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Original Research |
1 Division of Abdominal Imaging and Intervention, Department of Radiology,
Brigham and Women's Hospital, Harvard Medical School, 75 Francis St., Boston,
MA 02115.
2 Division of Gastroenterology, Department of Medicine, Brigham and Women's
Hospital, Harvard Medical School, Boston, MA.
Received September 16, 2005;
accepted after revision October 25, 2005.
Address correspondence to S. M. Erturk.
Abstract
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MATERIALS AND METHODS. Of 70 solid pancreatic masses, 43 (mean size,
4.4 cm; range, 1.5-10.3 cm) underwent fine-needle (20- to 22-gauge) aspiration
biopsy with CT guidance and 27 (mean size, 2.3 cm; range, 1.0-5.0 cm)
underwent fine-needle (22-gauge) aspiration biopsy with endoscopic sonography
guidance. The diagnostic rate, sensitivity, and negative predictive value
(NPV) for each technique were compared using Fisher's exact test before and
after stratifying masses by size as small (
3 cm) or large (> 3
cm).
RESULTS. The overall diagnostic rate, sensitivity, and NPV of fine-needle aspiration biopsies guided using CT (97.7%, 94.9%, and 60%, respectively) were not significantly different from those guided using endoscopic sonography (88.9%, 85%, and 57.1%, respectively). Among small masses, the diagnostic rate and sensitivity for biopsies guided using CT (100% and 100%, respectively) were not significantly different from those for biopsies guided using endoscopic sonography (90.9% and 93.8%, respectively). Among large masses, the diagnostic rate and sensitivity (96.6% and 92.3%, respectively) for biopsies guided using CT were not significantly different from those for biopsies guided using endoscopic sonography (83.3% and 50%, respectively).
CONCLUSION. When biopsying solid pancreatic masses with fine needles, procedures guided with CT and those guided with endoscopic sonography have similar test characteristics regardless of mass size.
Keywords: biopsy • CT • endoscopic sonography • fine-needle aspiration biopsy • imaging-guided biopsy • oncologic imaging • pancreas • pancreatic cancer
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CT-guided fine-needle aspiration biopsy is an established technique for the diagnosis of pancreatic masses [5-7]. Endoscopic sonography also has been used to guide pancreatic mass biopsy [1, 2, 8-10]. The accuracy rates for fine-needle aspiration biopsy with both guidance techniques are similar, with sensitivities up to 100% for CT guidance and 96% for endoscopic sonography guidance [1, 2, 11-13]. However, endoscopic sonography guidance has been postulated to be more effective than CT guidance, especially for the diagnosis of small pancreatic masses [2, 8, 11]. Nevertheless, to our knowledge, this claim has been based on anecdotal descriptions and has not been evaluated [3, 13].
The purpose of our study was to compare test characteristics of pancreatic fine-needle aspiration biopsies guided using CT with those guided using endoscopic sonography and secondarily to evaluate for an effect of mass size.
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Among 50 masses in 50 patients that underwent endoscopic sonographically guided fine-needle aspiration biopsy during the same 4-year period, 30 were solid. All were biopsied using 22-gauge needles. Three masses were excluded because of inadequate follow-up. The remaining 27 masses were included in the study. The patients ranged in age from 34 to 88 years (mean age, 61.2 years). Sixteen (59.3%) of them were women, and 11 (40.7%) were men.
Pancreatic Masses
The maximum in-plane diameters of the pancreatic masses biopsied using CT
guidance were measured on contrast-enhanced CT images obtained before or after
the biopsy procedure (mean time difference between CT and biopsy, 8.6 days).
The mean diameter of the pancreatic masses biopsied using CT guidance was 4.4
cm (range, 1.5-10.3 cm): 14 masses (32.6%) were equal to or smaller than 3 cm
in maximum dimension (mean, 2.4 cm; range, 1.5-3 cm), and 29 masses (67.4%)
were larger than 3 cm (mean, 5.4 cm; range, 3.1-10.3 cm). Twenty-four masses
(55.8%) were located in the head of the pancreas, 11 (25.6%) in the body, and
eight (18.6%) in the tail.
The maximum diameters of pancreatic masses biopsied under endoscopic sonographic guidance were measured on static sonographic images obtained during the biopsy procedure. The mean diameter of pancreatic masses that were biopsied using endoscopic sonography was 2.3 cm (range, 1.0-5.0 cm). Twenty-two (81.5%) of the masses were equal to or smaller than 3 cm in maximum dimension (mean, 2.0 cm; range, 1.00-3.00 cm). Five (18.5%) of the masses were larger than 3 cm (mean, 3.9 cm; range, 3.3-5.0 cm). Seventeen masses (63.0%) were located in the head of the pancreas, 10 (37.0%) in the body, and none in the tail.
Biopsy Procedures
CT-guided fine-needle aspiration biopsy procedures were performed using a
CT scanner capable of CT fluoroscopy (Somatom Plus 4/Carevision, Siemens
Medical Solutions). CT fluoroscopic guidance was used for biopsy of 40 masses
(93%), and CT guidance without CT fluoroscopy was used for biopsy of the
remaining three masses (7%). In 31 biopsies (72.1%), only 20-gauge needles
were used, and in 12 biopsies (27.9%) only 22-gauge needles were used. Biopsy
needles were placed using the tandem technique: An initial needle was placed
and was then followed by the placement of additional needles in tandem
alongside the initial needle. A cytotechnologist was present during all the
procedures to evaluate the initial specimens for adequacy.
The endoscopic sonographically guided fine-needle aspiration biopsies were performed by gastroenterologists using a sonography scanner (ProSound SSD-5000 HD, Aloka) with curvilinear array echoendoscopes (GF-UC140P-AL5 and GFUCT140-AL5, Olympus) integrated into the unit. After endosonographic localization, the mass was punctured with 22-gauge needles using either a transgastric approach if the mass was located in the body or tail of the pancreas or a transduodenal approach if it was located in the head of the pancreas. A cytotechnologist was not routinely present during these procedures.
Cytopathologic Examination and Final Diagnosis
The cytology reports were reviewed, and the fine-needle aspiration biopsy
results were categorized as positive or negative, both of which were
considered diagnostic, or as nondiagnostic. Results were categorized as
positive if the cytopathology report described the specimen as containing
malignant cells or cells suspicious for malignancy. All the biopsy results
that were derived from specimens containing malignant cells were considered
true-positive. Positive results that were derived from specimens containing
suspicious cells were considered true-positive if a subsequent surgical biopsy
confirmed that diagnosis. Cases for which the cytopathology report described
specimens as containing no malignant cells or cells consistent with a benign
process were categorized as negative. Patients with biopsy results that were
categorized as negative were followed. Negative results were considered
true-negative if the results were confirmed on a subsequent surgical biopsy or
if the mass showed regression or lack of growth at imaging follow-up (minimum
of 12 months). Nondiagnostic results included biopsy reports that described
the specimens as inadequate.
Statistical Analysis
Diagnostic rate (proportion of procedures that resulted in biopsy reports
that were categorized as positive or negative) was calculated with 95% CIs.
Sensitivity and NPV, along with 95% CIs, were calculated for only the biopsies
with diagnostic specimens. The proportions of small and large masses in the CT
guidance and endoscopic sonography guidance groups were calculated. The
diagnostic rate, sensitivity, and NPV with 95% CIs were calculated for small
and large masses in the two study groups. All intergroup differences were
investigated using Fisher's exact test. The differences were considered
significant if the p value was less than 0.05.
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Among the malignant cases, 33 (89.2%) were diagnosed as adenocarcinoma, one as anaplastic giant cell tumor, and one as melanoma metastasis. In the remaining two masses, the diagnosis was malignant islet cell tumor of the pancreas. In three of the cases of adenocarcinoma, cells suspicious for adenocarcinoma were reported, and the diagnosis was confirmed with surgical biopsy.
Of the five masses with benign results, one was diagnosed as a well-differentiated islet cell tumor; this mass was classified as benign, was left untreated, and remained stable on CT for 22 months after the biopsy (Table 2). Another mass was diagnosed as extramedullary hematopoiesis of the pancreas. This diagnosis was corroborated on a subsequent bone marrow biopsy that revealed a chronic myeloproliferative disorder. The mass had not changed 12 months after the initial biopsy. In the remaining three cases that had benign results, benign-appearing pancreatic ductal and acinar cells were reported. One proved to be chronic pancreatitis with CT follow-up; this result was classified as true-negative. The remaining two proved to be pancreatic ductal adenocarcinoma at surgical resection and were classified as false-negative.
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There were a total of 37 true-positive, three true-negative, and two false-negative results. The sensitivity and NPV of CT-guided fine-needle aspiration biopsy were 94.9% and 60.0%, respectively.
All but three of the 27 biopsies performed under endoscopic sonographic guidance were diagnostic (88.9%) (Table 1). One of the three masses that yielded nondiagnostic biopsy results was diagnosed as benign manifestation of chronic pancreatitis because the mass was unchanged on CT follow-up 30 months after the initial biopsy. The other two masses were diagnosed as pancreatic adenocarcinoma at surgical resection in one and at CT-guided fine-needle aspiration biopsy in the other.
Of the 24 masses with diagnostic results, 17 (70.8%) were pancreatic adenocarcinoma and seven (29.2%) were benign. In five of the cases of adenocarcinoma, cells suspicious for adenocarcinoma were reported, and the diagnosis was confirmed with surgical biopsy. Of the seven masses that yielded benign biopsy results, three were proven with surgical biopsy and one with CT follow-up (Table 2). Two of the remaining three masses proved to be pancreatic ductal adenocarcinoma: One was proven with a CT-guided biopsy of the same pancreatic mass and the other with a CT-guided biopsy of a metastatic liver lesion. In the third patient, analysis of pleural fluid showed malignant cells consistent with adenocarcinoma. These three cases were classified as false-negative.
There were a total of 17 true-positive, four true-negative, and three false-negative results. The sensitivity and NPV of endoscopic sonographically guided fine-needle aspiration biopsy were 85% (17/20) and 57.1% (4/7), respectively.
There were no complications in either group. There were no significant differences in diagnostic rate, sensitivity, and NPV between the guidance techniques.
Mass Size
Fourteen (32.6%) of the 43 masses biopsied under CT guidance were small and
29 (67.4%) were large. Twenty-two (81.5%) of the 27 masses biopsied under
endoscopic sonography guidance were small and five (18.5%) were large
(p < 0.01). Biopsy procedures guided using CT had higher
diagnostic rates and sensitivities among both small and large masses than
those guided using endoscopic sonography
(Table 3); however, the
differences did not reach statistical significance. For small masses biopsied
under CT guidance, the NPV was not calculated because there were no
false-negative results. The NPV was not calculated for large masses biopsied
under endoscopic sonography guidance because there were no true-negative
results.
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When an appropriate indication for pancreatic mass biopsy is identified, the question often arises as to which guidance method, CT or endoscopic sonography, is appropriate to use to biopsy the mass. We sought to examine test characteristics using each guidance technique and the effect of mass size to help determine which technique to use in clinical practice.
We found that CT-guided and endoscopic sonographically guided fine-needle aspiration biopsy had diagnostic rates of 97.7% and 88.9%, respectively. Our results were comparable with those of previous studies. Tillou et al. [5] reported a diagnostic rate of 96.5% for diagnosing pancreatic masses via CT and transabdominal sonographically guided fine-needle aspiration biopsy. Recently, Shin et al. [8] reported a diagnostic rate of 86.8% for endoscopic sonographically guided fine-needle aspiration biopsy of pancreatic masses.
To the best of our knowledge, there are only two published studies that directly compare CT-guided and endoscopic sonographically guided fine-needle aspiration biopsies of pancreatic masses [3, 16]. In a retrospective study, Qian and Hecht [13] suggested that CT-guided biopsies may be more sensitive for diagnosing malignancy than endoscopic sonographically guided biopsies. In their study, CT-guided biopsies and endoscopic sonographically guided biopsies had sensitivities of 71% and 42%, respectively; the authors did not report whether the difference was statistically significant [13]. Likewise, in the study of Mallery et al. [3], CT- and transabdominal sonographically guided pancreatic biopsies (80%) had a higher sensitivity than endoscopic sonographically guided biopsies (74%); however, the difference was not statistically significant. We also found higher sensitivity for CT guidance (94.9%) compared with endoscopic sonographic guidance (85%). However, the difference did not reach statistical significance in our study either.
In the study of Qian and Hecht [13], the NPVs of CT- and endoscopic sonographically guided fine-needle aspiration biopsies were similar: 41% and 45%, respectively. Mallery et al. [3] reported NPVs of 23% and 27% for fine-needle aspiration biopsies performed under CT and endoscopic sonographic guidance, respectively. We found NPVs of 60% and 57.1% for CT-guided and endoscopic sonographically guided fine-needle aspiration biopsy, respectively.
The sensitivity and NPV of both techniques in our study were higher than those in the studies of Qian and Hecht [13] and Mallery et al. [3]. The reason for these discrepancies in results might be that cystic pancreatic masses were included in those studies, whereas we focused on solid pancreatic masses and excluded cystic ones from our analysis. The diagnostic workup of most cystic pancreatic masses involves analysis of cystic fluid for biochemical and tumor markers rather than cytology [17-19]; thus, the accuracy of fine-needle aspiration biopsy is related to both the ability to position a needle in a mass and the accuracy of the biochemical analysis of the cystic fluid [20]. The criteria for establishing a malignant diagnosis based on cystic fluid analysis and its precise role have not yet been completely established [21].
Both Qian and Hecht [13] and Mallery et al. [3] reported that endoscopic sonography was used more frequently than CT to biopsy small pancreatic masses. Also in our study, the frequency of small masses biopsied under endoscopic sonographic guidance (81.5%) was significantly higher than the frequency of those biopsied under CT guidance (32.6%). In fact, since the first report of the use of endoscopic sonographically guided fine-needle aspiration biopsy for the diagnosis of pancreatic cancer in 1994 [15], several groups of researchers have suggested that endoscopic sonographically guided fine-needle aspiration biopsy should be more accurate than CT-guided fine-needle aspiration biopsy, especially for the diagnosis of small pancreatic masses [3, 13, 22]. To evaluate the effect of mass size on biopsy performance, we stratified our study results by mass size and found that there were no significant differences in test characteristics for the guidance techniques after the data were stratified by mass size; small masses were not biopsied more effectively under endoscopic sonography guidance than under CT guidance.
Complication rates are low for both CT-guided and endoscopic sonographically guided fine-needle aspiration biopsy of the pancreas. Recently, in a meta-analysis, Chen et al. [7] reported complication rates of 4% for CT-guided procedures and 2% for endoscopic sonographically guided procedures [7]. We encountered no complications.
The most important limitation of our study is that we used a nonrandomized retrospective design. As a result, there may have been a referral bias that led to a significantly higher frequency of small masses biopsied under endoscopic sonographic guidance. Some referring physicians might have preferred that small pancreatic masses be biopsied under endoscopic sonographic guidance rather than CT guidance on the basis of other investigators' opinions in prior reports [3, 13, 22] that endoscopic sonographically guided biopsy is more accurate than CT-guided biopsy for the diagnosis of small masses. However, to our knowledge, no published study has found a statistically significant difference in test characteristics among small masses. Indeed, the test characteristics for small masses in our study were similar for both guidance techniques.
A second limitation is that a cytotechnologist was not routinely present during the endoscopic sonographically guided procedures to examine the adequacy of the sample. The diagnostic rate achieved with CT guidance was almost 100%. Although the diagnostic rate of biopsies performed under endoscopic sonographic guidance was slightly lower, there was no significant difference between the guidance techniques. Nevertheless, the diagnostic rate of endoscopic sonographically guided procedures might have been improved if a cytotechnologist had examined the initial specimens for adequacy.
In summary, the diagnostic rate and sensitivity of CT-guided fine-needle aspiration biopsy of solid pancreatic masses were slightly higher than those of endoscopic sonographically guided fine-needle aspiration biopsy; however, there were no significant differences between the techniques, and the NPVs of both techniques were almost equal. Hence, we conclude that when evaluating a solid pancreatic mass that needs a nonsurgical biopsy, either CT or endoscopic sonography may be chosen to guide the biopsy: CT has the advantage of not requiring oral intubation with an endoscope; endoscopic sonography the advantage of not requiring percutaneous puncture.
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