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1 All authors: Department of Radiology, University of Michigan Medical Center, 1500 E. Medical Center Dr., Taubman Center 2910R, Ann Arbor, MI 48109-9723.
Received December 10, 2001;
accepted after revision January 29, 2002.
Address correspondence to E. M. Caoili.
Abstract
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MATERIALS AND METHODS. We conducted a retrospective analysis of our imaging-guided procedures from January 1999 to June 2001. We performed 26 sonographically guided percutaneous core biopsies of renal masses in 26 patients. From two to five specimens were obtained from a single mass in each patient using an 18-gauge automated biopsy system. We examined the patients' medical records, pathology results, and imaging studies. Core biopsy results were compared with surgical pathology (n = 6) or clinical follow-up (n = 20).
RESULTS. All biopsies provided sufficient material for analysis. Biopsy findings were positive for malignancy in 19 (73%) of 26 masses. Histologic diagnoses included renal cell carcinoma were (n = 11), metastasis (n = 3), lymphoma (n = 2), and transitional cell carcinoma (n = 2). Specific cell type characterization could not be made on one biopsy, but the specimens were highly suspicious for malignancy. Biopsy revealed seven (27%) of 26 benign diagnoses: oncocytoma (n = 3), angiomyolipoma (n = 2), and fibrosis (n = 2). The average follow-up period for patients with benign diagnoses was 10 months. One case of surgically proven necrotic pyelonephritis was mischaracterized as fibrosis at core biopsy. Sonographically guided percutaneous core biopsy of renal masses showed a sensitivity of 100% and a specificity of 100% for the diagnosis of malignancy. The core specimens yielded a specific diagnosis in 92% (24/26) of masses. No immediate complications occurred after the procedure. One patient developed a pseudoaneurysm that presented 3 months after the biopsy.
CONCLUSION. Sonographically guided percutaneous core biopsy is a reliable and accurate method for evaluating renal masses.
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Since the description of percutaneous biopsy of renal masses in 1972 [5], investigators have reported some success with this technique [6,7,8,9,10,11,12]. Reported percutaneous biopsy techniques have mainly involved fine-needle aspiration. Reported diagnostic sensitivities for fine-needle aspiration vary from 75% to 90%; however, the diagnostic yield of fine-needle aspiration is controversial [3, 6,7,8,9,10,11,12,13]. Up to 60% of fine-needle aspirations have an insufficient amount of material for pathologic analysis [13]. The purpose of our investigation was to evaluate the reliability and the accuracy of sonographically guided percutaneous core biopsy of suspicious renal masses.
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During the procedure, patients received IV sedation consisting of midazolam hydrochloride (Versed; Ben Venue, Bedford, OH) and fentanyl citrate (Sublimaze; Akron, Decatur, IL) unless declined by the patient. Vital signs and oxygen status were monitored. All biopsies were performed by our cross-sectional interventional radiology service that comprised seven radiologists. At the time of biopsy, the mass was confirmed on transabdominal sonography using electronically focused sector transducers ranging in frequency from 2.5 to 5.0 MHz (GE Logiq 700, General Electric Medical Systems, Milwaukee, WI; and ATL 3000 and 5000, ATL, Bothell, WA). After an entry site was chosen, a 17-gauge introducer was directed toward the lesion via an attachable needle guide. The tip of the introducer was placed at the periphery of the renal mass to minimize the possibility of tumor seeding along the needle tract. Through the introducer, an 18-gauge automatic core biopsy system (ASAP; Boston Scientific/Medi-Tech, Spencer, IN) was deployed, which yielded a maximal 17-mm core. A minimum of two cores was obtained for each mass. All biopsies were performed without a pathologist present. The specimens were sent to the pathology department in specimen cups filled with formalin or saline and gluteraldehyde if there was a clinical suspicion of lymphoma. On one occasion, a nephrologist prepared the specimen before it was evaluated by our pathology department. After the procedure, patients were observed for a minimum of 4 hr during which pulse and blood pressure were monitored at 15-min intervals for the first hour and at 30-min intervals for the next 2 hr. The biopsy site was also observed for swelling or hematoma.
We reviewed the imaging studies and reports to determine the indication for biopsy, location and size of the mass, number of core biopsies, and complications. We also reviewed the medical records, surgical pathology, and follow-up information of these patients. The sensitivity and specificity of percutaneous core needle biopsy were calculated, including histology suspicious for malignancy as a positive result and excluding any insufficient sample.
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Imaging revealed a suspicious solitary renal mass in 22 patients, bilateral renal masses in three patients, and unilateral renal masses in one patient. In patients with multiple masses, the largest or most suspicious lesion on the basis of imaging was biopsied. Twelve of the biopsied masses were located in the right kidney, and 14 were in the left kidney. The range of size for the biopsied lesions was 3.0-17.0 cm (mean, 6.5 cm). Nine masses showed mixed solid and cystic or necrotic components, and 17 showed predominantly solid components.
All patients underwent one biopsy procdure in which a range of two to five cores per mass was obtained (mean, three cores). No aspirations were performed. A small perinephric hematoma (approximately 1-3 cm) was seen in five (19%) of 26 patients; however, postprocedural scanning was not routinely performed. All patients remained hemodynamically stable throughout the procedure and during the 4-hr recovery period without the need for fluid resuscitation or blood transfusion. All patients were discharged home the day of the procedure. One patient presented 3 months later with substantial gross hematuria and a perinephric hematoma associated with an intrarenal pseudoaneurysm likely caused by the percutaneous biopsy. This was treated successfully with selective arterial embolization. No evidence of tumor track seeding was found in those patients with surgical or imaging follow-up.
In 19 (73%) of the 26 specimens, the histologic diagnosis was positive for malignancy. Of the 19 masses, seven (37%) were non—renal cell malignancies such as lymphoma (n = 2), uroepithelial malignancy (n = 2), and metastases (n = 3). The malignancies that metastasized to the kidneys were melanoma (n = 1), neuroendocrine carcinoma (n = 1), and extramedullary myeloid cell tumor (n = 1). Eleven (58%) of the 19 biopsy procedures yielded renal cell carcinoma as the histologic diagnosis (Fig. 1A,1B,1C). The core specimens from one procedure showed a substantial amount of necrotic tissue. The sample was highly suspicious for malignancy; however, further cell type characterization could not be made.
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Percutaneous biopsy confirmed the diagnosis of renal cell carcinoma in three of the four patients with renal masses and evidence of extrarenal involvement and in two patients with solitary renal masses who were not surgical candidates. Renal cell carcinoma was diagnosed in two of the nine patients with known extrarenal neoplasms, in one of the four patients with multiple renal masses, in both patients with questionable adrenal masses, and in one of the five patients with a renal mass showing atypical imaging features for renal cell carcinoma.
Nephrectomy was the clinical treatment for four malignant masses. Pathologic analysis at nephrectomy confirmed the initial biopsy results of these masses (three renal cell carcinomas and one uroepithelial malignancy). Follow-up imaging revealed a decrease in mass size after initiation of appropriate therapy thus confirming four nonrenal cell malignancies. The range of duration for imaging follow-up was 4-24 weeks (mean, 11.5 weeks). The remaining patients with biopsy-proven malignant masses (11/19) have been clinically followed up. Four patients died and two patients were placed under hospice or nursing home care. In the remaining five patients, imaging or biopsy or both have shown metastatic disease, and further treatment was declined.
In seven (27%) of 26 biopsy procedures, the histologic diagnosis was benign. Biopsies revealed five benign tumors including two angiomyolipomas, three oncocytomas, and two fibrotic lesions. The diagnosis of angiomyolipoma was initially suspected on a prior sonogram in one patient and on a prior CT scan in another; however, fat was not evident in these masses on subsequent CT examinations in both patients (Fig. 2A,2B,2C). The angiomyolipomas were clinically followed up without incident. One oncocytoma that had shown minimal growth on CT was confirmed at surgery, whereas the other two oncocytomas have been stable on subsequent follow-up imaging with a minimal interval of 6 months (range, 6-12 months). One fibrotic lesion has also been stable on follow-up imaging with a minimal interval of 6 months and has been treated as presumed retroperitoneal fibrosis. The other fibrotic lesion did not match the clinical suspicion and was found to represent necrotic pyelonephritis at surgery (Fig. 3A,3B,3C).
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All 26 biopsy specimens had sufficient material for histopathologic analysis. Sonographically guided percutaneous biopsy of renal masses showed a sensitivity of 100% and a specificity of 100% for the diagnosis of malignancy. There were no false-negative or false-positive malignant diagnoses; thus, no benign or malignant lesion was mischaracterized according to our surgical and clinical follow-up. The core specimens yielded a specific diagnosis in 95% (18/19) of the malignant masses. The core specimens yielded a correct specific diagnosis in 86% (6/7) of the benign masses. One core specimen was correctly diagnosed as benign; however, its histologic diagnosis of fibrosis represented an area of necrotizing pyelonephritis at surgery.
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Recent investigations by Wood et al. [7] and Richter et al. [8] have concluded that percutaneous biopsy of renal masses is a safe, accurate, and useful procedure. They reported sensitivities from 76% to 93% for malignancy with false-negative rates ranging from 6% to 21%. However, these reports did not distinguish between sonographically, CT-, or fluoroscopically guided procedures. In addition, they did not distinguish between fine-needle aspiration and core biopsy. The purpose of our investigation was to evaluate the utility of sonographically guided percutaneous core biopsy to evaluate suspicious renal masses.
Earlier investigations have focused on imaging-guided fine-needle aspirations with occasional core biopsy also known as fine-needle aspiration biopsy. Reported sensitivities ranged from 64% to 85% for the detection of malignancy [10,11,12, 15]. These investigations also reported insufficient sample rates from 5% to 16% suggesting that a number of fine-needle aspiration biopsies did not provide enough material for adequate cytologic analysis. The associated false-negative rates ranging from 8% to 36% are another disadvantage of fine-needle aspiration biopsies [4, 10, 15,16,17]. These rates emphasize the degree of inaccuracy of this technique making a negative result difficult to manage clinically. Other known limitations of aspiration include the inability to diagnose oncocytomas and angiomyolipomas, two benign solid renal neoplasms that on occasion can mimic renal cell carcinoma. Fine-needle aspiration can reveal oncocytes; however, these cells can be seen in both oncocytomas and renal adenocarcinomas. Distinction between these masses based on cytology is limited at best [18, 19]. Aspiration of angiomyolipomas can be misleading because these benign masses may reveal features of nuclear atypia and pleomorphism and may be falsely mistaken for a malignancy [20]. Percutaneous needle aspirations and fine-needle aspiration biopsies can also require the presence of a pathologist to perform on-site cytologic analysis. Although the presence of a pathologist is a definite advantage, this may not always be practical or feasible in busy clinical practices.
Few reports describe imaging-guided core biopsies. Early investigations regarding core biopsy did not show improved sensitivities for malignancy compared with needle aspirations. In the series by Torp-Pedersen et al. [6], sonographically guided core biopsies revealed a sensitivity of 79% and a specificity of 100% for the detection of malignancy. Six percent of the biopsies yielded a false-negative finding, and 21% of their biopsies had insufficient material. The investigators studied core biopsies obtained with an 0.8-mm needle (21-gauge needle). We used an 18-gauge needle (1.3-mm) with a biopsy system that can yield up to a 17 x 1 mm core. The difference in core biopsy sizes likely explains our results. Using an intraoperative frozen needle biopsy of renal masses with an 18-gauge biopsy gun, Dehcet et al. [21] reported a sensitivity of 84% and a specificity of 73%. Results from up to 17% of their specimens were nondiagnostic. These biopsies were performed without imaging guidance, suggesting the importance of real-time visualization in defining the optimal site of biopsy.
A more recent study by Lechevallier et al. [22] evaluated core biopsy using an 18-gauge biopsy gun with the improved imaging technology of helical CT guidance. They reported an accuracy rate of 89% with the inclusion of repeated biopsies. Helical CT—guided core biopsy had a failed biopsy rate of 21% and a repeated biopsy rate of 8% [22]. Lechevallier et al. hypothesized that in their investigation of helical CT—guided procedures, the needle was manipulated outside the CT gantry allowing the needle to accidentally shift away from the intended mass. Also, these authors noted that with CT guidance, occasionally the needle would push away instead of pierce the mass, which may be another reason for the number of failed core biopsies under helical CT guidance.
Unlike CT, sonography allows continuous visualization of the needle as it enters the mass. The needle can be directed to solid components in the mass, and the needle location can be confirmed at the time of biopsy allowing more precise placement of the needle and a better core specimen (Fig. 1C). We found that using the current sonographic technology and newer biopsy equipment, percutaneous core biopsy of renal masses provided a reliable specimen. All biopsy specimens in our study were sufficient for analysis, and repeated biopsies were not performed. This technique showed a sensitivity and a specificity of 100% for the diagnosis of malignancy. Criticisms of percutaneous biopsy have included the poor accuracy of a negative malignant result. Using sonographically guided core biopsy, we had no false-negative or false-positive findings for malignancy.
The sonographically guided core biopsy established a specific diagnosis in 95% (18/19) of the malignant masses in our series. Metastases and lymphomas were easily distinguished from renal cell carcinomas. One case of malignancy could not be further characterized histologically in a patient with an unsuspected renal mass and radiographic evidence of metastases. Before undergoing treatment, the patient died within 4 weeks of the biopsy. Core biopsy established a specific diagnosis in 86% (6/7) of the benign masses. Angiomyolipomas and oncocytomas were distinguished from renal cell carcinomas. A case of necrotizing pyelonephritis was mischaracterized as fibrosis at core biopsy. On CT, a 4.5-cm complex renal mass with focal areas of low attenuation was identified. Surgical pathology revealed a case of necrotizing pyelonephritis with multiple small (<1 cm) abscesses. In retrospect, the needle targeted the periphery of one of the abscesses (to sample solid tissue) and obtained a nonrepresentative specimen (Fig. 3C). This biopsy was limited by the predominantly necrotic or fluid character of the mass and its small size.
Reported complications associated with percutaneous renal mass biopsy include hemorrhage and needle track seeding [7, 21,22,23]. Hemorrhage after this procedure is common. Ralls et al. [23] found that hematomas were seen after 91% of percutaneous renal biopsies. In five (19%) of 26 of our patients, a small perinephric hematoma was noted that was not clinically important. In fact, the number of hematomas that occurred after biopsy in our series is likely underestimated because postprocedural imaging was not routine. However, none of the patients in our study population showed hemodynamic compromise during the procedure or the recovery period. Tumor track seeding is a potential risk with any percutaneous procedure; fortunately, it is a rare occurrence. Six incidents of track seeding associated with renal biopsies involving primarily renal cell carcinoma and uroepithelial malignancies have occurred [23]. Since 1991, there has been a report of seeding a sarcoma in one of 36 renal mass biopsies [24]. We did not observe any cases of track seeding in those patients with surgical or radiologic follow-up. We do report a postprocedural renal artery pseudoaneurysm. Both pseudoaneurysm and arteriovenous fistula formation are well-recognized complications of percutaneous renal biopsy [25,25]. Typically, they are clinically silent; however, occasionally, they can cause retroperitoneal bleeding as in our case, which required arterial embolization.
Our study had several limitations, including renal mass size, nonstandardized short-term clinical follow-up particularly of benign biopsies, and a lack of generalizability. First, most masses in our series measured greater than 3 cm. The only mass that was misdiagnosed in this series comprised several small lesions measuring less than 1 cm. Further study is needed to evaluated the accuracy of this procedure with small renal lesions. Second, many of our biopsies did not have surgical confirmation or a standardized clinical follow-up. Clinical follow-up or the need for surgery varied depending on the biopsy result, the imaging appearance, and the clinical scenario. For example, specific diagnoses such as angiomyolipomas that were concordant with imaging findings and clinical history have not had any follow-up to date. Third, our study involved a small group of subjects (26 patients) who were evaluated at an academic tertiary center with all biopsies performed by a cross-sectional interventional radiology team. The reproducibility of our results in a larger sample population in the hands of less experienced individuals may differ.
Despite these limitations, sonographically guided percutaneous core biopsy is a safe procedure that can be performed in an outpatient setting. It is an effective method for establishing the presence of malignancy and a definitive diagnosis. In a select group of patients, sonographically guided percutaneous core biopsy is a useful option to evaluate suspicious renal masses and to guide appropriate clinical care.
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