Diagnostic Yield of 58 Consecutive Imaging-Guided Biopsies of Solid Renal Masses: Should We Biopsy All That Are Indeterminate?
Abstract
OBJECTIVE. The purpose of our study was to report the diagnostic yield of 58 consecutive imaging-guided biopsies of solid renal masses.
MATERIALS AND METHODS. We retrospectively reviewed all percutaneous renal biopsies of solid masses performed at our institution over 83 consecutive months from May 1998 to March 2005 through a query of our radiology department procedure database. Fifty-five CT and three sonographic biopsies were performed at our institution during this time. A solid renal mass was documented prior to biopsy by contrast-enhanced CT (n = 48), gadolinium-enhanced MRI (n = 6), or sonography (solid noncystic masses, n = 4). The average maximal mass diameter was 3.1 cm (range, 1.0-11.0 cm). Forty-seven (81%) of the 58 biopsies were performed immediately before percutaneous ablation. Forty-four (76%) of the biopsies were performed using a coaxial technique with side-cutting automated biopsy needles (16-20 gauge), and 14 (24%) were fineneedle aspirations with a Franseen needle (20 gauge) using a tandem technique. In 19 cases, immunohistochemistry or histochemistry (Hale colloidal iron stain) was used to establish or confirm the diagnosis. Medical records and radiology and pathology reports were reviewed for all patients.
RESULTS. An adequate sample size was obtained in 55 (95%) of 58 renal masses and led to a definitive diagnosis in 52 (90%) of the 58. Renal cell carcinoma accounted for 36 (69%) of 52 diagnostic biopsies. The diagnosis of a benign lesion was made in 14 (27%) of 52 biopsies. Lymphoma (1/58) and metastatic disease (1/58) accounted for the remaining two diagnostic biopsies. Three biopsy samples obtained inadequate sample volumes, and an additional three samples were thought to have adequate sample volume but were not diagnostic. A single false-negative biopsy result was identified after growth was seen on follow-up imaging and subsequent nephrectomy revealed renal cell carcinoma.
CONCLUSION. Imaging-guided biopsy of a solid enhancing renal mass was diagnostic in 52 (90%) of 58 consecutive biopsies. The diagnosis of a benign lesion was made in 27% of diagnostic biopsies. Because of the advances in biopsy and histology techniques, the role of imaging-guided biopsy should be reconsidered.
Introduction
The increasing indications for abdominal CT, MRI, and sonography have led to an increase in the detection of incidental solid renal masses [1, 2]. It is estimated that approximately 48% of renal tumors are detected incidentally on cross-sectional imaging [3]. Before the advent of CT and sonography, most renal masses were detected because patients presented with abdominal pain, hematuria, or symptoms of metastatic disease. Given the advanced state of disease in these patients, whether a renal mass was benign or malignant was usually not a diagnostic dilemma. However, it can be difficult to establish a diagnosis for small (1-2 cm) incidentally discovered renal masses based on imaging findings alone.
Traditionally, the treatment for an incidentally discovered solid renal mass has been nephrectomy without a biopsy. Thus, a certain percentage of nephrectomies (with their associated morbidities, cost, and loss of renal function) will be performed for benign disease. A recent study of 2,770 patients who underwent radical nephrectomy found that 376 (12.8%) of the masses removed were benign [4]. This number was substantially higher (46.3%) for tumors smaller than 1 cm. Although it is difficult to estimate the percentage of incidentally discovered solid renal masses that are benign, one recent study by Tuncali et al. [5] found that 37% of solid renal masses referred for imaging-guided tumor ablation were benign lesions, not renal cell carcinoma. Because of the increasing number of incidentally discovered renal masses detected on cross-sectional imaging, it would be useful to accurately characterize them as benign or malignant to avoid unnecessary interventional therapy for benign lesions.
During the past 20 years, marked advances have been made in histology techniques, including the development of monoclonal antibodies, that have improved the diagnostic yield of imaging-guided biopsies [6]. Immunohistochemistry has been used with increasing frequency at our institution to accurately characterize renal biopsy specimens. The purpose of our study was to determine the diagnostic yield of 58 percutaneous imaging-guided biopsies of solid renal masses performed over 83 consecutive months.
Materials and Methods
This study was approved by the hospital institutional review board and is compliant with the Health Insurance Portability and Accountability Act (HIPAA). Informed consent was waived by the hospital institutional review board. We retrospectively reviewed all percutaneous renal mass biopsies performed at our institution during the 83 months from May 1998 to March 2005 through a query of our radiology department procedure database. Fifty-nine renal mass biopsies were performed during this time. Entry criterion for this study was the presence of a solid renal mass. One mass was excluded because it was cystic and did not show contrast enhancement. Thus, 58 biopsies comprise the study cohort.
Imaging studies, biopsy reports, and the radiology department procedure database were reviewed to determine greatest diameter of the mass. Biopsy needle, gauge, technique, number of passes, and complications were also recorded. Pathology reports and biopsies were reviewed to document adequacy of specimen and diagnosis.
Fifty-five (95%) of fifty-eight biopsies were performed under CT guidance and the remaining three (5%) were performed using sonographic guidance. All biopsies were performed using standard sterile techniques and local anesthesia. Biopsies performed under CT guidance were done on a single-detector helical CT scanner (High-Speed CT/i; GE Healthcare) using CT fluoroscopic guidance, with a total of one to five passes being performed. Sonographically guided biopsies were performed with the use of a needle guide and a total of one to four passes. Forty-four (76%) of the biopsies were performed using the coaxial technique with 18- or 20-gauge side-cutting automated biopsy needles (Temno, Bauer Medical International). Fourteen (24%) biopsies were performed using a 20-gauge Franseen needle with a tandem technique. In the remaining four biopsies, 16-, 18-, and 22-gauge needles were used, but specific needle type and technique were not reported.
For this study, biopsy results were defined as adequate if sufficient tissue was present according to the pathology report. Inadequate specimens included inadequate material present or the finding of “suspicious” cellular material. Biopsy results were defined as “adequate but nondiagnostic” if normal renal parenchyma was obtained; predominantly necrotic material was obtained; or visualized cells were obscured by blood, inflammation, or artifact. Diagnostic samples were defined as benign if a specific benign diagnosis was made and were defined as malignant if a specific malignant diagnosis was made. Tumor histology was classified according to the World Health Organization (WHO) 2004 classification [7].
All specimens were prepared with H and E staining. Nineteen (35%) of the 55 adequate specimens also received adjunctive immunohistochemical staining. Immunohistochemistry was performed using the Envision Dual Link Polymer System with an automated immunostainer (Dakocytomation) for the following tumor markers: CD10 and RCC; CK7, CK20, CK (cytokeratin) cocktail AE1/AE3, E-cadherin, c-kit, WT1, and HMB-45; CAM5.2; MAK-6 (Zymed); AMACR; desmin; and SMA. One specimen underwent electron microscopy. The decision to perform immunohistochemical staining and electron microscopy was made by the pathologist reviewing the sample. If definitive diagnosis was made using H and E staining, immunohistochemical staining was not performed.
Statistical analysis was performed using Fisher's exact test (Statview, SAS Institute) to evaluate the relationship between needle type or gauge and diagnostic yield.
Results
A solid enhancing (> 15 H) renal mass was documented by CT in 48 patients. Sixty-nine percent (33/48) of the masses were evaluated at our institution on a 4-MDCT scanner (LightSpeed, GE Healthcare) using 5-mm collimation. After unenhanced imaging, dynamic contrast material-enhanced images were then obtained through the mass at approximately 65 and 240 seconds after the IV injection of 100 mL of nonionic contrast material ([iohexol] Omnipaque 350, Nycomed) at a rate of 3-4 mL/s. The diagnosis of an enhancing renal mass was determined by subtracting unenhanced attenuation (in Hounsfield units) from maximum contrast-enhanced attenuation (in Hounsfield units). At our institution, a renal mass is considered to enhance if the difference is greater that 15 H.
Fifteen patients were referred from outside institutions with CT already performed that showed a solid enhancing renal mass. Six masses were documented as enhancing solid masses by gadolinium-enhanced MRI. Multiple MRI scanners were used because most patients were referred from outside institutions. Examinations were reviewed, and decisions regarding enhancement were determined subjectively. In the remaining four patients from the patient cohort, a completely solid mass with no cystic features was documented on sonography before biopsy. Forty-seven (81%) of the 58 biopsies were performed just before percutaneous radiofrequency or microwave ablation. The remaining 11 biopsies were performed to determine the cause of the mass and to guide subsequent therapy. In these cases, sufficient clinical evidence suggested the possibility of an alternative diagnosis, such as coexistent neoplasia.
Fifty-eight percutaneous solid renal mass biopsies were performed in 56 patients. Two patients each had two biopsies performed. One of these patients had a repeat biopsy after the initial biopsy revealed predominantly necrotic material. The repeat biopsy in this patient offered an adequate sample size but again showed nondiagnostic necrotic tissue. The second patient had a biopsy of a new lesion in the left kidney 47 months after biopsy of the right kidney. Thirty-six (62%) of the biopsies were of right renal masses and twenty-two (38%) were of left renal masses. The average maximal mass diameter was 3.1 cm (range, 1.0-11.0 cm).
An adequate sample was obtained in 95% (55/58) of biopsies and was sufficient to render a definitive diagnosis in 90% (52/58) (Table 1). Three biopsy specimens contained inadequate material on pathologic review. An additional three samples were thought to have an adequate sample volume but did not include the lesion (n = 1) or contained predominantly necrotic material (n= 2).
| Needle | ||||
|---|---|---|---|---|
| Result | Franseen, 20-gauge | Automated Side-Cutting, 18-gauge | Automated Side-Cutting, 20-gauge | Other, 16- to 20-gauge |
| Adequate | 86 (12/14) | 100 (7/7) | 97 (32/33) | 100 (4/4) |
| Diagnostic | 86 (12/14) | 86 (6/7) | 91 (30/33) | 100 (4/4) |
| Benign | 14 (2/14) | 0 | 30 (10/33) | 50 (2/4) |
| Malignant | 71 (10/14) | 86 (6/7) | 61 (20/33) | 50 (2/4) |
| Nondiagnostic | 14 (2/14) | 14 (1/7) | 9 (3/33) | 0 |
Note—Data are percentages (numbers) of biopsies. Adequate = enough tissue qualitatively present according to pathology report; diagnostic = able to render a definitive diagnosis of benignity or malignancy; nondiagnostic = normal renal parenchyma, predominantly necrotic material, or obscured by blood, inflammation, or artifact.
Renal cell carcinoma accounted for 69% (36/52) of the diagnostic biopsies (Fig. 1A, 1B). Definitive benign diagnoses were made in 27% (14/52). Lymphoma (1/58) and metastatic disease (1/58) accounted for the remaining two diagnostic biopsies. Benign diagnoses included oncocytoma in 12% (6/52), angiomyolipoma in 4% (2/52) (Fig. 2A, 2B), and focal glomerulosclerosis in 4% (2/52). Single diagnoses (2% each) were made of metanephric adenoma (Fig. 3A, 3B), scar, infarct, and chronic glomerulonephritis.
Forty-seven (81%) biopsies were performed immediately before percutaneous ablation. Analysis of these patients showed 26% (12/47) had benign masses, 64% (30/47) had malignant masses, and 11% (5/47) were nondiagnostic.
Surgical resection or follow-up imaging was performed in 53 (91%) of 58 biopsies. Eight patients underwent surgical resection. The six patients who were not treated with ablation and had a biopsy result consistent with renal cell carcinoma all underwent surgical resection that confirmed the biopsy results. The patient diagnosed with a metanephric adenoma underwent nephrectomy, and the diagnosis was confirmed in the resected specimen. The biopsy specimen that was classified as a scar was thought to be nonconcordant with imaging findings. On follow-up imaging, the renal mass was enlarging and the patient underwent surgical resection; a diagnosis of renal cell carcinoma was made in the surgical specimen. This was the one falsenegative diagnosis in this study.
Mean imaging follow-up was 19.3 months (range, 1-86 months). Eight (57%) of the 14 patients with benign biopsy results had confirmatory negative follow-up imaging at a mean of 20.3 months (range, 1-86 months). Two patients with benign biopsy results had negative clinical follow-up at a mean of 16.5 months (15 and 18 months). Two patients were lost to follow-up, and one patient died from respiratory failure unrelated to the biopsy several days after the procedure.
No complications occurred in the patients who had percutaneous biopsy only. Two patients developed postprocedure perinephric hematomas after having radiofrequency ablation immediately after biopsy. Neither of these patients required transfusion or hospital admission.
No statistically significant difference was found in the diagnostic yield obtained from the automated side-cutting needle, Franseen needle, or other needles. Analysis of 18-versus 20-gauge coaxial cutting needle diagnostic yield was also not statistically significant (p = 0.84). Adequate samples were obtained in all cases in which two or more passes were made for all needle types. Of the 19 specimens prepared with immunohistochemistry, a definitive histologic diagnosis was made in 17 (89%) of 19 (Fig. 4A, 4B, 4C, 4D).
Discussion
Our study shows a diagnostic yield of 90% for imaging-guided biopsy of solid renal masses. This high yield differs from that reported in the older literature [8], probably because of improved biopsy techniques and rapid advances in pathologic analysis, including immunohistochemistry. Pathologists at our institution were able to make a definitive diagnosis of malignancy in 73% of solid renal masses and, just as important, a definitive diagnosis of benignity in 27% of diagnostic biopsies. These findings are important because traditionally all solid renal masses have been treated by surgery. One large surgical series of 2,770 patients showed that 13% of all renal masses treated by radical nephrectomy were benign and 46% of renal masses smaller than 1 cm were benign [4]. If imaging-guided biopsy is shown to be diagnostic and accurate, unnecessary surgery on benign masses may be prevented.
These results are particularly relevant given the increased cross-sectional imaging volume and the concurrent increased detection of incidental renal masses. As the utilization of cross-sectional imaging continues to grow, so does the rate of the incidentally detected solid renal mass [1, 2]. Despite advances in current imaging techniques, many small incidentally discovered enhancing renal masses will continue to be diagnostic dilemmas [8, 9].
Biopsy of the solid renal mass has not been routinely used before surgery; the reasons for this are probably many [8]. Historically, there has been difficulty distinguishing low-grade malignancies (chromophobe renal cell carcinoma) from oncocytomas, which are generally considered to be benign tumors [10]. Additional contributing factors include concern for the possibility of heterogeneous tumor composition with potential sampling error and the theory of tumor seeding of the biopsy track. Although concern for seeding of the needle track is frequently discussed, in fact this is a rare complication [11].
In addition to identification of benign disease, pretreatment diagnosis may offer other benefits. Malignancies other than renal cell carcinoma that are seen more rarely may portend different prognoses. There are also multiple histologic grades and subtypes of renal cell carcinoma, which may affect prognosis and type of treatment, which include chemotherapy, radiation therapy, and surgical resection [12]. Finally, the development of minimally invasive percutaneous therapies may replace surgical resection of small renal cancers [13-15], and in these circumstances definitive histologic characterization is helpful to determine appropriate treatment and follow-up.
Differentiating benign from malignant disease before intervention would likely decrease the incidence of unnecessary procedures [4]. Twenty-six percent (12/47) of patients in our study had a definitive histologic diagnosis of benign disease when the biopsy results became available after they were treated with percutaneous radiofrequency ablation. Alternatively, these patients may have been candidates for conservative therapy with interval follow-up to confirm benign disease.
These results are comparable to those reported by Tuncali et al. [5], who found 37% of renal masses referred for ablation were benign. Nineteen percent of patients in our study underwent percutaneous biopsies because of complicated clinical presentations or imaging findings and did not receive percutaneous treatment at the time of biopsy. Three of these patients (27%) had alternative diagnoses of primary renal lymphoma, metanephric adenoma, and acute infarct, which altered their prognosis, workup, and treatment.
Studies have reported positive predictive values of 95-100% and accuracies of 72-95% for the diagnosis of renal cell carcinoma at needle biopsy [16-19]. However, the negative predictive value of percutaneous biopsy is not as high. A range of values, from 38% to 100%, has been reported, depending on the method of imaging guidance, biopsy needle gauge, and size of the renal mass [16, 17, 20]. In these cases, correlation with imaging findings is critical. When a negative biopsy result is obtained, it must be reviewed carefully in the clinical and imaging context. If it is believed to be discordant, then either repeat biopsy or close interval imaging follow-up is necessary. One patient in our series with a benign diagnosis of scar on pathology showed enlargement of the mass on follow-up imaging, and resection showed a stage I renal cell carcinoma. This false-negative result may have been due to improper placement of the biopsy needle.
Concordant with advances in imaging techniques have been remarkable advances and increased use of immunohistologic stains during the past 5 years, greatly improving the diagnostic capabilities of the pathologist [9]. These advances are reflected in our study: Immunohistochemical staining was used in 19 (35%) of 55 diagnostic samples in which a definitive diagnosis could not be established by conventional H and E staining alone. Through immunohistochemical staining, a definitive diagnosis was then rendered in 17 (89%) of 19 nondiagnostic samples using H and E staining. Advances in monoclonal antibody technology have also had a major impact on the ability to diagnose and classify renal neoplasms [6, 21, 22].
Recent investigations using core needle biopsy have shown a high accuracy rate. A study by Lechevallier et al. [23] reported an accuracy of 89% using an 18-gauge core biopsy gun with CT guidance in 63 patients. Caoili et al. [24] found that using current sonographic technology and newer biopsy equipment, percutaneous core biopsy of 26 renal masses yielded a sensitivity and specificity of 100% for the diagnosis of malignancy with no false-positive or false-negative results. In addition, better characterization can be obtained with imaging, which can be used to monitor discordant results [25].
Because our data showed adequate samples were obtained in all cases in which two or more passes were performed, we recommend at least two passes be made regardless of the biopsy method. We also think that the type of needle used (side-cutting vs Franseen) should be chosen on the basis of individual preference because our study found no statistically significant difference in diagnostic yield between the various needle types and gauges used.
Our study has several limitations. Eighty-one percent of our biopsies occurred immediately before percutaneous ablation. However, most patients underwent either corroborative subsequent surgical resection or had followup imaging showing no interval growth of the remaining benign lesions. There will frequently be no surgical specimen because less invasive methods of treating malignancies continue to advance, such as imaging-guided ablation. In addition to excluding benign disease, obtaining a specimen before percutaneous treatment is important for establishing prognosis, frequency and duration of followup, and the possible use of adjuvant therapies. Although biopsy of large masses or masses showing clear evidence of malignancy may remain unnecessary, biopsy of small indeterminate renal masses may be appropriate.
Our results show a high diagnostic yield for imaging-guided percutaneous biopsies of solid renal masses. Because of these results and the advances in histologic evaluation, we believe a role exists for imaging-guided biopsy of small solid renal masses before intervention is planned.
Footnote
Address correspondence to W. W. Mayo-Smith ([email protected]).
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Submitted: March 24, 2006
Accepted: June 7, 2006
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