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1 Russell H. Morgan Department of Radiology, Johns Hopkins Hospital, Baltimore,
MD, and Department of Radiology, Johns Hopkins University, 601 N Caroline St.,
Rm. 4214, Baltimore, MD 21287-0801.
2 Department of Radiology, Stanford University Medical Center, 300 Pasteur Dr.,
H1307, Stanford, CA 94304-5105.
3 James Buchanan Brady Urological Institute, Johns Hopkins Hospital, Baltimore,
MD.
Received July 8, 2003;
accepted after revision September 9, 2003.
Address correspondence to S. S. Siegelman.
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed 213 consecutive
renal cell carcinomas resected at our institution from 1995 through 1999.
Three groups of lesions stratified by size (
3 cm, > 3–5 cm, >
5 cm) were compared with regard to pathologic findings. Statistical
significance was assessed using Fisher's exact test.
RESULTS. Of 50 lesions 3 cm or smaller, 19 (38%) had extension outside the renal capsule (T3 or T4) and 14 (28%) were a high nuclear grade (Fuhrman grade 3 or 4). Lesions 3 cm or smaller and those greater than 3 cm to 5 cm did not differ statistically with regard to T stage or nuclear grade. Lesions larger than 5 cm showed a statistically higher T stage (p < 0.001) and nuclear grade (p = 0.001) than the other smaller lesions. More non–clear cell tumors were found in the two groups of smaller lesions (p = 0.105) but without statistical significance. The majority (58%) of the tumors were asymptomatic and had been detected incidentally on cross-sectional imaging. Lesions larger than 5 cm were significantly more likely to be symptomatic (p < 0.001). Seventy-nine percent of the tumors 3 cm or smaller were incidental, and these lesions did not differ significantly from the symptomatic lesions with regard to stage, grade, or histology.
CONCLUSION. In our study population, renal cell carcinomas up to 3 cm, including asymptomatic lesions, showed a significant incidence of high nuclear grade and tumor extension beyond the renal capsule; these findings support aggressive management of small lesions. Symptomatic status was not an adequate discriminator to guide management. A longitudinal study is necessary to further evaluate the efficacy of current patterns of therapy.
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The study of small renal cell carcinomas potentially involves several areas of current controversy, including the appropriate management of incidental small lesions and the usefulness of screening CT. A key consideration in the management of solid renal masses detected by serendipity is the nature of these lesions: Can we anticipate that a significant percentage of the small renal cell carcinomas we detect are aggressive tumors that will grow, invade adjacent structures, and produce metastases? To contribute to the study of this issue, we examined a series of renal carcinomas resected during a recent 5-year period to determine the relationship between tumor diameter and tumor subtype, nuclear grade, and T stage of each lesion.
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In several cases for which clinicians used an older tumor staging scheme, stage was reassigned using the 1997 TNM criteria. All cases of reassignment involved tumors between 3 and 7 cm without capsule transgression; these tumors were down-graded from stage II to stage I. In cases with intermediate nuclear grade (i.e., lesions having characteristics of two nuclear grades), lesions were assigned the higher of the two grades. Direct review of pathology samples was performed in cases in which histologic subtype, tumor stage, or nuclear grade was ambiguous in the original report.
For data analysis, lesions were stratified by size into three groups: 3 cm or smaller, group A; greater than 3 cm to 5 cm, group B; and greater than 5 cm, group C. Fisher's exact test was used to test the independence of the data acquired for the three groups with regard to tumor stage, nuclear grade, histologic subtype, and mode of presentation. Symptomatic and asymptomatic lesions were likewise compared.
Patients with known or suspected renal masses were examined using a Somatom 4 helical CT scanner (Siemens, Malvern, NJ). The examination began with unenhanced consecutive 3-mm scans to encompass the kidneys. Next, 115 mL of iohexol (Omnipaque 350, Nycomed, Princeton, NJ) was injected at a rate of 3.5 mL/sec. Patients weighing less than 115 lb (< 52 kg) were injected with 1 mL/lb (2.2 mL/kg) of iohexol. Three-millimeter-thick contiguous scans were obtained starting 25 sec after the beginning of the injection. The examination concluded with a series of 3-mm scans after a 4-min delay (Figs. 1A, 1B, 1C, 2A, 2B, 2C, 3A, 3B, 3C).
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All lesions that enhanced more than 15 H were diagnosed as renal neoplasms. Compliance with advice for excision was high, with fewer than 1% of patients refusing surgery.
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During the 5 years encompassed by this review, 213 renal cell carcinomas were resected in 211 patients. Of these lesions, 162 were conventional clear cell carcinoma; 33, papillary; 10, chromophobe; zero, tubular; two, mixed; and two, unknown. The remaining four were categorized as "other," which included lesions with sarcomatoid change and with oncocytic components. With regard to nuclear grade, 12 were F1; 105, F2; 79, F3; 16, F4; and one, unknown. TNM staging revealed 81 T1, 18 T2, 105 T3, and nine T4 lesions.
Group A consisted of 50 lesions that were 3 cm or smaller. Of these lesions, 31% were not pure clear cell. Seventy-two percent were a low nuclear grade (grade 1 or 2), and 62% were confined to the kidney. The mode of presentation was documented in 43 of the lesions in this group, with 34 presenting incidentally and nine symptomatically. Of the incidental lesions in this group, 74% were a low nuclear grade, and 53% were confined to the kidney.
Group B consisted of 59 lesions that were larger than 3 cm but less than or equal to 5 cm. In this group, 26% were not pure clear cell. Sixty-seven percent were nuclear grade 1 or 2, and 63% were confined to the kidney. The mode of presentation was documented in 55 of the lesions in this size stratification, with 39 presenting incidentally and 16 presenting symptomatically.
Group C was composed of 104 lesions that were larger than 5 cm. Of these lesions, 18% were not pure clear cell. Forty percent were nuclear grade 1 or 2, and 30% were confined to the kidney. The mode of presentation was documented in 86 of the lesions in this size stratification, with 34 presenting incidentally and 52 that were symptomatic.
Analysis using Fisher's exact test showed no statistically significant difference between groups A and B with regard to histologic subtype (p = 0.93), nuclear grade (p = 0.881), or tumor stage (p = 0.731). Further analysis showed no significant difference in the percentage of lesions that were a high nuclear grade (F3 or F4, p = 0.992) or a high tumor stage (T3 or T4, p = 0.731).
Comparison of groups B and C showed a statistically significant difference
in nuclear grade (p = 0.001) or tumor stage (p 0.001).
Accordingly, there was a significant increase in the percentage of lesions
with nuclear grade high enough (F3 or F4) to have prognostic significance
(p = 0.001) and tumor stage high enough (T3 or T4) to have prognostic
significance (p < 0.001) in group C. A trend of higher probability
of clear cell histology was also documented (p = 0.105).
Comparison of the frequency of incidental lesions showed no statistically significant difference between groups A and B (p = 0.247), but a significant decrease was found in incidental lesions in group C (p < 0.001) when compared with group A or B. A trend of higher tumor stage (p = 0.05) and higher nuclear grade (p = 0.202) was noted for symptomatic lesions; however, given our sample size, we did not show this trend to be independent of tumor size except in group B, which was composed of symptomatic lesions that were significantly more likely to be a higher stage (p = 0.05).
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The debate regarding the appropriate size criteria for staging has fueled a great deal of analysis about how tumor size affects survival. Not surprisingly, smaller tumors generally portend higher postoperative survival rates [16], with various statistically significant break-points reported [15, 16]. Our goal was not to duplicate these efforts, but to correlate renal cell carcinoma size with other factors that may independently influence management and outcome. We correlated tumor size with incidence of extracapsular spread (T3 or T4 status), Fuhrman nuclear grade, and histologic subtype, all of which have been validated as independent prognostic factors [15].
Siegelman et al. [18] conducted a study of 100 consecutive patients diagnosed with renal cell carcinoma in the 1960s to evaluate the relationship between the manner of clinical presentation and the eventual outcome after nephrectomy [17]. There were 16 patients in whom a tumor was detected by serendipity during excretory urography. The indication for the studies was hypertension, prostatic enlargement, or another condition considered unrelated to a suspicion of renal neoplasm. The mean size of the 16 tumors was 6.2 cm, which is considerably smaller than renal carcinomas detected because of hematuria (mean size, 10 cm), flank pain (mean size, 11.7 cm), or palpation of a mass (mean size, 12.1 cm). Fifteen of these 16 patients were long-term survivors free of recurrent tumor [18]. From that study, the authors concluded that, as one would intuit, the ideal time to detect renal cell carcinoma is when the lesions are small and asymptomatic. These researchers asserted that every patient who had an imaging study that included the kidneys should be screened for early renal cell cancer. The subsequent introduction of CT, sonography, and MRI greatly increased the number of subjects available for evaluation. Serendipity has become the most frequent means by which renal cell carcinomas is detected.
Radiologists scrutinizing each kidney on imaging studies performed for other purposes are performing a screening study. They should be ready to deal with the criticisms that have been directed at such efforts [19]. A key issue is whether length-time bias is a serious consideration in current practice. This concept holds that if there is great variability in the biologic behavior of renal cell carcinomas, the less aggressive, slower-growing neoplasms are more likely to be detected at screening because they are present in the preclinical state for a longer period. Are we making surgical candidates of patients with renal neoplasms that might remain dormant for decades and never become clinically evident during their lifetimes? It is not possible to provide a definitive answer to this challenging question. The issue of screening bias is particularly pertinent because screening of asymptomatic adults for renal cancer using sonography has been used in Japan [20] and Germany [21] for several years. This study offers support to justify an aggressive approach to the management of small renal cell carcinomas detected by serendipity.
In our study population, small renal tumors up to 3 cm in diameter were found to exhibit several statistical trends of interest. Of clinical prognostic significance, 28% were nuclear grade 3 or higher, and 38% extended beyond the renal capsule. Even for asymptomatic lesions, these figures were 26% and 47%, respectively. These percentages were similar to those for lesions in the next group (i.e., > 3–5 cm) but were significantly less than those in the group composed of lesions larger than 5 cm.
Nuclear grading according to the Fuhrman classification system [11] is widely accepted and has been shown to confer prognostic significance. A sharp increase in metastases and a decrease in survival have been noted for patients with lesions that are nuclear grade 3 or 4 [22]. TNM tumor staging is even more predictive than the Fuhrman classification system. Capsular transgression defines a T3 lesion, with a significant increase in metastases and a decrease in survival for patients with T3 or T4 lesions [23].
The significant number of small lesions, including asymptomatic lesions, found to have high nuclear grade and high TNM tumor stage suggests that many of these lesions would have progressed to regional distant metastases and potentially would have become a source of morbidity and mortality. This finding clearly supports resection of small tumors, whether incidental or symptomatic.
Some may argue that the similar incidence of high nuclear grade and tumor
stage for lesions in groups A ( 3 cm) and B (> 3–5 cm) suggests
that a group A lesion may be safely followed up until it is in the 3- to 5-cm
range and may subsequently be resected if found to grow or to grow rapidly.
However, this proposition is suspect, unless the incidence of interval
metastases is known to be very low. The risk–benefit ratio of such an
approach might deserve examination in patients less tolerant of surgery or
with shorter life expectancy.
As for histologic classification, renal cell carcinoma includes several subtypes. Clear cell ("conventional") histology accounts for 70–80%, followed by papillary (10–15%) and chromophobe (5%), both of which have been shown to be associated with a higher rate of survival and lower rate of metastasis than the clear cell subtype [15]. The tubular subtype and sarcomatoid change are less common and confer a worse prognosis. These subtypes cannot be reliably differentiated on imaging.
We found the largest lesions (> 5 cm) to include more clear cell tumors and fewer papillary and chromophobe tumors than the smaller tumors. The distribution of histologic subtypes was similar between the two groups of smaller lesions. Of the three most common histologic subtypes, we did not find a significantly different distribution for incidental and symptomatic lesions when corrected for size.
We acknowledge several inherent limitations of this retrospective study. By searching the pathology database, we defined our study population as patients with renal cell carcinoma treated by resection. This criterion excludes most patients with known metastases, patients unwilling to undergo or unsuitable for surgery, and those treated with percutaneous ablation. However, few patients were treated by percutaneous ablation during the time frame of our study, and selection for this option was primarily based on small size (usually < 4 cm) or the need to spare nephrons and not on other independent predictors of outcome. Our conclusions therefore apply to a close approximation of the defined study population— namely, those with renal cell carcinoma who are candidates for resection.
In fact, despite exclusion of most patients with known metastases with presumably [24] higher average nuclear grade and tumor stage, we found a significant percentage of small lesions to have high nuclear grade and tumor stage. Exclusion of metastatic disease obviously does however preclude correlation of metastatic incidence with tumor characteristics at presentation. Also, follow-up would be required to determine survival after resection and metastasis-free survival.
Our study also excludes masses radiologically presumed to be renal cell carcinoma but later found to be other malignant or benign entities at tissue diagnosis. Exclusion of these lesions is mitigated by the fact that most nonspecific solid enhancing renal masses are renal cell carcinoma or collecting system transitional cell carcinoma, which also requires resection for cure. Therefore, the argument for treatment of small presumed renal cell carcinoma remains strong.
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