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1
Department of Radiology, Hospital General de
Castellón, Avda. de Benicasim, s/n, 12004,
Castellón, Spain.
2
Department of Radiology, Hospital General Univeritario de Alicante, Pintor
Baeza, s/n, 03010, Alicante, Spain.
3
Department of Radiology, Hospital de la Ribera, Ctra Alzira-Corbera, Km 1,
46600 Alzira (Valencia), Spain.
Received February 22, 2000;
accepted after revision June 12, 2000.
Address correspondence to S. F.
Marco-Doménech.
Abstract
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MATERIALS AND METHODS. We performed 42 biopsies in 41 patients (age range, 14-81 years; mean age, 57.5 years). We performed biopsies with real-time sonographic guidance using graded compression, with a 3.5-5—MHz microconvex transducer. In 39 biopsies, core specimens were obtained with an 18-gauge automatic needle gun; fine-needle aspiration biopsy was obtained in 28 patients with a 22-gauge needle and in the other four patients with a 21-gauge needle. In the remaining three patients, a coaxial technique with 20- and 22-gauge needles for cytology was used.
RESULTS. In 40 (95.2%) of 42 core biopsies performed, a specific diagnosis was obtained. A positive diagnosis was obtained in 16 (45.7%) of 35 fine-needle aspirations. The lesions were located from the pharynx to the sigmoid colon. Twenty-eight patients had malignant lesions, and 13 had benign lesions. Only one serious complication, bile peritonitis, was observed.
CONCLUSION. Percutaneous biopsy with sonographic guidance can be used safely and efficiently to diagnose digestive tract lesions that can be visualized on sonography and are not accessible endoscopically.
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The imaging modality chosen for biopsy guidance depends on the radiologist's personal experience and preference. Improved resolution of current real-time equipment, particularly electronically focused phased array transducer designs, together with the new cutting needle designs, have made sonography competitive with CT, if not superior in some situations [2]. Sonography as an imaging modality for biopsy guidance is gaining acceptance [2] and is being used in locations previously reserved for CT, such as the retroperitoneum, mediastinum, lung, pleura, and skeleton [3]. However, biopsies in the digestive tract are practically always performed by endoscopy, except when the lesion cannot be reached by that modality [4]. In these patients, the biopsy is usually performed by laparoscopy or open surgery.
The objective of this paper was to report our experience with sonographically guided biopsies of the digestive tract and to determine the effectiveness and safety of this technique.
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The day before the biopsy, we obtained sonograms to determine whether the lesions detected on barium studies or CT could be visualized well enough with sonography for us to perform the biopsy. Furthermore, in many patients, we assessed the vascular structures around the targets with Doppler color sonography, trying to avoid large vessels in the needle path. In all patients, we could visualize the lesions to be biopsied, and none of the patients were excluded from the procedure. However, our series of patients was selected for sonographic biopsy only after review of the corresponding CT scan. The lesions appeared as a thickened gut wall or as a hypoechoic mass with an echogenic center (pseudokidney sign) [5] in 26 patients (Figs. 1A,1B and 2A,2B,2C) and as an eccentric mass in the remaining 15 patients (Fig. 3A,3B).
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We performed the first 11 biopsies with gray-scale equipment and the remainder with two color Doppler sonography machines. In 24 biopsies we used a model Logiq 400MD (General Electric Medical Systems, Milwaukee, WI), and a model EUB-525 (Hitachi, Tokyo, Japan) was used in the last seven biopsies. All lesions were biopsied with a 3.5-5—MHz microconvex transducer with a biopsy guide attachment. The procedure was carried out on an inpatient basis, and the patients were observed at least overnight to rule out complications. Coagulation parameters and platelet counts were routinely obtained before biopsy. Informed consent was required from all patients after the potential risks and benefits were explained. Patients fasted for at least 8 hr before the procedure. An IV line was used as security, and sedation was achieved with IV administration of midazolam as necessary. No antibiotics were administered.
We performed 42 biopsies in 41 patients. Core specimens alone were obtained in seven biopsies; no biopsies were performed with fine-needle aspirates alone. Both fine-needle aspirates and core specimens were obtained in 35 biopsies. In 39 biopsies core specimens for histopathologic diagnosis were obtained with the following 18-gauge automatic needle guns: in 17 patients with Biopince (Amedic, Sollentuna, Sweden), in 12 with Autovac (Angiomed, Karlsruhe, Germany), and in 10 with Monopty (Bard, Covington, GA). In 32 of these biopsies, we added fine-needle aspiration for cytologic analysis: 28 with a 22-gauge Chiba needle and four with a 21-gauge needle. In the remaining three biopsies, we used a coaxial technique with a 20-gauge Chiba needle for histologic assessment and a 22-gauge needle for cytology. A 20-gauge Chiba needle was advanced to the lesion. After satisfactory positioning, the inner stylet of the biopsy needle was removed, and a 22-gauge Chiba needle was passed through the 20-gauge sheath into the lesion.
Percutaneous biopsy was performed by two radiologists, with one holding the transducer while the second manipulated the needle. The first radiologist was seeking the shortest and safest path to the target. In abdominal lesions, we used graded compression by pressing the transducer steadily and progressively to separate the normal bowel loops and to have an optimal view of the lesion.
Once the needle route was chosen, using aseptic technique we infiltrated the path from the skin through peritoneum with 5-10 mL of lidocaine with a 22-gauge spinal needle through the biopsy guide attachment. In pseudokidney lesions, we performed the biopsy tangentially, planning the needle path through the hypoechoic rim representing the diseased layer and avoiding traversing the echogenic center that corresponded to the mucosa and lumen. In eccentric masses the samples were taken from the solid areas.
In fine-needle biopsies, the needle tip was observed advancing into the lesion on real-time imaging. After removing the stylet, we connected a 10- to 20- mL syringe to the needle. We performed tissue sampling with a pushing and turning motion while maintaining 5- to 20-mL continuous suction, depending on the amount of blood aspirated. The material obtained was placed on four to six slides, and particulate fragments were placed in biopsy flasks with formaldehyde for histologic study. The slides were smeared and rapidly placed in alcohol for cytologic analysis. Finally, core biopsy was performed with real-time guidance, and the specimen was placed in formaldehyde.
No cytopathologist was present during the procedures to determine if an adequate sample was obtained and to provide a preliminary interpretation. For each patient, one or two needle passes were made for either cytologic or histologic diagnosis, according to the macroscopic aspect of the sample.
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For each patient, one or two passes were made for either cytologic or histologic diagnosis. We analyzed the number and types of complications related to gastrointestinal tract biopsies. Most biopsies were well tolerated. There were seven minor complications and one major complication in 42 biopsies. The minor complication was moderate abdominal pain that disappeared spontaneously without any treatment in seven patients. The major complication, bile peritonitis, was observed and percutaneously treated.
In eight patients fragments of mucosa were seen in the core specimen, showing that the mucosa and the lumen were perforated without adverse consequences, such as peritonitis or pneumoperitoneum (Fig. 4A,4B).
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Sonographically guided percutaneous biopsy of most body organs has achieved worldwide acceptance in daily practice [1, 2]. However, the use of imaging guidance to biopsy the digestive tract has been anecdotal, because of good results of the endoscopic biopsy and the general belief that imaging-guided biopsy is risky. Percutaneous biopsies of lesions located in the digestive tube have generally been unintentional when radiologists biopsied an abdominal mass of uncertain anatomic dependence [4, 6, 7].
Sonography is being used more extensively for evaluation of the digestive tract, not only in tumoral lesions but also in a wide range of situations [8]. However, sometimes assessment of the digestive tube can be problematic because of gas content in the lumen, making visibility difficult and even impossible. Intraluminal fluid may mimic cystic masses, and fecal material may create a variety of artifacts and pseudotumors. Gut wall abnormality creates characteristic sonographic patterns. Most familiar is the target pattern first described by Lutz and Petzoldt in 1976 [5]. They referred to the pattern as a pseudokidney, in which the external hypoechoic rim corresponds to the pathologically thickened gut wall, whereas the echogenic center relates to residual gut lumen or mucosal ulceration. Some digestive tract diseases present a thickened wall but otherwise do not show a perfect concentric target and eccentric pseudokidney or eccentric mass, as in 15 patients in our series. Sener et al. [9] reported two intestinal lymphomas that showed a pseudokidney sign with luminal dilatation and called this finding a "hydronephrotic pseudokidney sign." We found this pattern in two patients (Fig. 5A,5B). However, according to another report [10], this sign is not specific for lymphoma and may be observed in nonlymphomatous neoplasms, as in a jejunal hemangiopericytoma of our series. The presence of digestive tract thickening is not specific for any determined disease; it does not always represent malignancy [8]. In fact, seven of our 27 patients had benign lesions.
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The choice of CT or sonography as imaging guidance for percutaneous biopsy depends on the radiologist's experience and equipment availability. However, in biopsies of the digestive tract, in our opinion, the advantages of sonography are important. One advantage is the ability to use the transducer as a compressive tool for one radiologist while the second radiologist manipulates the needle. The graded compression technique described by Puylaert [11] in the diagnosis of acute appendicitis produces the following effects: fixing and immobilizing the lesion, which is important in lesions that are located in mobile structures; displacing the normal bowel loops and therefore the abdominal gas, improving the sonographic view of the target; decreasing the skin-to-lesion distance, thus decreasing the difficulty of the biopsy technique. Another important advantage is the ability to control the needle tip in realtime imaging and, with color Doppler sonography, to identify vessels without the need for contrast agents. Finally, sonography facilitates the use of automatic needle guns.
Transversing the digestive tract during percutaneous biopsy is not a contraindication [12]. In dogs Petit et al. [13] showed no untoward effects from transgressing the bowel with needles and a catheter. In our experience and in other authors' experiences [14], there were no problems passing through overlying loops of digestive tract for pancreatic biopsies. Brandt et al. [14] performed 269 pancreatic biopsies in which the needle passed through the gastrointestinal tract in 66 patients: 41 passes through the stomach, 18 through the small bowel, and seven through the colon. None of the 66 patients had complications related to the biopsy. The same results have been reported when radiologists biopsy other structures such as lymph nodes [15, 16]. In eight of our patients, portions of the mucosa were obtained, without adverse effects.
The two false-negative findings belonged to the same patient, a 70-year-old man previously diagnosed with non-Hodgkin's lymphoma in total remission. At follow-up a pseudokidney sign was observed in the transverse colon. In the first biopsy both cytologic and histologic studies could not provide a specific diagnosis, and the biopsy was repeated with the same result. At surgery an adenocarcinoma was found. We have no explanation for this repeated failure.
Only one major complication, bile peritonitis, was observed. A 44-year-old man with a duodenal leiomyosarcoma had one pass performed through the gallbladder with a coaxial technique because we considered this route the most appropriate. In the ensuing hours the patient experienced acute abdominal pain. Sonography showed free peritoneal fluid. Percutaneous drainage showed bile in the peritoneal cavity. Percutaneous cholecystotomy was performed, and the patient recovered completely. On the cholangiogram obtained through the cholecystotomy, an extrinsic stricture in the distal common bile duct was found. We believe that the biliary obstruction was the cause of the bile leak. This patient illustrates an unusual complication of percutaneous biopsy of gastrointestinal tract lesions, which, in our experience, can usually be treated successfully with percutaneous techniques.
The biopsies were performed on an inpatient basis, and the patients were observed at least overnight to rule out complications. In our opinion, there is a remote chance of complication from the procedure. However, if we carry out percutaneous biopsy in deep organs such as the liver, pancreas, or gastrointestinal tract, the patient remains in the hospital for an observation period of 12-24 hr after the procedure.
Fine needles can usually retrieve an adequate sample for cytologic analysis and often retrieve tissue fragments for histologic assessment. Large-bore cutting automatic needles substantially improve the result rate in some instances [12]. In addition, the pathologist can easily determine the specific pathologic process, especially in benign situations. Like other authors [12, 17], we usually use an 18-gauge needle in core biopsies because it obtains good specimens, without increasing complications. Although we routinely use both fine-needle aspiration biopsy and core biopsy for percutaneous sonographically guided biopsies because they increase the overall results [17], on the basis of our results, we recommend using core biopsy devices in these specific types of biopsies reported in our study.
Articles about sonographically guided percutaneous gastrointestinal tract biopsies accomplished with 18-gauge cutting biopsy needles are scarce [18]. Only one large series has been published [19]. Carson et al. [19] reported 46 biopsies, but only 10 patients underwent core biopsy after negative findings on fine-needle biopsy. Recently, Tudor et al. [20] reported a series of 10 biopsies with 18-gauge needles. Another study reported sporadic core biopsies of the digestive tract included in a large series of abdominal biopsies [6]. Series about digestive tract lesion biopsies performed with fine-needle aspiration are more numerous [7, 21].
In conclusion, because of the safety, efficiency, and capability of sonography as a guiding imaging technique for percutaneous biopsy of lesions located in the digestive tract, we recommend this technique when the lesion is seen on sonography and is not accessible for endoscopic biopsy.
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