n = 1; pancreas, n = 1; stomach, n = 1). Finally, of the 226 patients with HCC on CT, 13 (5.7%) had intrahepatic biliary duct dilatation. Thus, there was a statistically significant (p < 0.001) higher prevalence of intrahepatic biliary duct dilatation in patients with colorectal liver metastases compared with patients with noncolorectal liver metastases and HCC. A Pearson's chi-square test was performed to assess whether the prevalence of intrahepatic biliary duct dilatation in patients with colorectal liver metastases was significantly different from the prevalence in those with noncolorectal metastases or HCC.

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Fig. 2 Contrast-enhanced CT image in 62-year-old man with colorectal liver metastases (white arrow) shows intrahepatic bile duct dilatation (black arrows) in immediate peripheral relation to one of metastatic lesions.

Lesion Size and Probability of Intrahepatic Biliary Duct Dilatation

The mean size of the lesions and the mean caliber of the dilated bile duct from colorectal metastases, noncolorectal metastases, and HCC were 5.3, 3.9, and 5.6 cm, respectively, and 5.1, 4.6, and 4.8 mm, respectively. Table 1 shows the range, mean, and median sizes of the lesions causing intrahepatic biliary duct dilatation in each group. With reference to Table 1, odds ratio are expressed per 1 cm change in lesion size. For example, for colon cancer, an increase in lesion size of 1 cm is associated with an estimated 4% increase (or 1.04 times increase) in the probability of dilatation. This increase is, however, not significantly different from zero (p = 0.59). The odds ratio and the associated 95% CIs and p values were obtained from logistic regression models.

TABLE 1: Probability of Intrahepatic Biliary Duct Dilatation in Relation to Lesion Size

Overall lesion size irrespective of diagnosis had no significant correlation with the probability of bile duct dilatation (p = 0.16; odds ratio = 1.08; 95% CI, 0.97–1.20). Lesion size also did not have a significantly different effect on the probability of dilatation within each of the three groups (p = 0.71). Although the mean lesion size for HCC is suggestive of the possibility of a difference in lesion size between those with and without dilatation (mean = 5.6 vs 3.9 cm, respectively), this difference is not significant (p = 0.19). The caliber of the dilated intrahepatic biliary duct was not significantly different among the three groups (p = 0.70) (Table 2).

TABLE 2: Comparison of Caliber of Dilated Intrahepatic Biliary Duct Between Diagnostic Groups

Discussion
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Intrahepatic biliary duct dilatation is generally not a feature associated with liver metastases but is well recognized with cholangiocarcinoma and HCC. Liver metastases from colorectal carcinoma causing tumor growth within the bile duct (Figs. 2 and 3A, 3B, 3C) have been reported predominantly in the pathology literature and occasionally in the radiology literature [912]. In this study, we found a statistically significant higher association of colorectal liver metastases causing intrahepatic biliary duct dilatation (16.5%) over noncolorectal liver metastases (3%) and HCC (5.7%) irrespective of the size of the lesion or mass. This imaging prevalence approximates the pathologically documented prevalence of macroscopic bile duct invasion in 20% and microscopic bile duct invasion in 40% of colorectal liver metastases [13].

In one prior study [12] of 90 cases of surgically resected colorectal liver metastases from 1990 to 1994, only five cases (5.6%) showed biliary dilatation. This frequency of bile duct dilatation is far less compared with what we observed as well as that previously reported in the pathology literature. The cause of this discrepancy is worth discussing because based on that earlier study some could infer that the frequency of intrahepatic biliary duct dilatation from colorectal liver metastases is not different from that of intrahepatic biliary duct dilatation from other liver metastases or HCC, which clearly is not the case based on our study and previous reports in the pathology literature. One possibility is that the sensitivity of detecting mild intrahepatic biliary duct dilatation has very likely improved since 1990 because CT and other imaging technologies have seen massive leaps over the past decade. Of course another possibility is that microscopic bile duct involvement as seen on pathology review does not always cause bile duct dilatation to be visible on imaging studies.

The imaging significance of observing the finding of intrahepatic biliary duct dilatation with a liver nodule or mass is related to the differential diagnosis. Although in our study HCC had a modest association with intrahepatic biliary duct dilatation, most radiologists would agree that the distinction of typical HCC from liver metastases is usually not a diagnostic dilemma because of characteristic features of HCC, such as arterial phase hypervascularity with portal phase washout and the presence of a capsule, fatty degeneration, and portal venous invasion. Most of the hypovascular liver metastases do not generally have any distinctive features on imaging to hint toward the primary malignancy. When one is faced with the scenario of having diagnosed liver metastases presumptively in the presence of an unknown primary, the presence of intrahepatic biliary duct dilatation could hint to the primary malignancy being colorectal carcinoma. This information can then lead to a quicker and more focused search for the primary malignancy. Awareness of this finding with colorectal liver metastases must also lead to considering it as an important close differential diagnosis to the peripheral type of cholangiocarcinoma. It can be difficult to distinguish colorectal liver metastases from cholangiocarcinoma on the basis of laboratory and imaging data; nevertheless, the distinction is imperative [14]. Both tumors can show elevated carcinoembryonic antigen (CEA) and carbohydrate antigen (CA) 19-9 levels. On CT, both are generally hypovascular and can show intrahepatic biliary duct dilatation and delayed enhancement after IV contrast injection. In general, it is also difficult to distinguish metastatic adenocarcinoma from colorectal carcinoma from cholangiocarcinoma with a conventional histologic examination using H and E staining [9]. Further examination by immunohistochemistry using the anticytokeratin antibody is necessary to achieve that distinction [1518]. Thus, before surgical management of a presumed diagnosis of chol angiocarcinoma based on detection of a liver mass with biliary dilatation, it is important to consider excluding colorectal carcinoma as a possibility, particularly when faced with a liver mass with intrahepatic biliary duct dilatation.

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Fig. 3A 62-year-old man who underwent liver lobe resection. Photograph of gross specimen of resected liver lobe shows tumor (arrow) inside dilated bile duct.

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Fig. 3B 62-year-old man who underwent liver lobe resection. Low-power microscopic view shows bile duct (white arrow) is distended by invading metastatic adenocarcinoma (black arrow) of colorectal origin. (Masson trichrome stain, ×25)

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Fig. 3C 62-year-old man who underwent liver lobe resection. Higher-power microscopic view of colorectal adenocarcinoma inside bile duct shows native benign bile duct epithelium (arrow). Arrowhead points to tumor. (Masson trichrome stain, ×100)

Surgical resection has been accepted as a reasonable treatment of patients with hepatic metastases from colorectal carcinoma [1921]. The clinical and surgical significance of observing intrahepatic biliary duct dilatation is twofold. First, the intrahepatic biliary duct dilatation is caused by intrabiliary growth of tumor [912]. Liver resection closely along the tumor margin without adequate attention being given to the bile duct stump has potential for leaving tumor tissue in the bile duct and resulting in a positive margin, which has been reported to be one of the most important determinants of poor survival [2224]. Thus, preoperative identification of intrahepatic biliary duct dilatation must be communicated to the operative surgeon to obtain adequate anatomic resection margins and ensure a negative resection margin postoperatively. Second, although it may sound paradoxical, macroscopic intrabiliary growth due to colorectal liver metastases is associated with an indolent nature of the tumor and a better prognosis after hepatic resection [10, 25]. Okano et al. [10] reported the actuarial 3- and 5-year survival rates to be 62% and 57%, respectively, for patients with no bile duct involvement versus 56% and 48% for patients with microscopic bile duct invasion and 94% and 80% for patients with macroscopic bile duct invasion.

We accept that there are several limitations to our study. First, this study was a retrospective review. However, considering the large number of patients we included in our study, it would have taken many investigators a few years to achieve this cohort even in a tertiary center such as ours. We also believe that including a larger cohort to obtain reliable statistical data was more important than having a prospective study that would have failed to give us a truer representation of the actual frequency of the finding in question here.

Second, we did not perform radiologic–pathologic correlation in patients with intrahepatic biliary duct dilatation in this study. This, however, was never the purpose of this study: The purpose was to assess the frequency of intrahepatic biliary duct dilatation in colorectal liver metastases rather than analyze the imaging features in correlation to pathologic findings. Although previous imaging studies have reported this finding, most are case reports or case series, and to our knowledge, no systematic review assessing the frequency in colorectal liver metastases compared with other malignant liver tumors has been published in the radiology literature. Also in many of our cases, liver biopsy was not performed before surgery or chemotherapy if the imaging diagnosis was obvious for liver metastatic disease. It has been well documented in the surgical and pathology literature that patients with bile duct invasion and colorectal liver metastases have a better prognosis, so we did not attempt to study this issue again because it was not the focus of our study. We did not include cholangiocarcinoma in this study because it is well established that cholangiocarcinoma is associated with intrahepatic biliary duct dilatation and the objective of our study was not to assess imaging features of colorectal liver metastases in comparison with cholangiocarcinoma but rather to highlight how closely colorectal liver metastases can mimic cholangiocarcinoma when intrahepatic biliary duct dilatation is seen on imaging.

Third, we did not specifically assess the impact of the number and location of metastases on the prevalence of intrahepatic biliary duct dilatation. During our review we, however, did not observe any obvious consistent pattern to suggest a relation between tumor number or location. Our goal was to assess whether there was any relation between the presence of bile duct dilatation and the histology of the lesion, which did show a statistically significant correlation. We also did not assess the relation of nodal metastases with intrahepatic biliary duct dilatation because we believe this issue is unrelated to the question we were trying to answer.

In conclusion, intrahepatic biliary duct dilatation is an interesting, peculiar imaging feature associated with colorectal liver metastases, making it a very close differential diag nostic companion to cholangiocarcinoma. Observation of this finding has important surgical and prognostic implications that make it necessary to highlight this finding while communicating with clinical colleagues.

Address correspondence to K. S. Jhaveri ().

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