ORIGINAL ARTICLE

Survival Disparities in Non–Small Cell Lung Cancer by Race, Ethnicity, and Socioeconomic Status Stacey L. Tannenbaum, PhD, RD,* Tulay Koru-Sengul, PhD,*† Wei Zhao, MD, MS,* Feng Miao, MS,* and Margaret M. Byrne, PhD*†‡ Purpose: Non–small cell lung cancer (NSCLC) is among the leading causes of cancer death in the United States. Previous studies found mixed results regarding disparities in survival by race, ethnicity, and socioeconomic status (SES). However, race comparisons were usually limited, with comparisons made between black and white patients only or by merging race and ethnicity together as non-Hispanic black, non-Hispanic white, and Hispanic patients. Even fewer studies included race, ethnicity, and SES together while controlling for extensive confounding variables. Thus, because we have access to a large and unique population-based database that includes tumor characteristics and patient comorbidities, the purpose of this study was to explore disparities in NSCLC survival. Methods: We linked data from the 1996 to 2007 Florida Cancer Data System registry to the Florida's Agency for Health Care Administration and the US Census (n = 98,541). Survival time was from date of diagnosis to death or last contact. Race was white, black, Native American, Asian, Pacific Islander, Asian Indian/Pakistani, or other. Ethnicity was nonHispanic or Hispanic. Socioeconomic status was measured as percentage of the participant’s census tract living below the federal poverty line. Median survival and survival rates were calculated by Kaplan-Meier method. Cox proportional hazards regression models produced unadjusted and adjusted hazard ratios (HRs) and 95% confidence intervals (95% CIs). Results: The majority of patients were white (91.9%) and non-Hispanic (94.1%). Blacks had the lowest median survival (8.4 months). At 5 years after diagnosis, survival rate was highest in whites (16.3%) and lowest for Pacific Islanders (6.4%). In the adjusted model, Asians had significantly improved survival compared with whites (HR, 0.85; 95% CI, 0.76–0.95). Patients in middle-low (HR, 0.96; 95% CI, 0.94–0.99), middle-high (HR, 0.92; 95% CI, 0.89–0.94), and highest (HR, 0.87; 95% CI, 0.84–0.91) SES areas had significantly improved survival compared with those in lowest areas. Significantly worse survival was found for patients with complicated diabetes (HR, 1.05; 95% CI, 1.01–1.08), weight loss (HR, 1.08; 95% CI, 1.06–1.11), fluid and electrolyte disorders (HR, 1.08; 95% CI, 1.06–1.11), and alcohol abuse (HR, 1.11; 95% CI, 1.07–1.14). Discussion: We found strong evidence for racial and socioeconomic disparities in Floridian NSCLC survival. Asians had improved survival compared with whites, a novel finding. Our findings confirmed that patients living in lower socioeconomic neighborhoods have worse outcomes than their wealthier neighborhood counterparts. Finally, we found an association between some modifiable factors/comorbidities and worse survival. Clinicians may be able to use this information to improve patients’ likelihood of better outcomes.

Key Words: Non–small cell lung cancer, disparities, overall survival, population characteristics, comorbidities (Cancer J 2014;20: 237–245)

N

on–small cell lung cancer (NSCLC) is the most common type of lung cancer, comprising 85% to 90% of all lung cancers.1 It is estimated that in 2013 there will be 228,190 incident cases and 159,480 deaths from lung cancer.2 If diagnosed early, the prospect for survival is greatly improved; however, limited information exists regarding modifiable comorbidities and survival in NSCLC patients. Furthermore, few studies have comprehensively examined NSCLC survival disparities by race, ethnicity, and socioeconomic status (SES) while controlling for extensive confounding factors. Many studies only examined white versus black race,3,4 whereas others did not distinguish between race and ethnicity.5–7 Numerous studies did not control for comorbidities,8,9 whereas others did not differentiate NSCLC from small cell lung cancer.10 To truly understand the factors that affect survival and identify modifiable factors for clinician intervention, all relevant variables must be included in the analyses. Our study does this in a racial, ethnic, and socioeconomically diverse population using the Florida Cancer Registry.

METHODS Data The Florida Cancer Data System (FCDS) registry (1996–2007) was linked with Florida’s Agency for Health Care Administration (AHCA) data and the US Census databases using a unique patient identifier. Data matches were confirmed with the patient's date of birth and Social Security number. Incident NSCLC cases were identified from FCDS (International Classification of Diseases, Ninth Revision codes). The FCDS collects information on patient demographics, stage of disease, treatment, and date of death through linkage with the National Death Index.11 Florida’s AHCA data set contains diagnoses and procedure codes for all inpatient and outpatient encounters (from 1995 forward) on all patients treated at hospitals and freestanding surgical and radiological treatment centers.

Variables From the *Sylvester Comprehensive Cancer Center, †Department of Public Health Sciences, and ‡Department of Surgery, University of Miami Miller School of Medicine, Miami, FL. Funding for this study was provided by the James & Esther King Florida Biomedical Research Program (grant 10KG-06). The authors have disclosed that they have no significant relationships with, or financial interest in, any commercial companies pertaining to this article. Reprints: Margaret M. Byrne, PhD, University of Miami Miller School of Medicine, 1120 NW 14th St, Miami, FL 33136. E-mail: MByrne2@med. miami.edu. Copyright © 2014 by Lippincott Williams & Wilkins ISSN: 1528-9117

The Cancer Journal • Volume 20, Number 4, July/August 2014

The primary clinical end point, overall survival, was considered as elapsed time from NSCLC diagnosis to date of death or last follow-up. The FCDS data were used to determine date of death. If FCDS did not have a date of death, patients were considered to have censored data. The FCDS and AHCA data were compared through 2010 (at least 3 years’ follow-up for all patients) to obtain the latest date of contact. Loss to follow-up may have occurred if the patient had stopped using the health care system or moved out of state. Our main predictors of interest were race, ethnicity, and SES. Patients were grouped into 1 of 7 race categories: white, black, www.journalppo.com

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237

238 100.0 91.9 7.4 0.0 0.4 0.0 0.1 0.2 94.1 5.9 12.5 31.7 37.6 18.2 17.7 82.3

44.0 56.0 10.6 57.6 29.3 2.4 3.6 20.6 3.7 59.4 1.6 0.1 6.8

Total

98,541

90,534 7249 26 387 36 85 224

92,722 5819

12,315 31,250 37,049 17,927

17,418 81,123 70.0 18–104

43,338 55,203

10,493 56,782 28,859 2407

3547 20,311 3644 58,494 1623 144 6733

Variable

Total patients Race White Black NA Asian PI AIP Other Hispanic origin No Yes SES Low Middle-low Middle-high High Vital status Alive Dead Median age at diagnosis, y Range of age at diagnosis, y Sex Female Male Marital status Never married Married Divorced/separated/widowed Unknown Insurance status Uninsured Private insurance Medicaid Medicare Defense/military/veteran Indian/public Insurance, not otherwise specified

Percent

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3.1 20.5 3.0 60.7 1.7 0.1 6.8

9.2 59.1 29.3 2.3

44.5 55.5

17.9 82.1 71.0 18–104

8.9 32.0 39.7 19.3

93.8 6.2

100.0 — — — — — —

90,534

White

9.1 21.3 11.4 45.2 1.5 0.4 6.7

28.1 38.4 29.6 4.0

36.7 63.3

13.9 86.1 65.0 19–97

57.0 28.2 10.9 3.9

7.7 7.7 3.8 57.7 — — 19.2

15.4 57.7 15.4 11.5

42.3 57.7

30.8 69.2 67.0 43–85

15.4 38.5 30.8 15.4

96.2 3.8

— — 100.0 — — — —

— 100.0 — — — — — 98.1 1.9

26

NA

7249

Black

9.6 26.9 7.0 39.0 3.1 0.8 8.0

8.8 69.0 19.9 2.3

51.7 48.3

26.1 73.9 66.0 33–94

12.7 31.3 36.4 19.6

96.1 3.9

— — — 100.0 — — —

387

Asian

Race

8.3 25.0 8.3 47.2 2.8 — 8.3

16.7 58.3 22.2 2.8

55.6 44.4

22.2 77.8 67.0 37–83

13.9 13.9 55.6 16.7

83.3 16.7

— — — — 100.0 — —

36

PI

5.9 18.8 10.6 42.4 5.9 2.4 10.6

12.9 67.1 16.5 3.5

48.2 51.8

23.5 76.5 67.0 32–98

10.6 30.6 35.3 23.5

98.8 1.2

— — — — — 100.0 —

85

AIP

9.4 29.9 6.7 39.7 1.3 — 9.4

16.5 53.6 25.0 4.9

47.3 52.7

31.7 68.3 67.0 19–91

8.0 29.9 42.0 20.1

75.9 24.1

— — — — — — 100.0

224

Other

3.3 20.2 3.3 60.2 1.7 0.1 6.9

10.3 57.7 29.5 2.4

44.6 55.4

17.5 82.5 70.0 18–104

11.5 31.3 38.4 18.7

100.0 —

91.6 7.7 0.0 0.4 0.0 0.1 0.2

92,722

No

8.3 26.6 10.7 45.9 0.3 0.1 5.5

15.8 56.2 25.6 2.5

34.3 65.7

21.2 78.8 69.0 19–100

7.2 18.9 8.7 52.9 1.7 0.3 6.0

21.2 43.0 32.5 3.2

38.8 61.2

13.5 86.5 68.0 20–99

100.0 — — —

86.7 13.3

— 100.0 28.1 37.9 24.2 9.8

65.8 33.5 0.0 0.4 0.0 0.1 0.1

12,315

L

96.3 2.4 0.0 0.3 0.1 0.0 0.9

5819

Yes

Hispanic Origin

TABLE 1. Demographic and Clinical Characteristics of Non–Small Cell Lung Cancer by Race, Ethnicity, and SES (Column %)*

MH

4.3 20.5 5.0 56.5 1.9 0.2 7.1

11.3 55.6 30.5 2.6

41.8 58.2

2.6 20.9 2.2 61.9 1.6 0.1 6.9

8.5 60.3 29.0 2.2

46.2 53.8

18.6 81.4 71.0 19–104

— — 100.0 —

— 100.0 — — 16.2 83.8 70.0 18–104

96.2 3.8

97.1 2.1 0.0 0.4 0.1 0.1 0.3

37,049

SES

92.9 7.1

92.7 6.5 0.0 0.4 0.0 0.1 0.2

31,250

ML

2.0 21.3 1.2 63.5 1.2 0.1 6.9

6.8 65.5 25.6 2.1

46.9 53.1

21.1 78.9 71.0 18–101

— — — 100.0

96.8 3.2

97.6 1.6 0.0 0.4 0.0 0.1 0.3

17,927

H

Tannenbaum et al The Cancer Journal • Volume 20, Number 4, July/August 2014

© 2014 Lippincott Williams & Wilkins

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Unknown Tobacco use Never History Current Unknown Geographic location Urban Rural Teaching hospital No Yes Hospital volume Low High Comorbidity None 1–2 3–4 >4 SEER stage Localized Regional, direct extension ± lymph nodes Regional, lymph nodes only Distant Unknown/unstaged Grade Undifferentiated Poorly differentiated Moderately differentiated Well differentiated Unknown/not stated Regional nodes positive No Yes Unknown Histological type Adenocarcinoma Squamous/combine complex Neoendocrine

4.1 9.5 43.9 35.6 11.1 93.5 6.5 91.3 8.7 66.3 33.7 5.2 3.3 7.7 83.8 22.0 14.4 10.1 39.9 13.6 3.1 31.5 17.9 5.1 42.4 17.6 9.3 73.1 43.9 29.8 2.6

4045

9326 43,270 35,035 10,910

92,179 6362

89,940 8601

65,337 33,204

© 2014 Lippincott Williams & Wilkins

5130 3266 7583 82,562

21,697 14,219

9959

39,278 13,388

3100 31,006 17,640 4990 41,805

17,380 9126 72,035

43,265 29,336 2580

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44.1 29.6 2.7

18.0 9.3 72.7

3.1 31.3 18.1 5.1 42.4

39.3 13.7

10.2

22.5 14.3

5.0 3.3 7.8 83.9

66.1 33.9

91.9 8.1

93.5 6.5

9.2 44.8 34.9 11.1

4.1

40.3 32.3 2.0

13.1 8.2 78.7

4.2 33.5 16.0 4.2 42.1

46.7 11.9

9.0

16.7 15.7

6.4 2.7 6.1 84.8

69.1 30.9

84.1 15.9

94.1 5.9

10.9 33.5 45.2 10.4

4.4

46.2 38.5 —

53.7 22.2 1.3

16.5 10.9 72.6

2.1 29.5 18.1 8.0 42.4

— 42.3 15.4 3.8 38.5 11.5 — 88.5

50.1 10.9

8.3

20.2 10.6

16.0 4.4 13.2 66.4

65.9 34.1

83.5 16.5

96.4 3.6

34.6 34.4 23.0 8.0

5.7

34.6 26.9

11.5

19.2 7.7

19.2 — 7.7 73.1

76.9 23.1

96.2 3.8

88.5 11.5

11.5 34.6 38.5 15.4

3.8

41.7 25.0 —

11.1 13.9 75.0

— 33.3 19.4 2.8 44.4

41.7 16.7

8.3

16.7 16.7

19.4 2.8 13.9 63.9

72.2 27.8

97.2 2.8

100.0 —

13.9 27.8 41.7 16.7



51.8 22.4 —

18.8 10.6 70.6

2.4 27.1 20.0 8.2 42.4

43.5 14.1

5.9

20.0 16.5

22.4 5.9 8.2 63.5

60.0 40.0

85.9 14.1

92.9 7.1

24.7 42.4 17.6 15.3

3.5

46.0 18.8 4.9

18.3 8.9 72.8

1.8 29.5 16.5 4.5 47.8

43.8 16.1

6.3

20.1 13.8

20.1 7.1 7.6 65.2

62.5 37.5

91.5 8.5

94.2 5.8

15.6 38.4 25.9 20.1

3.6

43.8 29.9 2.5

17.7 9.3 73.0

3.1 31.6 18.0 5.1 42.1

39.7 13.5

10.2

22.2 14.4

5.0 3.3 7.7 84.0

66.3 33.7

91.7 8.3

93.3 6.7

9.0 44.3 35.5 11.2

4.2

45.2 27.5 4.1

16.3 8.6 75.1

3.4 28.8 15.7 5.0 47.1

42.8 14.3

8.7

19.4 14.8

8.7 3.0 7.2 81.1

67.0 33.0

85.0 15.0

98.2 1.8

16.4 37.4 36.5 9.7

2.6

39.5 33.9 2.1

14.4 8.0 77.6

3.6 33.2 16.5 4.3 42.4

44.0 12.4

9.5

18.9 15.1

6.2 2.8 6.8 84.2

65.9 34.1

85.7 14.3

90.2 9.8

9.3 36.0 44.3 10.5

4.3

41.9 31.7 2.5

16.6 9.0 74.5

3.6 31.1 17.8 4.6 42.9

40.1 14.6

9.8

21.1 14.3

5.3 3.3 7.7 83.7

69.2 30.8

90.7 9.3

87.4 12.6

9.1 41.3 38.5 11.1

4.6

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47.6 25.5 3.0

19.7 10.5 69.8

2.8 31.2 18.1 5.6 42.3

38.7 12.3

10.9

23.7 14.3

5.1 3.7 8.2 83.1

59.9 40.1

92.3 7.7

99.6 0.4

10.5 48.6 30.4 10.5

3.7

Continued next page

45.3 28.8 2.7

18.6 9.3 72.1

2.8 31.3 18.4 5.4 42.1

38.8 13.7

10.1

23.0 14.3

4.9 3.3 7.8 84.1

67.1 32.9

93.1 6.9

96.9 3.1

9.3 46.5 32.7 11.6

3.8

The Cancer Journal • Volume 20, Number 4, July/August 2014 Non–Small Cell Lung Cancer Disparities

239

240

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64.2 31.3 4.5 55.3 42.5 2.2 69.4 29.3 1.3

63,289 30,796 4456

54,470 41,898 2173

68,347 28,885 1309

68.6 30.0 1.3

55.4 42.4 2.2

64.5 31.0 4.5

8.0 15.5

White

78.3 20.4 1.2

52.4 45.0 2.6

61.1 34.0 4.9

8.8 16.7

Black

84.6 15.4 —

53.8 42.3 3.8

50.0 46.2 3.8

3.8 11.5

NA

70.5 28.9 0.5

62.3 34.9 2.8

62.3 33.1 4.7

5.7 17.1

Asian

Race

66.7 33.3 —

52.8 41.7 5.6

58.3 38.9 2.8

2.8 30.6

PI

69.4 30.6 —

61.2 37.6 1.2

67.1 30.6 2.4

5.9 20.0

AIP

70.1 28.1 1.8

71.4 27.7 0.9

61.6 33.9 4.5

4.9 25.4

Other

69.3 29.4 1.3

55.0 42.8 2.2

64.5 31.1 4.4

8.0 15.7

No

70.0 28.5 1.5

59.8 37.4 2.8

59.6 33.4 7.0

8.5 14.7

Yes

Hispanic Origin

76.2 22.8 1.0

53.3 44.6 2.2

64.4 31.0 4.6

9.0 15.6

L

70.8 27.7 1.5

54.7 42.8 2.5

65.1 30.3 4.7

8.9 14.9

ML

SES

67.9 30.8 1.3

56.3 41.5 2.2

64.6 30.8 4.5

7.3 15.9

MH

65.0 33.6 1.4

55.5 42.9 1.7

61.8 34.0 4.2

7.5 16.3

H

Total columns and total-patient row denote sample size. All other columns and rows are percentages, with the exception of age and age range. *All demographic and clinical characteristics were significantly different (P < 0.05) among race, ethnicity, and SES, with the exceptions that hospital volume, regional nodes positive, and surgery did not vary between Hispanics and non-Hispanics. NA indicates Native American; PI, Pacific Islander; AIP, Asian Indian or Pakistani; SEER, Surveillance, Epidemiology, and End Results Program; and SES (percent living below poverty line): L, lowest (≥20%); ML, middle-low (≥10% and

Survival disparities in non-small cell lung cancer by race, ethnicity, and socioeconomic status.

Non-small cell lung cancer (NSCLC) is among the leading causes of cancer death in the United States. Previous studies found mixed results regarding di...
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