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Original Research |
1 Department of Radiology, UH B1D407, University of Michigan Hospitals, Ann
Arbor, MI.
2 Present address: Department of Radiology, Stanford Hospital and Clinics, 300
Pasteur Dr., H1307, Stanford, CA 94305-5105.
3 Department of Diagnostic Radiology, William Beaumont Hospital, Royal Oak,
MI.
4 Department of Surgery-Urology, University of Michigan Hospitals, Ann Arbor,
MI.
Received February 9, 2006;
accepted after revision May 16, 2006.
Address correspondence to K. E. Maturen
(katematuren{at}yahoo.com).
Abstract
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MATERIALS AND METHODS. With institutional review board approval, we retrospectively reviewed imaging-guided renal biopsies performed by radiologists at our institution between February 1999 and July 2005. Patient records, pathology reports, and imaging studies were reviewed. Concordance of biopsy diagnosis and follow-up data was assessed. Significant impact on clinical management was determined in collaboration with two experienced urologists and was defined as a change from no therapy to therapy, including surgery, tumor ablation, chemotherapy, or radiation.
RESULTS. Two hundred seventy-six renal biopsies were performed during the study period. Of these, 123 were random biopsies and fine-needle technique was used for one; these 124 were excluded. One hundred fifty-two renal mass biopsies were performed using coaxial 18-gauge core needle technique in 125 patients (55 women, 70 men; average age, 60 years; range, 28-90 years). There were two (1.3%) postprocedural hematomas (one [0.7%] requiring blood transfusion) and one (0.7%) delayed renal pseudoaneurysm attributed to biopsy. No tumor seeding was identified. In 85 biopsies (56%), malignant neoplasm was found, 61 biopsies (40%) yielded benign findings, and six (4%) were nondiagnostic. The sensitivity for malignancy was 97.7%; specificity, 100%; positive predictive value, 100%; and negative predictive value, 100%. At least 92 (60.5%) biopsy results significantly impacted clinical management.
CONCLUSION. Imaging-guided percutaneous core needle biopsy of renal masses is safe and highly accurate. Tissue diagnosis alters clinical decision making in a majority of the cases and may allow a number of unnecessary nephrectomies to be avoided.
Keywords: core biopsy • kidney • renal disease • renal mass
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Methods of renal mass assessment have become an important question in the care of an increasing number of patients: Renal cell carcinoma (RCC) is among the 15 most common malignancies in both men and women and has steadily increased in incidence since 1975 [10]. Increasingly, these cancers are recognized incidentally as small (< 3 cm) masses [11]. Although advances in sonography, CT, and MRI technology allow accurate differentiation between solid and cystic lesions, the ability of imaging to differentiate benign from malignant renal masses remains limited [12-16]. Tissue diagnosis may be needed to direct therapy and potentially to avoid unnecessary nephrectomies. Meanwhile, both the reliability of percutaneous biopsy and the appropriate clinical context for the procedure remain matters of debate. Many published reports evaluate relatively small patient populations, while studies of larger populations assembled over 15- to 30-year periods at multiple institutions are limited by heterogeneity in biopsy technique and clinical follow-up [17, 18].
We report our experience in performing renal mass biopsy with specific attention to two questions: assessment of the accuracy of imaging-guided percutaneous core needle technique and whether the information provided by biopsy alters management.
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50,000/mm3 or were corrected. Coagulation status was also corrected
when appropriate, with an international normalized ratio (INR) of 
1.5 at
the time of biopsy in all patients. Biopsies were performed with the patient
under conscious sedation (IV fentanyl [25-100 µg], midazolam [0.5-2.0 mg],
or both) except when performed as part of a combined procedure with
radiofrequency ablation, for which general anesthesia was administered. Local
anesthesia was administered with 1% lidocaine buffered with bicarbonate. CT or
sonographic guidance was used to direct the biopsy depending on operator
preference, lesion imaging characteristics, or both. Four patients received
75-100 mL of iodinated contrast material IV to improve lesion conspicuity on
CT. Patient position depended on the location of the mass, with biopsies
performed with the patient prone (Fig.
1) or in a lateral decubitus position. Coaxial technique was uniformly implemented using a 17-gauge introducer and an 18-gauge spring-loaded biopsy gun (ASAP and Easy Core needles and Pinpoint introducer, Boston Scientific). The introducer remained in position while multiple passes were made with the cutting needle. Up to four cores were obtained from each tumor, with three or four cores obtained in most patients. Postbiopsy images were not routinely obtained. Samples were placed in normal saline, formalin, or both and were hand-carried to the pathology laboratory; neither a pathologist nor a cytology technician was present in the biopsy suite.
Due to operator preference or because the patient was bleeding around the introducer, procoagulant agents were injected along the needle track in some patients: absorbable bovine collagen (Helitene, Integra Life Sciences) in 40 patients and absorbable pork gelatin powder (Gelfoam, Pharmacia & Upjohn) in one patient. All patients were hemodynamically monitored in the radiology recovery area for 4 hours after the procedure, and any complications were recorded. We did not routinely perform imaging to evaluate for postprocedural hematomas, but all cases of hemorrhage identified either by postprocedural imaging or by clinical signs or symptoms were included among the reported complications. Subsequent clinical notes and imaging reports were reviewed to assess for any delayed complications such as tumor seeding.
Terms
"Definitely benign" masses were those that had surgical or
autopsy histologic confirmation of benignity, resolved, decreased in size on
cross-sectional imaging without treatment, or were stable on cross-sectional
imaging for 2 years. "Probably benign" masses were those that
were stable on cross-sectional imaging for between 6 months and 2 years. Core
needle biopsy diagnoses of oncocytoma in patients with multiple renal masses
including at least one surgically proven oncocytoma were also considered
"probably benign." "Indeterminate" masses had no or
insufficient follow-up to confirm benignity. "Significant impact on
clinical management" was determined in collaboration with two urologists
experienced in oncology and was defined as a change between no therapy and
therapy, meaning either the addition or removal of any of the following to or
from the therapeutic plan: surgery, percutaneous ablation, catheter-based
ablation, external beam radiation, or systemic chemotherapy. "Imaging
follow-up" consisted of dedicated contrast-enhanced CT or MRI of the
abdomen.
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Two patients (1.3%) had postprocedural hematomas: One was managed conservatively and the other required transfusion of 4 U of packed RBCs. One of these patients had received Helitene in the needle track, and the other had not received a procoagulant injection. The final diagnoses were RCC and interstitial fibrosis, respectively. Regarding other immediate complications, one patient had transient difficulty in urination that resolved after bladder catheterization and saline flushes. One patient had postprocedural lightheadedness that resolved without intervention.
Regarding long-term complications, one patient (0.7%) with biopsy diagnosis of oncocytoma presented with retroperitoneal bleeding 3 months after biopsy. Angiography revealed a pseudoaneurysm, and endovascular tumor embolization was performed. (We have previously reported the same patient in a smaller review of our experience with sono-graphic guidance [19].) No evidence of tumor seeding or of another delayed complication was identified after detailed record review. The average imaging follow-up was 9.7 months (range, 0-60 months).
Sensitivity for Detection of Malignancy
Of 152 biopsies, 85 (56%) showed malignant neoplasm, 61 (40%) yielded
benign findings, and six (4%) were nondiagnostic. The benign biopsies included
22 (14.5%) benign neoplasms and 39 (25.7%) nonneoplastic results. The biopsy
results are detailed in Table
2. Fuhrman's nuclear grade in RCC is not routinely reported by our
pathology department.
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Eighty-seven masses were confirmed malignant by surgical excision or natural history. Of these, 85 had biopsies positive for malignancy and two had nondiagnostic biopsies. Thus, to our knowledge, the sensitivity for detection of malignancy was 97.7%, given the two nondiagnostic biopsies of malignant masses. Because no malignant biopsy results have been identified as false-positives, both specificity and positive predictive value are 100%. Of the 61 (40%) benign biopsy results, 19 (12.5% of 152 total) were definitely benign, 28 (18.4%) were probably benign, and 14 (9%) were indeterminate on review of follow-up data. None of the benign biopsies has subsequently been proven malignant. The negative predictive value of benign biopsy results to exclude malignancy is considered to be 100% (regarding nondiagnostic biopsies as a separate group).
The six (4%) nondiagnostic biopsies were performed on renal masses ranging from 2 to 12 cm in size, with an average size of 6.4 cm. Four were performed under sonographic guidance and two under CT guidance. No specific difficulties were noted by the operators at the time of biopsies. Two were solid (Fig. 4A, 4B), two were cystic, and two were mixed. Two were subsequently shown to be malignant; one, definitely benign; one, probably benign; and two, indeterminate.
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One hundred twelve patients (74%) had no known extrarenal malignancy at the time of biopsy. Among these, 18 were undergoing repeat biopsy after radiofrequency ablation, of whom one had residual RCC, one had residual oncocytoma, and one had a nondiagnostic biopsy. It should be noted that the patient with residual RCC had a biopsy report indicating a "few residual nests of tumor cells" only. Histologic diagnosis was made without the use of nicotinamide adenine dinucleotide (NADH) stain, which later became customary for our evaluation of patients after radiofrequency ablation [20]. Biopsy was considered to have affected management of the 17 radiofrequency ablation patients who had diagnostic biopsies because additional ablation sessions or potential surgery hinged on the biopsy result.
In the remaining 94 patients with no history of malignancy or radiofrequency ablation, RCC was the anticipated diagnosis. Five of these patients had nondiagnostic biopsies, which did not impact management. Twenty-eight had benign biopsies, including angiomyolipomas (n =4) (Fig. 10) and oncocytomas (n = 11) among other nonneoplastic lesions such as sarcoidosis (Fig. 11). These 28 patients clearly had a change in management due to biopsy results because the diagnostic alternative was nephrectomy. The remaining 61 biopsy results confirmed malignancy. These included RCCs (n = 48) and carcinoma not otherwise specified (NOS) (n =6) that were not considered to affect management because they were among the expected outcomes. One patient with a mass that was included in the RCC group had a biopsy result showing "oncocytic neoplasm with suspicious features highly concerning for chromophobe RCC"; RCC was confirmed at nephrectomy. However, seven occult malignancies including lymphoma (n =4), sarcoma (n = 2), and melanoma (n =1) (Fig. 12) were also discovered in this group. Biopsy results clearly affected management for these seven patients, for whom inappropriate treatments were avoided by preoperative histologic diagnosis.
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Thus, of 152 masses biopsied, 92 (60.5%) biopsy results significantly impacted clinical management, when significant impact is defined as a change between no therapy and therapy, including surgery, percutaneous ablation, transcatheter ablation, external beam radiation, or systemic chemotherapy.
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At least two groups have examined core biopsies performed ex situ on surgical specimens of kidneys containing masses. Dechet et al. [3] biopsied 100 masses at total or partial nephrectomy using 18-gauge core biopsy technique, with a 31% nondiagnostic rate from biopsy. Among the diagnostic specimens, the sensitivity for the detection of malignancy was just over 80%. This finding is significantly worse than that of the current study and most reports of core needle technique in situ [6-9]. It is difficult to understand the low diagnostic yield given direct visualization and palpation of the tumors. It is possible that imaging provides more accurate assessment of lesion characteristics, allowing the operator to target nodular areas and avoid necrotic areas, or that inexperience with percutaneous technique resulted in poor tissue yield. Whatever the cause, this discrepancy underscores the difficulty in extrapolating ex situ biopsy results to percutaneous in situ technique, although the findings are rather the reverse of what might have been expected. By contrast, Wunderlich et al. [25] biopsied 50 masses using apparently identical ex situ technique and found 98% sensitivity for the detection or exclusion of malignancy.
We performed six (4%) nondiagnostic biopsies. Again, this is in keeping
with reports of core technique and is better than reports of FNA. Although we
did not identify specific imaging features predisposing to nondiagnostic
biopsy, some authors have noted diminished sensitivity for the detection of
malignancy and loss of accuracy in tumor grading in small lesions ( 3-4
cm) [6,
9,
22] and in predominantly
cystic lesions [17]. We did
not find significant differences in biopsy accuracy arising from mode of
imaging guidance (CT or sonography). A few reports have emphasized the utility
of sonographic guidance [5,
19] and potential technical
difficulties of CT guidance
[6], but no direct comparison
of these methods has been undertaken, to our knowledge. Most authors appear to
select imaging guidance on the basis of the operator's preference and the
imaging features of individual masses.
Two (1.3%) or our patients experienced immediate postprocedural hemorrhages that did not affect long-term outcomes. This finding is comparable to those of prior studies reporting occasional subcapsular hematomas [2, 5, 6, 21] that rarely required transfusion and had no long-term effect on patient outcome, but many authors do not report complications. Our standard procedure is 4 hours of observation after biopsy without further imaging unless signs or symptoms suggest hemorrhage. Routine post-procedure or delayed imaging might reveal higher rates of hemorrhage, but without compromise of hemodynamic stability the clinical significance is questionable.
Regarding long-term complications, one (0.7%) of the patients in our study experienced delayed retroperitoneal hemorrhage due to arterial pseudoaneurysm formation and rupture. Pseudoaneurysm formation is a recognized complication of biopsy [26, 27], although the incidence is unknown because most are probably asymptomatic. We identified no other long-term complications—specifically, no tumor seeding. None of the cited studies describe evidence of seeding, whereas some authors with extensive longitudinal follow-up [7, 8, 18, 28] specifically note the absence of seeding. Some speculate that their routine use of coaxial biopsy technique may aid in preventing RCC seeding [7, 18], which we have also noted in hepatocellular carcinoma [29]. However, seeding in slow-growing tumors such as RCC may be temporally remote from the biopsy and attention to the body wall on follow-up imaging is certainly appropriate.
In the end, biopsy techniques and accuracy rates are only as significant as their impact on clinical management. We found that of 152 biopsies, just over 60% significantly impacted clinical management. Several groups have attempted to quantify the impact on patient management with roughly similar results [6, 17, 21]. Ours is likely a conservative estimate because the 59 patients with RCC may have had subtler changes in management depending on biopsy histology such as partial versus total nephrectomy or laparoscopic versus open surgical approach. We suggest that 60% alteration in management represents an important and substantive change in the care of many patients, particularly those who avoid nephrectomy by means of biopsy diagnosis. In particular, biopsy data were essential to the appropriate care of 35 patients without extrarenal malignancy who were thought to have RCC but found to have benign masses (n =28) or malignancies other than RCC (n =7). Unfortunately, our data do not allow us to specifically predict which patients will be among the 60% with altered management. We summarize the clinical indications that were of particular importance in our study and in the recent literature [4, 6, 22, 24, 30] in Appendix 1, noting however that no decrease in sensitivity of biopsy was noted in other patient groups.
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The nonstandardized clinical follow-up and absence of surgical confirmation of benignity in some of the benign biopsies are the major limitations of the study. We did not include these as false-negative biopsies because we considered it unlikely that all were in fact undiagnosed malignancies. Some uncertainty may be inherent because the biopsy diagnosis was often used to avoid the nephrectomies that might have confirmed benignity. For example, 16 biopsies had a benign result of oncocytoma. Among these, only one biopsy result was confirmed at resection, four patients had prior surgically confirmed oncocytomas, eight masses were definitely benign, and three masses were probably benign or indeterminate by imaging follow-up. This is a benign tumor that can be diagnosed percutaneously [20, 31]; thus, 15 additional nephrectomies would have been needless. To perfectly quantify sensitivity in our study, it would be necessary to resect all 152 masses, which would be unethical in cases in which the urologist's judgment and a tissue diagnosis of benignity coincide.
Other limitations include the absence of tumor grading information in RCC and specific histologic confirmation in some of the biopsies revealing inflammation or infection, which were treated without surgical excision. Finally, we are unable to comment on specific imaging features of benign and malignant lesions in our population because of the heterogeneity of the prebiopsy imaging evaluation in this retrospective study. A prospective approach with dedicated imaging protocols might enable biopsy recommendations based on specific imaging features.
In summary, we found that imaging-guided percutaneous renal mass biopsy performed with an 18-gauge coaxial core needle technique is highly sensitive for the detection of malignancy, with relatively few nondiagnostic biopsies and very few procedure-related complications. Biopsy results significantly affected clinical management—meaning a change between therapy and no therapy—in a majority of the patients. We conclude that percutaneous core biopsy is a safe and accurate means of characterizing renal masses that may allow a number of unnecessary nephrectomies to be avoided.
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3 cm) renal masses: correlation of spiral CT features and
pathologic findings. AJR 1994;163
: 597-605
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