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Ann Thorac Surg 2005;79:996-1003
© 2005 The Society of Thoracic Surgeons

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Original article: General thoracic

Can We Predict Long-Term Survival After Pulmonary Metastasectomy for Renal Cell Carcinoma?

^a Department of Thoracic and Cardiovascular Surgery, Hematology and Medical Oncology
^b Department of Quantitative Health Sciences, The Cleveland Clinic Foundation, Cleveland, Ohio

Accepted for publication August 13, 2004.

^* Address reprint requests to Dr Murthy, The Cleveland Clinic Foundation, 9500 Euclid Ave/Desk F25, Cleveland, OH44195 (E-mail: murthys1{at}ccf.org).

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Appendix Variables Used In... References

 
BACKGROUND: The purpose of this study is to identify factors associated with time-related survival after pulmonary metastasectomy for renal cell carcinoma and to confirm the safety of metastasectomy.

METHODS: From January 1986 to July 2001, 417 patients were diagnosed with pulmonary metastases from renal cell carcinoma; 92 underwent pulmonary metastasectomy. Median disease-free interval after nephrectomy was 3.0 years. Half the patients had 1 or 2 pulmonary nodules; 37% had 5 or more. Median size of the largest nodule (pulmonary metastasis) was 15 mm. Complete resection was obtained in 63 patients (68%). Twenty-nine patients received preoperative immunotherapy. Multivariable hazard function analysis was used to identify continuous, ordinal, and true dichotomous risk factors.

RESULTS: Predictors: The strongest risk factor for time-related mortality was incomplete resection. Five-year survival was 8% for incomplete and 45% for complete resection. Other risk factors included the following continuous and ordinal variables: larger nodule size (p = 0.0001), increasing number of involved lymph nodes (p = 0.01), and decreased preoperative 1-second forced expiratory volume (p = 0.02). Immunotherapy did not improve survival. For completely resected patients, shorter disease-free interval was a risk factor (p = 0.01). Fewer pulmonary nodules predicted higher probability of complete resection (p < 0.0001). Safety: No operative deaths occurred. Nine patients (10%) experienced a total of 12 complications, with persistent air leak and atrial arrhythmia accounting for 5 (42%).

CONCLUSIONS: Because pulmonary metastasectomy for renal cell carcinoma is safe, survival depends on complete resection of pulmonary disease and adequate pulmonary reserve. Preoperative determination of resectability is thus critical, and computed chest tomography and mediastinoscopy are valuable tools for optimizing patient selection.

	Introduction

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Many reports suggest a role for pulmonary metastasectomy in managing metastatic renal cell carcinoma [1–9]. Collectively, these studies variably implicate size and number of pulmonary nodules, completeness of resection, degree of differentiation of the primary renal cell carcinoma, disease-free interval, and regional lymph node involvement as important factors associated with survival. However, inconsistency among reports has led to confusion regarding the importance of each factor (Table 1). To help clarify the role of pulmonary metastasectomy and resolve published inconsistencies, this study was designed to (1) identify continuous, ordinal, and true dichotomous factors associated with time-related survival and (2) confirm the safety of pulmonary metastasectomy for renal cell carcinoma.

	Patients and Methods

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Preoperative assessment included spirometry, radiographic metastatic survey, and performance status. Size (long axis) and number of nodules were determined by preoperative chest computed tomography (CT). Criteria for metastasectomy were subjective, but included good performance status (93% of patients were in Eastern Cooperative Oncology Group [ECOG] 0 to 1), acceptable pulmonary reserve (median preoperative FEV₁ was 87% of predicted normal), and younger age (median = 60 years) (Table 2). Patients were not deemed inoperable because of a large number of pulmonary nodules (37% had 5), synchronous presentation of renal and pulmonary disease (15 patients, 16%), or disease at other metastatic sites (11 patients, 12%). Histologic examination of resected nodules suggested renal cell carcinoma in all patients, although specific histopathologic characterization of carcinoma subtype was not uniformly available.

Metastasectomy
Thoracotomy was the usual incision (56 patients, 61%), while sternotomy (20 patients, 22%), video assistance (12 patients, 13%), and thoracolaparotomy (4 patients, 4%, for combined nephrectomy and pulmonary metastasectomy) were used less frequently. Anatomic resection was part of therapy in 23% of patients (Table 3). Pathologic data from intraparenchymal and mediastinal lymph nodes were available in 32 patients (35%). Regardless of relation to the pulmonary nodules, all lymph nodes (N1–N3) were considered collectively because paucity of information precluded independent analyses. Fifty percent of involved lymph nodes were mediastinal (N2–N3).

Follow-Up
Patients were followed cross-sectionally in May 2002 by telephone interview or examination at the Cleveland Clinic. Two patients were lost to follow-up after 1.8 and 6.8 years of previous follow-up. Mean follow-up was 3.7 ± 3.1 years, with 338 patient-years of information available for analysis.

Data Analysis: Descriptive Statistics
Categorical variables are summarized by frequencies and percentages and continuous variables by medians and 25th and 75th percentiles.

Survival Estimates
Nonparametric estimates of overall survival were obtained by the Kaplan–Meier method. A parametric method was used to resolve the number of phases of instantaneous risk of death (hazard function) and to estimate shaping parameters (for additional details, see http://www.clevelandclinic.org/heartcenter/hazard). Thereafter, multivariable analysis was performed in the hazard function domain.

Multivariable Analysis
Variables examined in multivariable analyses are listed in the Appendix. Continuous and ordinal variables were retained in their original state to maximize information content. Original measurement scales were calibrated to the assumptions of the analysis by transformation, as necessary. Selection of risk factors utilized bootstrap aggregation with (1) automated analysis of 1,000 random data sets using p less than or equal to 0.05 as the criterion for retaining factors in each model, followed by (2) aggregation of results, expressed as frequency of occurrence of both single factors and closely related clusters of factors, as previously detailed [10]. Only factors occurring in at least 50% of these analyses were considered statistically significant.

Two analytic challenges associated with timing of resection were managed as follows. (1) Separate analysis of the complete resection group indicated that shorter disease-free interval was associated with shorter survival, but this was not found in the group with incomplete resection. The final multivariable analysis, therefore, included an interaction term representing completeness of resection and disease-free interval. (2) To account for nephrectomy occurring after diagnosis of pulmonary nodules, a term representing such patients was also incorporated into the model. The important matter of complete versus incomplete resection was explored by multivariable logistic regression using the same variable selection strategy cited above.

The relation to survival of any induction or adjuvant immunotherapy was assessed by first constructing a propensity model for receipt of this therapy using nonparsimonious logistic regression [11]. A propensity score was obtained for each patient on the basis of this model. Greedy matching was performed using this score as its sole criterion to yield 21 well-matched pairs. Survival was compared between the two groups using the log-rank test.

Presentation
To illustrate graphically the relations of risk factors to mortality, the parametric multivariable equation was solved in either time-related fashion or at 5 years. To present this information in risk-adjusted fashion, all other factors in the model were fixed at representative values: disease-free interval 3 years, FEV₁ 87% of predicted normal, complete resection, no lymph node involvement, and largest nodule 15 mm. Evident differences were also identified that signify nonoverlap of 68% confidence intervals along the continuous or ordinal scale.

	Results

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Risk Factors for Time-Related Mortality
Overall survival was 82%, 49%, and 31% at 1, 3, and 5 years, respectively. The strongest predictor of survival was completeness of resection (Fig 1); 1-year, 3-year, and 5-year survivals were 86%, 59%, and 42% for completely resected patients versus 65%, 22%, and 8% for incompletely resected patients. The greater the number of pulmonary nodules identified by preoperative chest CT, the higher the probability of incomplete resection (p < 0.0001; Table 4, Fig 2). The likelihood of incomplete resection reached 80% when there were six or more nodules identified on preoperative CT, but only 20% when there were three or fewer (for example, complete resection was achieved in 34% of 35 patients [97%] having a single pulmonary nodule detected on preoperative CT). Because of this relation, increasing number of pulmonary nodules was a risk factor for death only in analyses that did not consider completeness of resection (Table 5). Interestingly, preoperative count of pulmonary nodules accurately reflected the number of nodules actually resected (r = 0.6, p < 0.0001). Preoperative radiographically defined mediastinal adenopathy was not a risk factor for incomplete resection (nor did it correlate with lymph node involvement).

View larger version (21K): [in this window] [in a new window]   Fig 1. Survival after pulmonary metastasectomy stratified by complete (squares) and incomplete (circles) resection. Vertical bars represent 68% confidence limits (equivalent to 1 standard error) of nonparametric estimates; numbers in parentheses represent patients remaining alive. Solid lines (enclosed by dashed 68% confidence limits) are parametric survival estimates.

View larger version (16K): [in this window] [in a new window]   Fig 2. Probability of incomplete resection according to number of pulmonary nodules on preoperative computed tomography (CT). Filled circles are actual probabilities, and solid line (enclosed within dashed 68% confidence limits) is logistic regression estimate.

View larger version (12K): [in this window] [in a new window]   Fig 3. Five-year survival according to size of largest pulmonary nodule. This is a nomogram of the risk factor equation for death (see Table 6 and Presentation). Solid line is point estimate and dashed lines 68% confidence limits. There is an evident difference in survival for nodules larger than 30 mm compared with 5 mm.

View larger version (10K): [in this window] [in a new window]   Fig 4. Five-year survival according to number of involved lymph nodes. This is a nomogram of the risk factor equation for death (see Table 6 and Presentation). Closed circles are point estimates and vertical bars their 68% confidence limits. There is an evident difference for 0 involved lymph nodes versus 2 involved nodes and 1 versus 3 involved nodes.

View larger version (12K): [in this window] [in a new window]   Fig 5. Five-year survival according to forced expiratory volume in one second (FEV1). This is a nomogram of the risk factor equation for death (see Table 6 and Presentation). Solid line is point estimate and dashed lines 68% confidence limits. There is an evident difference in survival for patients with an FEV1 65% of predicted normal versus 100%.

View larger version (16K): [in this window] [in a new window]   Fig 6. Five-year survival according to disease-free interval and two specific sizes of largest nodule. This is a nomogram of the risk factor equation for death (see Table 6 and Presentation). Solid lines are point estimates and dashed lines 68% confidence limits. There is an evident difference in survival for patients presenting with synchronous disease versus those whose disease-free interval is greater than 5 years.

When the previous factors were taken into account, gender, age, tumor stage, immunotherapy, type of resection, and number of pulmonary nodules were not found to be independently associated with mortality. Immunotherapy did not improve survival (p = 0.5) in propensity-matched patients.

Safety
No patient died in-hospital after pulmonary metastasectomy. Nine (10%) experienced a total of 12 complications (Table 7). Persistent air leak and atrial arrhythmia accounted for 5 of the 12 complications (42%); of 3 patients experiencing 2 complications, 1 had been treated with concomitant renal and pulmonary resection.

	Comment

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Feasibility of pulmonary metastasectomy for renal cell carcinoma was first reported by Barney and Churchill in 1939 [18]. A number of subsequent studies have demonstrated a central role for metastasectomy in managing this disease [1–9]. Collectively, they show a 20% to 50% 5-year survival, which is higher than the 3% to 11% survival reported for nonoperated patients [4]. However, although some common risk factors have been identified, there is little consensus regarding patient or tumor factors important for long-term survival after pulmonary metastasectomy (see Table 1). This may be attributed in part to arbitrary dichotomization of continuous and ordinal variables that has made it difficult to prioritize risk factor effects and evaluate interaction among factors. Consequently, continuous gradation of prognosis has been undocumented until now. Therefore, we examined our 15-year experience with pulmonary metastasectomy using hazard function analysis of continuous, ordinal, and true dichotomous variables to identify independent and interacting factors associated with mortality.

Risk Factors for Mortality
Five variables (including incomplete resection, as explained in Table 6 footnote) were associated with mortality following pulmonary metastasectomy for renal cell carcinoma. Because continuous and ordinal variables were treated as such in the analysis, bias imparted by arbitrary dichotomization was avoided.

All identified factors did not affect survival equally; incomplete resection was the strongest. Dichotomization of continuous and ordinal variables, differing composition of groups studied, and differential impact of risk factors explain lack of consensus of other studies regarding risk factors (see Table 1). This may be best understood from our finding that disease-free interval was uncovered as a risk factor for mortality only when completely resected patients were studied by subset analysis (see Tables 5 and 6).

That one third of patients had incomplete resection is both disconcerting and enlightening. Many patients underwent resection for diagnosis or alternative therapy (immunotherapy) purposes. Complete resection was accomplished in some of these patients.

Preoperative CT proved to be an effective modality for predicting incomplete resection, and consequently survival, by quantifying the number of pulmonary nodules. Computed tomographic scanning also provides valuable information about resectability of specific nodules. Interestingly, chest CT-defined lymphadenectomy did not correlate with either completeness of resection or survival, to some degree strengthening our contention that lymph node involvement does not preclude complete resection if the regional lymph nodes are included in en bloc resection.

Shorter disease-free interval was not an important risk factor for mortality in incompletely resected patients, suggesting that residual disease after resection is the more ominous factor. In patients who are completely resected, it is conceivable that longer disease-free interval reflects less aggressive cancer.

A novel finding was that lower preoperative FEV₁ is an important risk factor for mortality. This might be the first time this variable has been examined. Because a quarter of our patients had an anatomic pulmonary resection as part of their therapy, spirometry was a standard component of preoperative evaluation. We suspect that preoperative FEV₁ is a more important factor in anatomic resection than in wedge resection, although specific investigation of an interaction between extent of resection and FEV₁ did not reveal such an interaction.

There is an increasing appreciation of the deleterious effect of regional lymph node metastases on outcome of patients with carcinoma metastatic to the lung [2, 7, 19]. Lymphatic spread of renal cell carcinoma to mediastinal sites has been well documented [20]. This study confirms that greater lymph node burden (number of involved nodes) is an important risk factor for mortality after pulmonary metastasectomy for renal cell carcinoma. We believe that regional lymph node metastases arise from the pulmonary nodules and therefore favor treating solitary pulmonary nodules similarly to primary lung cancer.

Safety
This study confirms previous ones documenting the safety of pulmonary metastasectomy [1–8]. That metastasectomy is safe becomes important in the context of the limited effectiveness of nonsurgical management strategies. The ability of patients to tolerate metastasectomy is likely a function of their generally excellent preoperative performance status. However, this clearly reflects selection bias in identifying and referring candidates for surgery.

Limitations
This study is limited by several factors: (1) It represents the clinical experience of a single center; (2) quality of the data depends on complete and accurate documentation and interpretation of medical records; (3) observer bias (patient referral patterns; physician, surgeon, and patient preferences; and even availability of clinical trials of therapy) is an important component that affects patient selection and management; (4) details of immunologic tumor management prescribed outside the context of clinical trial protocols were not clearly documented in our records.

Conclusions
The results of this and other studies (see Table 1) suggest practical guidelines for pulmonary metastasectomy in managing renal cell carcinoma (Fig 7). Preoperative identification of patient and tumor risk factors is imperative when selecting patients for metastasectomy. Because incomplete resection is the dominant risk factor, the focus of evaluation should be on identifying patients likely to be completely resected. Because number of pulmonary nodules is inversely related to ability to achieve complete resection, high-resolution spiral CT is an essential component of the work-up (see Fig 2). Although the relation is continuous, if a patient has three or fewer nodules identified on preoperative CT, chance of complete resection exceeds 80%; conversely, if more than six nodules are seen on CT, chance of incomplete resection is 80% or higher.

View larger version (23K): [in this window] [in a new window]   Fig 7. Survival of three hypothetical patients. This is a nomogram of the risk factor equation for death (see Table 6). For the patient with complete resection and considered low risk: disease-free interval 6 years; forced expiratory volume in one second (FEV1) 100% of predicted normal; no lymph node involvement; largest pulmonary nodule 7 mm. For the patient with complete resection and considered high risk: disease-free interval 1 year; FEV1 75% of predicted normal; 1 lymph node involved; largest pulmonary nodule 30 mm. For the patient with incomplete resection: disease-free interval 1 year; FEV1 75% of predicted normal; 1 lymph node involved; largest pulmonary nodule 45 mm.

For solitary nodules, we recommend anatomic resection when possible, because our bias is that these cancers utilize pulmonary lymphatic drainage similar to lung cancers. This is supported by finding pN1 lymph node involvement in 9% of patients. When multiple nodules are present, anatomic resection becomes less feasible because of the desire to preserve pulmonary function; yet in our series, anatomic resection was safely combined with wedge resection in 11% of patients.

Determining regional lymph node status is important because of the impact of lymph node involvement on survival (see Fig 4). We recommend assessing a patient with pulmonary nodules similar to one with primary lung cancer. Specifically, we have now begun incorporating both mediastinoscopy and lymph node dissection to define metastases to N2 or N3 stations. Patients with metastases in the mediastinum are unlikely to benefit from pulmonary metastasectomy unless lymph node disease can be completely resected.

Although synchronous presentation of the renal primary and pulmonary metastases affects prognosis, it does not in itself preclude operation if complete resection is predicted and can be achieved. Similarly, extrathoracic sites of metastases, if they can be completely resected, do not preclude pulmonary metastasectomy. Disease-free interval and largest nodule size are prognosticators, but should not in isolation affect treatment decisions.

Immunotherapy regimens (preoperative or postoperative) were not associated with improved survival. Accepting an incomplete resection with the hope that adjuvant immunotherapy will complement surgery cannot be supported. Similarly, unresectable pulmonary metastases appear not to be rendered resectable by present induction immunotherapy strategies.

Surgeons must be aware that although multiple factors are independently associated with survival, it is the composite analysis of all factors that yields the most accurate prognostic information. We have provided representative survival curves for groups of patients with three different composites (see Fig 7). The hazard equation generated from this study can be used to predict the outcome of any patient undergoing pulmonary metastasectomy for renal cell carcinoma and thus forms an important component of therapeutic decision making.

	Appendix Variables Used In Analyses

Top Abstract Introduction Patients and Methods Results Comment Appendix Variables Used In... References

 

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Sudish C. Murthy Kwhanmien Kim Thomas W. Rice Malcolm M. DeCamp Eugene H. Blackstone Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Murthy, S. C. Articles by Blackstone, E. H. Search for Related Content PubMed PubMed Citation Articles by Murthy, S. C. Articles by Blackstone, E. H. Related Collections Lung - other