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Vascular and Interventional Radiology |
1 From the Departments of Urology (E.L., D.B., C.E., M.D.F., D.R., C.C.), Radiology (M.A.), and Pathology (L.D.), Hôpital Salvator, 249 Blvd Ste Marguerite, 13274 Marseille, France. Received April 12, 1999; revision requested June 14; final revision received November 29; accepted November 2. Address correspondence to E.L. (e-mail: elechevallier@mail.ap.hm.fr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: In 63 patients (mean age, 62 years), 73 biopsies were performed. The median tumor size was 4.0 cm. Tumor biopsy was performed with an 18-gauge needle by using helical CT guidance in an outpatient setting. Two to four cores per tumor were obtained.
RESULTS: Biopsy material was insufficient for analysis in 15 (21%) procedures. The median tumor size of failed or successful biopsies was 3.0 or 4.8 cm, respectively (P = .03). A benign lesion was found at eight biopsies. Two samples were suspicious for renal cell carcinoma (RCC). RCC was found in 38 biopsy samples. The remainder were transitional cell carcinoma, metastasis, lymphoma, or sarcoma. Twenty-six patients underwent nephrectomy. The accuracies of biopsy for histopathologic and Fuhrman nuclear grade evaluation were 89% and 78%, respectively. For tumors of 3.0 cm or smaller or larger than 3.0 cm, 37% (11 of 30) or 9% (four of 43) had failure of biopsy, respectively (P = .006). No substantial morbidity occurred.
CONCLUSION: Fine-needle biopsy with helical CT guidance is accurate for the histopathologic evaluation of renal masses without morbidity. Indications are renal lesions that do not have the typical radiologic features of RCC, Bosniak category III or IV cystic lesions, and locally advanced or metastatic RCC.
Index terms: Computed tomography (CT), guidance, 81.1261, 81.1262 • Kidney, biopsy, 81.1261, 81.1262 • Kidney neoplasms, 81.20, 81.3141, 81.317, 81.318, 81.321, 81.324, 81.327, 81.336, 81.34 • Kidney neoplasms, CT, 81.12111, 81.12115 • Kidney neoplasms, diagnosis, 81.1261, 81.1262 • Kidney neoplasms, metastases, 81.336
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The purpose of our study was to determine the feasibility, the accuracy, and the clinical role of helical computed tomography (CT)-guided percutaneous biopsy of suspicious renal masses with current techniques.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Percutaneous biopsy was performed by a single operator (M.A.). The 18-gauge needle (ASAP; Boston Scientific/Medi-Tech, Spencer, Ind) allowed a 1.7 x 0.1-cm core to be obtained. Biopsy was performed with helical CT guidance (CT Twin; RTS Elscint Picker France, Chatenay-Malabry, France) and with local anesthesia (20 mL of xylocaine 1% [Lidocaine; Astra, Monts, France]) of the track. The patient was placed in a prone position. The biopsy site was chosen in the peripheral area of the tumor; the necrotic area was avoided. The tip of the needle was placed 0.1 cm outside the tumor to obtain a sample of the renal capsule in the core. With this technique, the outer cannula of the needle had little contact with the tumor to minimize the possibility of tumoral track seeding. At least two cores per tumor were obtained, with a maximum of four cores in four patients. CT was performed immediately after the removal of the needle to check for postbiopsy complications. All biopsies were performed in an outpatient clinic setting.
Histopathologic evaluation of the cores was performed with hematoxylin-eosin staining after the cores were fixed in Bouin solution. RCCs were graded according to the Fuhrman nuclear system. Non–renal cell tumors were stained with specific techniques (Hale staining) and even with immunohistochemicals.
Parameters evaluated in the study were patient age, patient sex, tumor size, left or right kidney location of the tumor, unilateral or bilateral involvement of the tumor, benign or malignant histopathologic finding in the lesion, type of malignant lesion, and Fuhrman nuclear grade of the RCC.
Patients with localized or locally advanced N0M0 tumors underwent surgery. A final histopathologic analysis was performed and included the same parameters used in the biopsy samples. Perirenal and peritumoral fat was analyzed specially to detect tumor track seeding.
For statistical analysis, the Student t test was performed to compare continuous variables between groups. The 
2 test and the Fisher exact test were performed to compare qualitative variables. A significant difference was considered to be indicated when P was less than .05. In patients who underwent surgery, the biopsy results and the final histopathologic findings were compared, and the accuracy of biopsy was calculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The median tumor size was 4.0 cm (range, 1.0–15.0 cm). There were eight Bosniak category III cystic tumors. Twenty-nine (40%) of the 73 tumors were in the right kidney. Tumors were bilateral in five patients, and biopsy was performed on both sides. The tumors were on a renal transplant by the iliac fossa in two patients. Five (8%) of the 63 patients underwent two biopsies of the tumor.
In 15 (21%) of 73 biopsies, material was not sufficient for histopathologic examination ("failed" biopsy) (Fig 1). The median tumor size in the failed biopsy specimens was 3.0 cm (size range, 1.0–7.0 cm). This was significantly lower than the tumor size in the "successful" biopsies, which was 4.8 cm (size range, 1.0–15.0 cm) (Student t test, P = .03). Biopsy failed in two (25%) of eight cystic tumors and in 13 (20%) of 65 solid tumors (P = .52). Biopsy failed in six (21%) of 29 right-sided tumors and in nine (21%) of 42 left-sided tumors with successful biopsy (P = .98).
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Eight (11%) of 73 lesions were benign. There were four benign tumors: two oncocytomas, one angiomyolipoma, and one cystadenoma. There were four benign lesions: two with fibrosis, and two with infection. In the two oncocytomas, chromophobic RCC was ruled out at Hale staining of the section.
Of the eight Bosniak category III lesions, four were RCC, one was transitional cell carcinoma, one was cystadenoma, and two had negative biopsy findings.
Forty-eight (66%) of 73 lesions were malignant. There were 31 clear cell RCCs, four papillary RCCs, three chromophobic RCCs, four primitive transitional cell carcinomas, three renal metastases (two small cell pulmonary carcinomas and one melanoma), two lymphomas, and one sarcoma (Fig 1). The median Fuhrman nuclear grade of the 38 RCCs was II (range, I–IV). There were 30 low-Fuhrman-grade (I or II) and eight high-Fuhrman-grade (III or IV) RCCs.
Twenty-one (33%) patients had a malignant lesion at biopsy and did not need surgery: Three had a metastatic lesion, two had lymphoma, two had a metastatic transitional cell tumor, and 14 had metastatic RCC.
Sixteen patients with metastases did not undergo surgery for ethical reasons. Twenty-six patients underwent surgery because of positive biopsy findings. Biopsy was used to avoid surgery in 12 (19%) of 63 patients: in seven patients for a benign lesion at biopsy, in two patients for renal lymphoma, and in three patients for renal metastasis of a primary cancer. The rest of the 21 patients with malignant lesions at biopsy who did not need surgery remained under medical surveillance and treatment.
In four patients, biopsy revealed a transitional cell RCC that was not suspected on the basis of imaging results. Two of these patients underwent nephroureterectomy instead of radical nephrectomy. The two other patients had metastases and underwent systemic chemotherapy instead of immunotherapy. Surgery was performed in four of eight cystic lesions because of RCC at biopsy. There were no false-positive findings.
Twenty-seven nephrectomies were performed in 26 patients for an N0M0 tumor. Twenty radical nephrectomies, five partial nephrectomies, and two nephroureterectomies were performed. The other nine patients who underwent surgery underwent nephroureterectomy, partial nephrectomy, and total nephrectomy for non–RCC. There were no false-positive biopsy findings. The histopathologic findings are summarized in Table 1. The accuracy of biopsy for the diagnosis of malignant or benign tumors was 89% (24 of 27). The accuracy of biopsy for the histopathologic lesion type was 78% (21 of 27).
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2 test, P = .006). No track seeding was noted at the final histopathologic analysis. In the RCC group, there was only a 7.0-cm pT3a RCC. The other RCCs were of a low stage (<pT3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Indications for renal mass biopsy have been summarized by Herts and Baker (7). Asymptomatic renal masses are being discovered with increasing frequency. Surgical management of these tumors is not always needed (8,9). Some locally advanced or metastatic RCCs can be managed with first-line nonsurgical treatment. On the other hand, some solid renal masses do not fit the radiologic findings of typical RCC, especially small lesions (2,5). These small lesions can be benign (10,11) and are indistinguishable from malignant lesions at radiologic examination (6). In these settings, biopsy can be used to avoid unnecessary surgery, which could be performed as an absolute last resort.
In our series, biopsy revealed a benign lesion in eight (13%) patients and revealed a nonsurgical malignant tumor in 21 (33%) patients. In theory, biopsy could have been used to avoid surgery in 29 (46%) of 63 patients with renal masses that were suspicious for cancer at imaging. In theory, all were candidates for surgery. Sixteen patients with metastases did not undergo surgery for ethical reasons, and 35 patients underwent surgery because of positive biopsy findings. Biopsy really was used to avoid surgery in 12 (19%) patients with benign lesions or with nonsurgical malignant tumors. Wood et al (12) used biopsy to avoid surgery in 32 (44%) of their 73 patients.
One of eight patients with a benign lesion initially underwent surgery because of the size of the mass. The seven remaining patients were followed up with CT and had no tumor progression at the time this article was written (median follow-up, 14 months). In four (50%) of eight cystic masses, surgery was indicated by biopsy results.
Moreover, in four of 63 patients, biopsy revealed a transitional cell carcinoma that was not suspected on the basis of imaging results. Two of these patients underwent nephroureterectomy instead of radical nephrectomy. The two others had metastases and underwent systemic chemotherapy instead of immunotherapy. On the basis of these findings, we advocate biopsy of metastatic renal tumor before the initiation of an immunotherapy protocol.
Wood et al (12) recently reported on a series of 79 imaging-guided biopsies of renal masses in 73 patients. The indications for biopsy in that series were similar to the indications in our series, and the tumor sizes were the same. But in Wood et al’s series, 45 (57%) of 79 biopsies were performed with CT guidance; the remainder, with US guidance. The biopsy needle sizes were 17–20 gauge. The sensitivity and accuracy of biopsy in their series were 93% and 95%, respectively. Forty-one patients underwent surgery, and there were five false-negative results. In Wood et al’s (12) series, 22-gauge–needle aspiration was performed at the time of the biopsy. One lesion (in one of 73 patients) was missed at core biopsy but was established on the basis of fine-needle aspiration findings. In contrast with Wood et al (12), we did not perform fine-needle aspiration at the time of biopsy. It would probably be an interesting adjunct to perform aspiration at the time of biopsy, especially in a cystic lesion.
The accuracy of fine-needle aspiration is controversial. Juul et al (13) published a 93% accuracy rate. More recently, Goethuys et al (3) reported that fine-needle aspiration of renal masses lacks sensitivity and has a 5% false-positive rate. In Wood et al’s (12) series and in our series, there were no false-positive biopsy findings. The quantity of tumor is not always sufficient for analysis. Campbell et al (4) reported that 10 (40%) of 25 aspirations yielded malignant cells. For these authors, the diagnostic yield appeared to be too low to justify the potential morbidity of needle aspiration.
The purpose of our study was to evaluate the feasibility, accuracy, and clinical role of fine-needle biopsy of suspicious renal masses with new biopsy technologies.
In 15 (21%) of 73 masses, biopsy failed. The median size of the tumors in which biopsy failed was significantly lower than that of the tumors in which biopsy results were positive. But the Bosniak category III cystic feature and the side on which the mass was located were not associated with a higher rate of failed biopsy. Biopsy was repeated in four cases; findings were positive for RCC in three cases. By including these repeat biopsies, the success rate was 84%. Imaide and Saitoh (14), in 100 renal tumor biopsies, had a higher success rate, 97%. The sensitivity and specificity of renal tumor biopsy reported in the literature was 70%–92% and 100%, respectively, with accuracy close to 90% (7), which is close to the accuracy in our series.
In our series, for renal masses of 3.0 cm or smaller, the success rate of fine-needle renal biopsy appeared weak, with 37% failed biopsies, compared with 9% failed biopsies for masses larger than 3.0 cm. This probably was due to technical requirements such as manipulation and breathing in patients during the puncture, which was performed outside the gantry of the CT scanner. When no tissue was obtained after a first attempt, the sheath of the needle was reinserted in the appropriate position after another CT section was obtained, and biopsy was repeated. Technical refinements could be made to avoid these drawbacks, especially in small renal masses. In actuality, we performed the biopsies by using CT fluoroscopy, which allows biopsy gun activation in real-time mode. By using this technique, we discovered that in some cases the needle pushes the tumor instead of penetrating it. This phenomenon could explain our high failure rate in small mobile tumors, but further evaluation is needed.
A malignant lesion, mainly RCC (79%), was identified in 66% of the biopsy specimens. With the biopsy specimen, the histopathologic type could be accurately identified as clear cell RCC, papillary RCC, or chromophobic RCC, as well as other types of malignant renal tumors.
Surgery was performed on 27 N0M0 tumors. In three cases, biopsy specimen analysis showed suspect cells, and RCC was found at the final analysis. In one case, the tumor was a clear cell RCC at biopsy and proved to be papillary RCC. In all other cases (89%), the biopsy findings were correlated with the final histopathologic findings.
All RCCs could be graded according to the Fuhrman nuclear system at core biopsy, but the biopsy grade had only a fair correlation with the final tumor grade. This lack of correlation was due to the heterogeneity of the tumors. But no tumor was graded erroneously by more than one point. If the tumor was pooled in a low (I or II) or a high (III or IV) grade, biopsy accuracy was improved. Herts and Baker (7) and Cajulis et al (15) reported a good concordance of grading between biopsy and final analysis, but our series was a short one with few high-grade tumors.
Similar to other investigators (12,16), on removal of the biopsy needle, we observed a subcapsular or localized perirenal hematoma on the immediate postbiopsy CT scan in 28 cases. This hematoma had no clinical importance. Similar to Imaide and Saitoh (14), we did not observe the potential complications reported in the literature (17) after needle aspiration or biopsy. In Sateriale et al’s (17) series, biopsy was performed with a 14-gauge needle. Track seeding does not depend on the size of the needle but probably is more frequent with noncutting needles than with cutting needles (7). This risk appears to be small but does exist (1,18,19). Abe and Saitoh (20) reported one case of track seeding in a sarcoma in 36 renal tumor biopsies performed with US guidance. There was no track seeding in Wood et al’s (12) series. In our series, all patients who underwent surgery have been followed up (mean follow-up, 29 months ± 11) with clinical examination and with helical CT every 6 months for 3 years, then annually. At the time this article was written, no patient had local recurrence or track seeding, not even a patient with transitional cell carcinoma. But patients with transitional cell carcinoma could have an increased risk of track seeding (7,19), and biopsy of transitional cell carcinoma must be avoided.
In contrast with the study by Goethuys et al (3), in our study, at the time of nephrectomy performed within 1 month after biopsy, no gross postbiopsy sequela was observed, and, as in the study by Wood et al (12), surgery, not even partial nephrectomy, did not appear to be more difficult. However, such complications are possible (1,7,20,21), and the patient’s condition must be monitored.
Fine-needle biopsy of renal tumors with helical CT guidance is an accurate tool for the histopathologic evaluation of renal masses. It can be performed in an outpatient setting with a low morbidity rate. Biopsy is accurate for histopathologic evaluation. Biopsy is less effective for preoperative Fuhrman nuclear grade evaluation. We recommend biopsy for patients with solid renal tumors that do not have the typical radiologic features of RCC, for patients with Bosniak category III or IV cystic lesions, for patients with locally advanced and metastatic RCC, and for patients with tumors that do not require surgery, such as renal metastases, lymphomas, and benign tumors. In these cases, histopathologic evaluation through biopsy is necessary for patient treatment.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, E.L.; study concepts, E.L., M.A.; study design, C.C.; definition of intellectual content, D.R.; literature research, E.L., D.B.; clinical studies, E.C., D.B., C.E., L.D., M.D.F; data acquisition, E.L., M.A., C.E.; data analysis, E.L.; statistical analysis, E.L.; manuscript preparation, E.L., M.A.; manuscript editing, E.L., M.A., C.C.; manuscript review, M.A., D.R., C.C.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3 cm) hyperechoic renal masses: comparison of helical and conventional CT for diagnosing angiomyolipoma. AJR Am J Roentgenol 1996; 167:877-881.This article has been cited by other articles:
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 M. K. Hatfield, R. A. Beres, S. S. Sane, and G. X. Zaleski Percutaneous Imaging-Guided Solid Organ Core Needle Biopsy: Coaxial Versus Noncoaxial Method Am. J. Roentgenol., February 1, 2008; 190(2): 413 - 417. [Abstract] [Full Text] [PDF]
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M. D. Beland, W. W. Mayo-Smith, D. E. Dupuy, J. J. Cronan, and R. A. DeLellis Diagnostic Yield of 58 Consecutive Imaging-Guided Biopsies of Solid Renal Masses: Should We Biopsy All That Are Indeterminate? Am. J. Roentgenol., March 1, 2007; 188(3): 792 - 797. [Abstract] [Full Text] [PDF]
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K. E. Maturen, H. V. Nghiem, E. M. Caoili, E. G. Higgins, J. S. Wolf Jr., and D. P. Wood Jr. Renal Mass Core Biopsy: Accuracy and Impact on Clinical Management Am. J. Roentgenol., February 1, 2007; 188(2): 563 - 570. [Abstract] [Full Text] [PDF]
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S. G. Silverman, Y. U. Gan, K. J. Mortele, K. Tuncali, and E. S. Cibas Renal Masses in the Adult Patient: The Role of Percutaneous Biopsy Radiology, July 1, 2006; 240(1): 6 - 22. [Abstract] [Full Text] [PDF]
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K. Tuncali, E. vanSonnenberg, S. Shankar, K. J. Mortele, E. S. Cibas, and S. G. Silverman Evaluation of Patients Referred for Percutaneous Ablation of Renal Tumors: Importance of a Preprocedural Diagnosis Am. J. Roentgenol., September 1, 2004; 183(3): 575 - 582. [Abstract] [Full Text] [PDF]
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M. A. Bosniak, M. G. Harisinghani, M. M. Maher, D. A. Gervais, and P. R. Mueller Should We Biopsy Complex Cystic Renal Masses (Bosniak Category III)? Am. J. Roentgenol., November 1, 2003; 181(5): 1425 - 1426. [Full Text] [PDF]
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F. J. Rybicki, K. M. Shu, E. S. Cibas, J. R. Fielding, E. vanSonnenberg, and S. G. Silverman Percutaneous Biopsy of Renal Masses: Sensitivity and Negative Predictive Value Stratified by Clinical Setting and Size of Masses Am. J. Roentgenol., May 1, 2003; 180(5): 1281 - 1287. [Abstract] [Full Text] [PDF]
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E. M. Caoili, R. O. Bude, E. J. Higgins, D. L. Hoff, and H. V. Nghiem Evaluation of Sonographically Guided Percutaneous Core Biopsy of Renal Masses Am. J. Roentgenol., August 1, 2002; 179(2): 373 - 378. [Abstract] [Full Text] [PDF]
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