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Ann Thorac Surg 2007;84:973-980
© 2007 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Sarcomatoid Carcinoma of the Lung: A Predictor of Poor Prognosis

Linda W. Martin, MD, MPHa, Arlene M. Correa, PhDa, Nelson G. Ordonez, MDb, Jack A. Roth, MDa, Stephen G. Swisher, MDa, Ara A. Vaporciyan, MDa, Garrett L. Walsh, MDa, David C. Rice, MB, BCha,*

a Department of Thoracic and Cardiovascular Surgery, The University of Texas MD Anderson Cancer Center, Houston, Texas
b Department of Pathology, The University of Texas MD Anderson Cancer Center, Houston, Texas

Accepted for publication March 26, 2007.

* Address correspondence to Dr Rice, Department of Thoracic and Cardiovascular Surgery, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 445, Houston, TX 77030 (Email: drice{at}mdanderson.org).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Sarcomatoid cancer (SARC) of the lung is a rare histologic type of non-small cell lung cancer (NSCLC). Although believed to be associated with poor prognosis, its effect on survival and recurrence has not been well defined. Our goal was to determine the prognostic significance of SARC histology in patients undergoing pulmonary resection.

Methods: We retrospectively evaluated all patients who underwent pulmonary resection for NSCLC during a 20-year period at the University of Texas MD Anderson Cancer Center and compared recurrence and survival rates of patients with SARC with a cohort of patients with typical NSCLC. To account for known prognostic factors such as smoking status, age, gender, pathologic stage, and adjuvant therapy, we used one-to-one matching based on propensity scores.

Results: The study included 63 SARC patients and 1133 NSCLC patients with complete data. Propensity score matching identified 63 NSCLC patients that were similar to the 63 SARC patients from known clinical factors. The 5-year survival for SARC patients was 24.5% compared with 46.3% for NSCLC patients (p = 0.01); median time to recurrence was 11.3 months and 61.4 months, respectively (p = 0.001).

Conclusions: Compared with other histologic subtypes, SARC behaves in an aggressive fashion. These tumors are frequently symptomatic, are locally advanced, and have higher rates of recurrence. Future investigation of novel treatment approaches is warranted. Nonsurgical treatment modalities may be appropriate for patients with clinically advanced disease.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Sarcomatoid carcinoma (SARC) of the lung is defined in the most recent World Health Organization classification as "poorly differentiated non-small cell carcinoma that contains a component of sarcoma or sarcoma-like elements ... [These tumours] represent an overall continuum of epithelial and mesenchymal differentiation" [1]. SARC tumors often occur as part of a heterogeneous lung tumor, rather than a tumor consisting of a pure cell type, and most pathologic series classify lung cancer as SARC when at least 10% of the tumor is composed of a sarcomatoid element based on histologic appearance and tissue marker studies [2].

Sarcomatoid histology is rare and found only in 0.1% to 0.4% of all patients with non-small cell lung cancer (NSCLC) [1]. Its prognostic significance is controversial, with some reports suggesting a poor prognosis [2–10] and others showing no difference between SARC and typical NSCLC [11, 12]. However, most publications on SARC have been small case series focusing on pathologic descriptions [2–5, 8–11, 13–19], with little information about clinical outcomes. The existing literature lacks a stage-adjusted, concurrent comparison of a large series of SARC patients with typical NSCLC patients treated at the same institution. Therefore, the goal of this study was to assess the prognostic significance of SARC versus typical NSCLC by comparing propensity score–matched patients from a single institution for recurrence and survival outcomes.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Study Design
The study was approved by the Institutional Review Board of the University of Texas MD Anderson Cancer Center (UTMDACC), and individual consent for the study was waived. This investigation was designed as a retrospective cohort study. The study population consisted of lung cancer patients who had undergone pulmonary resection at UTMDACC. Patients from this cohort with typical NSCLC were compared with patients from this cohort who had SARC. The end points chosen to evaluate prognosis were recurrence of disease and overall survival after surgical resection.

Patients
An institutional database was used to identify 3574 patients who underwent any form of pulmonary surgical procedure for primary lung cancer at UTMDACC from the beginning of 1984 through June 2003. The study included 1133 patients with complete clinical data available who underwent resection of typical NSCLC and 63 who were identified with a pathologic diagnosis of SARC. NSCLC patients with carcinoid histology as the criterion for primary lung cancer were excluded owing to a better-than-usual prognosis for this subgroup [20] that could overestimate the differences in survival seen when SARC and NSCLC patients were compared.

Most patients were staged preoperatively with chest roentgenogram and computed tomography scan of the chest. Additional staging studies such as mediastinoscopy, brain and bone imaging, and positron emission tomography were performed at the discretion of the surgeon or oncologist. Complete anatomic lung resections were done whenever possible and appropriate. Mediastinal and hilar lymph nodes were sampled or completely dissected, depending on surgeon preference. Pathologic stage was assigned according to the New International Staging System for Lung Cancer [21], irrespective of the staging system in use at the time of surgery.

Patients were followed up with a chest roentgenogram and a clinical visit 1 month postoperatively, then at 6-month intervals for 2 years, and annually thereafter, unless new symptoms prompted more intensive evaluation. Vital status was determined from the medical record and the Social Security Death Index. Demographics, smoking history, comorbidities, clinical and pathologic stage, treatment strategies, operative data, follow-up duration, and survival and recurrence data were collected on all patients.

Pathology
Surgical pathology slides of patients with SARC were reviewed by lung pathologists at UTMDACC to ensure accuracy of histologic diagnosis. In all cases, hematoxylin-and-eosin stained histologic slides and, when available, immunohistochemical preparations were used to confirm the epithelial differentiation (eg, keratin positivity) of the tumor. The diagnosis of SARC was confirmed when at least 10% of the tumor contained a sarcomatoid component consisting of spindle or pleomorphic giant cells, or both.

Data Analysis
Associations between categoric variables were assessed by Pearson {chi}2 or Fisher exact tests. Continuous data were compared using the Student t test and expressed as mean ± standard deviation. Factors associated with SARC histology were identified using multiple logistic regression with Wald stepwise backwards elimination, followed by a test for forward selection.

Because other studies have suggested that SARC occurs more often in heavy smokers and tends to present at a more advanced stage, both of which would confound survival results, we chose to match SARC and NSCLC patients in a one-to-one fashion by using all available clinical data. This was performed by constructing propensity scores [22–24] using all preoperative variables that might influence recurrence and survival, including age, gender, year of operation, pathologic tumor stage (T), nodal stage (N), and metastatic stage (M), preoperative chemotherapy, preoperative radiation, smoking history, timing of smoking cessation, prior cancer, and prior treatment with chemotherapy or radiation. Pair-wise matches were based on the nearest propensity scores. Because of clustering of scores, higher order matching was not done. The propensity-matched NSCLC and SARC subjects (63 in each group) were compared using the McNemar nonparametric test for two-by-two categoric data [25], the marginal homogeneity test for multinomial data [26, 27], and two-sample t test for continuous data.

Survival time was calculated from date of treatment initiation to date of death to avoid biasing survival times against patients receiving preoperative treatment. All-cause mortality was used as the survival end point. Recurrence was calculated from date of treatment initiation to the date of the first documented recurrence. Recurrence and survival curves were calculated using the Kaplan-Meier method [28], and group comparisons were made by using the log-rank test. A value of p ≤ 0.05 was considered statistically significant. All data entry and analyses were performed using SPSS 13.0 software (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Preoperative demographics and comorbidities, treatment factors, and pathologic staging for unmatched SARC and NSCLC patients are listed in Table 1. Median potential follow-up was 63.3 months for all patients. SARC histology was more common earlier in the study period, and SARC patients tended to be a few years younger, have a history of smoking, receive preoperative chemotherapy, experience higher perioperative mortality, and have more advanced pathologically staged tumors by both T and N status compared with unmatched NSCLC patients. Factors independently associated with SARC histology on multivariable logistic regression included a more distant history of smoking, earlier year of treatment, use of preoperative chemotherapy, and more advanced (T3 or T4) pathologic T stage, and more advanced (N3) pathologic N stage (Table 2).


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  		Table 1 Patient Characteristics in Unmatched Groups
 

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  		Table 2 Factors Associated With Sarcomatoid Cancer Histology by Multivariable Logistic Regression Analysis
 
The 3-year and 5-year survival rates for unmatched patients with typical NSCLC were 66.7% and 55.9%; in contrast, the rates for SARC patients were 34.9% and 24.5%, respectively (p < 0.001; Fig 1). Median survival for NSCLC and SARC patients was 79.1 and 17.4 months, respectively.


Figure 1
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  		Fig 1. Survival after treatment initiation for 1133 patients with unmatched non-small cell lung cancer (NSCLC, solid line) and 63 patients with sarcomatoid carcinoma (SARC, dashed line).

 
The SARC patients identified in our study differed from typical NSCLC patients in several factors that could potentially confound survival and recurrence rates. To attempt to compensate for variables other than histology that are known to influence survival, one-to-one propensity matching was performed. When the 63 matched NSCLC controls were compared with the patients with SARC, there were no longer any significant differences for any of the prognostic factors tested except for prior cancer and pathologic T stage. In both of these cases, the control (NSCLC) patients had higher proportions of the risk factors that may affect survival, which would be expected to bias the results towards showing no difference between the two groups for survival outcomes. Otherwise, the two groups were well matched (Table 3). Overall survival for these matched patients is displayed in Figure 2. For control patients with NSCLC, median survival was 80.3 months and 58.9% at 3 years and 46.3% at 5 years, which was significantly better than the respective survival rates for patients with SARC of 17.4 months and 34.9% and 24.5% (p = 0.01).


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  		Table 3 Characteristics for Sarcomatoid Cancer and Non-Small Cell Lung Cancer Patients in Propensity-Matched Groups
 

Figure 2
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  		Fig 2. Survival after treatment initiation in propensity-matched patients with sarcomatoid carcinoma (SARC, dashed line; n = 63) and non-small cell lung cancer (NSCLC, solid line; n = 63).

 
Survival outcomes for the two groups of matched patients were compared stage-by-stage using pathologic stage. The number of patients for each stage is relatively small, limiting statistical strength; however the trends for each stage consistently demonstrated poorer outcomes in SARC (Fig 3A-D). Despite the small numbers, there was a significant difference in median survival for stage III of 10.3 months for SARC versus 25.3 months for NSCLC (p = 0.006).


Figure 3
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  		Fig 3. Survival after treatment initiation in propensity-matched patients with sarcomatoid carcinoma (SARC, dashed line) and non-small cell lung cancer (NSCLC, solid line) for each pathologic stage: (A) I; (B) II; (C) III; (D) IV.

 
Patients with SARC were more likely to present with earlier recurrence as well. Median time to recurrence was 11.3 months for SARC patients, but was 61.4 months for NSCLC-matched controls, which was significantly longer (p = 0.001, Fig 4). The distribution of recurrence sites is listed in Table 4.


Figure 4
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  		Fig 4. Freedom from recurrent cancer for propensity-matched patients with sarcomatoid carcinoma (SARC, dashed line; n = 63) and non-small cell lung cancer (NSCLC, solid line; n = 63).

 

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  		Table 4 Sites of Recurrent Disease in 63 Sarcomatoid Cancer Patients
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
The 63 patients with SARC in our study were similar to those in previously reported series [3–8, 12, 13, 15, 19, 29] with respect to age, smoking history, symptoms, and advanced tumor stage. We did not see a significant gender effect, contrary to a strong male predominance that has been reported in other series. Other authors have documented short median survival of between 8 and 19 months [2, 4, 5, 7, 8, 13, 15, 19] for patients with SARC, suggesting an inferior prognosis to typical NSCLC. However, only some of the patients in these series underwent surgical resection.

Another study that investigated comparative survival for SARC and NSCLC within the same institution was by Nakajima and colleagues [11], who described 37 patients with SARC and compared outcomes with 647 patients who underwent surgical resection for typical NSCLC. No significant differences in survival were found between groups, which is surprising considering 57% of SARC patients were p stage III. Specific survival rates were not described, however, and they did not perform multivariable analysis or stage-matched comparisons.

A study by Pelosi and colleagues [12] examined outcomes of 31 patients with SARC from two separate time periods and from two separate institutions and compared survival of SARC patients with typical survival rates for NSCLC patients, but there was no control group of patients treated under the same circumstances as the SARC patients. Unlike the series we report, only 13% of SARC patients were stage III, and comparisons of survival were limited to patients with early stage disease (p stage I) and were based on cancer-related deaths only. The authors did not identify any significant survival differences, and specific survival rates were not described. Nonetheless, the fact that survival in early stage patients was similar to that of patients with typical NSCLC is interesting.

It has been postulated that the aggressive nature of SARC is at least in part attributable to the sarcomatoid elements, which are believed to develop enhanced angiogenic activity as well as tumor cell motility [12]. The proportion of sarcomatoid elements frequently correlates with tumor size, and it is therefore possible that smaller, earlier-stage tumors may not contain sufficient sarcomatous elements to negatively impact survival rates compared with typical NSCLC.

Unfortunately, these reports are limited in their ability to truly define the prognostic significance of sarcomatoid histology because of confounding variables that prevent accurate survival comparisons to be made between SARC and typical NSCLC groups. We attempted to compensate for known prognostic variables such as pathologic stage, treatment received, age, gender and other factors possibly influencing survival; therefore, the contribution of SARC histology to the biologic tumor behavior can be more accurately determined. We found significantly worse survival and higher recurrence rates associated with SARC histology.

The median survival of patients with SARC was 17.4 months, which is slightly longer than that reported in other published series, even though 43% of patients were stage III or higher. It is possible that this is related to an inherently better prognosis for patients who were fit enough to undergo surgery, but an aggressive multimodality therapeutic approach may have also contributed. Patients in many other series reported in the literature have either been identified from autopsy results or were not uniformly treated with curative intent. However, despite a policy of aggressive treatment for patients with SARC, survival was significantly less than that of stage-matched controls and was particularly poor for patients with SARC of advanced clinical stage. There were no 5-year survivors among patients with tumors of p stage III or greater.

Compared with patients with typical NSCLC, both local and distant recurrence rates were high in SARC patients. Although the benefit of postoperative radiation therapy has not been shown to improve survival for patients with typical NSCLC, that 27% of recurrences occurred locally in the chest wall argues strongly for its use in cases where tumors invade the parietal pleura or chest wall.

There are little published data on the use of adjuvant chemotherapy in patients with SARC. Raveglia and colleagues [7] described 14 patients with p stage II or III SARC who underwent resection, followed by cisplatin-based chemotherapy. Median survival was 7 months versus 26 months for 6 patients with stage I disease who did not receive adjuvant therapy. Because the efficacy of adjuvant chemotherapy has been documented for patients with NSCLC stage IB or higher [30–32], and 87% of patients in our series who recurred did so at distant sites (52% overall), it seems prudent to consider the use of adjuvant chemotherapy after resection. Preoperative chemotherapy or radiation therapy was administered to 28% and 30% of matched SARC and NSCLC patients, respectively. Because of the small sample size, their contribution to outcome is uncertain, however. In addition, the ability to apply a preoperative regimen depends upon the diagnosis of SARC histology being made before the surgical procedure. In practice, this is frequently not possible, either because not all lung masses are routinely biopsied preoperatively or because of tumor sampling error.

This study has several limitations that must be considered when interpreting the results. Being a retrospective study, it is subject to inherent biases of patient selection, therapeutic decision-making, and variations in quality of recorded data. It is certainly possible that a greater proportion of patients with advanced SARC were referred to our tertiary referral center for care; however, by performing propensity scoring, we attempted to compensate for this potential imbalance. This study included only patients who underwent a surgical procedure, therefore excluding what are likely to be more advanced stage patients. There may be a disparity in nonsurgical patient distribution in the two groups, and our study design does not allow us to determine this distribution.

A retrospective, histologic review of pathology from the control NSCLC patients was not performed. It is therefore possible that some patients with SARC histology were misclassified in the NSCLC group. However, if this were the case, we would expect a reduction in the observed differences in survival and recurrence between groups.

Finally, because of the rarity of SARC, our sample size is small, thus limiting generalizability. Nevertheless, it would be difficult to obtain a larger sample size of SARC patients unless data from multiple institutions were pooled.

In summary, in patients undergoing surgical resection for NSCLC, the SARC histologic variant is associated with significantly worse prognosis, both for long-term survival and for early recurrence of disease. Use of adjuvant chemotherapy and radiation should be considered for patients with bulky tumors, chest wall invasion, or nodal involvement because of the high incidence of both local and distant failure after resection. For patients with stage III or IV SARC tumors identified preoperatively, nonoperative treatment may be appropriate given the poor outcomes with surgical resection in advanced stage patients.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Dr B. Nebiyou Bekele, PhD, Department of Biostatistics and Applied Mathematics, The University of Texas MD Anderson Cancer Center, for his assistance with propensity score matching. We also thank Drs Craig L. Hanis, PhD, and David Lairson, PhD, University of Texas at Houston School of Public Health, for their critical review of this project.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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