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Renal Cell Carcinoma Recurrence After Nephrectomy for Localized Disease: Predicting Survival From Time of Recurrence

Scott E. Eggener, Ofer Yossepowitch, Joseph A. Pettus, Mark E. Snyder, Robert J. Motzer, Paul Russo

From the Genitourinary Oncology Service, Division of Solid Tumor Oncology and Department of Urology, Memorial Sloan-Kettering Cancer Center, New York, NY

Address reprint requests to Paul Russo, MD, Department of Urology, Sidney Kimmel Center for Prostate and Urologic Cancers, Memorial Sloan-Kettering Cancer Center, 353 E 68th St, New York, NY 10021; e-mail: russop{at}mskcc.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
PURPOSE: Prognostic factors for patients with metastatic renal cell carcinoma (RCC) are well established. However, the risk profile is unknown for patients with recurrent RCC after a nephrectomy for localized disease.

PATIENTS AND METHODS: From January 1989 to July 2005, we identified patients with localized RCC treated by nephrectomy who subsequently developed recurrent disease. We applied a validated prognostic scoring system previously developed for patients with metastatic RCC. Each patient was given a total risk score of 0 to 5, with one point for each of five prognostic variables (recurrence < 12 months after nephrectomy, serum calcium > 10 mg/dL, hemoglobin < lower limit of normal, lactate dehydrogenase > 1.5x upper limit of normal, and Karnofsky performance status < 80%). Patients were categorized into low- (score = 0), intermediate- (score = 1 to 2), and high-risk subgroups (score = 3 to 5).

RESULTS: Our final cohort included 118 patients, with a median survival time of 21 months from the time of recurrence. Median follow-up time for survivors was 27 months. Overall survival was strongly associated with risk group category (P < .0001). Low-risk, intermediate-risk, and high-risk criteria were fulfilled in 34%, 50%, and 16% of patients, respectively. Median survival time for low-risk, intermediate-risk, and high-risk patients was 76, 25, and 6 months, respectively. Two-year overall survival rates for low-risk, intermediate-risk, and high-risk patients were 88% (95% CI, 77% to 99%), 51% (95% CI, 37% to 65%), and 11% (95% CI, 0% to 24%), respectively.

CONCLUSION: At disease recurrence after nephrectomy for localized disease, a scoring system based on objective clinical and laboratory data provides meaningful risk stratification for both patient counseling and clinical trial entry.

	INTRODUCTION

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The prognosis for patients with renal cell carcinoma (RCC) is primarily dependent on disease stage. Organ-confined disease (pathologic stage pT1-2) confers the best prognosis, with 5-year cancer-specific survival rates after nephrectomy ranging from 71% to 97%.¹ For patients with locally advanced tumors, 5-year cancer-specific survival rates after nephrectomy decrease to 20% to 53%¹, and once RCC has metastasized, the 5-year survival rate is less than 10%.^2,3

Predictive tools have been developed for application at different points in the natural and treated history of RCC. Numerous models exist to predict disease recurrence after nephrectomy for all histologic subtypes of RCC^4-6 and also specifically for patients with clear cell RCC.⁷ The natural history and risk group stratification have also been evaluated in those with newly diagnosed metastatic RCC,^2,3,8 specifically in metastatic non–clear cell RCC patients⁹ and in patients with previously treated metastatic disease.¹⁰ Motzer et al¹¹ identified the following five objectives and easily obtained values to calculate a prognostic score in patients with metastatic RCC: time from initial diagnosis to start of systemic therapy less than 12 months, Karnofsky performance status less than 80%, serum corrected calcium more than 10 mg/dL, hemoglobin less than the sex-specific lower limit of normal, and a lactate dehydrogenase (LDH) more than 1.5x the upper limit of normal. Because these values and the resulting score were devised from a large cohort and validated externally through another large institutional data set, it has become a widely used method of estimating prognosis for patients with metastatic RCC.²

Although standard treatment for localized RCC remains surgical removal, either by partial or radical nephrectomy, additional treatment options include watchful waiting¹² and investigational ablative therapies.¹³ For patients choosing excision of localized RCC, approximately 20% will subsequently experience disease recurrence.^4,5 For patients diagnosed with disease recurrence, no specific risk stratification tool is available at the time of recurrence. Therefore, in this study, we sought to evaluate the utility of the prognostic score suggested by Motzer et al¹¹ in patients with disease recurrence after nephrectomy. Using a large institutional cohort to analyze these patients, our objective was to assess if the five values provided meaningful risk stratification from the time of disease recurrence.

	PATIENTS AND METHODS

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Study Cohort
Using our departmental surgical database at Memorial Sloan-Kettering Cancer Center, from January 1989 to July 2005, we identified 1,554 patients undergoing radical (n = 1,081) or partial (n = 473) nephrectomy for unilateral, clinically localized RCC. Before nephrectomy, all patients were staged with an abdominal computed tomography (CT) scan, chest imaging (x-ray or CT scan), a comprehensive serum metabolic panel, and, if indicated, brain or bone imaging.

A total of 150 patients (10%) developed disease recurrence after nephrectomy. Among the patients undergoing radical nephrectomy, 142 (13%) of 1,081 experienced a recurrence compared with eight (2%) of 473 patients after a partial nephrectomy. Metachronous disease in the contralateral kidney was not considered a recurrence. All RCC pathologic subtypes were included. Clinical, pathologic, and laboratory data at the time of nephrectomy and disease recurrence were collected. Patients with von Hippel-Lindau (n = 1), a previous history of RCC (n = 3), no laboratory data at the time of disease recurrence (n = 11), or inadequate follow-up after disease recurrence (n = 17) were excluded, leaving 118 patients available for analysis. Tumor stage was determined according to the 2002 American Joint Committee on Cancer staging system.¹⁴

Natural History and Prognostic Model
Surveillance methods after nephrectomy were set at the discretion of the surgeon. Most patients, at the minimum, had annual follow-up with history, physical examination, serum chemistries, and a chest x-ray. Although many patients underwent regular abdominal CT scans, there was not a standardized patient selection criteria or imaging interval. We defined disease recurrence as radiographic evidence of disease on chest x-ray, CT, magnetic resonance imaging, or bone scan with or without pathologic confirmation.

We chose to apply the validated prognostic scoring system of Motzer et al¹¹ for patients with metastatic RCC to our study cohort. This model includes the following five adverse predictive variables: corrected serum calcium more than 10 mg/dL, hemoglobin less than sex-specific lower limit of normal, LDH more than 1.5x normal, Karnofsky performance status less than 80%, and time from initial diagnosis to systemic treatment of less than 12 months. Because not all patients in our cohort underwent systemic therapy, we substituted time from initial diagnosis to systemic treatment of less than 12 months with time from nephrectomy to disease recurrence of less than 12 months. Corrected serum calcium was calculated as total calcium (mg/dL) minus 0.7 x [serum albumin (g/dL) –3.4].¹⁵ On the basis of the laboratory at our institution, the lower limits of normal hemoglobin for men and women were 13.0 and 11.5 g/dL, respectively, and the upper limit of normal for LDH is 200 U/L. Karnofsky performance status was assessed at the time of disease recurrence.¹⁶ All five parameters were collected and recorded at the time of disease recurrence. One or more values was missing from 11 patients (7.3%), most commonly LDH, hemoglobin, and calcium; therefore, these patients were excluded from analysis on a case-wise basis. We compiled the number of adverse prognostic factors for each patient and, similar to Motzer's original report,¹¹ categorized them into low- (zero risk factors), intermediate- (one to two risk factors), and high-risk (three to five risk factors) groups.

Treatment after disease recurrence complied with era-specific local standards of care. Surgical metastasectomy was recommended if a solitary site of recurrence amenable to resection was identified in a patient considered an appropriate surgical candidate. Survival curves were then constructed for each of these groups using the Kaplan-Meier method and compared using the log-rank test. Survival was defined from time of disease recurrence to death or last follow-up. All P values were two sided, and P < .05 was considered statistically significant.

	RESULTS

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Patient Characteristics at Time of Nephrectomy
In our study cohort of 118 patients, 69% were male, the mean age was 61.1 years (standard deviation, 12.6), and 96% had a radical nephrectomy (Table 1). Only 4% of our patients with disease recurrence had a partial nephrectomy. Clear cell carcinoma was present in 79% of patients, and pathologic extracapsular disease extension (pathologic stage T3 or higher) was present in 60% of patients.

Risk Groups and Survival
Overall, median follow-up time from disease recurrence was 21 months; for the patients alive at last follow-up, median follow-up time from disease recurrence was 27 months. Median survival time for all patients from the time of recurrence was 21 months. Disease-specific survival equaled overall survival because all deaths were attributed to metastatic RCC. We observed an inverse correlation between the number of risk factors and survival (log-rank P < .0001; Fig 1A). Median survival times for patients with zero, one, two, three, four, or five risk factors was 76, 25, 19, 5, 8, and 4 months, respectively. On the basis of these findings, risk categories were defined as follows: low-risk group has zero risk factors, intermediate-risk group has one to two risk factors, and high-risk group has three to five factors. Significant differences in survival were noted between the low-, intermediate-, and high-risk groups (log-rank P < .0001; Fig 1B).

View larger version (14K): [in this window] [in a new window]   Fig 1. Patients with disease recurrence after nephrectomy for localized disease. (A) Overall survival based on risk stratification score (log-rank P < .0001) and (B) overall survival based on modified risk stratification score: low risk (zero risk factors), intermediate risk (one to two risk factors), and high risk (three to five risk factors); error bars are 95% CIs (log-rank P < .0001).

Excluding patients who underwent a surgical metastatectomy (n = 30), median survival time was 67 months for the low-risk group (n = 21, 24%), 24 months for the intermediate-risk group (n = 49, 56%), and 6 months for the high-risk group (n = 18, 20%). Survival differences were noted between low-, intermediate-, and high-risk groups (log-rank P < .0001).

	DISCUSSION

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Our study shows that, for patients with disease recurrence after a partial or radical nephrectomy for localized RCC, an estimation of survival from the time of disease recurrence can be obtained using a simple prognostic tool. After a partial or radical nephrectomy for localized RCC, an estimation of the probability of disease recurrence can be obtained from currently available predictive tools.^5,17 The risk stratification produced by these nomograms is valuable for patient counseling, treatment decisions, and entry onto clinical trials. Using this information available after surgery, retrospective analyses of large cohorts have provided the likelihood of site-specific recurrence,¹⁸ and based on these estimations, risk-specific surveillance protocols can be instituted.¹⁹ Using these resources, the patient and urologist can decide on the method, intensity, and frequency of surveillance. For patients under surveillance after partial or radical nephrectomy, disease recurrence is typically discovered by one of the following methods: evaluation of new symptoms, physical examination, or surveillance imaging. However, once diagnosed with disease recurrence, it was previously unknown what factors predict outcome. To our knowledge, we offer the first report determining risk stratification from the time of disease recurrence after nephrectomy for localized RCC.

We chose to incorporate well-established and previously validated variables into our model rather than introduce another system. We specifically chose to include objective data, such as laboratory values or time to recurrence, to avoid the potential bias introduced when evaluating subjective measures, such as the decision to perform a metastasectomy or administer adjuvant therapy. All five values used to calculate a patient's score (time to recurrence, Karnofsky performance status, corrected calcium, hemoglobin, and LDH) are easily obtained and objective and were readily assessable in our patient cohort. Therefore, we chose to study these factors.

By applying these five factors to a patient at the time of disease recurrence, a risk stratification score can be obtained. Using this tool, the 5-year survival rate may be estimated to be as high as 69% or as dismal as 0%. This fosters realistic disease-specific expectations and can be used when deciding on further treatment or enrollment onto adjuvant or salvage protocols. Patients in our study with a low-risk score were more likely to have pulmonary-only metastases or have undergone a surgical metastatectomy. This explains why low-risk patients had improved survival because long-term survival can be achieved after surgical metastasectomy,²⁰ and patients with low-volume metastatic disease, particularly when pulmonary, typically respond best to immunotherapy.²¹ However, because patients undergoing a metastasectomy may represent a biased subset, we separately analyzed patients not undergoing a metastasectomy. When excluding the potential subjectivity of metastasectomy, the risk stratification categories continued to provide powerful prognostic information. We specifically chose not to study disease burden and the impact of treatment because these can be subject to investigator bias at the time of assessment.

Our findings are particularly pertinent in light of a recent tyrosine kinase inhibitor trial showing heretofore unparalleled activity against metastatic RCC, potentially heralding a new era of promising treatment strategies.²² Consequently, there are a number of single-agent and combination-therapy trials using these agents that are ongoing or in the planning stages, and now, more than ever, it is essential to accurately and reliably risk stratify these patients before study entry.

For the following three reasons, we strongly believe our findings build on previous studies to provide novel and clinically relevant prognostic information. First, compared with previous studies providing risk stratification for patients with metastatic RCC,^2,3 most patients in our study cohort were not enrolled onto a clinical trial because they underwent a surgical metastasectomy, were treated with standard era-specific systemic therapy outside of a clinical trial, or elected observation over treatment. For this reason, we feel that our findings more accurately represent the cohort of patients experiencing recurrence after a nephrectomy rather than reflecting the potential bias inherent in studying only patients entered onto clinical trials.

Second, similar to previous studies,^2,3 we found median survival time to be considerably longer in patients experiencing recurrence after nephrectomy compared with all patients with metastatic disease, which is a factor that requires consideration when randomly assigning patients for future clinical trials.

Lastly, we identify a group of objectively identified low-risk patients with an unprecedented median survival time of more than 6 years from the time of recurrence, which is much longer than the median survival times of 20 to 26 months^2,3 previously noted in low-risk patients with metastatic disease using the same risk criteria. This observation is likely due to of a number of reasons. Our study population represents a select group of patients undergoing nephrectomy, postoperative surveillance, and, in many patients, early recognition of disease recurrence with prompt treatment. Because relatively few patients were entered onto clinical trials, overall, they may have been a group with more favorable expected outcomes. Additionally, our survival analysis began at the time of disease recurrence in contrast to the previous reports beginning at the time of systemic therapy. Because the interval from disease recurrence to treatment may be prolonged in some patients (for instance, to confirm recurrent disease by serial imaging) this may, in part, explain the different median survivals noted. We chose to calculate survival from the time of recurrence rather than from the start of treatment because most discussions regarding patient counseling and expectations occur at this time and some patients elected to forego treatment.

A few limitations regarding our study deserve mention. Although most patients were routinely evaluated and imaged, surveillance for disease recurrence after nephrectomy was both surgeon and patient specific. The risk score was originally established based on patients from multi-institutional clinical trials, including many treated at our institution. Only six of our 118 patients were included in these trials; therefore, our study population essentially represents a distinct cohort. The variables we included in calculating the risk score, although proven and validated, do not represent every known predictive factor. There are others, such as site of metastases, number of metastases, platelet count, and cachexia, that may correlate with outcome.^2,23,24 Furthermore, molecular biomarkers, such as carbonic anhydrase IX, vimentin, p53, and PTEN (phosphatase and tensin homologue), have been shown to assist in the risk stratification of patients with metastatic RCC.²⁵ Lastly, we observed a recurrence rate of 13% after radical nephrectomy and 2% after partial nephrectomy, which is similar to rates reported by some groups^7,19 and lower than others.^26,27

In conclusion, we used five easily obtained and previously validated prognostic factors to risk stratify patients with recurrence after nephrectomy for localized disease. The ability to categorize these patients into low-, intermediate-, and high-risk groups with median survival times of 76, 25, and 6 months, respectively, is valuable to establish realistic patient expectations, guide treatment decisions, and create the appropriate design and analysis of clinical trials.

	Authors' Disclosures of Potential Conflicts of Interest

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
The authors indicated no potential conflicts of interest.

	Author Contributions

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 

Conception and design: Scott E. Eggener, Paul Russo Administrative support: Mark E. Snyder Provision of study materials or patients: Robert J. Motzer, Paul Russo Collection and assembly of data: Scott E. Eggener, Mark E. Snyder Data analysis and interpretation: Scott E. Eggener, Ofer Yossepowitch, Joseph A. Pettus Manuscript writing: Scott E. Eggener, Ofer Yossepowitch, Joseph A. Pettus, Paul Russo Final approval of manuscript: Scott E. Eggener, Ofer Yossepowitch, Joseph A. Pettus, Mark E. Snyder, Robert J. Motzer, Paul Russo

 

	NOTES

 
Supported by National Institute of Health Ruth Kirchstein National Research Service Award No. T32-CA82088-06 (S.E.E.).

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
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Submitted November 4, 2005; accepted April 20, 2006.

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