(Chest. 2001;120:55-63.)
© 2001
American College of Chest Physicians
Impact of Race in Lung Cancer*
Analysis of Temporal Trends From a Surveillance, Epidemiology, and End Results Database
Shirish M. Gadgeel, MD;
Richard K. Severson, PhD;
Ying Kau, MPH;
John Graff, MS;
Linda K. Weiss, PhD and
Gregory P. Kalemkerian, MD
*
From the Division of Hematology and Oncology (Drs. Gadgeel and Kalemkerian) and the Department of Family Medicine (Drs. Severson and Weiss, Ms. Kau, and Mr. Graff), Wayne State University and the Barbara Ann Karmanos Cancer Institute, Detroit, MI.
Correspondence to: Gregory P. Kalemkerian, MD, University of Michigan Medical Center, 1366 Cancer Center, 1500 E. Medical Center Dr, Ann Arbor, MI 48109-0922; e-mail: kalemker{at}umich.edu
 |
Abstract
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Study objectives: We analyzed data from a
community-based cancer database over a 26-year period in order to
characterize clinicopathologic differences between black and white
patients with lung cancer, and to identify relevant temporal trends in
incidence and survival.
Design, setting, and patients:
Data on demographics, stage, histology, and survival were obtained on
all black and white patients with primary bronchogenic carcinoma
registered in the community-based metropolitan Detroit Surveillance,
Epidemiology, and End Results database from 1973 to 1998.
Results: Of 48,318 eligible patients, 23% were black. Lung
cancer incidence rates decreased for men of both races from 1985 to
1998, with a greater decline occurring in black men (p < 0.0001).
Although incidence rates declined over time for men of both races
< 50 years of age, this decrease was greater in white men, resulting
in an increase in the racial differential in younger men. Temporal
trends in incidence rates were similar for women of both races. The
incidence of distant-stage disease was higher among blacks throughout
the study period. The incidence of local-stage disease decreased for
both races, though this decline was greater in blacks. A significant
racial difference in 2-year and 5-year survival rates developed during
the study period, due to a distinct lack of improvement in black
patients. In a multivariate model, the relative risks of death for
black patients, relative to white patients, were 1.24 (p < 0.0001)
for local stage, 1.14 (p < 0.0001) for regional stage, and 1.03
(p = 0.045) for distant stage.
Conclusion:
Significant racial differences exist in the incidence and survival
rates for lung cancer in metropolitan Detroit. Since 1973, several
disturbing trends have developed, particularly with regard to the lack
of improvement in overall survival in black patients. Further study is
required to determine the factors responsible for these temporal
trends.
Key Words: epidemiology • incidence • lung cancer • race • survival
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Introduction
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During
this century, lung cancer has evolved from a disease of limited
significance to the leading cause of cancer-related mortality in both
men and women in the United States. Although ethnic variations in lung
cancer incidence and survival rates have been
reported,1
2
3
temporal trends in these differences have
not been fully evaluated. Prior to the
1960s, lung cancer mortality rates were significantly lower in
nonwhite patients than in white patients.4
However, in
recent years, the recognition of higher incidence rates and lower
survival rates for lung cancer in black patients compared to whites
patients has received increasing public attention. These racial
differences have been attributed to a variety of factors, including
smoking habits,5
6
socioeconomic status,7
8
genetic susceptibility,9
10
occupational
exposure,11
diet,12
13
and
treatment.14
In order to further characterize the
clinicopathologic differences in lung cancer patients of different
races and to more clearly define recent temporal trends in the Detroit
area, we analyzed data collected by the metropolitan Detroit
Surveillance, Epidemiology and End Results (SEER) database from 1973 to
1998.
|
Materials and Methods
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Patients
The SEER Program is a National Cancer Institute-funded database
that has been collecting clinicopathologic data on cancer patients in
selected geographic areas since 1973. The data for this study were
collected by the Metropolitan Detroit Cancer Surveillance System
(MDCSS) of the Barbara Ann Karmanos Cancer Institute, a
population-based database that is part of the SEER program. The MDCSS
records information on all incident cases of cancer in residents of the
Detroit metropolitan area, which consists of Wayne, Oakland, and Macomb
counties. Data are collected from hospitals in the tri-county area,
selected neighboring hospitals, physicians’ offices, clinics,
radiation therapy facilities, hospice facilities, nursing homes and the
Michigan Office of Vital Statistics, resulting in an estimated capture
rate of 99% of all cancer cases. Continuous data regarding
demographics, extent of disease, tumor histology, and survival were
available throughout the study period. Extent of disease is defined in
three categories: (1) local disease, an invasive neoplasm confined
entirely to the organ of origin; (2) regional disease, extension beyond
the organ of origin directly into surrounding tissues and/or into
regional lymph nodes; and (3) distant disease, spread to parts of the
body remote from the primary tumor by discontinuous metastases,
excluding regional lymph nodes. Survival is defined as the time between
date of diagnosis and date of death. The MDCSS database was screened to
identify all patients with primary bronchogenic carcinoma diagnosed in
the metropolitan Detroit area from 1973 to 1998. Exclusion criteria
were as follows: race other than black or white; diagnosis of cancer
prior to lung cancer; report only by autopsy or death certificate;
clinical diagnosis without biopsy; unknown race or age at diagnosis;
in situ carcinoma; and histology other than small cell,
large cell, squamous cell, or adenocarcinoma. A total of 264 patients
with primary invasive lung cancer were excluded based on race other
than black or white or unknown race or age at diagnosis.
Statistical Analysis
Differences in distribution of age, gender, tumor histology, and
cancer stage between white and black patients were evaluated with a
2 heterogeneity test. All reported p values
are two sided. All incidence rates are per 100,000 person-years. Linear
regression analysis was used to examine the trends of age-adjusted
incidence rates. Relative survival rates at 2 years and 5 years after
diagnosis were calculated using software (SEER*Stat 1.1; National
Cancer Institute SEER Program; Rockville, MD).15
A
parallel survival analysis using the Cox proportional hazard model was
performed to evaluate the relative risk of death of black patients vs
white patients by adjusting for selected covariates, namely age at
diagnosis, stage, histology, and gender.16
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Results
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Patient Characteristics
A total of 48,318 eligible patients with primary bronchogenic
cancer were identified. Of these patients, 77% were white and 23%
were black. The clinicopathologic characteristics of the two racial
groups are compared in Table 1
. The proportions of men (69% vs 65%) and patients < 50 years of age
(11% vs 7%) were significantly greater in black patients than in
white patients. Squamous cell carcinoma was the most common histologic
subtype in black patients, while adenocarcinoma was the most common
subtype in white patients. Stage distribution also differed
significantly between the two racial groups, primarily due to a higher
proportion of distant disease in black patients (49% vs 45%).
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Table 1. Clinicopathologic Characteristics of Lung Cancer
Patients in the Metropolitan Detroit SEER Database (1973 to
1998)*
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Incidence Rates
Age-adjusted incidence rates for the entire study period according
to race and gender are presented in Table 2
. While overall incidence rates were similar in women of both races,
they were 37% higher in black men as compared to white men. The annual
age-adjusted incidence rates according to race and gender are presented
in Figure 1
. The incidence of lung cancer in women of both races increased steadily
throughout the study period, resulting in an overall relative increase
of > 100%. The incidence rates for black men and white men peaked in
the mid-1980s, with a slightly earlier peak in whites (1983) than in
blacks (1985). Although the lung cancer incidence rates for men of both
races steadily declined from 1985 to 1998, the relative decrease was
significantly greater in black men than in white men (43% vs 27%;
p < 0.0001).
Over the entire study period, the racial difference in incidence rates
was more pronounced in younger men, with the incidence in black men
< 50 years of age being twice that of their white counterparts (Table 2)
. The temporal trends in lung cancer incidence according to race and
age were analyzed by comparing rates from two time periods (from 1973
to 1985 vs from 1986 to 1998). In men < 50 years of age, the
incidence rate decreased in men of both races, but this decline was
greater in white men, resulting in an increase in the racial risk ratio
from 1.88 to 2.38 (Table 3
). In contrast, while the incidence of lung cancer increased in older
men of both races, the disparity between blacks and whites narrowed
slightly over time (risk ratio, 1.37 to 1.28). In women, the incidence
rate differential between the races was small in both younger and older
age groups (Table 2)
, and did not change significantly over time (data
not shown).
Overall, the incidence rates for all histologic subtypes, except small
cell carcinoma, were significantly higher in black men than white men,
while in women, only the rates of squamous cell carcinoma differed
significantly between the racial groups (Table 2) . The greatest racial
difference was observed for squamous cell carcinoma, with higher
incidence rates in black men (risk ratio, 1.61) and women (risk ratio,
1.40) compared to their white counterparts. The race-specific and
gender-specific trends in the incidence rates for the four major
histologic subtypes of lung cancer are shown in Figure 2
. The incidence rates for adenocarcinoma have increased over time among
men of both races, while the rates for squamous cell carcinoma have
declined. The relative increase in the incidence of adenocarcinoma was
significantly greater in black men than in white men (p < 0.0001).
The incidence of squamous cell carcinoma peaked in the mid-1980s for
men of both races, and has since declined steadily in men of both
races. The relative degree of this decline has been greater in black
men than in white men (42% vs 30%; p < 0.0001). The incidence
rates for both large cell and small cell carcinoma remained similar for
men of both races throughout the study period. In women, the incidence
of all four histologic subtypes increased over time with no significant
differences between the races. As in men, the largest relative increase
occurred in the incidence of adenocarcinoma.
The incidence rates of all stages of lung cancer were higher in black
men than white men, with the greatest differential for distant-stage
disease (risk ratio, 1.48). The incidence rates for all stages of
disease were similar in women of both races. Temporal trends in stage
incidence were analyzed by comparing rates from 1973 to 1985 to those
from 1986 to 1998. Between these two study periods, the incidence of
distant-stage disease increased in both blacks (23.2 to 28.9) and
whites (16.4 to 22.0; Fig 3
), while the proportion of patients with distant-stage disease increased
from 44% to 53% in black patients and from 42% to 48% in white
patients. The incidence rates for local disease declined in blacks
(11.6 to 9.7) but increased slightly in whites (8.9 to 9.2).
Survival
Overall and stage-specific relative 2-year and 5-year survival
rates for black and white patients are presented in Figure 4
and Table 4
. From 1973 to 1985, overall survival rates in black and white lung
cancer patients were not significantly different, while from 1986 to
1997, 2-year and 5-year survival rates in white patients were
significantly greater than those in black patients (p < 0.001; Table 4
). In black patients, overall survival rates remained essentially
unchanged over the 23-year study period. In contrast, overall 2-year
and 5-year survival rates improved by 20% and 29%, respectively, in
white lung cancer patients. In patients with local-stage disease,
survival rates increased over time in both racial groups, with relative
increases in 2-year and 5-year survival rates of 19% and 21% in black
patients and 21% and 29% in white patients, respectively. However,
survival rates for patients with local-stage disease remained
significantly greater in white patients than in black patients
throughout the study period (Table 4)
. For the time period from 1973 to
1985, survival rates for white patients and black patients with
regional-stage disease were not significantly different. However,
although survival rates for patients with regional-stage disease
increased in both racial groups from 1985 to 1997, this increase
was much greater in white patients than in black patients, resulting in
the development of significant differences in both 2-year (p = 0.012)
and 5-year (p < 0.001) survival (Table 4)
. The survival rates for
patients with distant-stage disease were dismal in both groups and have
exhibited little absolute change over time.
Results of a multivariate analysis of risk of death incorporating the
clinical variables of age, gender, race, stage, and histologic subtype
are presented in Table 5
. Overall, stage of disease at presentation was the most significant
predictor of survival. Race, gender, and histologic subtype were also
identified as a significant prognostic factors. The relative risk of
death for black patients relative to white patients differed
substantially by stage of disease, with associated relative risks for
local, regional, and distant stage of 1.24, 1.14, and 1.03,
respectively.
|
Discussion
|
|---|
This population-based study demonstrates that significant racial
disparities exist in lung cancer incidence and survival, and that many
of these differences have become more prominent in recent years.
Although the designation of race is an imperfect and complex variable
with strong socioeconomic associations and questionable biological
significance, analyses of racial differences in a diseased cohort can
identify clinicopathologic variations that may lead to interventions
based on the specific needs of a target subpopulation.17
In the current analysis, the overall incidence of lung cancer in black
men was 37% higher than in white men, while the incidence in black
women was only 9% higher than in white women. This finding may be
explained by significantly less racial disparity in smoking rates
in women than in men,18
and is in agreement with prior
reports that racial differences in lung cancer incidence are primarily
due to variations in men.1
The recent decline in the
incidence of lung cancer in men has been attributed to a decrease in
smoking prevalence that began in the mid-1960s.1
We have
noted a similar decrease in lung cancer incidence in men since 1985,
with the rate of decline being greater in black men than in white men.
Various factors, including the prevalence and patterns of tobacco use,
have been evaluated in an attempt to explain racial differences in the
incidence of lung cancer. In the early 1950s, the prevalence of
cigarette use was similar in whites and blacks, but since the 1960s,
smoking prevalence has increased to a greater extent in blacks,
particularly in men.4
5
However, the increases in smoking
prevalence and lung cancer incidence in blacks appear to have occurred
simultaneously, making it unlikely that differences in smoking
prevalence are entirely responsible for the racial variations in lung
cancer incidence. Smoking patterns also differ between the races.
Although black smokers generally start smoking at a later age and
consume fewer cigarettes per day than white smokers, they are less
likely to quit and therefore have a higher rate of long-term cigarette
use.5
6
In addition, blacks are more likely to smoke
mentholated cigarettes and cigarettes with higher tar and nicotine
contents than whites, potentially enhancing their risk of lung
cancer.6
19
20
21
Racial differences in the metabolism of
nicotine have also been proposed as a cause for the higher incidence
rates of many smoking-related illnesses in
blacks.9
10
22
23
Many studies have evaluated the importance of socioeconomic parameters
as cancer risk factors and prognostic markers. Socioeconomic factors
such as lower income and education level have been associated with
higher smoking prevalence and nicotine dependence rates, and greater
usage of nonfilter, high-tar cigarettes.3
5
24
25
Socioeconomic status also correlates with other lifestyle factors that
may impact on lung carcinogenesis, such as diet and exposure to
environmental pollutants.13
26
Additionally, lower
socioeconomic status is associated with higher overall cancer mortality
rates.27
A prior analysis7
of four SEER
database sites, including metropolitan Detroit, found that the majority
of black cancer patients live in high-density areas with lower median
incomes and education levels, and that age-adjusted lung cancer
incidence rates were inversely related to family income and level of
education. Socioeconomic status is also linked to occupational
carcinogen exposure. Swanson and colleagues11
previously
evaluated the relationship between race, occupation, and lung cancer
risk in metropolitan Detroit, and reported that among occupations
associated with an increased risk of lung cancer, the risk in black men
was consistently greater than in white men. Diet has also been
implicated as a risk factor for lung cancer, with diets rich in fruits
and vegetables and low in fat being associated with a lower
incidence.28
In general, the diet of American blacks
contains more fat and fewer fruits and vegetables than that of
whites.26
In a case-control study, Swanson and
colleagues29
noted that whites ate more raw vegetables,
while blacks ate more preserved and processed meat with greater
carcinogenic potential. It is likely that various socioeconomic and
tobacco-related factors play a significant role in the observed racial
differences in lung cancer incidence.
In the present study, the incidence rates for younger men of both races
declined over time, but this decrease was greater in young white men,
resulting in an increase in the proportion of blacks among younger lung
cancer patients. Such age-specific trends were not noted in women. An
analysis of the metropolitan Detroit SEER database from 1973 to 1982
found that the incidence rates of 10 types of cancer, including lung
cancer, increased at a younger age in black than in white men, with
age-specific differences being much less prominent in
women.30
These data are surprising in view of the fact
that blacks generally start smoking at a later age, and suggest an
increased susceptibility to tobacco carcinogens in black men.
In recent years, adenocarcinoma has replaced squamous cell carcinoma as
the predominant histologic subtype of lung cancer in the United States,
a trend that may be due to the introduction of filter tip and lower tar
and nicotine cigarettes.1
31
Although the incidence of
squamous cell carcinoma declined more in blacks than in whites during
the study period, the overall incidence of squamous cell carcinoma
remained higher in both black men and black women. This finding may be
due to greater use of nonfiltered, high-tar, high-nicotine cigarettes
by blacks or the existence of more long-term black
smokers.6
19
Stage of disease at presentation is one of the most important
prognostic determinants in lung cancer. Most patients present with
regional-stage or distant-stage disease for which long-term survival
rates remain poor. In the present study, the incidence of distant-stage
disease was significantly higher in blacks, with a similar increase in
distant-stage disease over time in both races. However, the decline in
the incidence of potentially curable local-stage disease during the
study period was significantly greater in blacks. Although overall
shifts in stage may be attributed to improvements in staging methods,
the racial differences remain unexplained. Prior
studies32
33
have also demonstrated that black patients
with lung cancer are more likely to present with advanced disease and
poor performance status. Racial differences in health-care access and
attitudes may account for some of these findings.34
35
36
In the present study, we have noted that a survival gap between black
and white lung cancer patients has developed and widened significantly
in the past decade. This gap is primarily due to modest improvements in
the survival rates for white patients with local-stage and
regional-stage disease that were not seen in black patients. Various
factors may account for these survival differences, including stage at
diagnosis, performance status, comorbidity, and access to health care.
These factors may be more important in the treatment of regional-stage
disease, where the greatest change in black vs white survival has
occurred. Since the late 1980s, the improvement in survival of patients
with regional-stage lung cancer has been due to the widespread use of
combined modality therapy, which is logistically complicated,
expensive, and requires a good performance status, all of which may
impede the availability of this treatment to black patients with lower
socioeconomic status. One prior study14
reported
that survival differences between elderly black and white patients with
early stage lung cancer were due to lower surgical resection rates in
black patients despite the lack of any racial difference in
comorbidity. Previous studies have also noted that white patients
undergo significantly more cancer-directed surgery than black
patients.32
Although our multivariate analysis is limited by the available
variables, we did find that the complex variable of race was a
significant prognostic factor, with stronger influence in earlier stage
disease. However, prior studies33
37
38
suggested that
when performance status, therapy, and socioeconomic factors are
included in a multivariate model, race was no longer a significant
independent risk factor for lung cancer mortality. The impact of
performance status and therapy on outcome could not be assessed in this
study due to limitations in the data available through the SEER
database. Our analysis does confirm the prognostic predominance of
stage, suggesting that efforts aimed at early diagnosis could
significantly benefit all patients with lung cancer.
The results of the present study must be interpreted cautiously due to
the complex nature of the race variable and the limitations of the SEER
database. Overall, significant declines in the incidence and mortality
of lung cancer in some subsets of the population are truly encouraging.
However, several disturbing racial trends have developed recently,
including the lower relative decline in lung cancer incidence in
younger black men, the greater trend toward advanced-stage disease in
blacks, and the widening racial disparity in survival. These findings
clearly demonstrate a need to develop and implement more effective
preventative and therapeutic strategies that will have a positive
impact on all patients with lung cancer.
|
Acknowledgements
|
|---|
The authors are grateful to Mary L. Varterasian,
MD, for helpful discussion and insightful review of the article.
|
Footnotes
|
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Abbreviations:
MDCSS = Metropolitan Detroit Cancer Surveillance System;
SEER = Surveillance, Epidemiology, and End Results
Supported in part by Surveillance, Epidemiology, and End Results
contract No. N01-CN-65064 from the National Cancer Institute, Bethesda,
MD, and by the Charlotte A. Woody Lung Cancer Research Fund, Detroit,
MI.
Received for publication July 7, 2000.
Accepted for publication February 16, 2001.
|
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J. P. Wisnivesky, T. McGinn, C. Henschke, P. Hebert, M. C. Iannuzzi, and E. A. Halm
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M. L. Margolis, J. D. Christie, G. A. Silvestri, L. Kaiser, S. Santiago, and J. Hansen-Flaschen
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R. S. D. Higgins, C. Lewis, and W. H. Warren
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G. A. Finlay, B. Joseph, C. R. Rodrigues, J. Griffith, and A. C. White
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TOP
Abstract
Introduction
