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1 Division of Abdominal Imaging and Intervention, Massachusetts General
Hospital, 55 Fruit St., Boston, MA 02114.
2 Department of Urology, Massachusetts General Hospital, Boston, MA 02114.
3 Department of Medical Imaging, University Health Network-Mount Sinai Hospital,
University of Toronto, 610 University Ave., Toronto, Ontario M5G 2M9,
Canada.
Received October 3, 2001;
accepted after revision August 20, 2002.
Address correspondence to M. G. Harisinghani.
Abstract
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MATERIALS AND METHODS. Three hundred ninety-seven renal biopsies were performed at our institution between 1991 and 2000. Between January 1997 and August 2000, 28 Bosniak category III lesions, based on established CT imaging criteria on helical CT scans, were identified for analysis. The incidence of malignancy, based on surgical pathology or imaging follow-up and percentage of lesions proceeding to surgery, among these 28 lesions, was determined. The surgical results were correlated with the biopsy findings.
RESULTS. Of the 28 biopsied category III lesions, 17 (60.7%) were malignant (16 renal cell carcinomas and one lymphoma), and 11 (39.3%) were benign (six hemorrhagic cysts, three inflammatory cysts, one metanephric adenoma, and one cystic oncocytoma). Seventeen of the 28 lesions (16 renal cell carcinomas and one inflammatory cyst) had surgical resection after the biopsy. All resected lesions had pathologic diagnoses identical to the percutaneous imaging-guided biopsy results. The remaining 11 patients who had undergone nonsurgical biopsies had radiologic follow-up for a minimum of 1 year, with benign lesions showing no interval change.
CONCLUSION. Renal biopsy and radiologic follow-up were useful in identifying nonmalignant lesions in complex cystic renal masses and avoided unnecessary surgery in 39% of patients.
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In 1986, Bosniak [4] classified renal cysts in four categories on the basis of imaging appearances in an attempt to predict the risk of malignancy. Subsequent studies have shown that the Bosniak system is helpful in assessing the risk of malignancy in cystic renal lesions [1, 5, 6]. The Bosniak system not only classifies lesions into categories on the basis of CT imaging appearances but also advocates treatment for each category. Categories I and II were considered leave-alone lesions, with follow-up imaging recommended for category II lesions [7]. Surgical resection was recommended for category III and IV lesions. The recommendation for surgical resection appears appropriate for category IV lesions, in which the incidence of malignancy is reported to be between 67% and 100% in most series [5,6,7,8]. However, the recommendation is not as clear-cut for category III lesions, in which the risk of malignancy varies from 31% to 100% [5]. In this category, applying the Bosniak criteria not only ensures a low incidence of missed cancers but also results in unnecessary surgery in up to 59% of patients.
We have noted an increase in the number of renal biopsies being performed at our institution, which is, in part, explained by the initiation of a radiofrequency ablation therapy program with the requirement for renal biopsy before radiofrequency ablation in all cases. This increase prompted us to review our institution's experience with renal biopsy in patients with Bosniak category III lesions. We sought to document the overall incidence of malignancy in Bosniak category III lesions diagnosed at imaging-guided biopsy and also to evaluate the diagnostic accuracy of renal biopsies in these patients. We evaluated the sensitivity of renal biopsies in these patients by correlating biopsy results with pathologic diagnoses in patients who underwent surgery and also by reviewing imaging follow-up in patients who did not undergo surgical resection.
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All cystic neoplasms that subsequently underwent percutaneous biopsy were reviewed and categorized by two specialty-trained radiologists by consensus, using the Bosniak classification [4]. The Bosniak criteria are described in Appendix 1. Those patients with Bosniak category III lesions formed the cohort evaluated in this study.
Using the institutional medical record system, we evaluated this group of patients retrospectively for patient demographics, indication for biopsy, and histologic and cytologic results of imaging-guided biopsy. The indication for renal biopsy was a Bosniak category III lesion in the presence of comorbidity, which would render the patients at high risk for surgery, or a single kidney in those patients in whom surgery could precipitate renal failure.
Patient outcomes were assessed by reviewing medical and operative records and surgical pathology records in those patients who underwent resection and in those patients who did not undergo surgery and clinical and imaging follow-up. We determined the incidence of malignancy. The histologic results after imaging-guided biopsy were correlated with surgical pathology in those patients who underwent surgery and by clinical and imaging follow-up in those patients who had benign pathologic findings after imaging-guided biopsy. We calculated the sensitivity, specificity, and diagnostic accuracy of imaging-guided biopsy and the false-positive and false-negative rates for this cohort of patients.
Patients
Of the 397 renal biopsies performed at our institution by interventional
radiologists for renal mass lesions between 1991 and 2000, 28 biopsies (7%) of
Bosniak category III lesions were performed between June 1997 and August 2000.
There were 18 men and 10 women whose ages ranged from 40 to 70 years.
Technique
The renal biopsies were performed with CT guidance using a 17-gauge Temno
coaxial system (Allegiance Healthcare, McGaw Park, IL). The 17-gauge
fine-needle aspirations were performed using a small 22-gauge Chiba needle
(Cook, Bloomington, IN), and core biopsies were taken using an 18-gauge
cutting needle (Allegiance Healthcare). The biopsies were carefully planned so
that the needle tip was directed to areas of the cyst wall, septation
thickening, or calcification. The number of needle passes ranged from four to
eight for fine-needle aspirations and from four to six for the core biopsies.
After satisfactory biopsies were performed, the cyst contents were aspirated.
An experienced cytologist was present in the CT suite for all biopsies.
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The Bosniak classification [4] was first described in 1986 as a means of differentiating benign renal cysts from cystic renal cell carcinomas on the basis of evaluation on sonography and CT. Studies have documented the value of the Bosniak classification system in differentiating benign renal cysts from cystic renal cell carcinomas [1, 5].
However, there are some difficulties with this system [1, 5, 7, 8]. Most categories I and IV cysts are easily categorized on CT performed with the correct protocol. The main difficulty encountered with the Bosniak system is in making the distinction between category II and category III lesions [5, 7, 8]. Siegel et al. [1] documented interobserver variability in the distinction of Bosniak categories II and III lesions, and this difficulty is undoubtedly one of the drawbacks of the system. Making the distinction between categories II and III lesions is important because category II lesions are considered benign and are managed conservatively. On the other hand, category III lesions are assumed to have significant risk of malignancy; therefore, most authors recommend surgical resection. Because the distinction between categories II and III lesions can be difficult, there is a tendency to upgrade category II lesions to category III when any uncertainty exists. Indeed, Bosniak [8] himself has advocated placing borderline II—III lesions, especially hyperdense cysts, into category III.
In general, the number of patients in studies evaluating the value of the Bosniak classification in predicting malignancy in a complex cystic lesion is small, particularly for categories II and III lesions [1, 3, 5]. In one series, the reported incidence of malignancy was 0% for category II, 60% for category III, and 100% for category IV lesions [5]. Our results correlate closely with previously published articles with the incidence of malignancy being 60.7% for patients with category III lesions [5]. The malignant Bosniak category III lesions included 16 renal cell carcinomas with one case of lymphoma in our series.
The recommended treatment for Bosniak category III lesions is surgical resection. However the disadvantage of this approach is that up to 40-60% of patients with Bosniak category III lesions undergo surgery for benign lesions. Surgery in these patients ranges from exploration and biopsy to enucleation, partial nephrectomy, and nephrectomy [7]. In general, these lesions occur in patients over 50 years old, and surgery in this patient population can result in significant morbidity. Presurgical cyst aspiration has been found to be of limited value in this patient group [7].
The advent of radiofrequency ablation in the treatment of renal cell carcinoma has increased the demand for preoperative renal biopsies. A definitive cancer diagnosis is necessary before the patient undergoes this procedure because radiofrequency ablation treatment destroys tissue without yielding a diagnostic specimen, which is routinely available after surgical resection. The relatively large number of cystic lesions biopsied was not apparently caused by candidacy of these patients for radiofrequency ablation. Otherwise, not all the renal cell carcinomas would have been resected. There were other reasons, including suspicion for lymphoma (as confirmed in one case) and coexistence of extrarenal malignancy raising the suspicion that the renal lesion might be a metastasis. Ultimately, most of these biopsies were requested because findings for the category III lesions were equivocal, and the referring urologist was prepared to accept and be guided by the result of the biopsy.
Our results document the accuracy of CT-guided renal biopsy in patients with Bosniak category III lesions. The incidence of malignancy of 60.7% of lesions in our series correlates closely with other series [1, 3, 5] and emphasizes that positive histologic diagnosis can be obtained by percutaneous imaging-guided biopsy. All renal biopsies of lesions in this category were performed during the period from 1997 to 2000, thus all imaging was performed using the helical technique.
Departing from the traditional recommendation of surgery for patients with Bosniak category III lesions, we obtained initial histologic diagnoses in all 28 patients in this series by imaging-guided renal biopsies. All patients with malignant pathologic results based on percutaneous CT-guided biopsies, with the exception of the patient with renal lymphoma, underwent surgery. The solitary patient with an inflammatory cyst underwent surgery because of continuing hematuria and the multiloculated thickened walls of the cyst mimicking a cystic neoplasm. In the cohort of patients (60%) who proceeded to surgery, no discrepancy was found between histologic diagnoses gained from the surgical specimens compared with specimens obtained by imaging-guided biopsies. Therefore, there were no false-positive findings, and concordance existed between histologic diagnoses from imaging-guided and surgically resected specimens. The diagnosis among those patients with malignant pathology was renal cell carcinoma in 16 (94%) of 17 patients and inflammatory cyst in the remaining patient. Among those patients with benign pathology, there were six hemorrhagic cysts, three inflammatory cysts, one metanephric adenoma, and one cystic oncocytoma.
This range of benign pathology encountered in Bosniak category III lesions correlates with the experience of other authors [10]. In all except one case in which benign pathology was diagnosed after imaging-guided biopsy, patients were followed up by imaging. Patients were followed up by clinical examination and serial imaging studies for periods greater than 1 year in all cases. No change in lesion size or imaging appearances occurred in this group of patients; thus, no patient underwent rebiopsy. Therefore, the negative predictive value of imaging-guided biopsy for the Bosniak category III lesions appears to be 100%. The imaging follow-up ensured that slow-growing cystic renal cell carcinomas were unlikely to be missed. Eleven patients avoided surgery on the basis of the results of their percutaneous biopsies. These results are encouraging but undoubtedly will require validation in a larger cohort of patients.
With regard to imaging follow-up, we found that most lesions did not change significantly in size or morphology after the biopsy. In those cases that did show changes in size or imaging appearance, the postprocedure scan was used as a baseline to which follow-up scans were compared. If postprocedure hematoma occurred, the patient was usually rescanned after an interval of 2 weeks to assess for resolution or reduction in size of the hematoma, and this study was used as a baseline with which follow-up scans were compared.
We suggest that malignant cells can be reliably obtained from Bosniak category III lesions. As a result, Bosniak category III lesions can be safely stratified into benign and malignant groups by imaging-guided biopsy, and surgery can be avoided in those patients in whom biopsies failed to detect malignancies, particularly in elderly patients with increased frequency of comorbidity, which makes surgery a higher risk than for those in the general population.
The limitations of this study should be emphasized. The retrospective nature of the study predisposes to selection bias. The number of patients in the study was small, and although imaging follow-up was a minimum of 1 year, pathologic proof of each lesion would be more reassuring in excluding the possibility of slow-growing lesions. Also, failure to follow up all nonsurgical patients for a minimum of 2 years is a limitation because cystic renal carcinomas can be slow-growing.
In conclusion, this study confirms an incidence of malignancy in 60% of patients with Bosniak category III lesions with histologic diagnosis made in all cases at imaging-guided biopsy. Our study also documents the diagnostic accuracy of CT-guided biopsy in patients with Bosniak category III lesions. Our results suggest that Bosniak category III lesions do not need surgical exploration initially and that these lesions can be stratified into malignant and benign groups at imaging-guided biopsy, thus preventing unnecessary surgery in up to 40% of patients.
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