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Originally published as JCO Early Release 10.1200/JCO.2005.02.1758 on December 19 2005 © 2006 American Society of Clinical Oncology. The Effect of Race on Invasive Staging and Surgery in Non–Small-Cell Lung CancerFrom the Division of Population Sciences, Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA Address reprint requests to Craig C. Earle, MD, MSc, FRCPC, Center for Outcomes and Policy Research, Dana-Farber Cancer Center, 44 Binney St, 454-STE 21-24, Boston, MA 02115; e-mail: craig_earle{at}dfci.harvard.edu
Purpose: Black patients with early-stage non–small-cell lung cancer (NSCLC) have worse overall survival than white patients. Decreased likelihood of resection has been implicated. To isolate the effect of decision making from access to care, we used receipt of surgical staging as a proxy for access and willingness to undergo invasive procedures, and examined treatments and outcomes by race. Patients and Methods: We examined registry and claims data of Medicare-eligible patients with nonmetastatic NSCLC in areas monitored by the Surveillance, Epidemiology, and End Results program from 1991 to 2001. Patients who obtained invasive staging, defined as bronchoscopy, mediastinoscopy, or thoracoscopy, were included. Logistic regression and Cox modeling calculated the odds of having staging and surgery, and survival outcomes. Results: A total of 14,224 patients underwent staging, and 6,972 had surgery for lung cancer. Black patients were less likely to undergo staging (odds ratio [OR] = 0.75; 95% CI, 0.67 to 0.83), and once staged, were still less likely to have surgery than whites (OR = 0.55; 95% CI, 0.47 to 0.64). Survival for blacks and whites was equivalent after resection (hazard ratio = 1.02; P = .06). Staged black patients were less likely to receive a recommendation for surgery when it was not clearly contraindicated (67.0% v 71.4%; P < .05), and were more likely to decline surgery (3.4% v 2.0%; P < .05). Conclusion: Black patients obtain surgery for lung cancer less often than whites, even after access to care has been demonstrated. They are more likely not to have surgery recommended, and more likely to refuse surgery. Additional research should focus on the physician-patient encounter as a potential source of racial disparities.
Lung cancer is the leading cause of cancer mortality in the United States, with 157,000 deaths each year.1 During the last 40 years, there has been a decrease in lung cancer incidence and mortality in all races; however, a significant differential in outcomes between black and white patients remains; both incidence and mortality rates are highest in black men.2 Previous investigators have found that black race was a negative predictor of obtaining curative surgery for early-stage lung cancer and chemotherapy for metastatic disease.3,4 It has been suggested that some of the disparities in early-stage lung cancer survival are related to the gap in obtaining potentially curative surgery.3 Invasive staging, which can include mediastinoscopy, bronchoscopy, and thoracoscopy, is usually part of the evaluation of non–small-cell lung cancer (NSCLC).5,6 It is also a marker of access to health care and a crude indication of willingness and ability to undergo invasive procedures. If access to care or willingness to accept surgery are the main reasons for observed disparities, as has been suggested,7 then disparities should not be apparent among a group of patients who have undergone invasive staging. Therefore, we have undertaken this analysis of the racial determinants of care among staged patients to evaluate whether disparities in treatment and outcomes still exist when these factors are controlled for in this way.
Data Sources Patients from 11 tumor registries participating in the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) Program were studied. The registries capture 97% of the incident cases,8 covering a nearly representative sample of 14% of the population in the United States.9 The registries collect data on patient age, sex, race, ethnicity, cancer site, stage, histology, and dates of death and diagnosis. Medicare claims, both inpatient and outpatient, have been linked to SEER for patients aged 65 and older.10 Census-level demographic data have been linked to these patients as well.
Cohort Selection
Identification of Staging and Surgical Procedures
Definition of Explanatory Variables
Statistical Methods
Patient Selection From an initial cohort of 21,219 patients, 14,224 patients underwent invasive staging: 13,030 (91.6%) white, and 1194 (8.4%) black. Table 1 shows the characteristics of the patients who underwent invasive staging by race. The most common histology for both races was squamous cell, followed by adenocarcinoma. The most common staging procedure in this cohort was bronchoscopy followed by mediastinoscopy. More black patients had bronchoscopy than white patients, and more white patients had mediastinoscopy and thoracoscopy. Black patients had a younger median age compared with white patients, and a much lower median income. Some patients had more than one surgical and/or staging procedure. In these patients, the most aggressive procedure is reported.
Likelihood of Obtaining Staging We evaluated the odds of patients obtaining any of the aforementioned staging procedures, while controlling for known confounders by logistic regression modeling. As listed in Table 2, black race (odds ratio [OR] = 0.75; 95% CI, 0.67 to 0.83) and older age significantly decreased the odds of obtaining an invasive staging procedure. Being treated in a teaching hospital, having stage II disease, and living in the South or the Mountain region all significantly increased the likelihood that the patients would obtain invasive staging. Notably, comorbidity, socioeconomic status, sex, and having stage III disease did not affect the likelihood of undergoing invasive staging.
Evaluation of Staged Patients We next examined the likelihood of surgery among staged patients (Table 3). Black race remained a powerful negative predictor of having surgery (OR = 0.55; 95% CI, 0.47 to 0.64). Increasing age, Charlson score, stage III disease, other race, female sex, and living in the Midwest and Mountain regions were also significant negative predictors. Being treated in a teaching hospital and having stage II disease were significantly positively associated with having surgery once staged. For sensitivity analysis we performed an additional analysis using the same logistic regression model on a cohort restricted to patients who obtained mediastinoscopy (data not shown). Black race remained a negative predictor of having surgery (OR = 0.58; 95% CI, 0.37 to 0.90).
Kaplan-Meier and Cox regression analyses demonstrated no statistically significant difference in survival between black and white patients who underwent surgery. The median survival for black patients who underwent a surgical procedure was 1,045 (95% CI, 888 to 1,248 days) v 1,109 days (95% CI, 1,077 to 1,157 days) for white patients. The adjusted hazard ratio for black patients was 1.02 (P = .06). Similarly, there was no difference in survival among those who did not have a surgical procedure; median survival for black patients was 246 (95% CI, 221 to 271 days) v 248 days for whites (95% CI, 226 to 271; log-rank P = .46). The hazard ratio for black race was nonsignificant (1.07; P = .09).
Reasons Cancer-Directed Surgery Was Not Performed
Our study, the first to examine the role of invasive staging in obtaining surgery for early-stage lung cancer, had many interesting findings. Black patients had invasive staging in the work-up of their lung cancer significantly less than white patients, when controlling for known confounders. Even when black patients had invasive staging, they remained far less likely than their white counterparts to have potentially curative surgery. Similar treatment resulted in similar outcomes, however. Review of the reasons that surgery was not performed indicated that black patients had surgery recommended less often than whites and also refused surgery more than white patients. The importance of invasive staging in lung cancer as a necessary part of the clinical assessment is well documented.5,15 Current recommendations advise the use of mediastinoscopy in addition to computed tomography scanning for patients with possibly operable NSCLC.6 Mediastinoscopy and bronchoscopy are the most common methods of obtaining staging and diagnosis information; however, thoracoscopy is used in certain situations as well.5,16 [18F]fluorodeoxyglucose positron emission tomography recently has been shown to be a valuable tool in staging for NSCLC.17,18 The SEER-Medicare database as of 2001 did not have a billing code for positron emission tomography imaging, and thus this modality could not be used in our analysis. Our aim in this study was to use staging as a proxy for access to health care, but also as a measure of the willingness and ability of the patient to undergo an invasive medical procedure. To obtain invasive staging, the patient needed to be seen by a specialist and then must have consented to an invasive staging procedure. The low frequency of mediastinoscopy is a potential concern—it suggests that many patients are not finding their way to the thoracic surgeons. This trend is exacerbated for black patients. Given this concern, subset analysis was performed on the patients obtaining mediastinoscopy. Our findings were unchanged. Therefore, our findings are not dependent on which specialist performs the staging procedures (pulmonologist or surgeon). Our finding that black patients obtained invasive staging less than white patients with comparable disease and comorbidities is consistent with other studies in this field.3,4,19,20 Studies in other medical fields have depicted disparities in the use of health care as well.21-23 Thus, the finding that black patients with nonmetastatic lung cancer are not staged at the same rates as their white counterparts is yet another example of racial disparities in health care. Although the observation that black patients obtained staging less than white patients was consistent with our initial hypothesis; the recognition that even when black patients did have staging, they did not have surgery at the same rate as white patients with comparable disease was a new observation. Given the marked difference in surgery between the races even when controlling for known confounders such as age, region, stage, and comorbid disease, the fact that staging did not ameliorate this result indicates that there is some selection factor occurring after the patient has demonstrated access to care, obtained a referral to a specialist, and shown willingness and ability to undergo an invasive medical procedure. Although our race category designated other is heterogeneous, those defined as other also obtained surgery less often than white patients. The most powerful negative predictor of surgery, as expected, was having stage III disease. The presence of comorbid disease did not significantly affect obtaining a staging procedure. For surgery however, comorbid disease was predictive, as we had expected. Region also seemed to have an effect on surgery in our model, but even in the face of these qualifiers, race remained a powerful negative predictor of obtaining surgery in our cohort. Starting with a population-based cohort with uniform insurance and examining only patients who had staging indicates that the racial effect possibly is happening at the level of the patient-physician encounter. The findings in Figure 1, that black patients were indeed having surgery recommended less often than whites and were refusing surgery at a higher rate, further supports this hypothesis. The exact reason that surgery was not recommended or was refused is not known, however. It has been proposed by some that black patients either refuse surgery because of an unclear understanding of the disease process24 or they present with symptoms that preclude surgery.7 Some have also suggested that black patients are simply not being referred to the appropriate specialist who would give adequate care.19,22 A recent study used SEER data during a 1-year period to show a wholesale decrease in therapy when blacks are compared to whites for surgery and chemotherapy.20 Clearly, the problem of racial disparities is multifactorial, including access to care, poor primary care, and perhaps some elemental mistrust of the medical system.23-25 There are some limitations to our study. Procedure codes can suffer from coding error, leading to over- or underestimation of procedure rates. In addition, comorbidity adjustment using administrative data might miss some relevant factors that physicians use in choosing who is appropriate for surgery or who would tolerate surgery,13,26 and is not a proxy for performance status. There may be other patient-specific factors or findings on invasive staging that may affect subsequent decisions. In addition, the greatest racial difference in morbidity and mortality in lung cancer occurs in younger age groups.2 Medicare generally only covers patients older than age 65, however; therefore, we are unable to comment on the care of younger patients. In addition, we had to exclude any patients who were enrolled in a health maintenance organization, and these patients may have different patterns of care. There is no clear reason to think that these limitations would differentially affect decisions for black and white patients, however. Black patients do not have surgery for early-stage lung cancer at the same rate as white patients with similar stage disease and comorbidity. They are less likely to be staged, and even when staged, they are still less likely than white patients to have surgery. When they do receive surgery, their survival experience is similar to that of whites. Black patients have surgery recommended significantly less often than white patients, and are also refusing surgery more often. More attention should be paid to the physician-patient encounter that leads to the decision to have surgery, to examine whether patient and provider expectations and biases affect medical decision making in lung cancer. Efforts must continue to ensure the appropriate quality care is available for all patients, regardless of race and ethnicity.
The authors indicated no potential conflicts of interest.
Presented in part at the 39th Annual Meeting of the American Society of Clinical Oncology, Chicago, IL, May 31-June 3, 2003. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
1. American Cancer Society: Cancer Facts and Figures 2003. American Cancer Society, 2003 2. Stewart J: Lung cancer in African Americans. Cancer 91:2476-2481, 2001[CrossRef][Medline] 3. Bach PB, Cramer CL, Warren JL, et al: Racial differences in the treatment of early-stage lung cancer. N Engl J Med 341:1198-1205, 1999 4. Earle C, Venditti LN, Nuemann PJ, et al: Who gets chemotherapy for metastatic lung cancer? Chest 117:1239-1246, 2000 5. Mentzer S, Swanson SJ, DeCamp MM, et al: Mediastinoscopy, thoracoscopy and VATS in the diagnosis and staging of lung cancer. Chest 112:239S-241S, 1997 (suppl 4)[Medline] 6. National Comprehensive Cancer Network: Clinical Practice Guidelines in Oncology v. 1.2004 Non Small Cell Lung Cancer, 2004 http//:www.nccn.org/professionals/physician_gls/PDF/nscl.pdf 7. Blackstock AW, Herndon JE III, Paskett ED, et al: Outcomes among African-American/Non-African American patients with advanced non small cell lung carcinoma: Report from the Cancer and Leukemia Group B. J Natl Cancer Inst 94:284-290, 2002 8. Zippin C, Lum D, Hankey BF: Completeness of hospital cancer case reporting from the SEER program of the National Cancer Institute. Cancer 76:2343-2350, 1995[CrossRef][Medline] 9. Nattinger AB, McAuliffe T, Schapira MM: Generalizability of the Surveillance, Epidemiology and End Results Registry population: Factors relevant to epidemiologic and health care research. J Clin Epidemiol 50:939-945, 1997[CrossRef][Medline] 10. Potosky AL, Riley GF, Lubitz JD, et al: Potential for cancer related health services research using a linked Medicare-tumor registry database. Med Care 31:732-748 1993[Medline] 11. Charlson ME, Pompei P, Ales KL, et al: A new method for classifying prognostic comorbidity in longitudinal studies: Development and validation. J Chronic Dis 40:373-383, 1986[CrossRef] 12. Deyo RA, Cherkin DC, Ciol MA, Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 45:613-619, 1992[CrossRef][Medline] 13. Kalbunde C: Development of a comorbidity index using physician claims data. J Clin Epidemiol 53:1258-1267, 2000[CrossRef][Medline] 14. Krieger N: Overcoming the absence of socioeconomic data in medial records: Validation and application of a census-based methodology. Am J Public Health 82:703-710, 1992 15. Sihoe AD, Yim AP: Lung cancer staging. J Surg Res 117:92-106, 2004[CrossRef][Medline] 16. Toloza E, Harpole L, Detterbeck F, et al: Invasive staging of non-small cell lung cancer. Chest 123:157-166, 2003 (suppl)[CrossRef] 17. Detterbeck FC, Falen S, Revera MP, et al: Seeking a home for PET: Part 2. Defining the appropriate place for positron emission tomography imaging in the staging of patients with suspected lung cancer. Chest 125:2300-2308, 2004 18. Lardinosis D, Weder W, Hany TF, et al: Staging of non-small-cell lung cancer with integrated positron-emission tomography and computed tomography. N Engl J Med 348:2500-2508, 2003 19. Earle CC, Neumann PJ, Gelber RD, et al: Impact of referral patterns on the use of chemotherapy for lung cancer. J Clin Oncol 20:1786-1792, 2002 20. Potosky AL, Saxman S, Wallace RB, et al: Population variations in the initial treatment of non-small cell lung cancer. J Clin Oncol 22:3261-3268, 2004 21. Ayanian JZ, Udvarhelyi IS, Gatsonis CA, et al: Racial differences in the use of revascularization procedures after coronary angiography. JAMA 269:2642-2646, 1993[Abstract] 22. Bach PB, Pham H, Schrag D, et al: Primary care physicians who treat blacks and whites. N Engl J Med 351:575-584, 2004 23. Gadgeel SM, Kalemkerian GP: Racial differences in lung cancer. Cancer Met Rev 22:39-46, 2003[CrossRef][Medline] 24. Margolis M, Christie JD, Silvestri GA, et al: Racial differences pertaining to a belief about lung cancer surgery. Ann Intern Med 139:558-563, 2003 25. McDavid K, Tucker CT, Slogett A, et al: Cancer survival in Kentucky and health insurance coverage. Arch Intern Med 163:2135-2144, 2003 26. Jazieh A, Kyasa MJ, Sethuraman S, et al: Disparities in surgical resection of early stage non small cell lung cancer. J Thorac Cardiovasc Surg 123:1173-1176, 2002 Submitted March 29, 2005; accepted August 11, 2005. This article has been cited by other articles:
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Copyright © 2006 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
2 tests for categoric variables. Given significant (P < .05) explanatory variables, we then constructed multivariable regression models to predict the likelihood of obtaining invasive staging, controlling for known confounders. We used multivariable regression models to predict the likelihood of surgery, stratifying by patients who had already received invasive staging versus those who did not. Kaplan-Meier curves were used to estimate survival statistics, and Cox regression analysis was performed to generate hazard ratios and adjust for known confounders. 
