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Original Research |
1 Department of Radiology, University of Michigan Hospitals, Ann Arbor, MI
48019-0030.
2 Present address: Department of Radiology, Stanford University Medical Center,
300 Pasteur Dr., Room H1307, Stanford, CA 94305-5227.
3 Present address: Department of Radiology, Beaumont Hospital, Royal Oak, MI
48073.
4 Department of Internal Medicine, Division of Gastroenterology, University of
Michigan Hospitals, Ann Arbor, MI 48019-0030.
Received August 3, 2005;
accepted after revision September 29, 2005.
Address correspondence to K. E. Maturen
(katematuren{at}yahoo.com).
Abstract
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MATERIALS AND METHODS. Retrospective review identified 128 patients with imaging-guided percutaneous liver biopsies positive for HCC. A coaxial cutting needle technique was uniformly used with a 17-gauge introducer and 18-gauge biopsy needle. Radiology and clinical reports were reviewed, and findings at clinical and imaging follow-up were assessed.
RESULTS. During the 6-year study period, 1,012 liver mass biopsies were performed, with 128 positive for HCC (100 men and 28 women; average age, 58.4 years). One hundred one patients had more than 30 days of clinical or imaging follow-up (or both) after biopsy (mean, 410 days; range, 33-1,989 days) and constituted the study population. The remaining 27 were excluded because of inadequate follow-up. No suspected or confirmed tumor seeding on imaging, physical examination, or laparotomy was identified.
CONCLUSION. We found no tumor seeding after percutaneous biopsy of HCC using a coaxial cutting needle technique. This rate, 0%, is lower than those reported with other techniques. The use of a needle introducer that remains in position during multiple cutting needle passes protects normal tissue along the track and may reduce seeding. This has particular importance for patients with stage I-II HCC, for whom liver transplantation may be curative.
Keywords: abdominal imaging • biopsy • hepatocellular carcinoma • liver cancer • liver disease
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-fetoprotein are often unreliable in
patients with chronic liver disease
[4]. Therefore, tissue
diagnosis may be crucial to appropriately direct therapy. However, the risk of
potential complications from percutaneous biopsy—in particular, the
deposition of viable tumor cells or "seeding" along the needle
track—has deterred some physicians from fully accepting this approach
and integrating it into standard clinical practice
[5,
6]. The reported literature encompasses a variety of biopsy and follow-up techniques in patients with HCC and perhaps, consequently, a variety of tumor seeding rates. The reported rates of seeding have ranged from 0.6% to 5.1% in most reports using fine-needle aspiration biopsy (FNAB) [7], with a single exceptional report of 12.5% seeding after FNAB and radiofrequency ablation in a small population [8]. Seeding rates from 0.76% to 3.4% have been reported using a cutting needle technique [9-12]. Seeding rates for a coaxial cutting needle technique have not been reported to our knowledge. To contribute to this debate, we undertook this study to assess the incidence of seeding in a single population treated using a uniform biopsy technique and undergoing clinical follow-up over a 6-year period.
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-fetoprotein levels were documented. Tumor characteristics
including size, number, location, and morphology were recorded from
prospective radiology reports of CT and MRI studies performed before
biopsy.
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50,000/µL
or were corrected. Coagulation status was also corrected, when appropriate, to
ensure an international normalized ratio (INR) of 
1.5 at the time of
biopsy in all patients. Biopsies were performed with all patients under
conscious sedation except one; in that patient, general anesthesia was used
due to autism and developmental delay precluding cooperation. Preprocedural
sonographically guided paracentesis was performed in 10 patients with marked
ascites to improve lesion accessibility. Biopsies were sonographically guided in all but three cases; in those cases, CT was used because of superior lesion conspicuity on CT compared with sonography. A coaxial cutting needle technique was uniformly used with a 17-gauge introducer and an18-gauge biopsy needle that has a side-cut specimen notch in the central stylet (ASAP and Easy Core needles and Pinpoint introducer, Boston Scientific) (Fig. 1). The needle introducer remained in position while multiple passes were made with the cutting needle. Up to four cores were obtained from each tumor, with three or four cores obtained in most patients. Neither a pathologist nor a cytology technician was present in the biopsy suite, so samples were prepared in formalin and hand-carried to the pathology laboratory. Because of operator preference or bleeding around the introducer, procoagulant agents were injected along the needle track in some patients: absorbable bovine collagen (Helitene, Integra LifeSciences) in 30 patients and absorbable pork gelatin powder (Gelfoam, Pharmacia & Upjohn) in four patients. All patients were observed in the radiology recovery area for 4 hours after the procedure, and any complications were recorded.
Follow-Up
The length of follow-up after the procedure was then established for all
patients. Adequate clinical follow-up was defined as laparotomy or a dedicated
physical examination of the abdomen by a hepatologist, transplant surgeon, or
other physician whose clinical emphasis was on the patient's liver disease.
Adequate imaging follow-up was defined as a contrast-enhanced MRI, CT, or
dedicated liver sonography examination. In several reviews, researchers have
noted reports of seeding as soon as 21 days after percutaneous biopsy
[7,
13], so we selected 1 month as
the minimum adequate follow-up interval. Seeding was defined as pathologically
proven deposition of tumor cells along the needle track, whether identified on
imaging or at physical examination.
Postprocedure clinical notes, pathology reports (including explant livers), and imaging reports were reviewed to determine whether seeding had been detected. When interval development of new masses or any subcutaneous or body wall abnormality was described in the reports, imaging studies were directly reviewed by two or more radiologists. Because there was no discrepancy between the prospective and retrospective interpretations, the dictated radiology report was used as the interpretive standard in all cases.
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Among the initial 128 patients, eight (6.25%) experienced immediate (within 24 hours after the procedure) bleeding complications. Four of these patients had received local injection of a procoagulant agent along the biopsy track at the end of the procedure. All eight were admitted to the hospital; three required only fluid resuscitation, and five required transfusion. Four of the five patients who needed transfusions underwent subsequent angiography examination for evaluation of persistent bleeding; of these, three patients underwent embolization of their liver masses specifically to stop postprocedural bleeding.
The average lesion size in patients with bleeding complications was 4.8 cm
(SD, ± 2.9 cm), although one patient had diffuse infiltrative disease.
No specific imaging features were identified with greater frequency in these
patients. However, six (75%) of eight patients had an elevated
-fetoprotein value (median, 176.8 ng/mL; range, 26-3,160 ng/mL),
whereas the median -fetoprotein value in the nonbleeding patients was
30.9 ng/mL. The mean age of patients with bleeding was 65.5 years, which is
slightly older than the mean age of the group as a whole. Sex ratio was very
similar to the larger population. There were no other immediate postprocedure
complications such as pneumothorax or adjacent organ injury.
Thirty-four patients underwent subsequent percutaneous radiofrequency ablation procedures performed at our institution, three underwent endovascular chemoembolization, and one underwent intraoperative cryoablation. Thirty-two patients underwent subsequent orthotopic liver transplantation at our institution. Four additional patients had laparotomies: two were exploratory and two for hepatic wedge resection.
One hundred one patients had greater than 30 days of adequate clinical or imaging follow-up (or both) after biopsy. Among these, the majority (84 patients) had imaging follow-up, whereas 17 were included on the basis of clinical follow-up as defined earlier. The remaining 27 patients had less than 30 days of follow-up and were excluded. Among the 101 patients constituting the final study population, the mean follow-up was 410 days (median, 1,011 days; range, 33-1,989 days). No cases of suspected tumor seeding by physical examination, imaging study, laparotomy, or pathologic examination of explant livers were identified despite careful review of all follow-up data.
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The fear of tumor seeding in patients with HCC may be more substantive than the evidence supporting it as a statistically significant complication, although a number of documented cases can be found in the literature. Several cases of seeding have been described after radiofrequency ablation or ethanol injection of HCCs [22-26], with some authors noting the difficulty in differentiating seeding from a prior biopsy or from the ablative intervention itself. Other authors have reported tumor seeding rates of 0-12.5% in their patients who underwent radiofrequency ablation [8, 27-29], with some suggesting a correlation between pretreatment biopsy and subsequent seeding. Regarding FNAB alone, multiple individual case reports and the results of larger reviews have been published and report that seeding rates range from 0.6% to 5.1%, with the time from biopsy to seeding detection ranging from 3 weeks to 6 years [5, 7, 13, 30, 31].
Reported seeding rates for cutting needle biopsy have always exceeded 0%, and the mean time to seeding detection has been highly variable. For example, a variety of case reports and smaller studies have described seeding rates of 1.6-3.4% after 14- to 20-gauge cutting needle biopsy, with time to seeding detection ranging from 2 months to 4 years [10, 11, 13, 32, 33]. Huang et al. [12] published a larger series in 1996 and reported a 1.6% incidence of histologically proven seeding in 420 patients with HCC biopsied using a cutting needle technique, with 24.7 months as the mean time to seeding detection. Most recently, Chang et al. [9] reported their findings from a series of 1,055 patients biopsied with an 18- to 19.5-gauge cutting needle technique, noting a 0.76% seeding rate and a mean time to seeding detection of 8.9 months. Seeding after the use of a coaxial technique with a needle introducer has not been specifically reported, to our knowledge.
The chief limitations of the current study include sample size and duration of follow-up. Although a few patients have only 1-2 months of follow-up, the mean follow-up in our population was greater than 1 year and many patients were followed for 3 or more years. Many cases of seeding have been reported in the first few months after biopsy [7, 11-13, 31, 33]. The largest published HCC population had a mean time to seeding detection of 8.9 months [9], which is shorter than the mean follow-up time of 410 days in our study.
Other limitations include minor variations in biopsy and seeding detection techniques. We injected procoagulant agents along the needle track in some patients, which has an unknown effect on tumor seeding and may have confounded our results. Regarding detection, we relied on physical examination to assess seeding in a subset of patients, which may be less sensitive than CT or MRI. Further, reliance on dictated reports for evaluation of seeding may limit sensitivity because the interpreting radiologists may not have been aware of the biopsy history or attuned to the possibility of seeding.
The literature encompasses a variety of biopsy techniques and tumor seeding rates. Although subject to the limitations mentioned earlier, our study presents a single population who were treated using a uniform biopsy technique. A coaxial cutting needle technique was consistently used and appears to affect outcomes in two ways that differ from most of the prior studies. First, we identified no evidence of seeding, a rate that is lower than most previously reported. We suggest that this lower rate may be because of the presence of an outer needle guide that remains in place during multiple passes of the inner cutting needle and protects the tissue track as tumor cells are conveyed along it. Second, our study group experienced a 6.25% rate of hemorrhagic complications, which is higher than the 0-1.4% reported in the literature [10, 12, 34]. We are not certain why this occurred, but possible factors include the relatively large diameter (17 gauge) of the coaxial needle set. Given the hypervascular nature of HCC and the frequent impairment of hepatic synthetic function in this patient population, careful attention to coagulation parameters and an elevated index of suspicion for hemorrhage are certainly warranted. Again, the hemorrhagic complications in our population did not affect patient survival.
This discussion takes on its greatest weight in the context of liver transplantation, which has become an increasingly important therapeutic option for patients with stage I-II HCC. Accurate diagnosis before transplantation is essential to the appropriate allocation of donor livers. Indeed, analysis of explant livers from 666 patients who underwent transplantation under the auspices of the United Network for Organ Sharing revealed that at least 31% of patients receiving transplants for stage I HCC were misdiagnosed on the basis of imaging examinations performed before transplantation and actually had no evidence of liver tumor [3].
A dilemma emerges regarding potential transplant patients: Accurate diagnosis is of paramount importance, but seeding poses a greater threat because of their greater life expectancies. At the same time, the outcomes that have been reported in the cases of seeding discussed earlier illustrate that the biopsy track recurrences have been readily treated by excision, ablation, embolization, or radiation with no negative impact on patient survival [7, 9-13, 22, 25, 26, 28, 30, 33, 35].
Because we found no detectable seeding risk using a coaxial cutting needle technique despite detailed follow-up, we suggest that percutaneous biopsy by this means provides a safe and appropriate technique with which to diagnose HCC before therapy, particularly when transplantation is a consideration.
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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-fetoprotein for diagnosis of hepatocellular carcinoma in patients with
chronic liver disease: influence of HBsAg and anti-HCV status. J
Hepatol 2001; 34:570
-575[CrossRef][Medline]
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