Published online before print February 27, 2004, 10.1148/radiol.2311030420
(Radiology 2004;231:150-155.)
© RSNA, 2004
Experimentally Induced Small-Bowel Tumor in Rabbits: US-guided Percutaneous 18-gauge Core Biopsy1
Se Hyung Kim, MD,
Joon Koo Han, MD,
Kyoung Ho Lee, MD,
Chang Jin Yoon, MD,
Young Il Kim, MD,
Hye Seung Lee, MD and
Byung Ihn Choi, MD
1 From the Departments of Radiology, Institute of Radiation Medicine (S.H.K., J.K.H., K.H.L., C.J.Y., Y.I.K., B.I.C.) and Pathology (H.S.L.), Seoul National University College of Medicine, 28 Yongon-dong, Chongno-gu, Seoul 110–744, Korea. Received March 19, 2003; revision requested June 13; revision received June 23; accepted August 8. Supported by S.N.U. Research Fund 2001. Address correspondence to J.K.H. (e-mail: hanjk@radcom.snu.ac.kr).
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ABSTRACT
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PURPOSE: To evaluate the safety and diagnostic yield of percutaneous 18-gauge core biopsy for an experimentally induced small-bowel tumor in a rabbit model.
MATERIALS AND METHODS: Small-bowel tumors were induced by injecting VX2 tumor into 20 rabbits. After 3 weeks, the small bowel was filled with 100 mL of 2% diluted contrast agent containing methylene blue by using a 5-F catheter. Fifty biopsy firings for small-bowel tumor were performed with ultrasonographic (US) guidance by using an 18-gauge automatic gun. Computed tomography (CT) was performed before and immediately after biopsy. Any procedure-related complications, including leakage of air or fluid, hematoma, and perforation as seen at CT and identified at laparotomy, which was performed 48 hours after biopsy, were evaluated. White blood cell (WBC), red blood cell, and platelet counts; hemoglobin and hematocrit levels; and erythrocyte sedimentation rate were also obtained before and 48 hours after biopsy. Comparison was performed with paired t test. The diagnostic yield was calculated, and the specimen was evaluated whether fragments of mucosa were included or not.
RESULTS: No contrast agent leakage or pneumoperitoneum suggesting perforation was identified at CT or laparotomy. Fluid leakage was observed with manual squeezing at two biopsy sites (4%). In two rabbits, hemoperitoneum was observed at CT or laparotomy. Hematoma larger than 3 cm was observed in six rabbits. WBC count and erythrocyte sedimentation rate slightly increased, and red blood cells, hemoglobin, hematocrit, and platelets counts had decreased slightly after biopsy but were not significant (P > .05). Definitive histologic diagnosis of tumor was obtained in 44 (88%) of 50 biopsy sites. Fragments of mucosa were observed in 13 (28%) specimens of 10 rabbits.
CONCLUSION: Core biopsies of small-bowel tumor can be performed safely with an 18-gauge gun without severe complications and allow histologic diagnosis of small-bowel tumor with a good diagnostic yield.
© RSNA, 2004
Index terms: Animals • Experimental study • Intestines, biopsy, 74.1261, 74.1262, 74.12985 • Intestinal neoplasms, 74.32 • Ultrasound (US), guidance, 74.12985
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INTRODUCTION
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The ultrasonographic (US) findings of gastrointestinal wall lesions have been well described (1–3). According to these reports, bowel wall abnormality reveals the characteristic US appearance of a "target" or "pseudokidney" pattern. However, this finding is nonspecific, and histologic diagnosis is difficult from US findings alone.
Percutaneous US-guided core biopsy of solid abdominal organs is a widely applied and accepted practice (4,5). However, reports about percutaneous US-guided biopsies, especially core biopsies in which large needles are used for bowel lesions, are limited (6–10). Although reports concerning the effectiveness and safety of percutaneous bowel biopsy reveal that the diagnostic yield of core biopsy (75%–100%) is slightly higher than that of fine-needle aspiration biopsy (FNAB) (59%–92%) and complications are minimal for both techniques, it is impossible to say whether diagnostic yield in core biopsy is really better than that in FNAB because these techniques have not been directly compared. Thus, the purpose of our study was to evaluate the safety and diagnostic yield of percutaneous 18-gauge core biopsy for experimentally induced small-bowel tumor in a rabbit model.
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MATERIALS AND METHODS
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Animal and Tumor Model
Approval for this protocol was obtained from the appropriate animal care committee at our institution. Twenty New Zealand White rabbits (Yonam College of Agriculture, Chonan, Korea) weighing 2–3 kg were used for the study. Prior to all procedures, including tumor injection, imaging, and percutaneous biopsy, the rabbits received an intramuscular injection of a mixture consisting of 10 mg per kilogram of body weight ketamine hydrochloride (Ketalar; Yuhan Yanghang, Seoul, Korea) and 10 mg/kg xylazine hydrochloride (Rumpun; Bayer Korea, Seoul, Korea). Intravenous access for blood sampling was then acquired via a marginal ear vein. Anesthesia was maintained with repeated intramuscular injections of the same mixture.
VX2 carcinoma, an undifferentiated carcinoma that grows rapidly in rabbits, was used as the experimental tumor. A VX2 carcinoma cell suspension was used rather than tumor fragments for the intraarterial injection. Fresh tumor tissue was cut finely with scissors until the tumor resembled a homogenate, and this was blended well with 10 mL of saline. This mixture was then passed through a gauze, and the strained VX2 tumor cell suspension was used for the injection. The femoral artery was exposed and cannulated with an 18-gauge angiographic catheter. A 3-F microcatheter was used for the intraarterial injection. The microcatheter was introduced into a distal portion of a jejunal branch of the superior mesenteric artery via a femoral artery with fluoroscopic control (Fig 1), and then 0.5 mL of the tumor suspension was injected. The rabbits were permitted to recover and were followed sonographically (Gaya; Medison, Seoul, Korea) at weekly intervals until the small-bowel tumors appeared to be more than 5 mm in size, which occurred at a mean of 3 weeks after the injection.
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Figure 1. Image obtained during fluoroscopy-guided injection of the tumor suspension into a distal branch of the superior mesenteric artery. The 3-F microcatheter was introduced into a distal portion (arrow) of a jejunal branch of superior mesenteric artery via the femoral artery, with fluoroscopic control. A 0.5-mL dose of the tumor suspension was then injected.
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Animal Preparation and Imaging
The experiments were performed 19–25 days after injection. All rabbits were not given food except water for 12 hours prior to biopsy, and no antibiotic prophylaxis was used. To facilitate the detection of any perforation at computed tomography (CT) and laparotomy, positive oral contrast agent and methylene blue were used. A 100 mL of 2% diluted meglumine diatrizoate and sodium diatrizoate solution (Gastrografin; Schering, Berlin, Germany) mixed with 5 mL methylene blue was prepared and inserted into the stomach of the anesthetized rabbit through a 5-F angiographic catheter (Fig 2). CT and subsequent biopsy were performed 1 hour after contrast agent administration, at which time the contrast agent was considered to fill the small bowel. Two CT scans (Somatom Plus 4; Siemens Medical Systems, Erlangen, Germany) were obtained, one just before and one immediately after biopsy, in the supine position. The helical CT parameters were 120 kVp, 200 mA, 3-mm collimation, 5-mm/sec table feed (pitch of 1.7), 2-mm reconstruction interval, and 512 x 512 matrix. No intravenous contrast agent was administered.
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Figure 2. CT scan of a small bowel filling with a mixture of positive oral contrast agent and methylene blue that was injected through the catheter with fluoroscopic guidance. The contrast agent filled the distended stomach (S) and the proximal small bowel (arrows).
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Percutaneous Biopsy
All rabbits were found to have two or more masses attached to the small bowel at US-guided biopsy. Masses appeared as low-echoic round lesions (Fig 3). The mean number of masses seen at US-guided biopsy was 4.7 (range, 2–8). Among them, two or three of the largest masses in each rabbit were targeted. The mean size of the lesions examined at biopsy was 12 mm (range, 8–18 mm). US-guided percutaneous core biopsy was performed by one of two radiologists (C.J.Y., Y.I.K.) by using a free-hand technique. All biopsies were performed with a 5–7-MHz linear probe (ATL 3000; Philips Ultrasound, Bothell, Wash) by using an 18-gauge automatic gun (ACECUT; TSK, Tochigi, Japan) that did not have an adjustable throw. The charged biopsy gun could be operated with one hand, which allowed for the US to be performed simultaneously with the other hand. When a lesion was located, the route to the target site was selected by using color Doppler US to avoid large vessels (Fig 3). In addition, to maximize intratumoral excursion of the biopsy gun and to minimize the chance of bowel wall perforation, the direction of the firing was adjusted in most cases to be parallel to the bowel wall. The biopsy needle was advanced until the lesion was observed to be indented. The trigger mechanism was then fired, and the needle was withdrawn. After the biopsy needle was withdrawn, dry gauzes were applied with pressure to the biopsy site until the bleeding had ceased. Two biopsies were performed on two different tumors in each of 10 of 20 rabbits, and three biopsies were performed on three different tumors in each of the remaining 10 rabbits. Therefore, a total of 50 biopsies were performed.
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Figure 3a. US-guided 18-gauge core biopsy of small-bowel VX2 tumor. (a) Transverse US scan shows a 1.5-cm homogeneous low-echoic mass (M) contacting the small bowel. (b) Power Doppler US scan reveals prominent vascular flow (arrows) within and around the mass. (c) During firing, the linear echogenic structure of the needle track (arrow) was well visualized.
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Figure 3b. US-guided 18-gauge core biopsy of small-bowel VX2 tumor. (a) Transverse US scan shows a 1.5-cm homogeneous low-echoic mass (M) contacting the small bowel. (b) Power Doppler US scan reveals prominent vascular flow (arrows) within and around the mass. (c) During firing, the linear echogenic structure of the needle track (arrow) was well visualized.
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Figure 3c. US-guided 18-gauge core biopsy of small-bowel VX2 tumor. (a) Transverse US scan shows a 1.5-cm homogeneous low-echoic mass (M) contacting the small bowel. (b) Power Doppler US scan reveals prominent vascular flow (arrows) within and around the mass. (c) During firing, the linear echogenic structure of the needle track (arrow) was well visualized.
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Analysis
During 48 hours after biopsy, all rabbits were monitored by a research assistant of our institute to evaluate change in bowel habit, such as hematochezia or melena. CT images were evaluated in consensus by two abdominal radiologists (S.H.K., K.H.L.) using the multistack mode in the picture archiving and communication system (Maroview; Marotech, Seoul, Korea). Bowel perforation was deemed present if contrast material or air was seen outside the small bowel. All rabbits were sacrificed with an overdose of intravenous ketamine 48 hours after biopsy. After sacrifice, the abdominal contents were exposed at midline laparotomy. Gross analysis was performed by one of the two radiologists to determine the presence of any complication, that is, a leakage of methylene blue or hemoperitoneum. The outer surface of the small bowel was examined for any hematoma caused by the biopsy. Hematomas were evaluated and recorded according to size. In addition, the small bowel was squeezed, and the presence of any leakage of air or fluid was noted. Platelet, white blood cell, and red blood cell counts; hemoglobin and hematocrit levels; and the erythrocyte sedimentation rate were obtained prior to and 48 hours after biopsy.
Tissue cores were stained with hematoxylin and eosin, and a histologic diagnosis of VX2 carcinoma was evaluated by a gastrointestinal pathologist (H.S.L.) using light microscopy. Particular attention was paid to the presence of fragments of mucosa, which would have suggested lumen penetration.
Statistical Analysis
Comparison of continuous laboratory data obtained before and after biopsy was performed to evaluate the hematologic change by using the one-sided paired-samples t test (version 11.0; SPSS, Chicago, Ill). P < .05 was required for null hypothesis rejection.
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RESULTS
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Forty-seven diagnostic samples were obtained from 50 biopsy firings; the remaining three biopsy sites contained inadequate samples. All lesions were accessible to biopsy with US guidance, and no procedure was abandoned because of poor access. All rabbits appeared normal 48 hours after biopsy, and no hematochezia or melena was observed.
No contrast material or air was observed outside the gastrointestinal tract on postbiopsy CT images (Fig 4). At laparotomy, any leakage of methylene blue or the intestinal contents was noted. At two (4%) biopsy sites, spillage of the intestinal contents through a biopsy defect was observed when the small bowel was manually squeezed. Hemorrhage in the abdominal cavity was observed in two (10%) rabbits (Fig 5). Hematomas of variable size were detected on the outer surface of the small bowel in 20 (40%) biopsy sites; three (6%) had a small hematoma of less than 1 cm in diameter, 11 (22%) had an intermediate hematoma of 1–3 cm, and six (12%) had a large hematoma of more than 3 cm (Figs 5, 6).
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Figure 4a. Transverse CT scans obtained immediately after biopsy. (a) Small and (b) large bowels were filled with contrast material. Several low-attenuating tumors (arrows) were seen mainly in the small bowel. No evidence of extraluminal leakage of contrast material or air was observed.
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Figure 4b. Transverse CT scans obtained immediately after biopsy. (a) Small and (b) large bowels were filled with contrast material. Several low-attenuating tumors (arrows) were seen mainly in the small bowel. No evidence of extraluminal leakage of contrast material or air was observed.
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Figure 5a. Hemoperitoneum occurring after biopsy. (a) Transverse CT scan obtained just before biopsy shows a mass (arrow). No extraluminal contrast material or air is evident. (b) Transverse CT scan obtained immediately after biopsy shows slightly high-attenuating fluid (arrows), suggesting hemoperitoneum at the left paracolic gutter. However, no extraluminal air was observed. (c) Photograph obtained during laparotomy shows a large hematoma (H), with gross hemoperitoneum in the abdominal cavity. Note multiple small whitish masses (arrows) attached to the small-bowel wall.
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Figure 5b. Hemoperitoneum occurring after biopsy. (a) Transverse CT scan obtained just before biopsy shows a mass (arrow). No extraluminal contrast material or air is evident. (b) Transverse CT scan obtained immediately after biopsy shows slightly high-attenuating fluid (arrows), suggesting hemoperitoneum at the left paracolic gutter. However, no extraluminal air was observed. (c) Photograph obtained during laparotomy shows a large hematoma (H), with gross hemoperitoneum in the abdominal cavity. Note multiple small whitish masses (arrows) attached to the small-bowel wall.
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Figure 5c. Hemoperitoneum occurring after biopsy. (a) Transverse CT scan obtained just before biopsy shows a mass (arrow). No extraluminal contrast material or air is evident. (b) Transverse CT scan obtained immediately after biopsy shows slightly high-attenuating fluid (arrows), suggesting hemoperitoneum at the left paracolic gutter. However, no extraluminal air was observed. (c) Photograph obtained during laparotomy shows a large hematoma (H), with gross hemoperitoneum in the abdominal cavity. Note multiple small whitish masses (arrows) attached to the small-bowel wall.
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Figure 6a. Hematomas that occurred after biopsy. (a) Small hematoma. Two discrete nodules (arrows) are shown. Patchy hyperemia and small (<1-cm) hemorrhage (*) are also present around the nodule, which was presumed to have been successfully targeted. (b) Small (<1-cm) hematoma (arrows) around the nodule subjected to biopsy was observed in another rabbit. Note multiple variably sized tumors (arrowheads). (c) Larger hematoma. Several whitish tumors (T) are shown on the bowel wall. Note a 2-cm elongated hematoma (arrows) attached to the surface of the tumor.
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Figure 6b. Hematomas that occurred after biopsy. (a) Small hematoma. Two discrete nodules (arrows) are shown. Patchy hyperemia and small (<1-cm) hemorrhage (*) are also present around the nodule, which was presumed to have been successfully targeted. (b) Small (<1-cm) hematoma (arrows) around the nodule subjected to biopsy was observed in another rabbit. Note multiple variably sized tumors (arrowheads). (c) Larger hematoma. Several whitish tumors (T) are shown on the bowel wall. Note a 2-cm elongated hematoma (arrows) attached to the surface of the tumor.
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Figure 6c. Hematomas that occurred after biopsy. (a) Small hematoma. Two discrete nodules (arrows) are shown. Patchy hyperemia and small (<1-cm) hemorrhage (*) are also present around the nodule, which was presumed to have been successfully targeted. (b) Small (<1-cm) hematoma (arrows) around the nodule subjected to biopsy was observed in another rabbit. Note multiple variably sized tumors (arrowheads). (c) Larger hematoma. Several whitish tumors (T) are shown on the bowel wall. Note a 2-cm elongated hematoma (arrows) attached to the surface of the tumor.
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Overall, the white blood cell count and erythrocyte sedimentation rate increased slightly after biopsy (9.1 x 103 µL and 1.13 mm/hr after biopsy vs 8.7 x 103 µL and 1.07 mm/hr before biopsy, respectively), but this increase was not statistically significant. Hemoglobin and hematocrit levels and platelet and red blood cell counts slightly decreased after biopsy, but again this decrease was not statistically significant (Table). Mean decreases in the levels of hemoglobin and hematocrit and in platelet counts were 1.69% (range, -2.59% to 8.82%), 1.07% (range, -2.27% to 4.73%), and 1.69% (range, -12.26 to 64.29%), respectively.
Among the 47 diagnostic samples obtained from 50 biopsies, 44 (88%) core biopsies provided adequate samples for the histologic diagnosis of VX2 carcinoma. The remaining three specimens contained only normal mesenteric fat or muscle. Fragments of mucosa were seen in 13 specimens (13 of 47, 28%) of 10 rabbits (10 of 20, 50%), which showed that the mucosa and lumen were perforated, but this caused no adverse effects such as pneumoperitoneum.
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DISCUSSION
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Percutaneous biopsy of bowel wall lesions has been reported in several articles (6–12) in which use of various modalities with imaging guidance and various needle sizes has been described. Although the selection of the guidance method for the percutaneous approach depends on the location of the target lesion, the position of critical adjacent structures, the quality of visualization provided, and the radiologist’s skill, US-guided biopsy remains the most widely used modality for imaging guidance in solid organs and in the gastrointestinal tract. Because of its real-time capabilities, US guidance allows quicker, more accurate procedures, which is important in lesions that are located in mobile structures like the gastrointestinal tract (13). A US probe acts like a compressor, which allows the user to fix and immobilize the lesion, displace the normal bowel loop, and decrease the skin-to-lesion distance; it therefore facilitates performance. In addition, the use of color Doppler US allows larger mesenteric vessels to be avoided.
There has been some debate in the literature regarding the diagnostic yield and the complication rates associated with the different needle gauges. The most important issues are whether the provision of histologic samples obtained with larger gauge needles, as opposed to the cytologic samples obtained with fine needles, improves diagnostic accuracy, and if so, whether the complication rate is higher with the larger needles. Although the risk of complication is presumed to increase substantially with larger needles, it is not clear whether the complication rate actually increases. In an experimental study conducted to evaluate the effect of needle size in biopsies of livers and kidneys, Gazelle and colleagues (14) found no significant differences in the bleeding rates with use of 18-, 20-, and 22-gauge needles. In a prospective review of 1,000 biopsies, Welch et al (15) found that larger needles pose a higher risk but that the differences in the complication rate were not statistically significant for 22- and 18-gauge needles.
The samples must be of a sufficient quality to allow a correct diagnosis. Although it is difficult to say whether a range of diagnostic yield in core biopsy is really better than that in FNAB because these have not been directly compared, many reports have revealed that use of larger needles results in an increased diagnostic yield (4,7,9,10,16–19). While the percentage of insufficient samples was 20%–41% for fine needles (7,9,10,20,21), it was 0%–10% for 18-gauge needles (4,7,9,10,19). It would appear, therefore, that 18-gauge cutting needles acquire an acceptable specimen in more than 90% of biopsies. In particular, the automatic gun we used is a rapid firing system that reduces fragmentation and crush artifacts in the sample and generally provides better quality samples. In our study, we were able to obtain adequate samples to diagnose tumors in 44 of 50 biopsies. Moreover, percutaneous biopsy of small-bowel VX2 tumor in the rabbit might have a better diagnostic yield than that in humans because the high-frequency linear transducer used produces good image quality and the sonic window is clearer because of the thin abdominal wall.
Most published studies about biopsy complications and efficacies have focused on solid organs rather than on the gastrointestinal tract. Since US-guided FNAB of bowel wall lesions was described in 1981 (22), authors of several articles have reported FNAB of lesions of the gastrointestinal tract. The number of cases in these articles has ranged from three to 78, and 21- or 22-gauge noncutting needles were used. The sensitivity for detecting malignancy was 59%–92% (7,9,10,11,22), and a case with an immediate complication of bowel perforation was reported (23). However, in contrast with FNAB, reports about core biopsies of gastrointestinal lesions are fewer. In these reports, no food restriction, bowel preparation, or prophylactic antibiotics were adopted. In addition, efforts were made not to traverse the lumen to minimize the risk of bowel perforation. Core biopsy was performed for various locations, from the stomach to the colon, and resulted in histologic findings that ranged from benign to malignant, which were mainly adenocarcinomas.
In our study, we tried not to traverse the lumen during biopsy. However, 13 of 47 specimens showed mucosa, which indicates that the lumen was traversed. Nevertheless, we did not experience any perforation that manifested as a leakage of contrast media or pneumoperitoneum on CT scans obtained immediately after biopsy. In addition, there was no spontaneous spillage of the intestinal contents.
Some limitations of our study should be mentioned. We could not evaluate the subjective symptoms of pain or febrility. Small-bowel tumor induced with injection through the mesenteric artery is a model for hematogenous metastasis rather than for a true mucosal lesion. However, because hematogenous metastases to the small bowel do occur, their importance should not be underestimated. Moreover, in a series of metastatic melanoma of the intestine, the metastases were the initial presenting sign that led to the diagnosis of melanoma in 50% of cases (24). Because we focused on short-term complications, we did not evaluate the long-term complications of needle tract implantation. The incidence of malignant cell seeding in the needle tract is reported to be variable (2.0%–5.1%) (25–27), although no report exists of tract seeding due to percutaneous biopsy for bowel tumor. The fact that the populations involved in the previous studies were relatively small and the period of follow-up was short indicates that findings of previous studies may possibly not reflect the real incidence of tract seeding. Thus, it is possible that the increased risk of tract implantation caused by the larger needle diameter used in a core biopsy may be balanced by a reduction in the number of needle passes, but no studies have compared the rate of tumor seeding according to needle size, to our knowledge. Large and long-term follow-up clinical trials capable of evaluating long-term complications of needle tract seeding in bowel tumor are needed because of the low incidence of this complication in percutaneous biopsy.
In conclusion, we believe that a US-guided 18-gauge core biopsy in a small-bowel tumor model establishes a definite diagnosis and is a safe procedure.
Practical application: Despite the limitations, we believe our results may have potential for clinical application. The needle used (18-gauge) is relatively larger for use in a small animal than what would be used in a human. However, despite the use of a relatively larger needle, no significant hemorrhage or frank perforation was observed. Second, we did not use prophylactic antibiotics before or after biopsy, and despite this, significant leukocytosis was not observed.
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FOOTNOTES
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Abbreviation: FNAB = fine-needle aspiration biopsy
Author contributions: Guarantors of integrity of entire study, S.H.K., J.K.H., B.I.C.; study concepts, S.H.K., K.H.L., C.J.Y., J.K.H.; study design, S.H.K., K.H.L., C.J.Y., Y.I.K., J.K.H.; literature research, S.H.K., K.H.L.; experimental studies, S.H.K., K.H.L., C.J.Y., Y.I.K.; data acquisition, S.H.K., K.H.L., C.J.Y., Y.I.K.; data analysis/interpretation, S.H.K., K.H.L., C.J.Y., H.S.L.; statistical analysis, S.H.K.; manuscript preparation, S.H.K.; manuscript definition of intellectual content, S.H.K., K.H.L., J.K.H., B.I.C.; manuscript editing, revision/review, and final version approval, all authors
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ABSTRACT
INTRODUCTION
