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Original Articles: General Thoracic

Temporal Trends in the Management of Potentially Resectable Lung Cancer

^a Surgical Outcomes Research Center, University of Washington, Seattle, Washington
^b Division of Cardiothoracic Surgery, Department of Surgery, University of Washington, Seattle, Washington
^c Department of Biostatistics, University of Washington, Seattle, Washington
^d Division of General Surgery, Department of Surgery, University of Washington, Seattle, Washington

Accepted for publication December 18, 2007.

^_* Address correspondence to Dr Flum, Department of Surgery, University of Washington, 1959 NE Pacific, Box 356410, Seattle, WA 98195-6310; (Email: daveflum{at}u.washington.edu).

Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.

	Abstract

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
Background: Standardized, evidence-based guidelines recommend lung resection for patients with stage I or II nonsmall-cell lung cancer (NSCLC), and select patients with stage IIIA disease. We hypothesized that the proportion of patients operated on would increase over time coincident with increasing adherence to practice guidelines and improved patient/provider education over time.

Methods: This investigation was a cohort study of tumor-registry data linked to Medicare claims.

Results: Between 1992 and 2002, 24,030 patients—mean age 75 ± 6 years, 55% men—were diagnosed with NSCLC. In each stage, the proportion of patients undergoing resection was lower in 2002 compared with 1992: stage I (68% versus 80%, p < 0.001), II (59% versus 74%, p < 0.001), and IIIA (23% versus 35%, p < 0.001). The mean age and comorbidity index of the cohort was higher in 2002 compared with 1992 (76 versus 74 years, p < 0.001; and 0.47 and 0.82, p < 0.001, respectively). The unadjusted odds of resection decreased by 6% per year (odds ratio 0.94, 99% confidence interval: 0.93 to 0.95), and adjustment for age, comorbidity index, race, and stage resulted in a slightly smaller (4% per year) but significantly decreasing trend in operative management over time (odds ratio 0.96, 99% confidence interval: 0.95 to 0.97).

Conclusions: Unexpectedly, the use of resection for lung cancer has decreased dramatically over time, and this decline is not fully accounted for by an older cohort with more comorbid conditions. Future investigations should determine whether increasing unmeasured contraindications to resection, barriers to accessing specialty care, an inadequate supply of thoracic surgeons, or bias against operative therapy are responsible.

	Introduction

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Lung cancer is the leading cause of cancer death and second most common malignancy in the United States [1]. Treatment requires the coordinated expertise of surgeons, medical and radiation oncologists, pulmonologists, and radiologists. Given the complexity of thoracic oncologic care, it is not surprising that some have found evidence of suboptimal health care delivery among lung cancer patients [2–4]. Various organizations have attempted to standardize care through the use of evidence-based practice guidelines [5–7]. As a result, well-defined treatment algorithms now exist for managing non-small cell lung cancer (NSCLC). All guidelines recommend lung resection as optimal therapy for stage I or II cancer, and include resection for select patients with stage IIIA disease.

Greater adherence to treatment guidelines and better patient and provider education would be expected to result in an increasing proportion of patients undergoing resection over time. Yet lung cancer patients are increasingly older and have more comorbid conditions, and there is concern that some providers may deny older and sicker patients a lung resection. Additionally, race may be a barrier to optimal management, with at least one study finding that black patients are less likely to receive resection for early-stage disease [8]. It is unknown if racial disparities have changed over time. We hypothesized that the use of resection has increased over time, and planned to explore whether potential changes in age, race, and comorbidity over time have impacted temporal trends in optimal management.

	Material and Methods

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A cohort study was conducted using the Surveillance, Epidemiology, and End-Results (SEER)–Medicare database to evaluate the management of patients diagnosed with stage I, II, or IIIA NSCLC between 1992 and 2002. The SEER database is tumor registry sponsored by the National Cancer Institute capturing roughly 14% to 25% of incident tumors in the United States. Medicare beneficiaries within the registry have had their tumor records linked to all their claims data. The quality, validity, generalizability, and use of data within SEER-Medicare are well established and described elsewhere [9–13]. The University of Washington Institutional Review Board approved this study and waived consent.

Among 221,369 lung cancer patients, the following sequential exclusions were made: patients diagnosed at death or autopsy (n = 5,128), age less than 66 years (n = 33,537), histology other than NSCLC (n = 66,870), diagnosis of a second malignancy within 6 months after lung cancer diagnosis (n = 3,274), partial fee-for-service or concurrent health maintenance organization enrollment, or both, in the year before or 6 months after diagnosis (n = 35,327), and patients with stage IIIB/IV disease or those with missing stage information (n = 53,203). Data were not available for lung cancer patients less than 65 years old who were not Medicare beneficiaries. To increase the generalizability of findings to elderly lung cancer patients, we excluded Medicare beneficiaries younger than 65 because they were either disabled, had end-stage renal disease, or both. Patients who were 65 years old at the time of diagnosis were excluded because they did not have claims in the year before diagnosis, and our method of calculating comorbidity index requires claims during that period [14]. Because we used claims to define therapy, we excluded patients with a second malignancy to avoid misclassifying lung cancer care with care for another malignancy. Only full fee-for-service beneficiaries not enrolled in other insurance programs would have complete claims records, and thus all other patients were excluded.

Resection was defined using the Healthcare Common Procedure Coding System (HCPCS) within the Carrier Claims file. Radiation therapy and chemotherapy were ascertained using HCPCS within the Carrier Claims or HCPCS, The International Classification of Diseases, 9th Revision (ICD-9) procedure codes, or both, and Revenue Center codes (RCCs) within the Outpatient Claims files. The Appendix provides a summary of these codes, all of which were in use at some time during, if not for the entire, study period. A modified Charlson comorbidity index was calculated using ICD-9 codes within both the Carrier and Outpatient claims in the year before diagnosis [14]. Stage of disease was classified according to the sixth edition of the American Joint Committee on Cancer. Ascertainment of stage and histology were dependent on the highest level of information within 4 months of diagnosis, including information obtained at the time of operation.

	Results

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
Overall, 24,030 patients with potentially resectable NSCLC met the inclusion criteria. Table 1 summarizes patient and tumor characteristics for the overall cohort as well as changes in these characteristics over time. Over the study period, the average age of the cohort increased by 2 years and there were 20% fewer patients with a comorbidity index of zero. Other notable changes were a 19% decrease in proportion of patients in the lowest income quartile, and significant changes in the distribution of geographic area. Increases in patients in the western states and rural areas were likely due to one expanding and three new SEER registries in 2000. The distribution of blacks did not change comparing distributions in 2002 and 1992 (7.7% versus 6.5%; p = 0.12).

View larger version (10K): [in this window] [in a new window]   Fig 1. Stage-based trends in lung resection over time.

	Comment

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

Several factors may explain the observed decline in operative management. Lung function is a strong determinant of therapy [15]. Although it is unknown whether the severity of underlying emphysema among lung cancer patients has changed over time, an increase in the prevalence of prohibitively low lung function might explain a decline in the use of resection. Increasing barriers to accessing appropriate care may provide another explanation. Certain providers appear to deliver higher quality surgical care, as evidenced by the associations between provider type and short- and long-term outcomes [16–20]. Although all patients in our sample had health insurance, their ability to access thoracic surgeons and comprehensive cancer centers was not known and cannot be determined using this dataset. Lung cancer treatment guidelines recommend that appropriate surgical consultation consists of review by "thoracic surgical oncologists who perform lung cancer surgery as a prominent part of their practice" [5]. It is not known whether the supply of specialists in general thoracic surgery has changed over time to meet the demands of lung cancer patients and nonsurgical providers. Appropriate referrals are another determinant of accessing thoracic surgeons. Survey data suggest that provider type (surgical versus nonsurgical), years since completing training, and case load influence beliefs regarding appropriate treatment and expected survival for lung cancer patients [21]. Lack of specialty training in thoracic surgery, low volume experience in thoracic surgery, or lack of experience in managing higher risk patients or complex resections may result in patients being declined appropriate surgical resection where they may have been a candidate for surgery in another center or with another surgeon. Differing views of optimal management may impact surgical referrals. Nonsurgical specialists may be reluctant to refer a patient for appropriate surgical consultation for a variety of reasons, including negative perceptions about surgical morbidity or cancer survival, misunderstanding of practice guideline recommendations, remunerative benefits of nonsurgical therapy, or lack of an adequate partnership with a legitimate thoracic surgical oncologist. Finally, our study spanned a period before and after publication of the earliest practice guidelines [6, 7]. As we found no evidence that temporal trends in operative management were impacted by these and subsequent guidelines, it raises a question about the effectiveness of practice guidelines on physician behavior.

It appeared that advancing age and an increasing burden of comorbid conditions accounted for a fraction of the declining trend in operative management over time. Several investigations have shown an acceptable level of perioperative risk after resection for lung cancer among select elderly patients [22–28], supporting the notion that age alone is not a contraindication to therapy. The number, type, and severity of comorbidities appear to be associated with higher morbidity and lower survival among resected patients [29–33], and yet it is debatable whether that risk sufficiently outweighs the benefits of resection. Disentangling the effects of age, comorbidity, and other preoperative predictors of outcome is challenging and requires a multidisciplinary team that includes an experienced thoracic surgeon. If providers limit referrals and surgical options on the basis of age and comorbidity alone, then there may be an opportunity to improve the quality of care through further education, advocacy, and encouraging the expansion of multidisciplinary teams that include a experienced thoracic surgical oncologist.

These findings must be considered in the context of several important limitations. Our analysis was limited to elderly, Medicare beneficiaries with full fee-for-service coverage and no concurrent health maintenance organization enrollment. If patterns of care were different for younger patients and those under different insurance plans, then our findings may not be generalizable. Theoretically, our exclusion criteria could have biased our results. We concluded that any such bias was unlikely because a sensitivity analysis revealed decreasing rates of resection over time in an cohort without exclusions and among the subgroup who were excluded. Our exclusions were necessary because they allowed for adjustment for comorbid conditions and a description of all modes of therapy, including chemotherapy. Another limitation is that the modified Charlson comorbidity index has not been validated for measuring temporal trends in comorbid conditions. It is possible that better coding over time has resulted in an apparent increase in comorbidities over time. Furthermore, this index does not measure the severity of underlying disease, and therefore we may not have sufficiently accounted for the relationship between comorbidity and the receipt of optimal therapy. It would have been preferable to measure well-established determinants of resection, such as pulmonary function, but these data were not available in SEER-Medicare. Because the stage of disease was based on the highest level of information within 4 months of diagnosis, it is possible that differential accuracy of staging by treatment (operative versus nonoperative) might have biased our results. Some patients with clinical stage I, II, or IIIA were likely upstaged to stage IIIB/IV as a result of intraoperative findings. These patients would have been excluded from our analysis. Such exclusions would bias our results if the rate of intraoperative upstaging to stage IIIB/IV increased over time. Yet, it is more likely that intraoperative upstaging has decreased over time as a result of better pretreatment staging (namely, with positron emission tomography) and patient selection. Finally, 7.3% of our cohort had missing covariate data, possibly biasing our findings; however, the proportion of missing data did not appear to change over time (5.9% in 2002 versus 5.7% in 1992, p = 0.79) nor were differences in the proportion of missing variables between operated and nonoperated patients clinically important (7.0% versus 7.8%, p = 0.02).

To the extent to which our results our generalizable, it is important to consider the implications of our findings in absolute rather than relative terms. Current estimates forecast 213,380 new cases of lung cancer in the United States in 2007 [1]. According to SEER estimates, 80% will have NSCLC and of those, 33% will have stage I, II, or IIIA disease for a total of 56,332 patients with potentially resectable NSCLC. A conservative estimate of the proportion of resected cases in 2007 would be the proportion of resected cases in 2002 (57%). Accordingly, 32,109 patients would be expected to undergo resection in 2007. Had the proportion of resected cases remained constant at levels observed in 1992 (70%), then 39,433 patients would be expected to undergo resection in 2007. The difference between these two estimates suggests that up to 7,323 patients might not receive appropriate therapy in 2007. Assuming that all 7,323 patients would otherwise be eligible for resection, and an operative mortality rate of 5.2% [2], 6,870 lives that could be saved in 2007 would unnecessarily be lost.

Ultimately, change in therapy over time is important if it results in change in outcomes over time. Overall mortality rates for lung cancer have been declining since 1992 [1], suggesting perhaps that the declining trend in operative therapy is inconsequential. However, these improvements in outcome have been attributed to smoking intervention programs that prevent lung cancer [34]. Other potential reasons for improved overall mortality rates include improvements in patient and treatment safety, earlier incidental detection of lung cancer associated with the increasing use of computed tomography for other indications, better staging with subsequent stage migration effect, and new institution of adjuvant therapy for resected lung cancer. Supporting this view is the observation that the overall mortality rates for all cancers combined have improved over the same period as lung cancer [35]. Since lung resection is widely considered primary therapy with curative intent, it will be important to reverse the declining trend in resection to further improve lung cancer outcomes.

In conclusion, the optimal care of potentially resectable lung cancer patients appears to be diminishing rather than improving over time. Future studies should aim to identify factors responsible for this trend, and provide information on how to improve access to appropriate thoracic surgical care and adherence to lung cancer practice guidelines.

	Discussion

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
DR KEITH S. NAUNHEIM (St. Louis, MO): Thank you, Dr Wood, Dr Mayer. I have no conflicts. I would like to congratulate Dr Farjah and his colleagues on this paper, which is both provocative and somewhat troublesome. It demonstrates a heretofore unrecognized and potentially dangerous trend in the treatment of lung cancer, the most common lethal malignancy in America. While surgical resection is inappropriate therapy for the majority of patients presenting with lung cancer, for those lucky few presenting with limited disease, it is the cornerstone of therapy and maximizes the patient's chance for cure. The notion that this time-tested and proven modality is being routinely underutilized is a chilling one. If these investigators' findings prove to be valid, then thousands of patients with lung cancer are being inadequately treated and placed unnecessarily at risk for tumor recurrence and death.

This is not a wholly new phenomenon for cardiothoracic surgeons. One has only to read last week's New England Journal article reviewing the New York State experience with percutaneous coronary intervention and coronary artery bypass graft surgery. Over the last decade, there has been consistently inappropriate management of complex coronary artery disease using coronary stents in an off-label fashion. One can argue whether the underlying cause is economic incentive, inadequate patient counseling, or just plain ignorance on the part of the referring physicians. The fact remains that thousands of patients across the country are being systematically treated inadequately, often because their physician wants to save them from the trauma of surgery.

A similar situation exists in the general thoracic surgery area. In 2002, the initial clinical results of the National Emphysema Treatment Trial were published. This was a randomized trial comparing lung volume reduction surgery to medical management in patients with end-stage emphysema. The trial demonstrated that significant and clinically remarkable improvements could be demonstrated in quality of life, exercise capacity, and long-term survival. It identified specific subgroups that benefited from the operation, and these patients comprise 60% of all randomized patients. If one applied the same selection criteria to the emphysema population at large, literally tens of thousands of patients are likely to benefit and should be referred for consideration of lung volume reduction surgery. Yet in 2004, the first full year after publication of this study, Medicare reported only 247 patients undergoing lung volume reduction. The following year, in 2005, it was worse, at 233 lung volume reduction procedures. Thus, we as a specialty have witnessed the inappropriate underutilization of thoracic surgical procedures that would in fact likely save many patients' lives. The motivation behind this behavior is likely multifactorial and may include physician ignorance, patient's reluctance to undergo surgery, poor access to specialty care, and economic incentives on the part of both physicians and industry.

This presentation should serve as a wake-up call to what may prove to be yet another systematic underutilization of potentially curative surgical procedures. Of course, caution is warranted in interpreting these data and drawing conclusions.

This manuscript involved analysis of the SEER-Medicare database. This links clinical information regarding tumor type and stage with an administrative database designed primarily for the collection and analysis of billing information. Our own Society's experience comparing the STS clinical database to the Medicare administrative database suggests that any conclusions derived solely from administrative data must be viewed with some caution owing to the inherent limitations of such data. Indeed, it has become clear that utilization of an administrative database for the purpose of making clinical decisions is fraught with hazard. However, for many large populations studies, administrative databases such as that maintained by Medicare are the only available source for information and its utilization by these investigators was certainly appropriate. With these limitations in mind, I have three questions for Dr Farjah.

First, while it is true that comorbid conditions may contraindicate resection, your risk analysis suggests that comorbidities cannot completely account for the decrease in lung resection over the decade. As you know, listing these comorbidities is usually the work of medically unsophisticated clerical personnel and often such listings are rife with error. In addition, the listing of a comorbid condition tells us little or nothing regarding the severity of that disease. How confident can one be regarding the risk analysis built on such a foundation?

Second, is it possible that progressively more accurate preoperative staging occurred over time with the addition of more positron emission tomography scans or helical computed tomography scans? Such scans allow for the identification of subtle but advanced regional or distant metastatic disease which may preclude surgery. A progressively increasing utilization of such technology over this time could lead to progressively decreasing incidence of resection. Did you or could you correct for such testing in your risk analysis?

And lastly, where do we go from here with this new and alarming study? All such studies require confirmation, so how do we as a specialty go about trying to confirm these observations? Just as importantly, if we can confirm the validity of the observation, how do we as a specialty begin addressing this problem? Pay for performance is one option, but how do we go about educating the other specialties and primary care physicians so that they can make more appropriate referrals?

Once again, this is a remarkably interesting paper that should serve as a red flag to our speciality. I would like to congratulate the investigators on their work and thank them for sending the manuscript in advance of their presentation. I would also like to thank the Society for the privilege of reviewing this work. Thank you.

DR FARJAH: Thank you for your comments, Dr Naunheim. Regarding your first question about the confidence of the risk adjustment for comorbidities, you point out key limitations. You have highlighted that the severity of the comorbid conditions could not be accounted for. In time, we saw an increase in comorbidity, and that too certainly may have been an artifact of better coding. So it remains a possibility that the decrease in rates of resection may be due to an increasing proportion of patients with legitimate contraindications to surgery.

As for preoperative staging, our cohort was restricted to patients who were determined to have stage I, II, or IIIA lung cancer. Better preoperative staging over time might in fact lead the surgeon to have greater confidence in their decision to perform pulmonary resection. Patients who were upstaged as a result of better preoperative staging were excluded from our analysis.

In regard to your third question, I think that the challenge in thoracic oncology is that care involves many different types of providers. It will take more than the involvement and interest of thoracic surgeons. It will take the involvement of all stakeholders, whether it is other providers, patient, or payers. I think for groups of surgeons, such as those in this Society, advocacy is important. In terms of the individual thoracic surgeon I believe, as you have already mentioned, that reaching out to the community is important, educating patients, nonsurgical providers, and the so-called gatekeepers of lung cancer patients.

	Appendix

 

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
This study used the linked Surveillance, Epidemiology, and End Results (SEER)–Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the Applied Research Program, National Cancer Institute; the Office of Research, Development and Information, CMS; Information Management Services (IMS), Inc.; and the SEER program tumor registries in the creation of the SEER-Medicare database. Farhood Farjah was supported by a Cancer Epidemiology and Biostatistics Training Grant (T32 CA09168-30) and Ruth L. Kirschstein by a National Research Service Award (F32 CA130434-01) from the National Cancer Institute. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health. The authors are also grateful for additional resources made available through the University of Washington's Department of Surgery and the Surgical Outcomes Research Center, and the generosity of the Schilling Family.

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Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 

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