Published online before print May 18, 2006, 10.1148/radiol.2401050061
(Radiology 2006;240:6-22.)
© RSNA, 2006
Renal Masses in the Adult Patient: The Role of Percutaneous Biopsy1
Stuart G. Silverman, MD,
Yu Unn Gan, MD, FRCR,
Koenraad J. Mortele, MD,
Kemal Tuncali, MD and
Edmund S. Cibas, MD
1 From the Division of Abdominal Imaging and Intervention, Department of Radiology (S.G.S., Y.U.G., K.J.M., K.T.), and Division of Cytology, Department of Pathology (E.S.C.), Brigham and Women's Hospital, 75 Francis St, Boston, MA 02115. Received January 14, 2005; revision requested March 17; revision received April 8; accepted May 2; final version accepted June 13; final review by S.G.S. January 19, 2006.
Address correspondence to S.G.S. (e-mail: sgsilverman{at}partners.org).
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ABSTRACT
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Although percutaneous renal mass biopsy with cross-sectional imaging guidance has long been considered to be safe and accurate, there have been recent advances in imaging, interventional, and cytologic techniques that have increased the role of percutaneous biopsy in the diagnosis of renal masses. Today, biopsy plays a fundamental role in the care of patients with a renal mass. Biopsy results are used to confirm the diagnosis of renal cancers, metastases, and infections, and there is increasing evidence to suggest that biopsy can help subtype and grade many primary renal cancers. Because a considerable fraction of small solid renal masses are benign and do not need treatment, there is an increasing need to diagnose them. Biopsy after a full imaging work-up can help prevent unnecessary and potentially morbid surgical and ablation procedures in a substantial number of patients. Although more data are needed to understand the overall accuracy of biopsy for the diagnosis of benign lesions, many can be diagnosed with the aid of biopsy findings. This article reviews reported experience with percutaneous renal mass biopsy, discusses the technical factors that contribute to results, and details seven specific clinical settings that should prompt the clinician to consider percutaneous biopsy when encountering a renal mass.
© RSNA, 2006
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INTRODUCTION
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The conventional approach for the detection and characterization of renal masses in adults is to use cross-sectional imaging: computed tomography (CT), ultrasonography (US), and magnetic resonance (MR) imaging. This time-tested practice represents an important contribution to the care of patients with kidney disease today (1). Indeed, most renal masses can be diagnosed accurately by using imaging alone. For example, simple cysts, inflammatory conditions (eg, focal bacterial pyelonephritis), and angiomyolipomas are benign entities that typically are diagnosed on the basis of imaging and clinical findings alone (2–4).
Despite the fact that some benign and malignant cystic renal masses look alike, the radiology literature is replete with detailed descriptions, case series, and landmark reviews that have allowed radiologists to diagnose confidently the majority of cystic masses as benign or malignant by using image-based features (2,5). When a renal mass has imaging findings characteristic of malignancy, a diagnosis can be rendered with such confidence that, as long as the tumor appears to be resectable, surgery may proceed in most cases without a preprocedural biopsy. In other words, the positive predictive value of imaging findings is so high that a negative biopsy result does not alter management (3,6). Although some renal masses cannot be diagnosed confidently with imaging alone, percutaneous biopsy has historically played only a limited role in the evaluation of renal masses (1–4,7). In the past, percutaneous biopsy was reserved mostly for aid in diagnosis of lymphoma or metastatic disease (for which surgery would typically be unnecessary), infection, or tumors in patients who have an increased surgical risk (1–3).
In recent years, several advances in imaging, interventional, and cytologic techniques have allowed percutaneous biopsy to play a larger role in the evaluation of renal masses in adults. The purpose of this article is to review these advances and to explain why biopsy has a clinically important role in the diagnosis of renal masses today. We will review reported experience with percutaneous biopsy of renal masses, discuss the technical factors that contribute to results, and highlight the capabilities and limitations of this procedure. Then, we will review specific clinical indications and explain the importance of biopsy in each of them. Overall, on the basis of this review the practicing radiologist will understand the current role of percutaneous renal mass biopsy in the diagnosis and management of renal masses in adult patients.
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FACTORS CONTRIBUTING TO THE INCREASING ROLE OF BIOPSY
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Percutaneous renal mass biopsy is indicated in more patients today for the following reasons. First, there is growing evidence that advanced multidetector CT, MR imaging, and US techniques result in the detection of more renal masses than ever before (1,8–10). As a consequence, the incidence of renal cell carcinoma has increased (11–14). The incidental detection of benign renal masses has increased concomitantly (15,16). The identification of incidental small renal cell carcinomas has been due, in part, to the ability of radiologists to use thin-section multidetector CT and MR imaging (which results in less partial volume averaging effects) to characterize confidently masses as enhancing and, therefore, solid. Excluding infections and angiomyolipomas, most solid renal masses in adults are renal cell carcinoma (20).
However, a substantial fraction of solid renal masses are benign (15–22). Authors of a report published in 2003 (19) studied 2770 resections of solid renal masses and found that 12.8% were benign. However, when stratified by size, the proportion of benign masses was 25% for masses smaller than 3 cm, 30% for masses smaller than 2 cm, and 44% for masses smaller than 1 cm (19). Hence, there was a direct correlation between malignancy and the size of the mass: The smaller the renal mass, the greater the percentage of benign causes. Benign masses in this series consisted of oncocytoma (70%), angiomyolipoma (18%), papillary adenoma (4%), and metanephric adenoma (1%); the remainder were not specified. Thus, the second factor that has led to the need for percutaneous biopsy is the fact that a substantial portion of small solid renal masses are benign and cannot be distinguished from malignant masses by means of imaging findings alone.
Few studies have identified diagnostic features that could be used as clues to a benign diagnosis (23–26). Homogeneously enhancing and hyperattenuating renal masses are one subset of solid renal masses that may prove to be benign angiomyolipomas with minimal fat (24). In general, however, imaging cannot be used to differentiate benign from malignant solid masses. Short of resection of these masses, diagnostic options are limited to observation and percutaneous biopsy.
Indeed, biopsy was used recently to help identify benign tumors that were referred for percutaneous ablation (27). In that study, 27 patients had renal masses that were enhancing on CT or MR images, were presumed to be renal cell carcinoma, and were referred for percutaneous ablation. Among these, the masses in 10 (37%) patients were benign. There were three angiomyolipomas with minimal fat; each was proved on the basis of biopsy results (27). This series further supported the notion that small solid renal masses cannot be presumed to be malignant.
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DIAGNOSTIC EFFECTIVENESS
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After the earliest reports of fluoroscopically guided percutaneous biopsy of renal masses (28–30), CT- and US-guided techniques were described for abdominal masses and included the kidney (31–38). The results of these studies demonstrated the feasibility and safety of diagnosing abdominal tumors on the basis of percutaneous biopsy findings. Indeed, many investigators demonstrated the utility of percutaneous biopsy for abdominal masses in general and established biopsy as an effective means for obtaining tissue diagnoses nonsurgically. In addition, percutaneous biopsy of abdominal masses has been shown to be cost-effective relative to surgical biopsy (39). An average per-patient cost savings of $3000 was calculated for percutaneous biopsy, compared with the cost of open surgical biopsy.
Since then, researchers focused their case series on renal masses and better defined the efficacy and the role of biopsy in different clinical settings. Several indications for biopsy have been reported in the radiology (40–45), pathology (46–49), and urology (50–56) literature. Renal mass biopsy was found to alter care in 41% of patients in one series (56); investigators have also demonstrated a substantial effect on patient care (46). Biopsy can be used to diagnose a variety of tumors, both malignant and benign.
Malignant Tumors
Renal cell carcinoma (1,57–59), transitional cell carcinoma (60), lymphoma (61), and metastatic tumors (62) can all be accurately diagnosed by means of percutaneous biopsy with fine needles (20-gauge or thinner) (Fig 1). Of 261 masses subjected to biopsy in one multicenter study (62), 11% were metastatic tumors. These capabilities are largely a result of advances in cytology, immunocytochemistry, and the cytogenetics of renal neoplasms. The cytomorphologic features of renal neoplasms, including renal cell carcinoma and its various subtypes, have been better described; and the immunocytochemical and cytogenetic profiles, better defined (Table).
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Figure 1a: Biopsy of solid 3.5-cm right interpolar renal mass in a 68-year-old woman referred for percutaneous ablation. (a) Percutaneous biopsy of the mass (arrowhead) with 25-gauge needle (arrow), shown on transverse CT image, yielded inadequate cellular material. (b) CT-guided biopsy, shown on transverse CT image, was repeated with 18-gauge needle (arrow). (c) Photomicrograph shows cells were immunoreactive (arrows) for renal cell carcinoma antibody. (Original magnification, x600.) (d) Photomicrograph of cell block section reveals clear cell renal cell carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 1b: Biopsy of solid 3.5-cm right interpolar renal mass in a 68-year-old woman referred for percutaneous ablation. (a) Percutaneous biopsy of the mass (arrowhead) with 25-gauge needle (arrow), shown on transverse CT image, yielded inadequate cellular material. (b) CT-guided biopsy, shown on transverse CT image, was repeated with 18-gauge needle (arrow). (c) Photomicrograph shows cells were immunoreactive (arrows) for renal cell carcinoma antibody. (Original magnification, x600.) (d) Photomicrograph of cell block section reveals clear cell renal cell carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 1c: Biopsy of solid 3.5-cm right interpolar renal mass in a 68-year-old woman referred for percutaneous ablation. (a) Percutaneous biopsy of the mass (arrowhead) with 25-gauge needle (arrow), shown on transverse CT image, yielded inadequate cellular material. (b) CT-guided biopsy, shown on transverse CT image, was repeated with 18-gauge needle (arrow). (c) Photomicrograph shows cells were immunoreactive (arrows) for renal cell carcinoma antibody. (Original magnification, x600.) (d) Photomicrograph of cell block section reveals clear cell renal cell carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 1d: Biopsy of solid 3.5-cm right interpolar renal mass in a 68-year-old woman referred for percutaneous ablation. (a) Percutaneous biopsy of the mass (arrowhead) with 25-gauge needle (arrow), shown on transverse CT image, yielded inadequate cellular material. (b) CT-guided biopsy, shown on transverse CT image, was repeated with 18-gauge needle (arrow). (c) Photomicrograph shows cells were immunoreactive (arrows) for renal cell carcinoma antibody. (Original magnification, x600.) (d) Photomicrograph of cell block section reveals clear cell renal cell carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)
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Several studies have evaluated the sensitivity, specificity, and overall accuracy of biopsy (43,44,46,47,50,52–54,58,59). These studies vary considerably with respect to patient population, tumor type, guidance modality, and needle size. Overall, the sensitivity of biopsy for diagnosis of malignancy is 80%–92%, regardless of needle size used or whether the specimens were examined cytologically, histologically, or both (63). False-negative results are most often due to failure to place the needle tip accurately in a small mass or to sampling of necrotic portions of a large tumor (45). Even in experienced hands, false-negative results do occur, which suggests that negative results should be viewed with caution in patients with a radiologically suspicious mass (49). In one study (7), biopsy yielded suspicious or atypical cells in 36% of 25 small (
5-cm) masses sampled with a fine needle. The value of retrieving suspicious or atypical cells is unknown. In a series (64) of abdominal masses (of which a small portion were of renal origin), specimens that contained atypical cells had a 71% chance of being malignant. Certainly, in order to be clinically useful a biopsy report should include as specific a diagnosis as possible. Biopsy specimens that contain no malignant cells cannot be used alone to conclude that the sampled mass is benign, and suspicious or atypical results cannot be used alone to conclude that the sampled mass is malignant.
Specificity ranges from 83%–100% (63). False-positive diagnoses of malignancy are rare but have been reported after biopsy of a calcified cyst (65), multilocular cystic nephroma (66,67), angiomyolipoma (47,53), and chronic pyelonephritis (47,58). There are too many individual cases to cite, but most were reported in 1990 or earlier (47,53,58,67) and, in our opinion, do not appropriately reflect current cytologic examination capabilities. In one study (54), 0.8-mm (approximately 20-gauge) needles were found to reduce false-positive results, but the sensitivity was higher for thinner 0.6-mm (approximately 23-gauge) needles.
Finally, of all the patient-related factors that affect the test characteristics of biopsy, the size of the mass is probably the most important. Indeed, the sensitivity of biopsy for the diagnosis of a small (3-cm) mass is lower than that for larger masses (45). Small masses are simply more difficult to target. As with all image-guided biopsies, the radiologist should strive to obtain at least one image that demonstrates the needle tip in the mass before the procedure is terminated (Fig 1).
Renal Tumor Subtype and Grade Determination
In addition to accurate diagnosis of renal cancer, there is an increasing need to evaluate tumor subtype and grade. The determination of cancer subtype and grade not only helps determine the patient's prognosis but may also be used to select appropriate treatment. This is particularly important in patients in whom partial nephrectomy or percutaneous ablation is considered. In a study of 38 primary tumors (68), fine-needle specimens were compared with resected specimens. Of the 34 primary tumors, 74% were correctly subtyped, including 15 of 18 clear cell renal cell carcinomas, four of eight papillary carcinomas, all four oncocytomas, and both chromophobe renal cell carcinomas. Two sarcomatoid renal cell carcinomas and three papillary renal cancers were misclassified as clear cell type.
Sarcomatoid renal cell carcinoma, which accounts for 5% of all renal cell carcinomas, has a worse prognosis than all other subtypes; therefore, an accurate diagnosis is important (69). For example, a nephron-sparing procedure may not be indicated for these tumors. In our experience, these tumors are generally too large at the time of presentation to be treated with a nephron-sparing procedure. Although this type of renal cell carcinoma can be identified percutaneously, the reliability of biopsy has not been shown. In our opinion, data regarding our ability to subtype renal cell carcinomas with percutaneous biopsy are promising, but more studies are needed to determine accuracy, particularly for the less common tumor subtypes (42,68,70).
With regard to tumor grade, the authors of several studies (7,70,71) have reported reasonable concordance of Fuhrman nuclear grade between biopsy and surgical specimens. The Fuhrman grading system is the standard for grading renal cell carcinoma. A grade from 1 to 4 is based on nuclear features, with increasing nuclear and nucleolar size resulting in a higher grade. In one series (70), fine-needle biopsy was performed in 49 renal cell carcinomas; there was a high concordance between fine-needle specimens and histologic results.
Large needles may be useful in increasing the number of cases in which renal cell carcinoma subtype and grade can be determined. Neuzillet et al (72) reported on 88 biopsies performed with CT guidance and 18-gauge needles in small (4-cm) solid masses. Histopathologic tumor type was identified accurately in 92%; but the Fuhrman nuclear grade, in only 69.8% (72). More studies will be needed to determine the accuracy of biopsy with respect to grading.
Benign Tumors
Although the radiology literature is replete with case series that show renal mass biopsy to be accurate overall, most data are derived from patients with renal cancers. To our knowledge, there are no large series in which most cases represent benign renal tumors. Indeed, most benign tumors are diagnosed with the aid of imaging, and biopsy is not performed. As a result, the sensitivity and specificity for the diagnosis of benign tumors with the aid of percutaneous biopsy are not known. Nevertheless, benign tumors can be diagnosed percutaneously. The series of Neuzillet et al (72) included 14 benign lesions: 10 oncocytomas, three angiomyolipomas, and one cystadenoma; only 5% of samples overall were inconclusive in that series. The authors concluded that biopsy could be used to obviate surgery in patients with benign solid tumors.
In another study (73), biopsy with an 18-gauge needle was performed in 106 masses. The biopsy results were accurate for 91 malignant lesions; however, of the 15 benign tumors that were sampled (11 of which were oncocytomas), one-third were not accurately diagnosed. The authors concluded that intraoperative biopsy should not be used to guide surgical decision making. Biopsy specimens in that study were analyzed as frozen sections, and hematoxylin-eosin staining was performed for a rapid evaluation. However, the results of that study should not be applied to percutaneous biopsy performed preoperatively. Percutaneous biopsy specimens undergo a more extensive cytologic evaluation, which includes a more thorough review of smears, cell block sections, and immunocytochemical studies. In a subsequent report (74), the same group performed intraoperative biopsy of the removed surgical specimen with 18-gauge needles in 100 patients with solid masses, 85% of which were malignant, and compared the biopsy results with whole-tissue-specimen analysis results. The authors concluded that they could not recommend preoperative percutaneous biopsy for renal masses because of the low specificity they observed. However, the specificity they observed might have been much higher had they used ancillary diagnostic methods, such as immunocytochemical analysis and cytogenetics, as adjuncts to morphologic evaluation with conventional stains.
Angiomyolipoma.—Angiomyolipoma, one of the most common benign solid tumors of the kidney, is almost always diagnosed by using imaging alone. It can, however, be diagnosed with the aid of biopsy (75–79). Biopsy can help diagnose angiomyolipomas that contain fat (76,80) and those with minimal fat (81).
Historically, biopsy of angiomyolipomas has been considered limited, particularly when fine needles alone are used, because these benign masses may reveal features of nuclear atypia and pleomorphism and be falsely diagnosed as cancers (80). Nowadays, the differentiation of angiomyolipoma from renal cell carcinoma can often be made with the aid of immunocytochemical analysis (75–77) (Table). The melanosome-associated protein HMB-45 is consistently expressed in angiomyolipomas but not in renal cell carcinomas or liposarcomas (82). Angiomyolipomas do not contain cytokeratin, a marker that is frequently present in renal cell carcinoma. The sensitivity and specificity of these markers has helped allay the concerns of skeptics who, in years past, argued against biopsy of suspected angiomyolipomas for fear of missing cancers (82).
Because angiomyolipomas are hypervascular and, when large, can bleed spontaneously, there has been a concern for bleeding after biopsy. However, on the basis of our experience and review of the literature, bleeding as a result of biopsy of an angiomyolipoma is no more common or severe than that of other renal tumors, particularly when fine needles are used (77,79,80,83).
Oncocytoma.—The role of percutaneous biopsy in the diagnosis of oncocytoma is currently controversial (84,85). The value of diagnosing these tumors lies in the fact that, in general, they are considered benign tumors (17,86). A confident diagnosis of oncocytoma would allow patients to avoid aggressive surgical approaches. Imaging features have been described that include the presence of a prominent central scar in an otherwise homogeneously enhancing tumor (23,87) and a "spoke-wheel" pattern on angiographic images (87). However, these radiologic findings are not present in all cases, and each has been described for renal cell carcinoma (88). Therefore, none can be used to enable a confident diagnosis of oncocytoma (86).
Historically, biopsy of oncocytoma has been considered limited for the following reasons. Oncocytic cells can exist in a variety of renal neoplasms, including renal oncocytoma and oncocytic renal cell carcinomas, many of which are renal cell carcinomas of low metastatic potential (89). These include granular cell carcinoma, chromophobe renal cell carcinoma, and eosinophilic variant of papillary renal cell carcinoma (84,85,90–92). While oncocytoma cannot be diagnosed with complete confidence on the basis of biopsy results, an oncocytic neoplasm can be diagnosed, and, in some cases, a diagnosis of oncocytoma can be strongly suggested on the basis of histochemical, immunocytochemical, and ultrastructural studies (Fig 2).
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Figure 2a: Incidental mass in interpolar region of left kidney in a 61-year-old man. (a) Transverse T1-weighted MR image (repetition time msec/echo time msec, 285/4.2) shows 2.5-cm mass (arrowhead) that enhanced homogeneously. CT-guided percutaneous biopsy was performed (not shown). (b) Photomicrograph of cytologic preparation reveals oncocytic cells (arrows). (Giemsa stain; original magnification, x600.) Immunocytochemical reaction for keratins AE1/AE3 (not shown) was positive. Hale colloidal iron stain (not shown) was negative. Diagnosis was renal oncocytoma.
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Figure 2b: Incidental mass in interpolar region of left kidney in a 61-year-old man. (a) Transverse T1-weighted MR image (repetition time msec/echo time msec, 285/4.2) shows 2.5-cm mass (arrowhead) that enhanced homogeneously. CT-guided percutaneous biopsy was performed (not shown). (b) Photomicrograph of cytologic preparation reveals oncocytic cells (arrows). (Giemsa stain; original magnification, x600.) Immunocytochemical reaction for keratins AE1/AE3 (not shown) was positive. Hale colloidal iron stain (not shown) was negative. Diagnosis was renal oncocytoma.
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A retrospective analysis of 19 oncocytic neoplasms was conducted in which fine-needle specimens were compared with surgical findings (84). Although there was considerable overlap among tumor types cytologically, oncocytomas could be reliably distinguished from oncocytic renal cell carcinomas with immunocytochemical analysis. All oncocytomas were negative for vimentin, whereas only granular cell carcinoma and eosinophilic variant of papillary renal cell carcinoma were positive for vimentin. The two vimentin-negative neoplasms, oncocytoma and chromophobe renal cell carcinoma, could be distinguished on the basis of Hale colloidal iron stain, which was present in all chromophobe renal cancers but only focally or not at all in oncocytomas (84) (Fig 3).
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Figure 3a: Small solid mass in interpolar region of left kidney in a 57-year-old man with a history of prostate cancer. (a) Transverse CT image shows enhancing 3.5-cm left renal mass (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with patient in the prone position by using a 25-gauge needle (arrow). Cytologic preparations stained with Wright-Giemsa stain (not shown) revealed oncocytic cells. At further staining with (c) epithelial membrane antigen, as demonstrated by brown color, and (d) Hale colloidal iron stain, as demonstrated by blue color, the cells obtained at biopsy were positive. Diagnosis was chromophobe renal cell carcinoma. (Original magnification for c and d,x400.)
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Figure 3b: Small solid mass in interpolar region of left kidney in a 57-year-old man with a history of prostate cancer. (a) Transverse CT image shows enhancing 3.5-cm left renal mass (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with patient in the prone position by using a 25-gauge needle (arrow). Cytologic preparations stained with Wright-Giemsa stain (not shown) revealed oncocytic cells. At further staining with (c) epithelial membrane antigen, as demonstrated by brown color, and (d) Hale colloidal iron stain, as demonstrated by blue color, the cells obtained at biopsy were positive. Diagnosis was chromophobe renal cell carcinoma. (Original magnification for c and d,x400.)
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Figure 3c: Small solid mass in interpolar region of left kidney in a 57-year-old man with a history of prostate cancer. (a) Transverse CT image shows enhancing 3.5-cm left renal mass (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with patient in the prone position by using a 25-gauge needle (arrow). Cytologic preparations stained with Wright-Giemsa stain (not shown) revealed oncocytic cells. At further staining with (c) epithelial membrane antigen, as demonstrated by brown color, and (d) Hale colloidal iron stain, as demonstrated by blue color, the cells obtained at biopsy were positive. Diagnosis was chromophobe renal cell carcinoma. (Original magnification for c and d,x400.)
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Figure 3d: Small solid mass in interpolar region of left kidney in a 57-year-old man with a history of prostate cancer. (a) Transverse CT image shows enhancing 3.5-cm left renal mass (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with patient in the prone position by using a 25-gauge needle (arrow). Cytologic preparations stained with Wright-Giemsa stain (not shown) revealed oncocytic cells. At further staining with (c) epithelial membrane antigen, as demonstrated by brown color, and (d) Hale colloidal iron stain, as demonstrated by blue color, the cells obtained at biopsy were positive. Diagnosis was chromophobe renal cell carcinoma. (Original magnification for c and d,x400.)
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Although these recent developments appear promising, there are insufficient study results to conclude that biopsy can help identify oncocytoma with complete confidence. However, there is sufficient evidence to conclude that an oncocytic neoplasm can be diagnosed with confidence, and, in some cases, oncocytoma can be strongly suggested on the basis of characteristic morphologic features and a negative Hale colloidal iron stain (Fig 2).
Other tumors.—Metanephric adenoma, an uncommon tumor, can be diagnosed on the basis of biopsy results (93). Leiomyoma is also rare and difficult to diagnose percutaneously, because it is often not possible to differentiate leiomyoma from leiomyosarcoma on the basis of needle biopsy samples alone (94). Renal adenomas are small tumors that are indistinguishable from low-grade papillary renal cell carcinomas in every way except size. Therefore, pathologists often reserve the term "renal adenoma" for very small (<2-mm) lesions detected at autopsy or in kidneys resected for other reasons (95). Masses of this size are too small to be successfully targeted for biopsy. In fact, most are not detectable with imaging.
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TECHNICAL CONSIDERATIONS
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Techniques for performing image-guided renal mass biopsy are common to those for performing other abdominal biopsies and have been described in detail elsewhere (34,96). The reader is also referred to reviews of renal mass biopsy in which techniques are described (51,63). Because this review focuses on the role of biopsy in the evaluation of renal masses, technique is discussed only as it relates to efficacy and safety. Indeed, efficacy and safety are a result of many factors, including patient cooperativeness, tumor type, tumor size, and operator expertise, to name a few. The two principal technical variables that affect efficacy and safety are image-guidance modality and needle size.
Percutaneous biopsy of renal masses is now most often guided by using CT (27,42,45,97–100), US (45,97,101,102), and rarely MR imaging (27,103). To our knowledge, there are no data to support the use of one modality for all masses. US can be used at the bedside and is a widely available, real-time, multiplanar modality that is free of ionizing radiation and less expensive than CT or MR imaging. However, not all renal masses are visible at US. Intervening bowel and pleural space cannot always be seen, and it may be difficult to visualize the location of the needle tip. CT can be used to visualize almost all renal masses (although intravenous contrast material may be needed on rare occasions) and is excellent in depicting bowel, pleural space, and the needle tip. MR imaging is typically reserved for the unusual mass that is not well depicted with CT or US or for masses in which MR-guided treatment is planned (104). In general, we recommend using the imaging modality that depicts the mass best and with which the radiologist is most familiar.
Percutaneous biopsy of renal masses can be performed with a wide range of needle sizes. In this review, we will consider percutaneous biopsy of a renal mass to refer to a procedure during which imaging is used to guide any needle into a renal mass percutaneously for the purpose of obtaining a tissue diagnosis. This includes biopsies in which fine (20-gauge or thinner) or large (19-gauge or larger) needles are used. Although many authors use this convention, some refer to 18-gauge (or thinner) needles as fine needles (42,54,72). Some authors distinguish between "fine-needle aspirations," during which only fine needles are used and the tissue is examined cytologically, and "biopsies," during which large needles are used to procure fragments of tissue, sometimes referred to as "cores," and are examined histologically. Although needle size has some bearing on the effectiveness and safety of the procedure, we prefer to consider all procedures that include the insertion of a needle into the body for the purpose of obtaining tissue for analysis, a biopsy, regardless of needle size. Also, we prefer not to use the term core when analyzing the literature. Cores of tissue may be obtained from both fine and large needles. The important distinction is the size of the needle used, as well as how the specimen is analyzed. Some series include biopsies in which each procedure is performed with either a fine or a large needle alone, and other series include procedures that are performed with both types of needles. In general, fine-needle aspiration biopsy specimens are analyzed cytologically, and large-needle biopsy specimens are analyzed histologically. Needles also differ by type: Some are end-cutting, others are side-cutting (42,54,72,105). There are no data to suggest that renal masses are better sampled with one type or the other. In one study (54), specimens obtained using fine needles were analyzed histologically. Therefore, it is difficult to ascertain from the literature the specific value of any one factor related to needle size or type.
The diagnostic sensitivity for percutaneous biopsy procedures in which only fine needles were used varies from 75% to 92% (7,45,51,54–59,100). Some authors have encountered poor results with fine needles, prompting them to conclude that biopsy is contraindicated if surgery is planned (57). In our opinion, poor results are likely due to problems with targeting, not needle size.
Biopsies performed with both fine and large (typically 18-gauge) needles have yielded similar sensitivities (56,100). These series showed that the sensitivity for detecting malignancies ranges from 76% to 93% (56,100). Since these series included biopsies in which both fine and large needles were used, it is difficult to distinguish the relative value of 18-gauge needles. Biopsy specimens obtained with 20- and 18-gauge spring-loaded biopsy devices and analyzed histologically provided a definitive diagnosis in 10 of 44 cases in which fine-needle aspiration biopsy specimens did not (101). However, there were four complications in this series, largely related to hemorrhage.
Lechevallier et al (42) evaluated biopsy specimens obtained with an 18-gauge needle and CT guidance; the results were similar to those that had been achieved with a combination of fine and large needles, including a failed biopsy rate of 21% and a repeat biopsy rate of 8%. Overall accuracy was 89% when repeat biopsies were included. Rybicki et al (45) used both fine and large needles to perform biopsy of 115 masses. The overall sensitivity was 90%; however, there were no false-negative biopsy specimens among the 23 masses sampled with a needle larger than 20 gauge. These data suggest that large needles may improve the yield of the procedure (Fig 1). In the series by Neuzillet et al (72), in which biopsy with an 18-gauge needle was performed in 88 patients' renal masses and the specimens were analyzed histologically, the material retrieved was sufficient in all but three procedures. Caoili et al (41) used an 18-gauge, automated, spring-loaded biopsy system and US guidance to sample masses. A specific diagnosis was rendered in 92% of masses, including five benign tumors. The authors suggested that real-time US guidance allowed better targeting and more consistent sampling of masses. Therefore, while there are data to suggest that the use of 18-gauge needles improves efficacy, to our knowledge no statistically valid comparison study has been performed to draw any definitive conclusions.
On the basis of current available data, it is reasonable to conclude that fine needles are adequate by themselves to sample the majority of renal masses. Large needles may be helpful in selected circumstances. Although the use of large needles may increase accuracy, we believe large needles also increase the risk of complications, particularly bleeding (105). In our practice, we begin with a fine needle and ask the cytologists to examine one or two specimens intraprocedurally. If the preliminary cytologic impression is that the specimen is adequate, the procedure is completed by using fine needles alone. If there is any question as to the specimen's adequacy, we obtain large-needle specimens for histologic analysis.
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COMPLICATIONS
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Percutaneous biopsy for renal masses is a safe procedure. Bleeding is the most frequent complication, but it is usually subclinical, detected only with a postprocedural CT scan, and self-limited. CT depicted some form of perinephric hemorrhage in 91% of 200 biopsies in one series (106). Major bleeding that requires a blood transfusion is uncommon (102). Hematuria may occur; microscopic amounts probably occur in most cases. However, gross hematuria is uncommon; it was estimated to occur in 5%–7% of cases in one series (37). In our experience, gross hematuria is rare and likely due to inadvertent transgression or biopsy of normal renal parenchyma. It is almost always self-limited but may persist owing to arteriovenous fistula formation (43).
In general, large-needle biopsies are associated with more bleeding complications than are fine-needles biopsies (107). Although there are no direct comparison data of which we are aware, we believe that perinephric hemorrhage that is important enough to warrant transfusion or hospitalization is more likely to occur with large needles, particularly when normal renal parenchyma is inadvertently included during the biopsy. Indeed, the rate of hemorrhage is higher after biopsy of renal parenchyma in which an 18-gauge or larger needle is used. In a series of 203 renal parenchymal biopsies (102), bleeding that required a blood transfusion or other intervention developed in 1.5% of procedures. Large-needle biopsy probably also increases the risk of pseudoaneurysm formation that may not clinically manifest until several months after the biopsy. Such a case was reported by Caoili et al (41) in a patient who presented 3 months after a renal mass biopsy with gross hematuria and a perinephric hematoma associated with an intrarenal pseudoaneurysm. This complication can be treated with arterial embolization, as was done in the reported case.
Pneumothorax may occur but, like major hemorrhage, is uncommon. The risk can be avoided by using a subcostal approach. When an intercostal approach is used, the rate of pneumothorax is still extremely low as long as the lung is not transgressed.
Seeding of the needle track with tumor is a possible consequence of percutaneous biopsy throughout the body, but it is extremely rare, estimated at less than 0.01% of cases (108). Six cases of needle-track seeding associated with renal mass biopsy, primarily involving renal cell carcinoma and transitional cell carcinoma, have occurred (50,56,109–113). There was an additional report (114) of seeding with a sarcoma in one of 36 renal mass biopsies. Our view is that the risk of needle-track seeding during biopsy of renal cell carcinoma is probably not more likely than that with cancers of other types. Only three of 23 cases of needle-track seeding reported by Smith (108) were from biopsies of renal cell carcinoma. However, an accurate assessment of the prevalence of tumor seeding during renal mass biopsy would require knowledge of both the number of cases of tumor seeding and the number of all renal mass biopsies. Some authors (51,113–115) consider transitional cell carcinoma to have a greater propensity to seed than renal cell carcinoma and therefore recommend that biopsy not be performed when transitional cell carcinoma is suspected.
The relationship between risk of seeding and size of needle is also not known. Needle-track seeding has been reported after biopsies with both large and fine needles, but there are too few cases to determine whether risk is related to needle size. Overall, needle-track seeding is rare and, therefore, should not be a deterrent to biopsy when there is an appropriate indication. When transitional cell carcinoma is considered, biopsy can still be performed if the diagnosis remains in question after urologic imaging (intravenous pyelography or CT urography), urine cytologic analysis, retrograde pyelography, and ureteroscopy have been considered.
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INDICATIONS FOR PERCUTANEOUS BIOPSY OF RENAL MASSES
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From the literature, two specific lists of clinical indications can be derived: one, which we refer to as "established" (Fig 4), and another, which we call "emerging" (Fig 5). Although the indications discussed herein may not apply to all patients, they should serve to guide clinicians, including radiologists, in determining when and why to consider percutaneous biopsy in specific clinical settings.
Established Indications
This group of indications is derived from sufficient data and clinical experience. Most patients in this group have a malignant renal mass. Most malignant renal masses represent renal cell carcinoma. The excellent performance of biopsy in these cases is largely a result of advances in cytologic analysis that allow a diagnosis of renal cell carcinoma and other malignancies to be made with confidence most of the time.
Patients with known extrarenal primary cancer.—One of the most common indications for percutaneous biopsy of a renal mass is in a patient with a renal mass and a known extrarenal primary malignancy. Percutaneous renal mass biopsy is indicated in these patients to help differentiate a surgically resectable renal cell carcinoma from a metastasis. A pretreatment diagnosis is needed because virtually all metastases are treated medically; renal cell carcinomas are treated surgically. Biopsy has been reported to be 90% sensitive for the detection of malignancies in this group of patients (45,63). The importance of a pretreatment tissue diagnosis in these patients is further emphasized in patients with lymphoma and lung cancer, two tumors that commonly spread to the kidney (116,117). In one series, despite the metastatic potential of these tumors, a renal mass was proved with biopsy findings to be renal cell carcinoma in half the cases (45). Therefore, when a mass is detected in a patient with an extrarenal primary malignancy, the mass should not be presumed to represent a metastasis; biopsy should be performed. In general, image-based features cannot be used alone to differentiate a primary renal cancer from a metastasis. However, in patients who present with a cystic renal mass and an extrarenal primary malignancy, it is unlikely that a cystic renal mass represents a metastasis (45).
Patients with imaging findings suggestive of unresectable renal cancer.—Percutaneous renal mass biopsy is also indicated in patients with no known malignancy but in whom imaging findings suggest an unresectable renal tumor. In these patients, a biopsy provides a tissue diagnosis that allows treatment to ensue, eliminating the need for surgery. In patients with extrarenal lesions in addition to a renal mass, biopsy of the renal mass could potentially result in less morbidity than would biopsy of an extrarenal lesion. For example, in a patient with both a lung mass and a renal mass, a pneumothorax could be prevented if the renal mass was subjected to biopsy. If the renal mass biopsy findings revealed metastatic lung cancer, a subsequent biopsy of the lung mass would not be needed. However, if the biopsy of the renal mass revealed renal cell carcinoma, biopsy of the lung mass would still be required to differentiate metastatic renal cell carcinoma from primary lung cancer. Test characteristics are excellent in this group of patients also (44,45). In a series that included 36 patients with unresectable renal cancers (45), biopsy helped identified the cell type in all but three cases. In most patients in this group, unresectable renal cell carcinoma is diagnosed.
Patients with comorbidity.—Percutaneous renal mass biopsy can also be helpful in patients with a renal mass suspected of being a resectable renal cell carcinoma but who have comorbidities that increase the risk of a surgical procedure. Examples of such comorbidities include heart and lung disease, the presence of a solitary kidney, and renal insufficiency. In our experience, urologists often prefer to avoid the risk of general anesthesia and surgery in these patients, particularly since, as discussed above, some enhancing renal masses thought on the basis of images to be renal cell carcinoma are actually benign (19,27). A preoperative tissue diagnosis of renal cell carcinoma allows the urologist to assess better the risks and benefits of surgery and, when appropriate, to plan the surgery more confidently.
Patients with a renal mass that may be caused by infection.—Focal bacterial pyelonephritis can appear masslike and mimic a renal tumor (118). Therefore, an infectious cause should be considered to prevent unnecessary surgery in a patient with an infectious mass. Renal infections are almost always managed successfully with antibiotics alone; neoplasms typically are resected or ablated. Signs and symptoms of a urinary tract infection are usually present; however, on rare occasions, a urinary tract infection may be subtle and escape detection by the referring physician (119). Therefore, renal masses should be evaluated for imaging findings of an infectious origin. These include ill-defined margins and perinephric stranding (120,121). On identification of these features, the referrer should be consulted and asked to reevaluate the patient for signs of infection. If, after a careful history and laboratory evaluation, there is still the possibility of an infectious cause, percutaneous biopsy can be used to help confirm the diagnosis of cancer or identify an infectious cause (Fig 6). This scenario is uncommon, because most renal infections can be diagnosed clinically. However, the consequences of inadvertent removal of an infected kidney are dire and can be prevented by considering an infectious cause and performing a biopsy. Xanthogranulomatous pyelonephritis is an uncommon reaction to a bacterial infection that can manifest as a mass. Aspirates typically contain histiocytes and multinucleated giant cells (95,122).
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Figure 6a: Leukemia and a small mass in a 46-year-old man. (a) Transverse T1-weighted MR image (5.9/1.9) reveals peripherally enhancing 2.1-cm mass in right renal upper pole (arrow) and perinephric stranding (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow). Hematoxylin-eosin–stained cell block section (not shown) revealed acute and chronic inflammatory cells. (c) Photomicrograph shows fungal organisms (arrows). The patient was treated for renal candidiasis. (Methanimine silver stain; original magnification, x600.)
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Figure 6b: Leukemia and a small mass in a 46-year-old man. (a) Transverse T1-weighted MR image (5.9/1.9) reveals peripherally enhancing 2.1-cm mass in right renal upper pole (arrow) and perinephric stranding (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow). Hematoxylin-eosin–stained cell block section (not shown) revealed acute and chronic inflammatory cells. (c) Photomicrograph shows fungal organisms (arrows). The patient was treated for renal candidiasis. (Methanimine silver stain; original magnification, x600.)
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Figure 6c: Leukemia and a small mass in a 46-year-old man. (a) Transverse T1-weighted MR image (5.9/1.9) reveals peripherally enhancing 2.1-cm mass in right renal upper pole (arrow) and perinephric stranding (arrowhead). (b) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow). Hematoxylin-eosin–stained cell block section (not shown) revealed acute and chronic inflammatory cells. (c) Photomicrograph shows fungal organisms (arrows). The patient was treated for renal candidiasis. (Methanimine silver stain; original magnification, x600.)
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EMERGING INDICATIONS FOR PERCUTANEOUS BIOPSY OF RENAL MASSES
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This group of indications is derived from fewer reports or less persuasive data than are the indications discussed above. As a result, we classify these indications as emerging rather than established because they are somewhat controversial. We accept them from time to time in our clinical practice, but more studies will be needed to consider them to be fully established and to understand completely the role of biopsy in these clinical settings. The problem is related mostly to the fact that, unlike the established indications, many patients in these clinical settings have a benign renal mass, and the diagnosis of a benign condition is more challenging. However, as described above, the percutaneous diagnosis of many benign masses is now possible. Because most of them can be diagnosed with imaging alone, there are no large studies that have established overall accuracy. Nevertheless, there are specific clinical settings for which a percutaneous biopsy can be helpful in making important management decisions.
Patients with a small, hyperattenuating, homogeneously enhancing renal mass.—As reviewed above, small (3-cm), hyperattenuating (relative to renal parenchyma), homogeneously enhancing renal masses may represent benign tumors. Among these are angiomyolipomas with minimal or no fat. While it is known that most angiomyolipomas contain fat and can be diagnosed with unenhanced CT alone, approximately 5% of angiomyolipomas contain little or no fat (24,25). As a result, they can be indistinguishable from a small renal cell carcinoma (24,78). In a series of 175 resected solid tumors, six (3%) were found to be angiomyolipomas with little or no fat (24); all of them were hyperattenuating and homogeneously enhancing. Only 2% of the resected renal cell carcinomas were hyperattenuating and homogeneously enhancing in that series. Therefore, we can postulate that when encountering a small, hyperattenuating, homogeneously enhancing renal mass, there is a reasonable chance that the mass is benign. Rather than presume the mass is renal cell cancer and proceed directly to treatment, it could be evaluated further.
MR imaging can help to differentiate clear cell renal cell carcinoma from angiomyolipoma with minimal fat. Angiomyolipoma with minimal fat is typically hypointense on T2-weighted MR images, likely due to the smooth muscle content of the tumor (123,124). Clear cell renal cell carcinoma is typically hyperintense on T2-weighted images (123,125,126). Therefore, if an enhancing, hyperattenuating renal mass is also hyperintense on T2-weighted images, clear cell renal cell carcinoma is likely. However, papillary renal cell carcinoma is also typically hypointense on T2-weighted images, likely because of iron-containing hemosiderin sometimes found in the cytoplasm of this tumor (123,124). Therefore, if an enhancing hyperattenuating renal mass is hypointense on T2-weighted images, both angiomyolipoma with minimal fat and papillary renal cell carcinoma are considerations. The only way to help distinguish them (short of surgical resection) is with a percutaneous biopsy (Figs 7, 8). Hyperattenuating, homogeneously enhancing renal masses may represent other benign tumors, including metanephric adenoma (127,128), oncocytoma, and leiomyoma.
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Figure 7a: Incidental hyperattenuating mass in interpolar portion of right kidney in a 67-year-old woman. (a) Transverse unenhanced CT image shows 2.3-cm mass (arrowhead) with hyperattenuating (54-HU) areas within the mass and no evidence of fat. (b) Transverse CT image shows enhancement (77 HU) of the mass (arrowhead). (c) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow), with patient in prone position. (d) Photomicrograph reveals spindle cells (arrow). (Papanicolaou stain; original magnification, x400.) (e) Photomicrograph of cell block shows fat cells (arrow). (Hematoxylin-eosin stain; original magnification, x400.) (f, g) Photomicrographs of immunocytochemical-stained specimens are positive for (f) smooth muscle actin and (g) MART1 (melanoma antigen recognized by T cells), which are both demonstrated as brown areas. Diagnosis was an angiomyolipoma with minimal fat. (Original magnification for f and g,x400.)
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Figure 7b: Incidental hyperattenuating mass in interpolar portion of right kidney in a 67-year-old woman. (a) Transverse unenhanced CT image shows 2.3-cm mass (arrowhead) with hyperattenuating (54-HU) areas within the mass and no evidence of fat. (b) Transverse CT image shows enhancement (77 HU) of the mass (arrowhead). (c) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow), with patient in prone position. (d) Photomicrograph reveals spindle cells (arrow). (Papanicolaou stain; original magnification, x400.) (e) Photomicrograph of cell block shows fat cells (arrow). (Hematoxylin-eosin stain; original magnification, x400.) (f, g) Photomicrographs of immunocytochemical-stained specimens are positive for (f) smooth muscle actin and (g) MART1 (melanoma antigen recognized by T cells), which are both demonstrated as brown areas. Diagnosis was an angiomyolipoma with minimal fat. (Original magnification for f and g,x400.)
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Figure 7c: Incidental hyperattenuating mass in interpolar portion of right kidney in a 67-year-old woman. (a) Transverse unenhanced CT image shows 2.3-cm mass (arrowhead) with hyperattenuating (54-HU) areas within the mass and no evidence of fat. (b) Transverse CT image shows enhancement (77 HU) of the mass (arrowhead). (c) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow), with patient in prone position. (d) Photomicrograph reveals spindle cells (arrow). (Papanicolaou stain; original magnification, x400.) (e) Photomicrograph of cell block shows fat cells (arrow). (Hematoxylin-eosin stain; original magnification, x400.) (f, g) Photomicrographs of immunocytochemical-stained specimens are positive for (f) smooth muscle actin and (g) MART1 (melanoma antigen recognized by T cells), which are both demonstrated as brown areas. Diagnosis was an angiomyolipoma with minimal fat. (Original magnification for f and g,x400.)
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Figure 7d: Incidental hyperattenuating mass in interpolar portion of right kidney in a 67-year-old woman. (a) Transverse unenhanced CT image shows 2.3-cm mass (arrowhead) with hyperattenuating (54-HU) areas within the mass and no evidence of fat. (b) Transverse CT image shows enhancement (77 HU) of the mass (arrowhead). (c) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow), with patient in prone position. (d) Photomicrograph reveals spindle cells (arrow). (Papanicolaou stain; original magnification, x400.) (e) Photomicrograph of cell block shows fat cells (arrow). (Hematoxylin-eosin stain; original magnification, x400.) (f, g) Photomicrographs of immunocytochemical-stained specimens are positive for (f) smooth muscle actin and (g) MART1 (melanoma antigen recognized by T cells), which are both demonstrated as brown areas. Diagnosis was an angiomyolipoma with minimal fat. (Original magnification for f and g,x400.)
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Figure 7e: Incidental hyperattenuating mass in interpolar portion of right kidney in a 67-year-old woman. (a) Transverse unenhanced CT image shows 2.3-cm mass (arrowhead) with hyperattenuating (54-HU) areas within the mass and no evidence of fat. (b) Transverse CT image shows enhancement (77 HU) of the mass (arrowhead). (c) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow), with patient in prone position. (d) Photomicrograph reveals spindle cells (arrow). (Papanicolaou stain; original magnification, x400.) (e) Photomicrograph of cell block shows fat cells (arrow). (Hematoxylin-eosin stain; original magnification, x400.) (f, g) Photomicrographs of immunocytochemical-stained specimens are positive for (f) smooth muscle actin and (g) MART1 (melanoma antigen recognized by T cells), which are both demonstrated as brown areas. Diagnosis was an angiomyolipoma with minimal fat. (Original magnification for f and g,x400.)
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Figure 7f: Incidental hyperattenuating mass in interpolar portion of right kidney in a 67-year-old woman. (a) Transverse unenhanced CT image shows 2.3-cm mass (arrowhead) with hyperattenuating (54-HU) areas within the mass and no evidence of fat. (b) Transverse CT image shows enhancement (77 HU) of the mass (arrowhead). (c) CT-guided percutaneous biopsy, shown on transverse CT image, was performed with a 25-gauge needle (arrow), with patient in prone position. (d) Photomicrograph reveals spindle cells (arrow). (Papanicolaou stain; original magnification, x400.) (e) Photomicrograph of cell block shows fat cells (arrow). (Hematoxylin-eosin stain; original magnification, x400.) (f, g) Photomicrographs of immunocytochemical-stained specimens are positive for (f) smooth muscle actin and (g) MART1 (melanoma antigen recognized by T cells), which are both demonstrated as brown areas. Diagnosis was an angiomyolipoma with minimal fat. (Original magnification for f and g,x400.)
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ABSTRACT
INTRODUCTION
