Published online before print June 13, 2002, 10.1148/radiol.2242011501
(Radiology 2002;224:725-730.)
© RSNA, 2002
Vascular and Interventional Radiology |
Bile Duct: Analysis of Percutaneous Transluminal Forceps Biopsy in 130 Patients Suspected of Having Malignant Biliary Obstruction1
Gyoo-Sik Jung, MD,
Jin-Do Huh, MD,
Sang Uk Lee, MD,
Byung Hoon Han, MD,
Hee-Kyung Chang, MD and
Young Duk Cho, MD
1 From the Departments of Diagnostic Radiology (G.S.J., J.D.H., Y.D.C.), Internal Medicine (S.U.L., B.H.H.), and Pathology (H.K.C.), College of Medicine, Kosin University, 34 Amnam-Dong, Seo-Gu, Pusan 602-702, South Korea. From the 2001 RSNA scientific assembly. Received September 10, 2001; revision requested November 9; revision received January 8, 2002; accepted January 29. Address correspondence to G.S.J. (e-mail: gsjung@ns.kosinmed.or.kr).
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ABSTRACT
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PURPOSE: To evaluate percutaneous transluminal forceps biopsy in patients suspected of having a malignant biliary obstruction.
MATERIALS AND METHODS: One hundred thirty consecutive patients (82 men and 48 women; mean age, 59 years) with obstructive jaundice underwent transluminal forceps biopsy during or after percutaneous transhepatic biliary drainage. The lesions involved the common bile duct (n = 58), common hepatic duct (n = 39), hilum (n = 14), ampullary segment of the common bile duct (n = 11), right or left intrahepatic bile duct (n = 5), or the entire extrahepatic bile duct (n = 3). In each patient, three to five specimens (mean, 4.1 specimens) were taken from the lesion with 5.4-F biopsy forceps. The final diagnosis for each patient was confirmed with pathologic findings at surgery, additional histocytologic data, or clinical and radiologic follow-up. Statistical analysis was performed with the 
2 test; a P value 
.05 was considered to indicate a significant difference.
RESULTS: Ninety-eight of 130 biopsies resulted in correct diagnoses of malignancy. Five biopsy diagnoses proved to be true-negative. There were 27 false-negative diagnoses and no false-positive diagnoses. The diagnostic performance of transluminal forceps biopsy in malignant biliary obstructions was as follows: sensitivity, 78.4%; specificity, 100%; and accuracy, 79.2%. Sensitivity of biopsy in the 82 patients with cholangiocarcinoma was higher than in the 43 patients with malignant tumors other than cholangiocarcinoma (86.6% vs 62.8%, P < .005). Sensitivity was significantly lower in the ampullary segment of the common bile duct than in other sites (P < .01). No major complications related to the biopsy procedures occurred.
CONCLUSION: Percutaneous transluminal forceps biopsy is a safe procedure that is easy to perform through a transhepatic biliary drainage tract. It provides relatively high accuracy in the diagnosis of malignant biliary obstructions.
© RSNA, 2002
Index terms: Bile ducts, biopsy, 76.1261 • Bile ducts, neoplasms, 76.321 • Biopsies, technology, 76.1261
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INTRODUCTION
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During the past 2 decades, many studies have verified the safety, reliability, and cost effectiveness of percutaneous fine-needle aspiration biopsy (FNAB) in the nonsurgical tissue diagnosis of various abdominal diseases (1–3). The advent of the automated biopsy device, or biopsy gun, has further improved the ability to obtain adequate specimens for histopathologic analysis (4,5). In addition, advances in imaging techniques have enabled the use of biopsy in virtually all anatomic areas (2,5). Nevertheless, this method of tissue diagnosis is not fully justified for biliary tumors, because these tumors are often too small to allow an accurate percutaneous puncture to obtain appropriate material (6,7), and they are often desmoplastic, making it difficult to establish a histologic diagnosis (7). The results of FNAB in the diagnosis of biliary tumors are generally inferior to results of FNAB in other tumors (7); overall reported sensitivities of FNAB for biliary tumors range from 42% to 67% (7–9). For this reason, other biopsy methods have been proposed for improving the rate of diagnosis of malignant biliary tumors.
Percutaneous transhepatic biliary drainage (PTBD) is a well-established interventional radiologic procedure used in patients with obstructive jaundice; it can also be used to provide access to the intrahepatic and extrahepatic bile duct for various biopsy instruments. Forceps biopsy via the bile duct during or soon after PTBD is an attractive method for diagnosing biliary tumors. Percutaneous use of biopsy forceps in the bile duct was first reported in 1980 (10), and successful transluminal biopsies have been performed since that time. Various published studies suggest that this technique is highly sensitive, especially for diagnosing cholangiocarcinoma, with a reported sensitivity of 30%–100% (11–15). However, to our knowledge, all published reports have involved only a small number of cases in studies (11–15) that have included more than six but fewer than 25 patients. The purpose of our study was to evaluate our experience with percutaneous transluminal forceps biopsy in a consecutive series of 130 patients suspected of having a malignant biliary obstruction.
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MATERIALS AND METHODS
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Patients
Between February 1995 and July 2000, 130 consecutive patients (82 men and 48 women; age range, 29–79 years; mean age, 59 years) with obstructive jaundice underwent percutaneous transluminal biopsy of the bile duct at our institution with a 50-cm, 5.4-F flexible biopsy forceps (Cordis, Miami, Fla). This biopsy forceps (Fig 1) was originally designed for endomyocardial biopsies and consisted of three parts: a three-pull ring handle, cutting jaws, and a coiled shaft. An interventional radiologist (G.S.J.) performed all biopsies through a PTBD tract during (n = 98) or after (n = 32) the procedure for decompression of the bile ducts.
Suspicion of a malignant obstruction was the main indication for the biopsy. The medical records, surgical reports, histopathologic reports, and diagnostic imaging reports of each patient were retrospectively reviewed by one of three authors (Y.D.C., S.U.L., B.H.H.). The following information was recorded from patient records: age, sex, history of malignant tumor, technical success of the biopsy procedure, approach site for the biopsy (right- or left-sided approach), site of the lesion, complications and their treatment, final diagnosis and means of establishing the final diagnosis, histopathologic results and adequacy of the biopsy sample, and radiologic and clinical follow-up of the patient.
Technical success of the biopsy procedure was defined as successful access to the lesion site with the biopsy forceps and successful acquisition of tissue samples. A biopsy sample was considered adequate for histopathologic examination if the pathologist was able to render a histologic diagnosis on the basis of the sample provided.
The usual routine at our institution for diagnostic imaging of patients suspected of having hepatobiliary malignancy includes both ultrasonography (US) and computed tomography (CT). US and CT scans of the abdomen obtained in all patients revealed biliary dilatation. Forty-six (35%) of the 130 patients had no evidence of a mass lesion responsible for the biliary dilatation—the presence of a mass lesion was inferred from ductal strictures—and 45 patients (35%) were suspected of having small ductal or periductal tumors at CT and/or at US. In the remaining 39 patients (30%), CT or US depicted a mass lesion responsible for the biliary dilatation.
Twenty-six patients had a history of malignant tumor (16 gastric carcinomas, four pancreatic carcinomas, two gallbladder carcinomas, one anal carcinoma, one bronchogenic carcinoma, one uterine cervical carcinoma, and one lymphoma) and had been treated with surgery and/or chemotherapy. Informed consent for the procedure was obtained from each patient. This study was approved by our university committee on human investigation.
Procedure
Broad-spectrum antibiotics, including 2 g of cefuroxime sodium (Alporin; Glaxo SmithKline-Korea, Seoul, South Korea) or 400 mg of ciprofloxacin hydrochloride (Ciprobay; Bayer-Korea, Seoul, South Korea), were routinely administered for both the drainage and the biopsy procedures. For conscious sedation, 1–2 mg of lorazepam (Ativan; Wyeth-Korea, Gunpo, South Korea) was administered intravenously before the procedure. Percutaneous transhepatic cholangiography and biliary drainage were performed with the standard technique as previously described (16). Biopsy was performed during the biliary drainage procedure in 98 patients. In 32 patients, the biopsy was delayed 2–12 days (average, 4 days) for alleviation of cholangitis or hemobilia.
The biopsies were performed as previously discussed (13–15). Briefly, after passage of a 145-cm, 0.035-inch guide wire (Radiofocus M, Terumo, Tokyo, Japan or Amplatz Superstiff, Medi-tech/Boston Scientific, Watertown, Mass) through the lesion to the common bile duct or down to the duodenum, a 25-cm, 8-F sheath (Cook, Bloomington, Ind) was advanced over the guide wire with its tip positioned within the stricture area. Subsequently, the dilator was removed and the outer sheath and guide wire were left in place. The biopsy forceps was then inserted through the sheath into the stricture, and biopsy was performed with fluoroscopic guidance (Fig 2). We tried to obtain specimens at the center of the stricture whenever possible. If the cutting jaws of the forceps could not open within the stricture due to the tightness of the lesion, specimens were obtained at the proximal part of the stricture. In each patient, three to five biopsy specimens (mean, 4.1 specimens) were taken from the lesion and were fixed with formalin to be sent for histopathologic examination. All biopsy specimens were examined by one pathologist (H.K.C.) whose specialty is hepatobiliary disease.
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Figure 2a. Images obtained in a 44-year-old woman with jaundice. (a) Percutaneous transhepatic cholangiogram shows a stricture (arrows) in the proximal common bile duct. (b) Percutaneous transhepatic cholangiogram shows the biopsy forceps (arrow), which is inserted through a sheath to enable biopsy of the region of the stricture.
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Figure 2b. Images obtained in a 44-year-old woman with jaundice. (a) Percutaneous transhepatic cholangiogram shows a stricture (arrows) in the proximal common bile duct. (b) Percutaneous transhepatic cholangiogram shows the biopsy forceps (arrow), which is inserted through a sheath to enable biopsy of the region of the stricture.
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The lesions involved the common bile duct (n = 58), common hepatic duct (n = 39), hilum (n = 14), ampullary segment of the common bile duct (n = 11), right intrahepatic bile duct (n = 3), left intrahepatic bile duct (n = 2), or the entire extrahepatic bile duct (n = 3). A stricture located within the distal 2 cm of the common bile duct and extending down to the level of the ampulla of Vater was considered to be a stricture of the ampullary segment of the common bile duct. After biopsy, an external or internal-external catheter was placed in all patients, and a cholangiogram was obtained to evaluate for potential extravasation of contrast material from the biopsy site. Placement of a biliary metallic stent, performed in 32 patients, was deferred until the biopsy results had been obtained. All procedures were performed on an inpatient basis.
The final diagnosis for each patient was rendered with histologic analysis at surgery or on the basis of other histologic or cytologic studies (ie, FNAB or a study of ascitic fluid). In the absence of histologic or cytologic studies, the final diagnosis was of malignancy if there was increase in size of the lesion and/or development of a metastasis on follow-up imaging studies or if there was progressive degradation of the patient’s general condition.
Statistical Evaluation
Sensitivity, specificity, positive and negative predictive values, and accuracy were calculated for the biopsy technique. For statistical purposes, a pathologic result reported as "inadequate" or as "suspicious" but not definitely diagnostic for a malignant tumor was regarded as a negative result. Overall sensitivity values were compared according to the type of primary tumor and the site of the lesion. Statistical analysis was performed with the 2 test, with a P value of .05 or less considered to indicate a significant difference.
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RESULTS
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All biopsy procedures were technically successful. Biopsies were performed with a right-sided approach in 127 patients and with a left-sided approach in three patients. Complications occurred in eight patients (6%); these included hemobilia (n = 6) and biloma (n = 2). All cases of hemobilia were transient and resolved within 24 hours. The two cases of biloma were successfully treated with percutaneous catheter drainage. There were no complications requiring emergency surgery or blood transfusion.
The final diagnosis was malignant disease in 125 patients (Table 1). The diseases included cholangiocarcinoma (n = 82), pancreatic carcinoma (n = 14), hepatocellular carcinoma (n = 3), lymphoma (n = 1), and metastatic carcinoma (n = 25). The diagnosis of malignant disease was confirmed with pathologic findings at surgery (n = 56); with histologic or cytologic findings after FNAB or sampling of ascitic fluid (n = 36); with evidence at radiologic follow-up of increase in size of the lesion (n = 7) or development of a metastasis to the lymph nodes (n = 5), liver (n = 6), or lung (n = 3); or with a deteriorating clinical course resulting in death (n = 12). One hundred twenty-one of the 125 patients died (median survival, 6 months; range, 1–45 months). Four patients were alive as of this writing, for a median survival of 12.5 months (range, 10–28 months); all four have histologically confirmed cholangiocarcinoma. The final diagnosis in the remaining five patients was benign disease, including chronic cholangitis (n = 3), chronic pancreatitis (n = 1), and Mirizzi syndrome (n = 1). All diagnoses of benign disease were confirmed with surgical biopsy results in conjunction with negative results during a median follow-up of 38 months (range, 15–55 months).
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TABLE 1. Final Diagnoses and True-Positive Results in 130 Patients Suspected of Having Malignant Biliary Obstruction
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The histologic results of forceps biopsy are shown in Table 2. Ninety-eight of the 130 biopsies resulted in a correct diagnosis of malignancy. The specific histologic diagnosis was made in 95 cases. The remaining three cases were definitely carcinoma, although the exact histologic type was not determined. There were five true-negative diagnoses. The remaining 27 diagnoses at biopsy were considered to be false-negative and included chronic inflammation (n = 21), findings suspicious for carcinoma (n = 3), and inadequate samples (n = 3). In the three cases of inadequate sample, necrotic or fibrinous materials were obtained from the specimens. There were no false-positive diagnoses. For the diagnosis of malignant biliary obstruction, transluminal forceps biopsy had a sensitivity of 78.4% and a specificity of 100%. Although the positive predictive value was 100%, the negative predictive value was only 15.6%. The overall accuracy of forceps biopsy for correct diagnosis of all biliary lesions was 79.2% (103 of 130 cases).
Patients with malignant tumors were placed into one of two groups according to the origin of the primary tumor: those with cholangiocarcinoma (n = 82) and those with biliary obstruction caused by direct extension of tumor or metastatic disease to perihepatic or portal lymph nodes (n = 43). The sensitivity of transluminal forceps biopsy was higher in patients with cholangiocarcinoma than in patients with malignant tumors other than cholangiocarcinoma (86.6% vs 62.8%, P < .005) (Table 3).
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TABLE 3. Comparison of Results of Forceps Biopsy according to Type of Primary Tumor in 125 Patients with a Final Diagnosis of Malignant Biliary Obstruction
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The sensitivity of forceps biopsy varied depending on the site of obstruction (Table 4). The sensitivity of forceps biopsy was significantly lower, usually more than two times lower, in cases of stricture at the ampullary segment of the common bile duct than in cases of stricture at other sites (P < .01).
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DISCUSSION
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An accurate diagnosis of the causes of biliary obstruction is of the utmost importance in providing appropriate treatment to patients with obstructive jaundice. It is not always possible to distinguish benign from malignant biliary obstruction with imaging studies alone (6). Therefore, histologic confirmation for correct diagnosis is often required from both a therapeutic and a prognostic viewpoint. Percutaneous FNAB with US or CT guidance, the standard method of tissue acquisition in various abdominal diseases, is frequently unsuccessful in biliary tumors, with a reported sensitivity of 42%–67% (7–9).
Currently, various transluminal techniques for acquiring tissue from biliary tumors are performed through a PTBD tract; PTBD is usually performed in patients with malignant or benign biliary obstruction for preoperative or palliative decompression of the bile ducts. Because most biliary tumors arise from ductal epithelium, tissue obtained through the bile duct from abnormal ductal segments seems appropriate for pathologic examination. Collection of bile for cytologic examination is a simple technique but is rarely used because of its poor results (17). Brush cytology performed during PTBD or during endoscopic retrograde cholangiography has proven to be a safe and popular technique but seems to be of limited diagnostic value because of its superficial sampling nature and reported sensitivity of 44%–67% (18–20). In an attempt to further increase the diagnostic value of biopsy of the bile duct, a transluminal biopsy technique has been developed that incorporates the use of biopsy forceps.
The present large series shows that transluminal forceps biopsy of biliary tumors provides a relatively high accuracy in the diagnosis of malignant biliary obstruction. The overall accuracy of forceps biopsy was 79.2%, with a sensitivity of 78.4% and a specificity of 100%. These numbers compare favorably with those of FNAB and brush cytology in the diagnosis of malignant biliary obstruction. Biliary tumors are particularly difficult to confirm with the conventional FNAB technique because, despite the presence of biliary strictures, the tumors are often small. In 91 (70%) of the 130 patients in the present study, the tumors were small or not even visible; their presence was inferred from the existence of ductal strictures. The transluminal approach offers a direct and accurate route for biopsy of biliary tumors, and a specimen can be obtained from a region that appears abnormal on a cholangiogram even when the tumor responsible for the stricture is not clearly visible at CT or at US. Forceps biopsy also enables the acquisition of deeper samples than does brush cytology. Although there is a large variation in the reported sensitivity of transluminal forceps biopsy, with values ranging from 30% to 100%, studies in relatively large groups of patients (12–14) obtained results comparable to ours (ie, overall sensitivities of 71%–78% were observed in 16–24 patients).
Other reported transluminal biopsy techniques include the use of a Simpson atherectomy catheter (21,22). The reported sensitivity of 79% (22) for this technique is comparable to that achieved with our technique. However, the main disadvantages of the use of a Simpson atherectomy catheter are the difficulties in passing this rigid instrument through an acutely angled transhepatic tract, the high cost of the device, and the risk of bile duct injury and hemorrhage. Schechter et al (22) reported that 11% of their patients experienced transient but clinically important hemorrhages.
Percutaneous cholangioscopic transluminal forceps biopsy of the bile duct offers the greatest chance to obtain malignant cells because it enables more accurate targeting and direct inspection of the lesion; its reported sensitivity in the diagnosis of cholangiocarcinoma is 96% (23). However, this technique is more difficult, time consuming, and expensive than other transluminal techniques because the PTBD tract must be dilated to accommodate the cholangioscope (15). Moreover, the utility of cholangioscopic forceps biopsy in the diagnosis of extrabiliary malignancy remains limited (23). Therefore, cholangioscopic forceps biopsy should be reserved for cases in which other, simpler techniques have failed (14,15).
The sensitivity of forceps biopsy in the present study varied according to the origin of the primary lesion causing the obstruction and according to the site of obstruction. Many extrabiliary cancers may cause biliary obstruction by metastasizing to the lymph nodes around the extrahepatic bile duct, through direct neoplastic invasion of the biliary tree, or by compressing the biliary tree without direct invasion (24,25). Sato et al (26) found that in percutaneous transhepatic cholangioscopy-guided forceps biopsy of the bile duct, biopsy specimens were obtained from only the mucosa and superficial part of the fibromuscular layer of the duct. They suggested that forceps biopsy is therefore less helpful for detecting extrinsic tumors or tumors in the deep part of the bile duct wall. Our study showed that the sensitivity of forceps biopsy in patients with malignant tumors other than cholangiocarcinoma (62.8%) was significantly lower than its sensitivity in patients with cholangiocarcinoma (86.6%). Terasaki et al (11) reported a sensitivity of 100% for forceps biopsy, even in five patients with extrinsic malignancy. This discrepancy may be explained by differences in depth of infiltration of the bile duct wall by the extrinsic malignancy.
In our study, the sensitivity of forceps biopsy was lower in the ampullary segment of the common bile duct (36.4%) than in other sites. In our experience, obstructions in the distal part of the common bile duct were difficult to sample satisfactorily at biopsy because the forceps jaws frequently faced the side wall of the duct rather than the wall of the obstructed region perpendicularly because of angulation in that area. In addition, in five of 11 cases of obstruction in the ampullary segment of the common bile duct, the cause was an extrabiliary tumor. These factors could explain the lower sensitivity.
A limitation of our study was the lack of confirmative histologic diagnoses in a large number of patients (25%), in whom the final diagnosis was rendered on the basis of follow-up only. However, multiple surgical biopsies occasionally reveal only inflammatory tissue due to the considerably inflammatory and/or desmoplastic nature of biliary and pancreatic tumors (27,28). Moreover, the distinction between cholangiocarcinoma and sclerosing cholangitis can be difficult for the pathologist to make, even with surgical specimens (29). Therefore, clinical or radiologic follow-up is sometimes useful in confirming a diagnosis of malignancy. We followed up such patients fully so that we could confirm the final diagnosis clinically.
As regards the feasibility of the procedure, we concur with other researchers (11–14) that this procedure is safe and easy to perform in conjunction with PTBD. In the present study, it was easy to get to the stenosis with the biopsy forceps, allowing specimens that were adequate for histologic examination to be obtained in most patients. The complication rate was low (6%); eight patients experienced minor complications of hemobilia or biloma. Theoretically, major hemorrhage resulting from injury to an adjacent blood vessel or a bile leak could occur as a complication of forceps biopsy of the bile duct (11). However, such complications have not been reported in the literature and were not seen in the present study. In our study, two cases of biloma were thought to be caused by the drainage process rather than by the biopsy procedure because the bilomas occurred in subcapsular locations far from the biopsy site.
In conclusion, percutaneous transluminal forceps biopsy is simple and easy to perform in conjunction with PTBD and has a low complication rate and relatively high accuracy for the diagnosis of malignant biliary obstruction. The overall sensitivity of forceps biopsy in the present study compares favorably with those of bile cytology and brush cytology, as well as with that of FNAB. This technique is particularly useful for the diagnosis of cholangiocarcinoma. Therefore, we believe that transluminal tissue sampling during PTBD should be the first-line approach for tissue diagnosis of biliary obstruction, with forceps biopsy as the preferred technique.
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ACKNOWLEDGMENTS
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We thank Bonnie Hami, MA, Department of Radiology, University Hospitals Health System, Cleveland, Ohio, for editorial assistance in preparing the manuscript.
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FOOTNOTES
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Abbreviations: FNAB = fine-needle aspiration biopsy,
PTBD = percutaneous transhepatic biliary drainage
Author contributions: Guarantor of integrity of entire study, G.S.J.; study concepts, G.S.J., S.W.L.; study design, all authors; literature research, G.S.J.; clinical studies, G.S.J., S.U.L., B.H.H.; data acquisition, G.S.J., J.D.H.; data analysis/interpretation, all authors; statistical analysis, G.S.J.; manuscript preparation and definition of intellectual content, G.S.J.; manuscript editing, J.D.H., H.K.C., Y.D.C.; manuscript revision/review, all authors; manuscript final version approval, G.S.J., Y.D.C.
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ABSTRACT
INTRODUCTION
