Disparities in lung cancer stage, treatment and survival among American Indians and Alaskan Natives

Lung Cancer 72 (2011) 160–164

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Disparities in lung cancer stage, treatment and survival among American Indians and Alaskan Natives Cardinale B. Smith a,b,∗ , Marcelo Bonomi a,b , Stuart Packer a , Juan P. Wisnivesky c a b c

Division of Hematology/Oncology, Department of Medicine, Tisch Cancer Institute, Mount Sinai School of Medicine, New York, NY, United States Hertzberg Palliative Care Institute of the Brookdale Department of Geriatrics, Mount Sinai School of Medicine, New York, NY, United States Division of General Internal Medicine and Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Mount Sinai School of Medicine, New York, NY, United States

a r t i c l e

i n f o

Article history: Received 1 February 2010 Received in revised form 6 August 2010 Accepted 16 August 2010 Keywords: Disparities Lung cancer American Indians Ethnicity Treatment Surgery

a b s t r a c t Background: Disparities in lung cancer care and outcomes have been documented for blacks and Hispanics. Less is known about the care received by the American Indian and Alaskan Native population (AI/AN). We sought to evaluate lung cancer outcomes in this population and to asses if potential disparities in survival are explained by differences in stage of disease at diagnosis and type of treatment received. Methods: We identified patients with potentially resectable (stages I–IIIA) non-small cell lung cancer (NSCLC) from the Surveillance, Epidemiology and End Results registry between 1988 and 2006. Kaplan–Meier curves were used to compare survival of AI/AN patients to those of other racial groups. Cox regression analysis was used to identify potential mediators of the association between AI/AN origin and worse survival. Results: Five-year lung cancer survival was 47% for AI/AN, 56% for whites, 51% for blacks, 55% for Hispanics and 59% for individuals of other race (p < 0.0001). AI/AN were more likely to be diagnosed with stage IIIA (p < 0.0001) and less likely to undergo resection (p < 0.0001) than whites. In multivariable regression analyses, controlling for patient characteristics and histology, AI/AN race was associated with worse survival than white patients. When stage, treatment and surgery were added to the model, AI/AN origin was no longer significantly associated with worse outcomes. Conclusions: AI/AN with potentially resectable NSCLC have survival rates comparable to other minority groups and worse than whites. These survival differences are partly explained by advanced stage at diagnosis, and lower rates of treatment. © 2010 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Lung cancer is the second most common cancer and the leading cause of cancer-related deaths in American Indian and Alaska Native (AI/AN) men and women [1] When non-small cell lung cancer (NSCLC) is diagnosed at an early stage it is potentially curable with surgery [2]. Five-year survival rates for resected patients with stage I disease is 65% (range, 55–72%) and 41% for patients with stage II disease (range, 29–51%) [3–7]. In contrast, patients that present with advanced disease or those that do not undergo surgical resection have a median survival of about 1 year [8,9]. Race, ethnicity and social factors have been previously identified in multiple studies as variables that can account for variations in lung cancer treatment and survival [10–12]. Most of these studies

∗ Corresponding author at: One Gustave L. Levy Place Box #1079, New York, NY 10029, United States. Tel.: +1 212 241 5398; fax: +1 646 537 8697. E-mail address: [email protected] (C.B. Smith). 0169-5002/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.lungcan.2010.08.015

have focused on blacks and Hispanics, the two largest minority populations in the United States (US) [13–15]. Black patients with early stage lung cancer have lower 5-year survival rates than whites, and this difference in outcome has been attributed to lower rates of resection among black patients [13]. Similar results have been reported in Hispanic patients [14]. Prior research has shown that the AI/AN population have an increased burden of lung cancer mortality [16–19]. However, little is known about the potential disparities in treatment and outcomes of lung cancer in AI/AN populations. In this study, we used the Surveillance, Epidemiology and End Results (SEER) registry, a nationally representative, populationbased cancer data source to evaluate the rates of treatment and survival of AI/AN patients with NSCLC. We hypothesized AI/AN have survival rates similar to other minority groups and worse than whites. We were also interested in examining whether potential differences in survival could be explained, at least in part, by inequalities in stage at diagnosis and rates of resection.

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Table 1 Baseline characteristics of study subjects. Characteristic

American Indian/Alaskan Native N = 274 No. (%)

White N = 56,029No. (%)

Black N = 6251No. (%)

Hispanic N = 2615No. (%)

Others N = 3969No. (%)

p-Value

Age (mean) ± SD (years) Sex Male Female Marital status Married Not Married Histology Adenocarcinoma Squamous cell carcinoma Large cell carcinoma Other Tumor size (cm), mean ± SD Stage IA IB IIA IIB IIIA Surgical resection No Yes Radiation therapy With surgery Alone No

65 ± 10

68 ± 11.4

64 ± 10.3

67 ± 10.6

68 ± 10.5

<0.0001

150 (55) 124 (45)

29,917 (53) 26,112 (47)

3640 (58) 2611 (42)

1451 (56) 1164 (44)

2356 (59) 1613 (40)

<0.0001

122 (45) 152 (55)

33,552 (60) 22,477 (40)

2492 (40) 3759 (60)

1490 (57) 1125 (43)

2717 (68) 1252 (32)

<0.0001

110 (40) 116 (42) 12 (5) 36 (13) 3.84 ± 1.95

28,244 (50) 18,719 (33) 3021 (6) 6045 (11) 3.41 ± 2.33

2744 (44) 2308 (37) 348 (6) 821 (13) 3.78 ± 2.73

1375 (53) 813 (31) 116 (4) 311 (12) 3.68 ± 2.31

2452 (62) 959 (24) 156 (4) 402 (10) 3.52 ± 2.30

<0.0001

103 (38) 92 (34) 10 (4) 23 (8) 36 (13)

25,032 (47) 17,723 (34) 2371 (4) 3428 (6) 5207 (9)

2395 (38) 2093 (33) 244 (4) 374 (6) 799 (13)

1027 (39) 880 (34) 84 (3) 165 (6) 298 (11)

1668 (42) 1296 (33) 188 (5) 272 (7) 421 (11)

<0.0001

86 (31) 188 (69)

13,153 (24) 42,695 (76)

2183 (35) 4046 (65)

735 (28) 1877 (72)

1009 (25) 2959 (75)

<0.0001

31 (11) 5 (2) 238 (87)

4380 (8) 521 (1) 50,94 (91)

527 (9) 73 (1) 5629 (90)

196 (7) 18 (1) 2398 (92)

346 (9) 24 (1) 3598 (90)

<0.0001

<0.0001

SD indicates standard deviation.

2. Methods Cases were selected from the SEER registry, a national database that collects data on all incident cancer cases in selected areas of the US, covers nearly 26% of the US population, and is sponsored by the National Cancer Institute [20]. From this registry, we identified all cases of histologically confirmed NSCLC diagnosed between 1988 and 2006. We limited the analysis to patients with stages I–IIIA cancers based on the American for Joint Committee on Cancer classification by referring to SEER information on extent of tumor involvement. The final cohort consisted of 69,138 NSCLC patients. Information on patient demographics such as age at diagnosis, gender, race, ethnicity, marital status, as well as tumor histology and stage was obtained from SEER. Ethnicity was coded in accordance with the federal Office of Management and Budget Directive [21], which defines ethnicity as “Hispanic origin” or “not of Hispanic origin”. For race, subjects are classified as white, Black or African-American, American Indian or Alaskan Native, and other. Any patient identified as Latino or Hispanic is categorized as Hispanic regardless of their race. Histologic subtypes were classified into categories of adenocarcinoma, squamous cell carcinoma, large cell carcinoma, and other histologic types. Tumor histology is coded in SEER using the International Classification of Diseases for Oncology, 3rd edition (ICD-O-3) [22]. Cases were classified as resected if the SEER site-specific variable indicated that a surgical procedure including segmentectomy, wedge resection, lobectomy, and partial or total pneumonectomy (SEER codes 20–90) had been performed. Any patient who had a code indicating external beam radiation was classified as receiving radiation therapy. Patients were divided into 3 categories: those who did not receive radiation therapy, those who had radiation therapy after surgery and those who had radiation therapy alone. Survival times were calculated as the period from lung cancer diagnosis to death. Those alive at December 31, 2006 were classified as censored observations. The cause of death reported in the SEER registry is abstracted from the National Center for Health Statistics

database of consolidated death certificates from the Vital Statistics Office in each state. 2.1. Statistical analysis Differences in the distribution of socio-demographic characteristics, tumor histology, stage and treatment type between whites, blacks, Hispanics, AI/AN and subjects of other race were evaluated using the chi-square and Kruskal–Wallis test as appropriate. The Kaplan–Meier method was used to estimate lung cancer-specific survival rates. Deaths attributed to causes other than the underlying cancer were treated as censored observations at the date of death. We used Cox regression to evaluate whether AI/AN patients had an increased risk of lung cancer death after adjusting for sex, age, marital status and histology. We then fitted a second model controlling for stage at diagnosis, surgical treatment and radiation therapy use to evaluate whether the potential increased risk of death among AI/AN patients was explained, in part, by these factors. Secondary analysis was performed to identify if the potential increased risk of death among AI/AN patients persisted after controlling for temporal trends in the treatment of lung cancer. Analyses were performed with SPSS version 16 (SPSS, Inc., Chicago, IL) statistical package. The study was exempt from Mount Sinai’s Institutional Review Board. 3. Results 3.1. Patient characteristics A total of 69,138 eligible patients with stages I–IIIA NSCLC were identified from the SEER registry. Of these patients, 56,029 (81.0%) were white, 274 (0.4%) were AI/AN, 6251 (9.0%) were black, 2615 (4.0%) were Hispanic, and 3969 (5.6%) of other race. The baseline patient characteristics are shown in Table 1. Overall the AI/AN were more likely to be male (p < 0.0001), less likely to be married (p < 0.0001) and had a higher likelihood of having squamous cell carcinoma (p < 0.0001). Compared to whites, AI/AN were

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C.B. Smith et al. / Lung Cancer 72 (2011) 160–164 Table 2 Five-year lung cancer-specific survival rates. Study group

Five-year lung cancer survival rate (%)

American Indian/Alaskan Native White Black Hispanics Others

47 56 51 55 59

95% CI 43.5–50.5 55.7–56.3 50.0–51.4 53.8–56.2 57.8–59.6

57.8–59.6%) for individuals in the other race category (Table 2). Rates of surgical resection also varied significantly among groups. The proportion of patients undergoing resection was 69% AI/AN, 76% of whites, 65% of blacks, 72% of Hispanics, and 75% of the other race group (p < 0.0001). Use of radiation treatment also varied significantly among groups (p < 0.0001). Fig. 1. Lung cancer-specific survival curves of stages I–IIIA non-small cell lung cancer patients. Lung cancer-specific survival was significantly different across groups (p < 0.0001). Survival of American Indians and Alaskan Natives was worse than white patients with stages I–IIIA NSCLC.

more likely to be diagnosed with more advanced stage disease (p < 0.0001). 3.2. Unadjusted survival analyses AI/AN had significantly worse lung cancer-specific mortality compared to other groups (p < 0.0001; Fig. 1). Five-year survival rates, were 47% (95% CI, 43.5–50.5%) for AI/AN compared with 56% (95% CI, 55.7–56.3%) for whites, 50.7% (95% CI, 50–51.4%) for blacks, 55% (95% CI, 53.8–56.2%) for Hispanics and 58.7% (95% CI,

3.3. Adjusted survival analysis We performed Cox regression analysis to assess survival among AI/AN compared to the other racial and ethnic groups after adjusting for baseline differences in age, sex, marital status and histology (Model A). This model, showed that AI/AN had a significantly increased hazard of lung cancer death (hazard ratio: 1.36; 95% CI, 1.15–1.62) compared to whites (reference category; Table 3). We then fitted a model controlling for stage at diagnosis, surgery and radiation therapy use (Model B) to evaluate if inequalities in stage at diagnosis and treatment could explain the observed association between AI/AN origin and survival in Model A. This model showed that lung cancer-specific survival among AI/AN and whites were similar (hazard ratio, 1.17; 95% CI, 0.98–1.39), suggesting that dif-

Table 3 Multivariate Cox regression analysis for risk of lung cancer death. Variable

Model A Hazard ratio

White AI/AN Black Hispanic Other Sex Male Female Age <60 60–70 >70 Marital status Not married Married Histology Adenocarcinoma Squamous Large cell Others Stage IA IB IIA IIB IIIA Surgery No Yes Radiation No Alone With surgery

Model B 95% CI

Hazard ratio

95% CI

Reference 1.36 1.21 1.05 0.93

– 1.15–1.62 1.16–1.26 0.98–1.12 0.88–0.98

Reference 1.17 1.03 0.98 0.84

– 0.98–1.39 0.99–1.07 0.92–1.05 0.79–0.88

Reference 0.78

– 0.76–0.80

Reference 0.81

– 0.79–0.83

Reference 0.76 1.09

– 0.71–0.81 1.02–1.17

Reference 1.10 1.42

– 1.06–1.13 1.38–1.46

Reference 0.83

– 0.82–0.85

Reference 0.88

– 0.85–0.90

Reference 1.25 1.46 2.04

– 1.21–1.33 1.38–1.53 1.97–2.13

Reference 1.00 1.18 1.09

– 0.97–1.03 1.12–1.25 1.04–1.13

– – – – –

– – – – –

Reference 1.64 2.03 2.65 2.29

– 1.59–1.68 1.92–2.15 2.54–2.78 2.19–2.41

– –

– –

Reference 0.10

– 0.08–0.11

– – –

– – –

Reference 2.24 0.66

– 1.97–2.55 0.58–0.74

CI, confidence interval; AI/AN, American Indian and Alaskan Native.

C.B. Smith et al. / Lung Cancer 72 (2011) 160–164

ferences in stage, resection rates and use of radiation therapy can partially explain the observed unadjusted relationship. Secondary analysis adjusting for temporal trends showed similar findings.

4. Discussion Using nationally representative data of patients with potentially resectable stages I–IIIA NSCLC we found that AI/AN had worse outcomes compared to non-minority groups. AI/AN were more likely to be diagnosed with more advanced disease and less likely to undergo resection. Our multivariate analyses suggests that the unadjusted difference in survival can be partially explained by differences in stage at diagnosis, use of radiation therapy and unequal rates of resection. Future efforts designed to improve the care received by AI/AN patients with NSCLC should target these potentially modifiable risk factors. Inequalities in surgical treatment and stage of diagnosis have been well documented to be a contributing factor for survival differences among black and Hispanic patients with lung cancer. Bach and colleagues [13] found important differences in survival among African Americans compared to white patients with stages I and II NSCLC which were largely explained by a lower rate of surgical resection among blacks. Similarly, Hispanics with stage I NSCLC have been found to have a worse survival when compared to whites due, in part, to lower rates of treatment among Hispanics [14]. Whether these disparities are also pertinent for other US minority groups has been less well studied. In the most recent report to the nation on the status of cancer by the Centers for Disease Control and Prevention, analyses of cancer death rates from 1975 to 2004 revealed declining trends in cancer death rates for all racial/ethnic groups except AI/AN, for whom cancer death rate trends remained level [1]. Ehrsam et al. [23] studied death certificates and the Indian Health Service (IHS) population estimates to create age-adjusted mortality rates for AI/AN and compared these data with US whites. This study showed that AI/AN were 40% more likely to die of lung cancer than whites (OR 1.4; 95% CI, 1.2–1.6). Similarly, in a case control study in Montana comparing lung cancer outcomes in AI and non-AI controls, stage at diagnosis and 5-year survival rates did not differ among groups, but AI were less likely to undergo surgical intervention (79 versus 86%, p = 0.02) [19]. Our study extends these findings by showing that AI/AN with stages I–IIIA NSCLC have rates of resection that are similar to other minority groups and significantly lower than whites. The observed disparity in surgical treatment for NSCLC in our study may be attributable to several patient-, physician-, and health-system-related factors. Patient-related factors may include mistrust of physicians or hospitals and lower satisfaction with healthcare [24–27]. Patients’ risk perception of surgery may be central to their willingness to undergo resection and higher risk aversion has been suggested as a potential reason for under treatment among minorities. For example, it has been shown that a common belief among blacks that the tumor can spread and disseminate when the cancer is exposed to air during surgery may be related to preferences towards surgery [10]. A community based survey of newly diagnosed cancer patients assessing their basic knowledge of cancer screening and beliefs about cancer management found that there were significant differences among minority patients in beliefs about the immediate impact of a cancer diagnosis and treatment on a person’s daily life [28]. In that study, 64% of AI patients agreed that cancer treatment “always takes many weeks of daily treatment” compared with 41% of white patients (p = 0.009). Moreover, 29% of AI patients agreed with the statement that cancer treatments “always make people so sick that they are unable to go about their daily lives”, com-

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pared to 1% of white respondents (p = 0.0001). Physician-related factors may include issues related to patient-provider communication or lack of cultural competency in caring for minority groups. A study evaluating patients with a diagnosis of lung cancer or a pulmonary nodule found that patients in racially discordant physician–patient pairs received less information and were less often prompted to actively participate in conversation compared with patients in racially concordant pairs [12]. Health-systemrelated factors may include issues related to the unique health care system (and its funding status) under which many AI/AN receive health care [29–31]. IHS, a federal health program for AI/AN, provides health care to members of federally recognized tribes through a system of hospitals and clinics on or near reservations. Some AI/AN are ineligible for the IHS, primarily because they are not members or descendants of federally recognized tribes. Because these services are predominately available through reservations, only 20% of Native Americans reported having access to IHS in 1997 [30,32]. In addition, most AI/ANs live in urban areas away from their home reservations and cannot access IHS services [33]. Moreover, there may be a lack of availability of specialty providers (medical oncologists, radiation oncologists, and cardiothoracic surgeons) as well as decreased access to care facilities that are able to provide optimal cancer therapy [29]. More information about these potential mechanisms are needed to understand and address disparate cancer-related health outcomes in this population. It may be important to assess whether these factors also play a role for lack of treatment among AI/AN lung cancer patients. There are several strengths and weaknesses of this study that should be noted. Comorbidity data is not available in the SEER database, thus it is possible that some of the observed inequalities in resection rates and outcomes may be explained by a higher frequency of AI/AN patients who had other coexisting illness or were poor candidates for surgery. Information about the cause of death in SEER is abstracted from death certificates. While this is an important source of data on disease incidence, prevalence, and mortality, inaccuracies have been reported [34,35]. For lung cancer, however, the underlying cause of death has been found to be more than 90% accurate in a large registry [36]. No individual level data is available in the SEER registry on income or insurance status, which may vary by race and could affect access to and quality of health care. However, given that all patients had a histologic confirmation of NSCLC suggests that they must have had some involvement with the health care system. Therefore, these findings are not a result of undiagnosed patients without any access to healthcare. AI/AN cancer incidence rates reported in SEER are dominated by the large AI population ascertained by the New Mexico Tumor Registry (NMTR), which is one of the original SEER cancer registries, and often cited as representative of all AI/AN populations in the United States. However, lung cancer incidence rates in the Southwestern AI population, as reflected in the NMTR data, are much lower than in other regions [37,38]. Second, AI/AN are often classified as belonging to other racial groups in medical records, vital statistics, cancer registries, and other databases [39]. However, It should be noted that the Alaska cancer SEER registry only collects information among Alaska Native populations. Despite this, SEER is considered the best source of population-based cancer death in the US. Despite the fact that a substantial proportion of patients with resectable NSCLC benefit from surgery, our study suggests there is underuse of surgical treatment in AI/AN patients. These differences in treatment have a direct effect on survival. As surgery is still the main intervention that can improve outcomes and lung cancer prognosis, future work should explore why AI/AN are less likely to undergo resection in an effort to improve these outcomes and reduce racial disparities.

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