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AJR 2003; 180:1563-1566
© American Roentgen Ray Society


Usefulness of Sonographic Guidance During Percutaneous Biopsy of Mesenteric Masses

Lisa M. Ho1, John Thomas1, Stephen A. Fine2 and Erik K. Paulson1

1 Department of Radiology, Duke University Medical Center, Box 3808, Rm. 2526 Blue Zone S., Durham, NC 27710.
2 Department of Radiology, Suburban Hospital, 8600 Old Georgetown Rd., Bethesda, MD 20814.

Received August 7, 2002; accepted after revision November 8, 2002.

 
Presented at the annual meeting of the Radiological Society of North America, November 2001.

Address correspondence to L. M. Ho.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of our study was to determine the usefulness of sonographic guidance for biopsy of mesenteric masses.

MATERIALS AND METHODS. Twenty-five sonographically guided percutaneous biopsies of mesenteric masses were performed in 23 patients. Biopsies were performed with an 18-, 20-, or 22-gauge self-aspirating needle or core biopsy device. Final pathology results and patient medical records were reviewed for biopsy accuracy and complications. A biopsy was considered successful if a specific benign or malignant diagnosis was rendered by the pathologist or if surgical–pathologic confirmation was obtained.

RESULTS. Open surgical biopsy was performed after sonographically guided biopsy in 13 patients and led to 12 concordant diagnoses (nine true-positives and three true-negatives) and one discordant diagnosis (false-negative). Specific pathologic diagnosis was rendered for the 10 percutaneous biopsies that were not confirmed by surgical biopsy: five biopsies matched known primary malignancies, consistent with metastases; four biopsies revealed primary tumors, and one biopsy revealed chronic inflammation (nine true-positives and one true-negative). Two biopsies were nondiagnostic because of insufficient material (n = 1) and necrotic tumor (n = 1). In the biopsies with diagnostic tissue specimens, sonographically guided biopsy achieved a sensitivity of 95% (18/19) and specificity of 100% (4/4) for allowing neoplastic tissue to be distinguished from nonneoplastic tissue. Complications included a mesenteric hematoma and abdominal wall cellulitis.

CONCLUSION. Percutaneous biopsy of mesenteric masses is a useful and safe procedure.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
In patients with a known primary malignancy, the discovery of a mesenteric mass likely indicates metastatic disease. However, a tissue diagnosis is usually needed to exclude the possibility of a benign cause such as resolving hematoma, inflammation, or new primary tumor. Percutaneous biopsy is therefore indicated to confirm or exclude mesenteric spread of malignancy. Traditionally, radiologists have used CT to guide biopsy of mesenteric masses. Radiologists have avoided using sonographic guidance for percutaneous biopsy of mesenteric masses because of concern that lesion visualization might be inadequate, the mesenteric mass could be displaced during needle passage, and the bowel could be transgressed [1, 2, 3]. As a result, literature about using sonographic guidance to biopsy mesenteric masses is limited. Compared with CT, sonography has been shown to be safer, more cost-effective, and faster [4, 5, 6]. Sonography does not require ionizing radiation and therefore poses no radiation risk to the patient or operator. In the hands of an experienced operator, sonographically directed biopsies can proceed faster than CT-guided biopsies because no time is wasted rescanning to check position of the needle. Moreover, the multiplanar capability of sonography allows the operator to position the transducer in any axis to avoid vessel, bowel, or organs. When compression is used, deeply located masses can be visualized and mobile masses can be fixed in position. Real-time visualization of the needle tip ensures that the targeted mesenteric mass is not displaced during the biopsy and therefore aids in successful performance of the procedure.

In our practice, we preferentially use sonography to perform biopsies of mesenteric masses. The purpose of this study was to evaluate our experience using sonography to guide biopsy of mesenteric masses to determine the usefulness and complications of this procedure.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
We retrospectively reviewed the records of 23 patients who underwent 25 sonographically guided percutaneous biopsies of mesenteric masses between October 1995 and July 2000. Of the 23 patients, 13 were women and 10 were men; the patients ranged in age from 29 to 85 years (mean, 57 years). Nine patients had a history of malignancy (ovarian carcinoma, n = 2; lymphoma, n = 1; cervical carcinoma, n = 1; colon carcinoma, n = 1; gastric carcinoma, n = 1; breast carcinoma, n = 1; cholangiocarcinoma, n = 1; and renal cell carcinoma, n = 1). Five patients presented with an isolated dominant mesenteric mass. In six patients without a known primary tumor, generalized lymphadenopathy that included lymph nodes in the mesentery was noted. Three patients presented with a dominant mass involving a single organ (bladder, n = 1; stomach, n = 1; uterus, n = 1) presumed to be malignant, and mesenteric masses potentially representing metastatic disease. Of the 23 patients, 14 were outpatients.

All patients underwent diagnostic CT before biopsy. CT scans were reviewed and used to plan a percutaneous approach to the mesenteric mass targeted for biopsy. All patients gave informed consent for the biopsy. Coagulation parameters and platelet counts were reviewed and found to be normal for each patient (platelet count: range, 150–450 x 109/L; prothrombin time: range, 11.3–13.3 sec; international ratio, < 1.3; activated partial thromboplastin time: range, 23.2–2.4 sec). The mesenteric masses were localized with sonography using graded compression to displace overlying tissue and bowel. The anticipated path of the needle was projected over the targeted mass using the needle guide software. The needle path was assessed with color Doppler sonography to ensure blood vessels would be avoided. The needle entry site on the patient's skin was marked, and the surrounding area was cleansed with a bactericidal soap. Local anesthetic (1–2% lidocaine hydrochloride [Xylocaine, Astra, Westborough, MA]) was applied subcutaneously with a 25-gauge needle and infiltrated into the abdominal wall. Conscious sedation was used as necessary with the IV administration of diazepam (Valium, Elkins-Sinn, Cherry Hill, NJ) and fentanyl citrate (Sublimaze, Akorn, Decatur, IL).

All biopsies were performed with either a Model 128 sonography unit (Acuson, Mountain View, CA) or a Logic 700 unit (General Electric Medical Systems, Milwaukee, WI). A 3- or 5-MHz sector transducer equipped with an attachable needle guide was used. For eight biopsies, either a 20- or 22-gauge self-aspirating Crown needle (Meditech/Boston Scientific, Watertown, MA) without suction was used. Both 20- and 22-gauge needles were used for one biopsy. For two biopsies, either an 18- or 20-gauge Achieve core biopsy device (Allegiance Healthcare, McGaw Park, IL) or a Meditech core biopsy device (Meditech/Boston Scientific) was used. A combination of a self-aspirating Crown needle and a core biopsy device (Achieve, Meditech, or Temno [Allegiance Healthcare]) was used for 14 biopsies. An average of four passes were made (range, 1–8 passes) for each procedure. A pathologist present at the biopsy reviewed the cytology specimens to ensure sample adequacy. The procedure was considered to be complete once the pathologist determined an adequate sample had been obtained or at the discretion of the attending radiologist.

After each procedure was completed, the patient was observed in the recovery area for 4 hr to monitor vital signs and assess for immediate complications. A nurse contacted all outpatients 1–2 days after the biopsy to determine whether any experienced complications such as persistent pain, fever, or bleeding at the puncture site. The inpatients were returned to the care of their clinical team. Discharge summaries were reviewed to determine whether peritonitis, unexplained fever, or abdominal pain or abscess had developed or blood transfusion had been required. Long-term follow-up was performed by reviewing medical records in 22 patients and direct contact in one patient.

Final pathology results and patient medical records were reviewed for biopsy accuracy and complications. A biopsy was considered successful if a specific benign or malignant diagnosis was rendered by the pathologist or if subsequent open surgical biopsy confirmed the results of the percutaneous biopsy.


Results
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Abstract
Introduction
Materials and Methods
Results
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References
 
Open surgical biopsy was performed after sonographically guided biopsy in 13 patients revealing 12 concordant diagnoses (nine true-positives and nine true-negatives) and one discordant diagnosis (one false-negative). The 12 concordant diagnoses were primary lymphoma (n = 3), gastrointestinal stromal tumor (n = 2), fibrosis (n = 2), metastatic cervical carcinoma, metastatic ovarian carcinoma, primary ovarian carcinoma, uterine carcinosarcoma, and benign lymph node. In the one false-negative biopsy, reactive mesothelium and atypical cells were obtained; however, open biopsy subsequently revealed metastatic gastric carcinoma.

A specific pathologic diagnosis was rendered for 10 percutaneous biopsy procedures; in these cases, open surgical biopsy was not performed. Five of these specimens matched known primary malignancies, consistent with metastases. These primary cancers included the following: squamous cell carcinoma of the bladder, colon adenocarcinoma, gastric adenocarcinoma, cholangiocarcinoma, and breast carcinoma. Four biopsies revealed primary tumors (lymphoma, n = 3; liposarcoma, n = 1). One biopsy revealed chronic inflammation (Figs. 1A, 1B). Therefore, of these 10 procedures, nine resulted in true-positive interpretations and one in a true-negative interpretation.



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Fig. 1A. 74-year-old man with 6-month history of nausea and diarrhea. Contrast-enhanced CT scan shows two mesenteric masses (arrows).

 


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Fig. 1B. 74-year-old man with 6-month history of nausea and diarrhea. Transverse sonogram of abdomen reveals well-defined hypoechoic mass (arrow) in mesentery. Mass corresponds in size and location to mass shown by left arrow in A. Anticipated path of needle is indicated by needle guide. Biopsy of mass revealed dense sclerotic fibroconnective tissue, consistent with chronic inflammation. Results were confirmed at exploratory laparotomy.

 

Two biopsies were nondiagnostic because of insufficient material (n = 1) and necrotic tumor (n = 1). However, note that both of these patients underwent a second percutaneous mesenteric biopsy that yielded diagnostic tissue (lymphoma and liposarcoma).

In the biopsies with diagnostic tissue specimens, sonographically guided biopsy achieved a sensitivity of 95% (18/19) and specificity of 100% (4/4) for allowing neoplastic to be distinguished from nonneoplastic tissue. If the two nondiagnostic biopsies are included as false-negative biopsies, then the sensitivity decreases to 86% (18/21).

For the nine inpatients, no immediate or delayed complications were reported. For the remaining 14 outpatients, two complications occurred. One day after biopsy, one patient developed abdominal pain and acute lower gastrointestinal bleeding. A CT scan revealed a mesenteric hematoma at the biopsy site. The patient was treated conservatively with IV fluids and was discharged from the hospital after several hours of observation in the emergency department. He subsequently recovered without needing additional treatment or a blood transfusion. Another patient presented with tenderness and erythema of her right lower abdominal wall in the region of her biopsy site 3 days after biopsy. She was diagnosed with abdominal wall cellulitis related to biopsy and admitted to the hospital for IV antibiotic therapy. Within 72 hr of antibiotic treatment, her symptoms resolved. The patient recovered fully and was subsequently discharged from the hospital.

The average long-term follow-up was 24 months (range, 1 week–66 months). No changes in diagnosis or long-term or chronic complications were reported for any of the patients.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The literature regarding the use of sonography to direct biopsy of mesenteric masses is limited. The reasons for this paucity may be related to the perceived increased risk and difficulty in performing this procedure with sonographic guidance. In 1983, Reuter et al. [7] first reported using sonography to specifically direct biopsy of omental masses. In their series of four patients, the fine-needle aspiration diagnosis of peritoneal mesothelioma was made using a 22-gauge spinal needle with free-hand guidance. Sistrom et al. [8] subsequently reported a series of 11 patients in whom they performed sonographically guided fine-needle aspiration biopsies of omental masses. These researchers also used a 22-gauge spinal needle for all biopsies and a free-hand technique to guide the needle into the target mass. Nine of their 11 patients had fine-needle aspiration cytology that was positive for carcinoma. In one patient, a mass had a true-negative interpretation that was subsequently diagnosed as omental hematoma at laparotomy. In another patient, the interpretation was a false-negative. In that case, fine-needle aspiration obtained atypical cells and mucin, and a subsequent transrectal biopsy revealed mucinous neoplasm of the ovary with pseudomyxoma peritonei. These researchers encountered no complications with any of their procedures. Spencer et al. [9] performed sonographically directed 18-gauge core needle biopsy in four patients with peritoneal carcinomatosis for the diagnosis of tumor type without any complications.

Our overall sensitivity of 95% and specificity of 100% are comparable with the results of Gottlieb et al. [10], who described sonographically guided biopsy of 54 extravisceral masses in 52 patients. Using a 20- or 22-gauge spinal needle (26 biopsies) or an 18-gauge core biopsy needle (12 biopsies) or both (16 biopsies), these researchers achieved a sensitivity of 93%, specificity of 100%, and nondiagnostic samples in 4%. Patients in this series did not develop any procedure-related complications.

In our series, we did not restrict our needle choice to a 22-gauge or smaller aspiration needle. We used either a 20- or an 18-gauge cutting needle in 64% (16/25) of our biopsies. The safety of sonography and CT-guided core needle biopsy in omental implants and peritoneal implants has been reported [9, 10, 11]. Eight of our procedures involved biopsy of lymph nodes deep within the small-bowel mesentery, which increases the possibility of bowel transgression during the procedure. In five of these eight patients, an 18- or 20-gauge core biopsy device was used. For most procedures, we used the sonography transducer to compress the abdominal wall to displace bowel, reduce skin to target distance, and fixate the target mass in the abdomen, as described by Fisher et al. [12]. We believe that this technique is particularly useful for the biopsy of masses in the mesentery.

The possibility of causing bowel injury or peritonitis resulting from bowel leaks due to inadvertent needle puncture of the bowel is a concern when performing percutaneous biopsy of mesenteric masses. We might have unknowingly transgressed loops of collapsed large or small bowel with the biopsy needle during some of the procedures because distinguishing compressed bowel from omental or fatty tissue is difficult with sonography. However, in spite of the risk of bowel transgression, our series as well as that of others [10] have shown this procedure to be safe.

Even with the use of 18- or 20-gauge cutting needles, we did not encounter a case of peritonitis or bowel perforation requiring surgery. Review of the literature reveals one report of peritonitis associated with colonic perforation during fine-needle aspiration of a colonic wall lesion [13]. To date, no cases of perforation after core needle biopsy of bowel wall lesions have been reported in the literature, possibly because of the relative infrequency of this procedure. In a study by Farmer et al. [14], five colonic wall biopsies were performed using 18-gauge core biopsy needles without complication. In another study, Marco-Doménech et al. [15] biopsied six colonic wall lesions using an 18-gauge core biopsy needle without complication. Furthermore, these researchers reported that several of their core specimens contained fragments of mucosa, thus indicating needle transgressions into the bowel lumen. One cecal wall biopsy was performed by Tudor et al. [16] using an 18-gauge core biopsy gun. No complication occurred in that case.

In an animal study, Petit et al. [17] used pigs to show that no significant complications developed from traversing the large and small bowel with 8-French catheters. Eighteen- or twenty-gauge core biopsy needles were also used in two studies for percutaneous biopsy of abdominal and retroperitoneal lymph nodes with sonographic guidance [12, 18]. In both of these studies, unintentional transgression of the bowel might have occurred; however, no complications of peritonitis were encountered. In a study of percutaneous pancreas biopsies by Brandt et al. [19], seven instances of needle passage through the colon using a 21-gauge cutting needle did not lead to peritonitis. Based on these reports, the risk of peritonitis associated with colonic transgression with an 18- or 20-gauge core needle biopsy appears to be small, and the use of this needle type during mesenteric mass biopsy should be considered safe. However, avoidance of colonic transgression whenever possible is still advised.

In cases of suspected lymphoma, some radiologists may choose to use an 18-gauge cutting needle to obtain samples suitable for histopathologic analysis. However, with the emergence of flow cytometric analysis, adequate tissue characterization may be achieved with 20- or 22-gauge aspirating needles [20].

We did encounter two complications. One patient developed a mesenteric hematoma after a mesenteric lymph node biopsy. The hematoma was presumably caused by inadvertent laceration of a mesenteric vessel. A review of this case revealed no unusual circumstances (e.g., coagulopathy) or increased difficulty associated with this biopsy. The number of passes performed in this case was close to our average of four passes per procedure. The incidence of this complication is likely rare because no similar cases could be found in the literature [1, 2, 3, 21]. There is one report of a mesenteric hemorrhage associated with CT-guided biopsy [22]. To reduce the risk of this complication, we emphasize the importance of using color or power Doppler sonography to identify and avoid intervening vessels before placing the needle.

Our second complication involved another patient who developed abdominal wall cellulitis at the site of needle entry. This patient underwent percutaneous biopsy of an omental mass that proved to be metastatic gastric carcinoma. During all of our procedures, we maintain strict standards of sterile technique. However, the possibility of causing an iatrogenic infection with any percutaneous procedure cannot be entirely avoided. In this case, there is also the possibility that skin infection may have been introduced retrograde from the abdomen in the event that the bowel was transgressed. A review of the procedure data does not indicate that colonic transgression was a known or likely occurrence during this biopsy. Continued adherence to strict sterile precautions and the use of abdominal compression to displace intervening bowel loops during needle passage are likely the best ways to avoid this complication.

There are limitations to this study. First, this review was retrospective. Patients were identified from a database of sonographic procedures performed. Therefore, it is possible that patients may have been referred for a sonographically guided biopsy in which it was not possible to visualize the lesion necessitating a biopsy using CT guidance. Another limitation to our study was that our sample size was small. Clearly, a larger sample size would allow more accurate estimate of the complication rate.

Finally, it should be noted that CT fluoroscopy may have advantages over sonography or traditional CT guidance for biopsy of mesenteric masses. Compared with traditional CT, CT fluoroscopy allows procedures to be performed more quickly. Patient and operator radiation dose may be minimized by limiting CT fluoroscopy time and by using a low-milliampere technique [23, 24, 25].

In conclusion, our experience indicates that sonography is an effective modality for the biopsy of mesenteric masses. We believe this procedure can be performed safely and effectively with either fine-needle aspiration or a core biopsy device. The advantages of using sonographic guidance include real-time needle tip visualization, multiplanar scanning, avoidance of ionizing radiation, visualization of intervening vessels with color Doppler sonography, and shorter procedure times compared with CT.


References
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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