Download Changing Relationship Between Socioeconomic Status and

Changing Relationship
Between Socioeconomic
Status and Prostate Cancer
Incidence
Lihua Liu, Wendy Cozen,
Leslie Bernstein, Ronald K. Ross,
Dennis Deapen
Background: Understanding the relationship between socioeconomic status
(SES) and prostate cancer incidence
could identify populations that should
be targeted for intervention and prevention programs. We examined this
relationship within the major racial/
ethnic groups during the period 1972
through 1997, which spans the introduction of prostate-specific antigen
(PSA) testing. Methods: We used data
from the population-based Los Angeles
Cancer Surveillance Program to examine age-adjusted prostate cancer incidence rates in five SES groups over
three specific calendar periods by racial/ethnic subpopulation (white, black,
Asian, and Hispanic) and by stage of
disease at diagnosis. Linear regression
analysis was used to test for trends in
the age-adjusted incidence rates that
were associated with increasing levels
of SES. All P values were two-sided.
Results: For men diagnosed with prostate cancer before 1987, when the test
for PSA was not widely available, we
found no association between SES and
the incidence of prostate cancer in any
of four racial/ethnic subpopulations or
between SES and the stage of disease at
diagnosis. In contrast, among men who
were diagnosed with prostate cancer
after 1987, SES was statistically significantly and positively associated with
prostate cancer incidence in men from
all racial/ethnic subpopulations except
Asians (P = .01 for white men, P = .001
for black men, P = .02 for Hispanic
men, P = .06 for Asian men, and P = .01
for all men combined). Higher SES was
statistically significantly associated
with cancers of earlier stage (P = .01 for
localized cancer and P = .00 for regional cancer) for men who were diagnosed with prostate cancer after 1987.
Conclusions: The association between
SES and prostate cancer incidence after 1987 may reflect more prevalent
PSA screening in populations with
higher SES due to their greater access
to health care. SES should, therefore,
be considered an important factor in
interpreting variations and time trends
in prostate cancer incidence. [J Natl
Cancer Inst 2001;93:705–9]
Socioeconomic status (SES) distinguishes subgroups within a population
from each other by economic opportunity,
education, lifestyle, and living environment. Socioeconomic environment can
influence health in many ways. For example, certain behaviors that are more
prevalent among individuals with low
SES than individuals of high SES (1,2),
such as tobacco smoking and excessive
alcohol consumption, have been causally
linked to lung, liver, and other cancers
(3,4) and to heart and non-cancer-related
pulmonary diseases. Understanding the
relationship between SES and cancer incidence may generate testable hypotheses
regarding the etiology of cancer and could
identify specific subpopulations that
would benefit the most from cancer intervention and prevention programs.
A number of studies have examined
patterns of SES among prostate cancer
patients. However, the methodologic approaches of these studies have varied, and
they produced inconsistent results, including reports of positive associations (5–
10), negative associations (11,12), and no
associations (13–23) between SES and
prostate cancer incidence. This inconsistency in results is likely to reflect the difficulty of obtaining an objective and reliable measurement of SES for cancer
incidence data.
One factor that could, in theory, affect
the relationship between SES and prostate
cancer incidence in recent years is the
prostate-specific antigen (PSA) blood
test. In 1986, the U.S. Food and Drug Administration (FDA) approved the PSA test
as a method to monitor the progression
of prostate cancer. The potential utility of
PSA testing as a cancer-screening tool
was quickly recognized and led to its
widespread use in early detection programs. The nationwide incidence of prostate cancer subsequently increased dramatically (24).
We were particularly interested to
know if the relationship between SES and
prostate cancer incidence would change
with the advent of the PSA test. We have
used data from the Los Angeles Cancer
Surveillance Program (CSP), the population-based cancer registry for Los Ange-
Journal of the National Cancer Institute, Vol. 93, No. 9, May 2, 2001
les County, CA, to examine the relationship between SES and prostate cancer
incidence among men who were diagnosed with prostate cancer during the
period from 1972 through 1997.
SUBJECTS
AND
METHODS
Identification of incident cases of prostate cancer by race/ethnicity of affected individual. The
CSP collected information on all male residents of
Los Angeles County who were diagnosed with primary invasive prostate cancer during the period
from 1972 through 1997 (n ⳱ 83 068). We examined this information for the date of cancer diagnosis, the race/ethnicity and the SES of the affected
individual, and the stage of the disease at diagnosis
to evaluate patterns of prostate cancer incidence
among different subpopulations in Los Angeles
County. Prostate cancer patients were classified into
five mutually exclusive racial/ethnic groups (white,
black, Hispanic, Asian, and “other”) on the basis
of information obtained from their medical records
and by the comparison of their surnames with those
contained on the U.S. Bureau of the Census 1980
Spanish surname lists. We used the same criteria
employed by the CSP to establish the race/ethnicity
of white men who were diagnosed with prostate
cancer: Only those men whose surnames appeared
on the list of Spanish surnames were classified as
Hispanic. Black men were not further distinguished
by Hispanic origin or Spanish surnames. The Asian
subgroup consisted of Chinese, Japanese, Korean,
and Filipino men. The remaining prostate cancer
patients, who included American Indians, Pacific
Islanders, and other very small groups of Southeast
Asians, were grouped together in the “other” category of race/ethnicity. The racial/ethnic composition of the prostate cancer patients in Los Angeles
County from 1972 through 1997 was 72.0% white,
14.1% black, 9.9% Hispanic, 3.3% Asian, and 0.7%
“other.” We excluded the men comprising the latter
subgroup (n ⳱ 546) from further analyses because it
was heterogeneous and contained less than 1% of
the prostate cancer patients in Los Angeles County.
Measurement of SES. We previously developed
a method for assigning an SES classification to each
cancer patient in the CSP database by using census
tract-specific population census data on median
household income and educational attainment for
adults aged 25 years and older who resided in each
census tract at the time of the 1970 census, the 1980
census, and the 1990 census (25). Census tracts in
the county were ranked separately by each of these
two characteristics for each census year. As a result,
Affiliations of authors: Department of Preventive
Medicine, Keck School of Medicine of the University of Southern California (USC), and USC/Norris
Comprehensive Cancer Center, Los Angeles, CA.
Correspondence to: Lihua Liu, Ph.D., Cancer
Surveillance Program, Department of Preventive
Medicine, Keck School of Medicine, University of
Southern California, 1540 Alcazar St., CHP-204,
Los Angeles, CA 90033 (e-mail: lihualiu@hsc.
usc.edu).
See “Notes” following “References.”
© Oxford University Press
REPORTS 705
each census tract had two ranking scores, one relating to income and one relating to educational level,
from each census. These two ranking scores were
equally weighted and summed for each census tract
for each census year to yield a composite ranking
score that defined SES. All census tracts in Los Angeles County for each census year were divided into
quintiles according to this composite ranking score.
The top quintile of census tracts has the highest
composite ranking score for SES and thus represents
the group of men with the highest SES (SES1). Likewise, the bottom quintile of census tracts includes
men with the lowest SES (SES5). The division of
census tracts into quintiles does not result in an
equal distribution of population of Los Angeles
County by quintiles. The classification of census
tracts by SES was irrespective of race/ethnicity.
Consequently, the population distribution by SES
also varies by race/ethnicity and does not necessarily
represent quintile distribution. Each prostate cancer
patient in our study was assigned the SES classification of the census tract in which he lived at the
time of his diagnosis. Men who were diagnosed
with prostate cancer during the period from 1972
through 1974 were assigned SES values derived
from the 1970 census; men who were diagnosed
with prostate cancer during the period from 1975
through 1984 were assigned SES values derived
from the 1980 census; men who were diagnosed
with prostate cancer in 1985 and later years were
assigned SES values derived from the 1990 census.
Because this method for assigning an SES classification requires that the patient’s address at diagnosis
be geographically coded into a census tract, we further excluded from our analysis 1818 prostate cancer
patients (2.2%) whose addresses could not be geographically coded.
Identification of stage of disease at prostate
cancer diagnosis. Complete information on the
stage of disease at prostate cancer diagnosis was
obtained from the CSP for men who were diagnosed
in 1977 or later. Because the information on the
stage of disease at prostate cancer diagnosis for men
who were diagnosed during the period from 1972
through 1976 was incomplete, we did not use it in
these analyses. The stage of prostate cancer at diagnosis was classified according to the Summary Staging Guide of the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER)
Program1 (26). Prostate cancer was classified as
localized if it was confined to the prostate gland and
had a tumor stage designation of T1 or T2; as regional if it extended beyond the prostate and had a
tumor stage of T3, T4, or N1; as distant if it had
metastasized and had a tumor stage designation of
M1; or as unknown if insufficient information was
available to assign a tumor stage.
Population estimates. We obtained annual estimates of the Los Angeles County population classified by sex, age, race/ethnicity, and SES for the
intercensal years of 1972 through 1979 and 1981
through 1989 by linearly interpolating results obtained from the 1970 census, the 1980 census, and
the 1990 census. We based our population estimates
for 1991 through 1997 on the 1990 census results
and the age-, sex-, and race-specific annual population growth rates estimated by the Department of
Finance of the State of California (27).
Statistical analysis. We calculated the ageadjusted incidence rates for prostate cancer by race/
706 REPORTS
ethnicity, SES, and stage of disease over time, using
the sex–age–race/ethnicity–SES-specific annual
population estimates as the denominators. Rates
were standardized to the 1970 U.S. population. We
performed a linear regression analysis to test for
trends in the age-adjusted incidence rates that were
associated with increasing levels of SES. All P values were two-sided.
RESULTS
We used the CSP database to examine
the incidence rate of prostate cancer in
different subpopulations of Los Angeles
County and found racial/ethnic differences in prostate cancer incidence that
persisted throughout the study period.
Black men had the highest prostate incidence rate, followed by white, Hispanic,
and Asian men (Fig. 1). For all groups
except Asians, the incidence rates of prostate cancer were relatively stable throughout the 1970s but then increased slightly
in the early 1980s. Little change in the
incidence rate of prostate cancer was observed among Asian men during this period. Following FDA approval of the PSA
test in 1986 and the subsequent adoption
of the PSA test as a screening tool for
prostate cancer, the incidence rates of
prostate cancer increased dramatically in
all racial/ethnic groups. From 1987
through 1992, the age-adjusted incidence
rates increased 110% among whites,
107% among blacks, 99% among Hispanics, and 106% among Asians (Fig. 1).
The age-adjusted incidence rate peaked
in 1992 among whites and Asians and in
1993 among blacks and Hispanics (Fig.
1). In each racial/ethnic group, the prostate cancer incidence rate dropped substantially after the peak, but it remained at
a level much higher than that of the prePSA era (Fig. 1).
We found no variations in the ageadjusted prostate cancer incidence rates
according to SES classification for men in
any racial/ethnic group who were diagnosed from 1972 to 1987, before the PSA
test was widely available (Table 1; Fig. 2,
A). In contrast, statistically significant
trends of increasing prostate cancer incidence with progressively higher levels of
SES were found for all men except Asians
(P ⳱ .01 for white men, P ⳱ .00 for
black men, P ⳱ .02 for Hispanic men,
P ⳱ .11 for Asian men, and P ⳱ .01 for
all men combined) who were diagnosed
with prostate cancer from 1988 through
1995, after the PSA test was widely available (Table 1; Fig. 2, B). The positive
relationship between SES and prostate
cancer incidence persisted for black, Hispanic, and white men diagnosed with
prostate cancer during the period from
1996 through 1997. Among Asian men,
the trend of a positive relationship between SES and prostate cancer incidence
became statistically significant only after
1995 (P ⳱ .04) (Table 1; Fig. 2, C).
For men who were diagnosed with
prostate cancer during the period from
1977 through 1987, SES was not associated with the stage of disease at diagnosis
(Fig. 3, A). For men who were diagnosed
with prostate cancer after 1987, however,
a higher SES was linked with earlier
stages of cancer at diagnosis. There were
positive and statistically significant trends
in the age-adjusted incidence rates of both
localized (P ⳱ .01) and regional (P ⳱
.00) disease with respect to SES (Fig. 3, B
and C). Higher SES also showed a weak,
albeit statistically significant (P ⳱ .02),
inverse relationship with the incidence of
prostate cancer diagnosed at a distant
stage after 1987 (Fig. 3, B and C).
Fig. 1. Time trends in the annual age-adjusted incidence
rates of prostate cancer by race/
ethnicity for Los Angeles
County, CA, from 1972 through
1997. Prostate cancer incidence
data by race/ethnicity were collected by the Los Angeles Cancer Surveillance Program. Rates
were standardized to the 1970
U.S. population.
Journal of the National Cancer Institute, Vol. 93, No. 9, May 2, 2001
Table 1. Average annual age-adjusted incidence rates of prostate cancer by SES, race/ethnicity, and calendar period for men in Los
Angeles County, CA, from 1972 through 1997*
Incidence rates (95% CIs) by socioeconomic group†
Calendar
period
Racial/ethnic
group
SES1 (high)
SES2
SES3
SES4
SES5 (low)
Ptrend‡
1972–1987§
White
Black
Hispanic
Asian
All
79.0 (77.1 to 81.0)
133.7 (114.6 to 152.8)
69.8 (57.9 to 81.6)
29.5 (22.8 to 36.3)
78.0 (76.1 to 79.8)
73.5 (71.7 to 75.3)
113.1 (97.6 to 128.6)
59.6 (51.5 to 67.6)
31.4 (24.9 to 37.9)
72.1 (70.4 to 73.8)
70.7 (68.9 to 72.4)
114.7 (103.2 to 126.1)
61.9 (56.0 to 67.9)
36.1 (30.3 to 41.9)
69.6 (68.0 to 71.2)
69.5 (67.5 to 71.5)
119.7 (112.7 to 126.7)
57.2 (52.8 to 61.6)
32.3 (27.4 to 37.3)
70.2 (68.6 to 71.9)
71.1 (68.4 to 73.9)
116.5 (111.8 to 121.1)
60.4 (56.9 to 64.0)
31.8 (27.2 to 36.4)
76.0 (74.1 to 77.9)
.09
.36
.19
.55
.69
1988–1995§
White
Black
Hispanic
Asian
All
171.5 (168.0 to 174.9)
301.0 (272.8 to 329.2)
257.6 (226.9 to 288.3)
55.1 (47.8 to 62.3)
167.9 (164.7 to 171.1)
140.2 (136.9 to 143.5)
262.8 (240.8 to 284.7)
163.0 (148.5 to 177.6)
59.4 (52.6 to 66.2)
137.7 (134.7 to 140.6)
126.9 (123.4 to 130.3)
228.4 (211.4 to 245.4)
135.4 (125.9 to 145.0)
56.8 (50.7 to 62.9)
124.4 (121.6 to 127.3)
112.1 (108.1 to 116.2)
206.3 (196.3 to 216.3)
106.0 (99.7 to 112.4)
51.7 (46.4 to 57.0)
114.5 (111.7 to 117.3)
103.4 (97.5 to 109.4)
168.4 (160.8 to 175.9)
93.0 (87.6 to 98.3)
41.8 (36.5 to 47.1)
106.0 (103.0 to 109.1)
.01
.00
.02
.11
.01
1996–1997§
White
Black
Hispanic
Asian
All
181.0 (173.8 to 188.2)
319.9 (265.8 to 374.0)
213.5 (166.4 to 260.7)
66.0 (52.4 to 79.5)
173.6 (167.1 to 180.1)
134.3 (127.6 to 141.1)
352.0 (393.9 to 400.1)
147.3 (123.9 to 170.6)
60.4 (48.9 to 72.0)
132.9 (127.2 to 138.7)
124.0 (116.8 to 131.1)
259.7 (226.0 to 293.3)
126.8 (111.2 to 142.4)
55.8 (45.5 to 66.1)
122.1 (116.5 to 127.7)
108.1 (99.5 to 116.7)
221.7 (202.0 to 241.4)
114.0 (102.7 to 125.3)
55.3 (46.0 to 64.7)
114.7 (109.3 to 120.2)
100.2 (87.3 to 113.0)
142.1 (128.4 to 155.7)
75.7 (67.3 to 84.1)
32.5 (24.4 to 40.6)
86.4 (81.2 to 91.6)
.02
.02
.01
.04
.01
*Prostate cancer incidence data by race/ethnicity were collected by the Los Angeles Cancer Surveillance Program. Rates were standardized to the 1970 U.S.
population. SES ⳱ socioeconomic status; CI ⳱ confidence interval.
†SES estimates were based on the quintiles of total census tracts in the county ranked by education and income. Quintiles of census tracts do not result in an equal
distribution of population by quintiles. The population distribution by SES also varies by race/ethnicity.
‡All P values are two-sided. Linear regression analysis was used to test the statistical significance.
§Time period during which men were diagnosed with prostate cancer.
Fig. 2. Average annual age-adjusted incidence rates of prostate cancer by socioeconomic status (SES) and race/ethnicity in Los Angeles County, CA. Prostate cancer incidence data by race/ethnicity were collected by the Los Angeles
Cancer Surveillance Program. SES estimates were based on quintiles of total
census tracts in the county ranked by education and income. Rates were standardized to the 1970 U.S. population. A) Relationship between SES and prostate
cancer incidence by race/ethnicity for men diagnosed with prostate cancer during
the period from 1972 through 1987, before the prostate-specific antigen (PSA)
test became available. B) Relationship between SES and prostate cancer inci-
DISCUSSION
Our analyses of the relationship between SES and prostate cancer incidence
during the period 1972 through 1997
shows that until 1987, when PSA testing
became widely available, there was no
relationship in any racial or ethnic group.
However, after 1987, a strongly positive
dence by race/ethnicity for men diagnosed with prostate cancer during the period
from 1988 through 1995, after PSA testing was introduced into clinical practice
and was widely used as a screening tool. Prostate cancer incidence rates peaked
for all racial/ethnic groups during this time period. C) Relationship between SES
and prostate cancer incidence by race/ethnicity for men diagnosed with prostate
cancer during the period from 1996 through 1997. Prostate cancer incidence
rates declined from their peak levels during this time period, but they remained
at levels higher than those observed before PSA testing became available.
and statistically significant relationship
appeared among all racial/ethnic populations except Asians. A positive relationship between SES and prostate cancer incidence was not evident in Asian men
until after 1995. The higher prostate cancer incidence rates with increasing SES
after PSA testing became available suggest that PSA screening was used differ-
Journal of the National Cancer Institute, Vol. 93, No. 9, May 2, 2001
ently by men in different SES groups,
regardless of their race or ethnicity. We
also found that men in the higher SES
groups were diagnosed more frequently
with localized disease than were men in
the lower SES groups. Likewise, men of
high SES were diagnosed less frequently
with distant disease than were men of low
SES. These trends further support the
REPORTS 707
Fig. 3. Average annual age-adjusted incidence rates of prostate cancer by socioeconomic status (SES) and stage of disease at diagnosis in Los Angeles
County, CA, for all races combined. Prostate cancer incidence data by stage of
disease at diagnosis were collected by the Los Angeles Cancer Surveillance
Program. The stage of prostate cancer at diagnosis was classified as localized if
it was confined to the prostate gland, as regional if it extended beyond the
prostate, as distant if it had metastasized, or as unknown if insufficient information was available to assign a tumor stage. SES estimates were based on
quintiles of total census tracts in the county ranked by education and income.
Rates were standardized to the 1970 U.S. population. A) Relationship between
SES and prostate cancer incidence by stage of disease at diagnosis for men
likelihood that access to PSA testing has
contributed to the changing relationship
between SES and prostate cancer incidence in recent years.
Our data support a familiar social phenomenon; i.e., individuals with greater
resources are more likely to benefit from
improvements in the detection of disease,
in treatments of disease, or in knowledge
about disease risks than individuals with
limited resources, who are disadvantaged
with respect to access, quality, and utilization of medical services (28,29). Despite having higher prostate cancer incidence rates, men of higher SES have a
better prostate cancer survival than men
of lower SES (10,30), almost certainly
due in large part to the early detection
provided by PSA testing.
It is not clear if the widespread use of
the PSA test and the dramatic increase in
prostate cancer incidence rate have contributed directly to any changes in prostate cancer mortality. Prostate cancer
mortality increased nationwide during the
late 1980s. That trend decreased substantially from 1991 through 1995 (24), even
though the magnitude of the decline in
mortality during this period was small
when compared with the dramatic increase in prostate cancer incidence. The
effect of PSA screening on prostate cancer mortality is not known (24,31–33).
708 REPORTS
diagnosed with prostate cancer during the period from 1977 through 1987,
before the prostate-specific antigen (PSA) test became available. B) Relationship
between SES and prostate cancer incidence by stage of disease at diagnosis for
men diagnosed with prostate cancer during the period from 1988 through 1995,
the time period during which PSA testing was introduced to clinical practice and
widely used and during which prostate cancer incidence rates for all racial/ethnic
subpopulations peaked. C) Relationship between SES and prostate cancer incidence by stage of disease at diagnosis for men diagnosed with prostate cancer
during the period from 1996 through 1997. Prostate cancer incidence rates declined from their peak levels during this time period, but they remained at levels
higher than those observed before PSA testing became available.
However, in Los Angeles County, the
age-adjusted prostate cancer mortality
rate was relatively stable from 1988
through 1997 among different racial/
ethnic populations; i.e., no statistically
significant changes were observed (our
unpublished data, available upon request).
These findings imply that there has been
no effect of PSA screening on prostate
cancer mortality in Los Angeles County.
Whether differential PSA screening by
SES will eventually affect mortality in
these groups differently is a matter of
conjecture at this point.
Whether or not PSA testing affects
prostate cancer mortality, the widespread
use of PSA testing has resulted not only
in the early detection of prostate cancer
but also in the discovery of a high proportion of latent and non-life-threatening
tumors (34). Screening has been an important means of controlling other cancers
(e.g., breast cancer and cervical cancer).
However, the specific benefits of screening for prostate cancer are uncertain
(35,36). The relationships between the
benefits of PSA testing and the potentials
for overdiagnosis and overtreatment resulting from PSA testing need to be carefully evaluated.
To our knowledge, this is the first
study to examine the relationship between
SES and prostate cancer incidence with
respect to the time periods before and after PSA testing became widely available.
Our measurement of SES, in contrast with
measurements used in previous studies
(5–23) on the relationship between SES
and prostate cancer incidence, was based
on a composite index that considered the
combined impact of education and income—two important indicators of SES.
The capability of capturing the changing
SES gradient in the incidence of prostate
cancer among diverse racial/ethnic populations demonstrates the usefulness and
the sensitivity of our SES measurement.
In conclusion, our data suggest that
SES is an important factor that has a substantial impact on prostate cancer diagnosis and secular trends in prostate cancer
incidence.
REFERENCES
(1) Stellman SD, Resnicow K. Tobacco smoking,
cancer and social class. IARC Sci Publ 1997;
138:229–50.
(2) Moller H, Tonnesen H. Alcohol drinking, social class and cancer. IARC Sci Publ 1997;138:
251–63.
(3) International Agency for Research on Cancer
(IARC). IARC Monogr Eval Carcinog Risks
Hum. Vol 38. Tobacco smoking. Lyon (France):
IARC; 1986.
(4) International Agency for Research on Cancer
(IARC). IARC Monogr Eval Carcinog Risks
Hum. Vol 44. Alcohol drinking. Lyon (France):
IARC; 1988.
Journal of the National Cancer Institute, Vol. 93, No. 9, May 2, 2001
(5) Richardson IM. Prostatic cancer and social
class. Br J Prev Soc Med 1965;19:140–2.
(6) Ross RK, McCurtis JW, Henderson BE,
Menck HR, Mack TM, Martin SP. Descriptive
epidemiology of testicular and prostatic cancer
in Los Angeles. Br J Cancer 1979;39:284–92.
(7) Rimpela AH, Pukkala EI. Cancer of affluence:
positive social class gradient and rising incidence trend in some cancer forms. Soc Sci Med
1987;24:601–6.
(8) Yu H, Harris RE, Wynder EL. Case–control
study of prostate cancer and socioeconomic
factors. Prostate 1988;13:317–25.
(9) Williams J, Clifford C, Hopper J, Giles G. Socioeconomic status and cancer mortality and
incidence in Melbourne. Eur J Cancer 1991;27:
917–21.
(10) Harvei S, Kravdal O. The importance of marital and socioeconomic status in incidence and
survival of prostate cancer. An analysis of
complete Norwegian birth cohorts. Prev Med
1997;26:623–32.
(11) Dorn JF, Cutler SJ. Morbidity from cancer in
the United States. Public Health Service,
Monogr No. 56. Washington (DC): U.S. Govt
Print Off; 1958.
(12) Gorey KM, Vena JE. The association of near
poverty status with cancer incidence among
black and white adults. J Community Health
1995;20:359–66.
(13) Clemmesen J, Nielsen A. The social distribution of cancer in Copenhagen, 1943 to 1947. Br
J Cancer 1951;5:159–71.
(14) Graham S, Levin M, Lilienfeld AM. The socioeconomic distribution of cancer of various
sites in Buffalo, N.Y., 1948–52. Cancer 1960;
13:180–91.
(15) Wynder EL, Mabuchi K, Whitmore WF. Epidemiology of cancer of the prostate. Cancer
1971;28:344–60.
(16) Krain LS. Some epidemiologic variables in
prostatic carcinoma in California. Prev Med
1974;3:154–9.
(17) Ernster VL, Winkelstein W Jr, Selvin S,
Brown SM, Sacks ST, Austin DF, et al. Race,
socioeconomic status, and prostatic cancer.
Cancer Treat Rep 1977;61:187–91.
(18) Ernster VL, Selvin S, Sacks ST, Austin DF,
Brown SM, Winkelstein W Jr. Prostatic cancer:
mortality and incidence rates by race and social
class. Am J Epidemiol 1978;107:311–20.
(19) Blair A, Fraumeni JF Jr. Geographic patterns
of prostate cancer in the United States. J Natl
Cancer Inst 1978;61:1379–84.
(20) Williams RR, Horm JW. Association of cancer
sites with tobacco and alcohol consumption
(21)
(22)
(23)
(24)
(25)
(26)
(27)
(28)
(29)
(30)
(31)
and socioeconomic status of patients: interview
study from the Third National Cancer Survey.
J Natl Cancer Inst 1977;58:525–47.
Hakky SI, Chisholm GD, Skeet RG. Social
class and carcinoma of the prostate. Br J Urol
1979;51:393–6.
Baquet CR, Horm JW, Gibbs T, Greenwald P.
Socioeconomic factors and cancer incidence
among blacks and whites. J Natl Cancer Inst
1991;83:551–7.
La Vecchia C, Negri E, Franceschi S. Education and cancer risk. Cancer 1992;70:2935–41.
Stanford JL, Stephenson RA, Coyle LM, Cerhan J, Correa R, Eley JW, et al. Prostate cancer
trends, 1973–1995. SEER Program, National
Cancer Institute. NIH Publ No. 99–4543.
Bethesda (MD): National Cancer Institute;
1999.
Liu L, Deapen D, Bernstein L. Socioeconomic
status and cancer of the female breast and reproductive organs: a comparison across racial/
ethnic populations in Los Angeles County,
California (United States). Cancer Causes Control 1998;9:369–80.
Cancer Surveillance, Epidemiology, and End
Results Reporting (SEER) Program. Summary
staging guide. NIH Publ No. 86–2313. Bethesda
(MD): National Institutes of Health, Public
Health Service, U.S. Department of Health and
Human Services; 1977.
State of California, Department of Finance.
Race/ethnic population with age and sex detail,
1970–2040. Sacramento (CA): State of California, Department of Finance; December
1998.
Adler NE, Boyce T, Chesney MA, Cohen S,
Folkman S, Kahn RL, et al. Socioeconomic
status and health. The challenge of the gradient. Am Psychol 1994;49:15–24.
Bennett CL, Ferreira MR, Davis TC, Kaplan J,
Weinberger M, Kuzel T, et al. Relation between literacy, race, and stage of presentation
among low-income patients with prostate cancer. J Clin Oncol 1998;16:3101–4.
Dayal HH, Polissar L, Dahlberg S. Race, socioeconomic status, and other prognostic factors for survival from prostate cancer. J Natl
Cancer Inst 1985;74:1001–6.
Hankey BF, Feuer EJ, Clegg LX, Hayes RB,
Legler JM, Prorok PC, et al. Cancer Surveillance Series: interpreting trends in prostate
cancer—Part I: Evidence of the effects of
screening in recent prostate cancer incidence,
mortality, and survival rates. J Natl Cancer Inst
1999;91:1017–24.
Journal of the National Cancer Institute, Vol. 93, No. 9, May 2, 2001
(32) Feuer EJ, Merrill RM, Hankey BF. Cancer
Surveillance Series: interpreting trends in prostate cancer—Part II: Cause of death misclassification and the recent rise and fall in prostate
cancer mortality. J Natl Cancer Inst 1999;91:
1025–32.
(33) Etzioni R, Legler JM, Feuer EJ, Merrill RM,
Cronin KA, Hankey BF. Cancer Surveillance
Series: interpreting trends in prostate cancer—
Part III: Quantifying the link between population prostate-specific antigen testing and recent
declines in prostate cancer mortality. J Natl
Cancer Inst 1999;91:1033–9.
(34) Catalona WJ, Smith DS, Ratliff TL, Basler JW.
Detection of organ-confined prostate cancer is
increased through prostate-specific antigenbased screening. JAMA 1993;270:948–54.
(35) Krahn MD, Mahoney JE, Eckman MH, Trachtenberg J, Pauker SG, Detsky AS. Screening for
prostate cancer. A decision analytic view.
JAMA 1994;272:773–80.
(36) Waterbor JW, Bueschen AJ. Prostate cancer
screening (United States). Cancer Causes Control 1995;6:267–74.
NOTES
1
Editor’s note: SEER is a set of geographically
defined, population-based, central cancer registries
in the United States, operated by local nonprofit organizations under contract to the National Cancer
Institute (NCI). Registry data are submitted electronically without personal identifiers to the NCI on
a biannual basis, and the NCI makes the data available to the public for scientific research.
Cancer incidence data were collected under a subcontract with the Public Health Institute, Berkeley,
CA, which manages the regional contracts for the
California Cancer Registry. The subcontract is supported by the California Department of Health
Services as part of its statewide cancer-reporting
program, as mandated by Health and Safety Code
Sections 103875 and 103885. Support was also
provided by Public Health Service contract
N01CN67010 from the NCI, National Institutes of
Health, Department of Health and Human Services.
The ideas and opinions expressed herein are those
of the authors, and no endorsement by the State
of California, Department of Health Services, or
the Public Health Institute is intended or should be
inferred.
We thank Frances Wang for programming assistance.
Manuscript received August 16, 2000; revised
February 13, 2001; accepted February 26, 2001.
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