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US-guided Percutaneous Biopsy of Small (1-cm) Hepatic Lesions¹

¹ From the Departments of Diagnostic Radiology and Organ Imaging (S.C.H.Y., C.M.), Anatomical and Cellular Pathology (C.T.L.), Surgery (W.Y.L.), and Clinical Oncology (T.W.L.), Prince of Wales Hospital, 30-32 Ngan Shing St, Shatin, New Territories, Hong Kong. From the 1999 RSNA scientific assembly. Received December 6, 1999; revision requested January 13, 2000; revision received March 20; accepted April 3. Address correspondence to S.C.H.Y. (e-mail: chymyl@netvigator.com).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To determine the accuracy of ultrasonography (US)-guided percutaneous biopsy in diagnosing malignant neoplasms for hepatic lesions 1 cm or smaller.

MATERIALS AND METHODS: In this prospective study, 64 consecutive patients with 74 discrete focal hepatic lesions depicted at US were referred for liver biopsy to confirm the exact nature of the lesions. Mean lesion size was 0.84 cm ± 0.13 (range, 0.5–1.0 cm). Biopsy was performed with an 18-gauge automated biopsy gun in 46 lesions (once [n = 37], twice [n = 7], three times [n = 2]) or a 22-gauge needle in 28 lesions (once [n = 23], twice [n = 4], three times [n = 1]). Measures were taken to ensure accurate and effective lesion sampling. The histologic diagnosis of malignant tumor and findings on follow-up US images of "benign" nodules for 15–39 months were the criterion standard.

RESULTS: No complications occurred. All specimens obtained were sufficient for diagnosis. Histologic examination revealed various types of primary and secondary malignant tumors (n = 44), hemangioma (n = 5), cirrhosis (n = 13), focal fatty change (n = 8), focal fatty sparing (n = 2), and abscess (n = 2). The diagnostic discrimination of US-guided biopsy in diagnosing malignant tumors in these small lesions was sensitivity, 98%; specificity, 100%; positive predictive value, 100%; negative predictive value, 97%; and accuracy, 99%.

CONCLUSION: Percutaneous biopsy under US control is highly accurate in providing a definitive histologic diagnosis of malignant neoplasms for small hepatic lesions if measures for ensuring precise and effective lesion sampling are taken.

Index terms: Biopsies, technology, 76.1261, 76.12985 • Liver, biopsy, 76.1261, 76.12985 • Liver, diseases, 761.21, 761.79 • Liver, nodules, 76.31, 76.32 • Liver neoplasms, diagnosis, 76.1261, 76.12985, 76.30 • Ultrasound (US), guidance, 76.12985

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
We are still in an era when surgical resection and its local ablative alternatives remain the preferential treatment for hepatic malignancies. Such treatment strategy demands accurate morphologic staging of the disease in terms of size and number of lesions and the extent of structure or organ involved. Therefore, it is not sufficient to have a specific hepatic malignancy diagnosed early on the basis of a tumor marker that is detected in the peripheral blood; we need to locate exactly where the tumor is before we can treat it. For the same reason, it is not sufficient to have small liver nodules detected early with imaging; we need to confirm the benign or malignant nature of those lesions, if not the definitive histologic diagnosis. Indeed, recent developments in tumor markers (1–3) have increased the specificity of serologic diagnosis for hepatic malignancies, and technical achievements in medical imaging have increased the sensitivity for detection of small liver lesions. Such advances have led to a decrease in the presenting size of focal liver lesions when they are detected. However, conventional imaging modalities to date are still inaccurate (60%) for diagnosing liver nodules 2 cm or smaller (4,5), and the supposedly highly specific technique of positron emission tomography (PET) is insensitive (43%) for lesions 1 cm or smaller (6); thus, biopsy often remains necessary for providing a definitive histologic diagnosis, which is mandatory for a treatment decision in patients in whom suspicious small liver lesions have been detected. The effectiveness of percutaneous biopsy in diagnosing small hepatic lesions of 3 cm or smaller (7,8) and 1.5 cm or smaller (9) has been evaluated in the literature. The purpose of our study was to determine the accuracy of ultrasonography (US)-guided percutaneous biopsy in diagnosing malignant neoplasms for small hepatic lesions of 1 cm or less.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
This was a prospective study including 64 patients (48 male patients, 16 female patients; mean age, 52 years ± 15; age range, 9–78 years) who were referred to our department of radiology between July 1996 and March 1999 for percutaneous biopsy of liver lesions. All patients who met the entry criteria during this period were included. The entry criteria were (a) the presence of at least one discrete and US-depictable small focal liver lesion of maximum diameter 1 cm or less and (b) a clear clinical indication for biopsy. All patients had a clinical suspicion of hepatic malignancy that needed to be confirmed and preferably also typed histologically or staged prior to the treatment decision of surgery, local ablative therapy, intraarterial therapy, or systemic chemotherapy. The patients had a history of hepatocellular carcinoma with liver resection performed (n = 6); nonhepatic malignancy including carcinoma of the cervix, fibrosarcoma of an ovary, nasopharyngeal carcinoma, and acute myeloid leukemia (n = 13); undiagnosed nonhepatic tumor mass (n = 17); or hepatitis B viral cirrhosis, with the patient undergoing screening for hepatocellular carcinoma (n = 28).

Altogether, biopsy was performed of 74 lesions in the 64 patients: biopsy of one lesion in 55 patients, two lesions in eight patients, and three lesions in one patient. No patient was required to come back for a repeat biopsy because of diagnostic failure in any of the lesions. The lesions measured 0.5–1.0 cm in maximum diameter (mean, 0.84 cm ± 0.13 [SD]). They were located 0.8–5.8 cm deep to the liver capsule (mean, 2.8 cm ± 1.3); 25 were in the left lobe and 49 in the right lobe. The lesions were not demonstrable in one of 15 lesions examined with spiral computed tomography (CT) with triphasic contrast material enhancement; in six of 22 lesions, with digital subtraction angiography; and in nine of 19 lesions, with iodized oil–enhanced CT. The reason these particular small lesions were selected for biopsy was (a) they were the only lesions in those livers (n = 23), (b) they were the only lesions in those liver lobes (n = 5), (c) they were more safely accessible (n = 8), (d) all the lesions in the liver were 1 cm or smaller (n = 15), or (e) just because of their small size (1 cm) (n = 23). Biopsy was performed with either an intercostal (n = 49) or subcostal (n = 25) approach.

The usual routines at our institution for patient preparation, local anesthesia, biopsy procedures and precautions, and postbiopsy patient care were followed (8,10). It is a routine practice at our institution to keep the patients at bed rest overnight after biopsy for observation. The time of patient discharge and any adverse effects were recorded. All biopsies were performed with a freehand technique under US guidance by one radiologist (S.C.H.Y.) who had 4 years and about 400 cases of experience in biopsy of liver lesions prior to commencement of this study. Commercially available US equipment with a 3.5-MHz curvilinear transducer (model SSD-2000; Aloka, Tokyo, Japan) was used.

A needle path from the skin surface was selected to aim at the lesion when the patient was in normal uninterrupted respiration. The patient was instructed to suspend respiration when the needle punctured through the liver capsule, but afterward the patient was allowed to breathe again so that there was sufficient time for accurate positioning of the needle. The needle was guided to pass through the center of the lesion at a plane in which the largest cross-sectional diameter of the lesion was visualized, with subtle bilateral tilting of the US transducer to ensure that the needle did not deviate from its destined path (Fig 1). The patient was requested to hold his or her breath again if necessary when the needle entered the lesion. Desirable positioning of the needle through the lesion was confirmed when a needle-free lesion was visualized in two additional planes on both sides of the needle.

View larger version (159K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Oblique US images of the right lobe of liver show precise positioning of the biopsy needle within the lesion. (a) Path of an 18-gauge side-cutting biopsy needle passing through the center of a small lesion (arrows). (b) Tip of a 22-gauge end-cutting biopsy needle positioned within a small lesion (arrows).

View larger version (178K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Oblique US images of the right lobe of liver show precise positioning of the biopsy needle within the lesion. (a) Path of an 18-gauge side-cutting biopsy needle passing through the center of a small lesion (arrows). (b) Tip of a 22-gauge end-cutting biopsy needle positioned within a small lesion (arrows).

The criterion for adequate lesion sampling was extraction of a sharply cut tissue core. Additional biopsy was performed if the specimen did not fulfill this criterion. The adequacy of the specimen obtained in each biopsy was determined by the radiologist, who made the judgment according to the gross appearance of the tissue cores without the help of an attending pathologist or a pathology technologist. For most of the lesions (n = 60), one biopsy with one pass of the needle was sufficient to obtain one or more tissue cores. Two biopsies were performed in 11 lesions, and three biopsies were performed in three lesions. There was no substantial difference in the proportion of numbers of repeat biopsy for the 18-gauge side-cutting and 22-gauge end-cutting needles. Among the 46 lesions for which the 18-gauge side-cutting needle was used, biopsy was performed once in 37 lesions (80%), twice in seven lesions (15%), and three times in two lesions (4%). Among the 28 lesions for which the 22-gauge end-cutting needle was used, biopsy was performed once in 23 lesions (82%), twice in four lesions (14%), and three times in one lesion (4%). The length of tissue cores obtained with 18-gauge side-cutting needles was 0.5–1.5 cm (mean, 1.3 cm ± 0.3); with 22-gauge end-cutting needles, the total length of whitish cores was 0.4–5.5 cm (mean, 1.5 cm ± 1.3). The tissue cores were preserved with formalin, and all were sent to the pathology department for histologic examination. For those 14 lesions in which multiple biopsies were performed, the tissue specimen of each individual biopsy was collected in a separate specimen bottle so that the histologic finding and diagnostic value of each individual biopsy could be evaluated.

The histologic finding of benign or malignant liver tumor in the biopsy specimen was taken as the true nature of the lesion that underwent biopsy. Lesions with a histologic finding of benign nonneoplastic conditions in their biopsy specimen were reexamined with US every 3 months for 15–39 months to confirm their benign nature. The "true nature of the lesions," which was taken as the criterion standard for evaluation of the diagnostic discrimination of biopsy, was therefore established according to (a) the histologic finding of typical features of a benign or malignant liver tumor in the biopsy specimen or (b) the US finding of unchanged or diminished size of the biopsy lesion on three subsequent monthly US follow-up examinations for 15–39 months, for lesions with a histologic finding of benign nonneoplastic conditions in the biopsy specimen.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
All patients were discharged well on the next day. The only adverse effect that occurred in some patients was abdominal discomfort or tolerable mild abdominal pain, which subsided after a few hours. All small lesions that were US accessible and depictable were accessible for biopsy. No lesion was excluded because of an accessibility problem. The sampling notch and cannula of the 18-gauge side-cutting needle and the tip of the 22-gauge end-cutting needle with and without the stylet were always visible with US. Nine of the 28 22-gauge end-cutting needles used in this study consisted of a microgranular surface at the distal shaft, which was designed for trapping microbubbles at the needle surface for echogenic enhancement. The distal shaft of these nine needles was visible at US.

Tissue cores of nonhemangioma liver tumors obtained with the 18-gauge side-cutting needles were usually light colored in the middle, sandwiched by reddish liver tissue at both ends (Fig 2a). Tissue specimens of nonhemangioma liver tumors extracted with the 22-gauge end-cutting needles usually comprised multiple light-colored tissue cores intermingled with reddish liver tissue or blood clots (Fig 2b). The presence of such features in the biopsy specimen was always indicative of precise and adequate lesion sampling. The specimen obtained for each lesion, with an end-point criterion of having a sharply cut tissue core extracted, was always of adequate amount and sufficient quality for histologic assessment in all 74 lesions. The specimens were free from notable crushing artifacts that created interpretation difficulties.

View larger version (34K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Photographs show the features that indicate precise and adequate lesion sampling of a nonhemangioma liver tumor: (a) a tissue core (obtained with 18-gauge side-cutting needle) with a light-colored lesion in the middle (large arrows) sandwiched by reddish liver tissue at both ends (small arrows) or (b) tissue cores (obtained with a 22-gauge end-cutting needle) with multiple light-colored cores of the lesion (large arrow) intermingled with reddish liver tissue or blood clots (small arrow). Many tissue cores can be extracted in a single biopsy with eight to 10 advancements and withdrawals of a 22-gauge end-cutting needle across the lesion, as illustrated in this case.

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Photographs show the features that indicate precise and adequate lesion sampling of a nonhemangioma liver tumor: (a) a tissue core (obtained with 18-gauge side-cutting needle) with a light-colored lesion in the middle (large arrows) sandwiched by reddish liver tissue at both ends (small arrows) or (b) tissue cores (obtained with a 22-gauge end-cutting needle) with multiple light-colored cores of the lesion (large arrow) intermingled with reddish liver tissue or blood clots (small arrow). Many tissue cores can be extracted in a single biopsy with eight to 10 advancements and withdrawals of a 22-gauge end-cutting needle across the lesion, as illustrated in this case.

Thus, there were 44 true-malignant and biopsy-malignant lesions, one true-malignant but biopsy-benign lesion, zero true-benign but biopsy-malignant lesions, and 29 true-benign and biopsy-benign lesions. The diagnostic discrimination of percutaneous biopsy in diagnosing malignant tumors in the present series of small liver lesions was as follows: sensitivity, 98% (44 of 45 lesions); specificity, 100% (29 of 29 lesions); positive predictive value, 100% (44 of 44 lesions); negative predictive value, 97% (29 of 30 lesions); and accuracy, 99% (73 of 74 lesions).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Great effort has been spent on developing new techniques for various imaging modalities to improve the accuracy for detection and characterization of focal hepatic lesions and include the application of Doppler US (11,12), a US contrast agent (13), magnetic resonance (MR) imaging sequences, and MR imaging contrast agents (14–18). The effectiveness of such techniques in liver nodule imaging is variable, and the findings of their application in small liver lesions are often not mentioned. Other studies in which the issue of small lesion diagnosis is addressed (4,5,6) show rather disappointing results. The accuracy of imaging diagnosis of small hepatocellular carcinoma with digital subtraction angiography and MR imaging decreased from 68% for nodules 1.1–2.0 cm to 45% for nodules 1 cm or smaller (4). Although PET is specific (95%) for diagnosing liver metastases, its sensitivity decreases from 97% for nodules larger than 1 cm to 43% for nodules 1 cm or smaller (6). For small nodules in cirrhotic liver, US is not specific and CT and MR imaging are not sensitive for diagnosis (5). Laparoscopic US increases the detection rate of small liver nodules but does not increase the characterization power in diagnosing these lesions (19).

Characterization problems and diagnostic inaccuracy for small liver tumors, more likely to occur in small liver tumors of 1 cm or less, may lead to incorrect patient treatment such as having the patient undergo unnecessary hepatectomy for a benign lesion or having the patient lose the chance of a curative hepatectomy, and perhaps even to receive systemic chemotherapy instead, because of overstaging. A definitive histologic diagnosis of small liver nodules detected in patients suspected or confirmed to have malignancy is often crucial for accurate tumor staging and allows selection of the most appropriate treatment for the individual patients.

Results of the present study indicate that US-guided biopsy can be highly accurate in providing a definite histologic diagnosis for small (1-cm) liver lesions that have commonly been a diagnostic problem for various imaging modalities. We believe such results are repeatable if measures to ensure precise and effective lesion sampling are taken, which include (a) confirmation of accurate positioning of the biopsy needle within the lesion (Fig 1) by visualization of a needle-free lesion in two additional planes on both sides of the needle, (b) the use of cutting needles for extracting uncrushed tissue cores for histologic assessment, and (c) confirmation of adequate sampling of the lesion specimen by obtainment of sharply cut tissue cores (Fig 2).

Small tumors of 1 cm or less are known to consist solely of a uniform distribution of cancerous tissue without hemorrhage, necrosis, or sclerotic change (21). The diagnostic accuracy of biopsy in these tumors is determined by the accuracy of lesion sampling and the degree of preservation of the specimen during the process of sampling, and the diagnostic accuracy of biopsy is likely a reflection of the advancements in the quality of the imaging device and the biopsy needle and the improvement of biopsy technique. The diagnostic accuracy of percutaneous needle biopsy in lesions 1 cm or smaller has increased from 79% (n = 24) in 1987 (20) to 87.5% (n = 24) in 1993 (7), and to 99% (n = 74) in 1999 (current study). The use of a freehand biopsy technique under US guidance is a common feature of all these series. The advantage of real-time and full-control multiplanar visualization provided by US is well known. A freehand technique allows subtle needle adjustments to compensate for respiratory movements and delicate bilateral transducer tilting for accurate lesion targeting. As compared with US, CT without the use of contrast agents cannot offer the high degree of clarity with which the vessels and small lesions are depicted at US. Also, respiratory movement is a big problem for CT of small lesions. In three previous studies (7,9,20), the decision on the adequacy of the specimen was made by a cytopathologist, and for that reason the biopsy procedure had to be withheld intermittently for a variable length of time. Sometimes up to six biopsies were required for a lesion (7). In the present study, the adequacy of the specimen was determined by the radiologist alone, without the need for an attending pathologist or pathology technologist. The adequacy of the specimen, as judged according to the gross appearance of the tissue cores, with the criterion of having a sharply cut tissue core extraction always sufficient for diagnosis (Fig 2). For most of the lesions, only one biopsy with one needle pass was required.

Although US-guided needle biopsy is applicable to the majority of small liver lesions, its feasibility is limited by the accessibility of the lesion to US. The degree of lung inflation, the size of the liver, the bowel position, and the amount of gaseous bowel content are all potential sources of limitation. For biopsy of small liver lesions, it is also essential that the patient be able to hold his or her breath; breathe in a normal, slow, regular, and shallow manner; and follow instructions of what to do and when.

This was a technique-based study in which the diagnostic accuracy of the procedure under evaluation was dependent on the skill of the operator who performed the biopsies. The fact that only one radiologist was involved in the biopsy procedure eliminates interoperator variability in this study, but the very same fact does not allow the assessment of interoperator variability in applying this technique. Therefore, we do not know to what extent the applicability of this technique can be generalized.

Percutaneous biopsy under US control is highly accurate for a definitive histologic diagnosis of small hepatic lesions of centimeter and subcentimeter size if measures ensuring precise and effective lesion sampling are taken; it is a highly applicable useful means for solving the common diagnostic imaging problem of the detection-characterization gap for small lesions of suspected malignant nature. Biopsy needles that produce good tissue cores increase the effectiveness of the biopsy procedure and eliminate the need for an attending cytopathologist.

	FOOTNOTES

 
Author contributions: Guarantors of integrity of entire study, all authors; study concepts and design, all authors; definition of intellectual content, all authors; literature research, S.C.H.Y.; clinical studies, S.C.H.Y., W.Y.L., T.W.L.; data acquisition, S.C.H.Y., C.T.L.; data analysis, all authors; statistical analysis, S.C.H.Y.; manuscript preparation, all authors; manuscript editing, S.C.H.Y., C.M.; manuscript review and final version approval, all authors.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Yu, S. C. H. Articles by Metreweli, C. Search for Related Content PubMed PubMed Citation Articles by Yu, S. C. H. Articles by Metreweli, C.