Philip Morris
Women and Lung Cancer: A Comparison of Active and Passive Smokers with Nonexposed Nonsmokers
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Cancer Detection ana Pretierttion, li8(6):321-330 (1994)
Women and Lung Cancer: A Comparison
of Active and Passive Smokers with
Nonexposed Nonsmokers
G. H. Miller, Ph.D., C. P. C., F.A.I. C.,a Joseph A. Golish, M.D., F.A. C. P.,
F.C.C.P.,b Charles E. Cox, M.D., F.A.C.S.,c and Donna C. Chacko, M.D.d
Stud+'es on Smoking, Inc., 125 High Street, Edinboro, PA 16412; °Department of Pulmonary
Disease, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44106; °8reast,
Cancer Center, H. Lee Moffit Cancer Center, 12902 Magnolia Drive, Tampa, FL 33682-0179;
and °Radiation Oncology Center, Palms of, Pasadena Hospital, St. Petersburg, FL 33707
A,ddross rcpnnt requests to Dr. G. H. Mi1kr.
ABSTRACT: Prior to the 1920s. lung cancer was a rare disease. However, the current increase in lung
cancer
appears to parallel the increase in smoking for both men and women wittt a 30- to 50-year delay:
National lung
cancer deaths continue to rise, with over 168.000totsl deaths estimated in 1992. VS%omen are now
showing higher
percenta¢e increases in lung cancer than men from active smoking. ~
The data from the Ene County Study on Smoking and Health (ECSSH), a population study. were used to
measure the effects of both active and passive smoking on women's lung cancer mortaliry: The three
major
categories of exposure (no known or minimal exposurepa.ssive smoking exposed, and active smoking)
were used
in the analyses.
The results from the population data in Erie County; PA, were based on 528 nonexposed nonsmoking
women. 3138 exposed nonsmoking women, and 1747 smoking women, Deaths due to lung cancer as a
percentage
of total deaths excluding traumatic deaths were 0.2% for the nonexposed nonsmoking women. 0.9% for
the
exposed nonsmoking women. and 8.0% for women who smoked The data showed'that women smokers died of
lung cancer ara rate 9 times greater than exposed'nonsmokers and42 times greater than nonexposed
nonsmokers.
KEY WORDS: life expectancy, lung cancer, mortality, passive smoking, second hand smoke,smoking,
women.
1. INTRODUCTION
Prior to the 1920s, lung cancer was a rare
disease.' Since that time the number of cases has
increased substantially. The American Cancer
Society estimated that over 168,0001ung cancer
deaths would be reported in the U.S. in 1992.2
The increased incidence of lung cancer cases ap-
pears to parallel the number of years of smoking
by both men and women.
During WW I and WW II, military personnel
were provided with cigarettes and smoking be-
came an accepted behavior pattern. Extensive
advertising by the cigarette companies glamoriz-
ing cigarettes made such deep inroads into the
American subconscious that over 60% of the male
0361-090XJ94/5.50
® 1994 by CRC Press, Inc.
population became cigarette smokers. Prior to WW
II few women smoked; after WW II over 30% of
the adult women reported themselves as smoking
regularly.
A number of studies in the 1940s, 1950s, and
1960s reported on the dangers of cigarette smok-
ing.3 The results of these studies were summa-
rized in a 1964 report prepared by Dr. Luther
Terry, the Surgeon General, showing how devas-
tating smoking is to health.3 The mortality rate
from lung cancer for men became significantly
higher than that of any other type of cancer.
The early reports on lung cancer in women
did not show a high mortality rate. However, the
cumulative smoking years of women compared
with men were very small at that time and thus
421

Women vnd'Lung Cancer
did not show the same high lung cancer mortality
rates as men.' Both health professionals and the
public, therefore, came to believe that women,
because of their low rate of lung cancer, were less
susceptible to the detrimental effects of cigarette
smoking than were men.
However, as more and more women contin-
ued to smoke and were joined by women in
younger age groups, mortali'ty and morbidity rates
increased dramatically for women. Lung cancer
mortality rates over the last 25 years for women
cigarette smokers has increased as much as 500%
and~ appears to have superseded breast cancer as
the prime cancer killer among women 3 Cigarette
smoking, apparently, is now achieving the same
devastating effect on women as it has on men
when cumulative years of smoking are taken into
account, as shown in Figure 1 where the percent-
age of lung cancer of women is converging with
that of men.
The most recent research on lung cancer
among women has examined active smoking and
exposure of nonsmokers to carcinogens in to-
bacco smoke, which has been classified as pas-
sive smoking. tobacco smoke pollution, or invol-
untary smoking. Before the late 1970s, passive
smoking has been assumed to have few harmful
effects for either men or women:
The recent review of the literature on passive
smoking and lung cancer can be separated into
three different types of reports: (a) comparisons
of active and passive smoking,b-12 (b) passive
smoking only;"-2' and (c) reviews summarizing
the effects of passive smoking.=5-'0 Nearly all of
the reports support the conclusiom that passive
smoking is responsible for lung cancer in non-
smoking women. Results from the Erie County
Study on Smoking and Health (ECSSH), which
was designed to provide population-based data
that could contribute the most representativeness
to the subsamples selected for analysis, are re-
ported in this article.
II. METHODS
Data from the ECSSH are based~on informa-
tion obtained from the Northwestern Pennsylva-
nia Study on Smoking and Health (NPSSH): -
now renamed the ECSSH because the data includes
only deceased residents of Erie County.4113 This
population study was initiated in 1973 to determine
0 10 20 30 40 50 60 70 80 90
PERCENTAGE OF LUNG CANCER DEATHS
FIGURE 1. Comparison of lung cancer deaths; male vs. female from 1955.
422

retrospectively the smoking habits of all deceased
residents (t-oth male and female) of Erie County,
PA. All information was based on telephone in-
terviews with close relatives of the decedents.
The standardized interview form was devel-
oped cooperatively by the director of the study,,
members of the local health associations, and the
Pennsylvania Department of Health. The inter-
view forms were designed so that the important
data could be obtained in a minimum amount of
time so as not to burden unnecessarily the rela-
tives being interviewed. Information was collected
on the decedent's smoking history - type of
tobacco used, amount used, lifetime duration of
smoking, amount of inhalation (none to deep),
percentage of tobacco product smoked (quartiles),
attempts to quit smoking, age at which the dece-
dent started smoking, occupation, other possible
moderate or high-pollution exposures, amount of
exercise. height and weight, cause of death and
diseases prior to death, including length of time
for these diseases.
In order to obtain information relating to pas-
sive smoking, additional questions were incorpo-
rated into the questionnaire concerning the smok-
ing histories of the spouses and parents of the
deceased (amount of their smoking, whether or
not they stopped smoking, age at death, year of
death, diseases and cause of death) and whether
the deceased had additional exposure in the house-
hold or other locations. In addition, information
was obtained on other sources of exposure out-
side of the household such as bingo halls and card
games where smoking is permitted. This informa-
tion was used to establish estimates of length of
exposure from all sources of tobacco smoke from
spouses. parents, others in the household, or from
other environments. This detailed type of data
have not been available in most studies on active
or passive smoking and provides important infor-
mation from detailed population data that can be
used to demonstrate the detrimental impact of
these forms of tobacco exposure.
Death notices and obituaries from the Erie
County newspapers for the years 1972 to 1976
and 1979 to 1984 provided the names of almost
every person who died in Erie County along with
the names of their closest surviving relatives. Lists
of all the deceased provided by the Pennsylvania
Department of Health made it possible to locate
Cancer Detecrion and Prevention
all those decedents who were not declared resi-
dents of Erie County, who died from accidental
causes, or who were under 30 years of age. In
order to provide the best estimates of the full
impact of both active and passive smoking, all
deaths listed as due to accident, homicide, or
suicide, all decedents under age 30, and all non-
residents of Erie County were omitted from the
analysis. Eliminating these members in the above
categories reduced the total population size by
approximately 23%.
In order to obtainl complete information on
the smoking histories of the decedents, as such
detailed informationi is not available in hospital or
other medical records, telephone numbers were
sought for up to three surviving relatives for each
decedent listed in the death notices and obituaries
in the Erie County newspapers. In Pennsylvania,
these listings provided the nearly complete popu-
lation of the deceased for all counties for each
year. Telephone numbers were obtained for 85%
of the surviving, relatives by research assistants
making use of telephone books for the different
years, which were supplied by the General Tele-
phone company (GTE).
The director of the study and interviewers
who were trained by the director called the
decedent's relatives up to a maximum of six times
for their responses and were able to contact 90%
of those called. Interviewers did not know the
cause of death while gathering the data. The inter-
viewers asked the relatives of the deceased the
cause of death of the deceased and any prior
illness. Although the cause of death obtained by
the interviewer was listed on the interview form,
only the designated cause of death based on the
Intemational Classification of Diseases (ICD)
codes were used in the final coding and analysis.
The ICD codes for all the deceased were provided
by the Pennsylvania Department of Health for
each year that was used in the analysis. A com-
parison of the accuracy of the off cial ICD code
and the reported diseases by the close relatives
showed high reliability in the range of 85 to 90%.
The additional diseases prior to death were re-
corded with the designated ICD code. Of the rela-
tives contacted, 95% cooperated in the study..
Three major categories of exposure were des-
ignated for the study. The fust was the nonexposed
category (NX) that contained only those women
423

Women and Lung Cancer
who had no known reported exposure to obacco
smoke. Although it is unlikely that anyone could
have avoided all tobacco exposure during their
lifetime, the nonexposed category was established
to classify decedents who had no known exposure
or at most a very limited exposure to tobacco
smoke.
The second category, the passive smoking
exposed group (EX), includes those nonsmoking
women who were reported to have had moderate
(20 years) to lifetime tobacco smoke exposure,
that is, women ~ nonsmokers with sources of expo-
sure to tobacco smoke such as a smoking spouse,
additional smokers in the home, smokers in the
workplace, and exposure in other environments.
Inasmuch as only two of the nonsmoking women
who contracted lung cancer had less than 20 years
exposure, 20 years exposure was selected as the
minimal exposure to passive smoking for these
analysis. The specific category of 20 years was
selected for those deceased who were exposed by
one or more parents since a pilot project estab-
lished 20 years as the best approximation for
childhood exposure. The 20 years was then: added
to the years of exposure by the spouse to obtain
the total years of exposure for those exposed dur-
ing childhood. If there was no childhood expo-
sure. then only the exposure by the spouse was
considered. In the present study no further break-
down of the categories of 20 years to lifetime
exposure was completed'as the ana]ysis was made
prior to the completion of the 20-year study -
1972 to 1991.
The third category, the active smoking cat-
egory (SM), was defined as women who smoked
more than 20 packs of cigarettes during their
lifetime.
Data were gathered for approximately 55%
of the deaths among Erie County women for the
months completed in the years 1972 to 1976 and
1979 to 1984. A total of 5413 interviews were
obtained from relatives of the deceased women:
3666 nonsmoking women - 528 NX, 3138 EX
- and 1747 Smoking women. Cause of death as
reported on the death certificate, supplied by the
Pennsylvania Department of Health listings, was
used for the analysis of the data following the
assumption that the physicians listing of cause of
death would be more accurate than that of the
relative's designations.
The decedents were placed into one of the
three different exposure categories for coding
according to the information obtained from their
smoking history as noted above (NX, EX, SM).
The population data were analyzed to deterrnine
the effects of both active and passive smoking as
wellias to determine the effects on those who have
had little to no exposure during their lifetime.
This report deals with comparisons of these three
levels of exposure of the population data to esti-
mate the incidence of lung cancer caused by the
different exposure levels.
In addition, the retrospective case-control tech-
nique, as embodied in the National Cancer
Institute's newest software, EPI INFO (Version 5),
was used to determine levels of significance. Lung
cancer deaths (cases) were computed as a percent
of total deaths (controls) for all three categories for
the analysis. Statistical analysis utilizing odds ra-
tios (OR) and standard mortality ratios (SMR) were
computedL
III. RESULTS
The results of the analysis of the population
data from the three groups of exposure levels is
presented in Figure 2. One of 528 deaths (0.2%)
among women with no known exposure to to-
bacco smoke (NX category) was due to lung can-
cer. Of 3138 deaths, 27 (0.9%) among nonsmok-
ing women who were exposed to some sources of
tobacco smoke (EX category) were reported as
due to lung cancer. Among women with a known
smoking habit (SM category), which included
former smokers and late-starting smokers, 140 of
the 1747 deaths (8.096) were due to lung cancer.
A comparison of the population of lung can-
cer deaths obtained in the Erie County Study on
Smoking and Health with the actual, population of
lung cancer deaths as a percentage of total deaths
for women in Erie County reported for the years
1972 to 1976 and 1979 to 1984 is found in Fig-
ure 3.
Using lung cancer as the cases and non-lung
cancer as the controls the three categories of ex-
posure levels were analyzed using the chi-square
test to determine any signif cant trends. A highly
significant chi-square value of 207 (p <001) was
computed for the 3 x 2 table (refer to Table I). The
424

Cancer Detecrior+ and Prerenrlort
NONEXPOSED EXPOSED SMOKING
LEVELS OF EXPOSURE
FIGURE 2. Lung cancer: nonexposed nonsmokers with exposed nonsmokers and
active smokers.
FiGURE 3. Erie County lung cancer data: Erie County data vs. Pennsylvania Department
of Health idata.

Womerr and Lung Cancer
TABLE I
A Retrospective Case-Control Analysis of the Erie County Population Data
of Women and Lung Cancer with the Comparison of Three Different
Groups: Nonexposed (NX), Exposed (EX) and Smoking (SM)
Group
NX Controls
(non-lung cancer)
527 Cases
(lung cancer)
1
Total
528
EX 3111 27 3138
SM 1607 140 1747
5235 168 5413
Chi-square anaJysis (3 x 2 table) - 207 p<0:00000001
Group Comparisons (2 x 2 tables)
Groups Odds ratio (confidence Intervals) Chi-square Prob. (test)
NX vs. EX 4.57 (0.67 < OR < 90.71) 1.87 0.07 (FISHER EXACT)
NX vs. SM 45.91 (6.97 < OR < 886.97) 41.36 0.000001 (YATES)
EX vs. SM M04 (6.51 < OR < 15.57) 171.76 0.000001 (YATES)
2 x 2 comparisons also showed significant re-
sults. A comparison of the NX and EX groups
showed a nearly significant chi-square value of
1.87 (p = 0.07). The comparison of the NX and
SM groups produced a highly significant OR of
45.91 (p <0.0001). The comparison of the EX and
SM groups also yielded another significant OR of
10.04 (p <0.0001).
The results (shown in Table II) of age adjust-
ment of the data based on observed death.rates in
Erie County show significant SMRs for nonsmok-
ing nonexposed (SMR = 17, p<0.01), passive
smoking (SMR = 37, p<0:001) and active smok-
ing (SMR = 170,,p <0.001).
IV. DISCUSSION
The data from this population study of 5-11'3
deaths among women in Erie County show some
very specific trends. Few women who had no
known exposure to tobacco smoke died of lung
cancer: only 1 in 528 deaths. The low rate of lung
cancer for the nonexposed nonsmoking women is
TABLE il
Age-Adjusted Data for Lung Cancer Making Use
of Erie County Death Rates to Compare
Nonsmoking Nonexposed Women with Both
Nonsmoking Exposed Women and Active
Smokers
Category Expected Observed SMR Probability
NX 5.8 1 17 .02
EX 45.7 17 37 .001
SM 44.6 76 170 .001 ~
Note: NX - nonsmoking nonexposed women; EX - ex-
posed nonsmoking women; SM - smoking women;
SMR - standard mortality ratio where the expected =
100%.
426

consistent with the results of a population study12
on- a comparison of lung cancer cases between
Amish and non-Amish men and women in
Lancaster County, PA. The single lung cancer
case reported among the Amish in the analysis of
the data from the Lancaster County Cancer Reg-
istry from 1971 to 1977 was that of a male cigar
smoker. Among the Lancaster County population
there were 3-18 deaths from lung cancer for women
out of approximately 16,000 total deaths for that
time period. During this time period very few
Amish smoked, and thus. they are one of the best
examples of a nonsmoking popul'ation in the U.S.
For the period studied there was not a single case
of lung cancer among the nonsmoking Amish
population.
For those women in the EX group, the pro-
portion of lung cancer deaths is 4.5 times higher
than those in the NX group, with lung cancer
reported in about 9 in 1000 deaths. This result is
consistent with the conjecture that exposure to
ambient levels of tobacco smoke does increase
the risk of lung cancer. Approximately 8.0% of
the deaths among SM women were due to lung
cancer, 42 times greater than in~ NX wornen and 9
times greater than those who were exposed to
passive smoking. Because of the vast differences
in lung cancer mortality among the three different
groups, NX, EX, and SM, of women, it can be
concluded that both active and passive smokers
are much more likely to die of lung cancer than
those women who had no known or minimal ex-
posure (Figure 2).
Figure 3 shows the percentage of deaths
due to lung cancer in this study (1:68 of the total
5413 decedents) is 3.1 %. The data reported
from the Pennsylvania Department of Health
for lung cancer for women in Erie County for
.he same time period is 360 cases of lung can-
cer of a total of 13,329 deaths among women,
or 2.7%. Thus, the data from the completed
interviews are very close to the actual lung
cancer death rate for Erie County, indicatingg
that the data from this population is likely to be
most representative of the actual total popula-
tion for that time period.
The computation of the SMRs is indicated in
Table II. The SMR in this instance is based on the
"observed" death rates of lung cancer for the
Cancer Detecnon~and'Preventton
three different categories of exposure (NX. EX,
SM) relative to the "observed" death rates of lung
cancer in the age-adjusted population of the women
in Erie County during the years under consider-
ation~ without regard to smoking exposure. The
comparison of the "observed" lung cancer death
rates with the "expected" lung cancer death rates
for these categories resulted in the following rela-
tive rates: 17% for NX, 37% for EX, and 170%
SM. The data show a progression of the minimal
effects of nonexposure, the moderate effects of
passive smoking exposure, and the greater detri-
mental effects of active smoking.
The NX classification in this study is an im-
portant distinction from most other studies on
passive smoking where both; NX and EX women
are combined in the passive smoking category or
the NX category is not considered in~the analysis.
This distinction is necessary in determining dif-
ferences that may exist between the nearly totally
nonexposed and those nonsmoking women who
are exposed: to other sources of passive smoking.
Therefore, we recommend that studies on passive
smoking make use of these three categories for
classification of exposure so that a comparative
analysis can be made between this study and'simi-
lar studies.
Another distinction between this study and
others is that this study attempts to include all
potential sources of exposure to passive smoking
in the EX category. For this reason, data have
been collected where possible on~ whether others
in the household in addition to a smoking spouse
were producing tobacco smoke exposure for non-
smokers, such as smoking children-or other smok-
ers in the household as well as other smoke-filled
environments. Because there appears to be expo-
sttre in the workpl.ace," working wives were placed
in the EX category. Although some women are
not exposed in certain environments, most women
who work are exposed and therefore should be
placed in the EX category. Additional substantia-
tion of the increased exposure of working women
to passive smoking is provided by Coughlin' and
Friedman'6
This reclassification of the nonexposed non-
smoker provides a much purer nonexposed group
than that of classifications that include these ex-
posed or potentially exposed groups in the
427

Women and Lung Cancer
nonexposed group. Again for comparative pur-
poses, it would be important for other studies to
be sure that their nonexposed groups be as free as
possible from potential tobacco smoke pollution.
Population studies involve greater time and
expense but such studies contribute greater repre-
sentativeness of the data, It would be valuable if
other whole-population studies could be con-
ducted, which would allow for the comparison of
population data.
Because this study contained so few women
exposed to hazardous pollutants, the results do not
include the potential synergistic and nonsynergistic
effects of exposure to pollutants other than tobacco
smoke - other locations where there are factories
or cities with substantial pollution. This additional
exposure could increase the incidence of lung cancer.
Those under age 30 years were not consid-
ered in this study because the detrimental effects
of active and passive smoking take many decades
to produce additional diseases and earlier mortal,
ity. Estimates of the exposure are based on close
relatives of the deceased whenever possible in
order to obtain the best estimates of exposure
without having to wait for the many decades nec-
essary for a completed prospective study when all
of the members of the study have died.
Analysis of the demographics of the popula-
tion shows that 15% more working women smoked
than nonsmoking women. In addition, smoking
women had greater passive smoking exposure at
home since 14% more of their husbands smoked
than those of nonsmoking women. Therefore,
smoking women received additional passive smok-
ing exposure at work and at home compared with
nonsmoking women, which could result in higher
rates of lung cancer. A larger population base is
needed to determine the approximate contribu-
tion of this increased exposure and its potential to
increase lung,cancer in both EX and NX women.
A recent report by Janerich" has attributed a
doubling of lung cancer for children exposed
during childhood for 25 or more smoking years.
This conclusion should be checked with analysis
of data from other studies that deal with exposure
during childhood and adolescence.
The analysis of the data from this study shows
that the comparison of nonsmoking women (com-
bined NX and EX categories) with the SM cat-
egory yields roughly the same pattern as that of
nonsmoking men with smoking men - a 10 to I
lung cancer ratio for the smoker vs. the non-
smoker as reported in most studies. However,
when the finer distinction is made between the
nonsmoking-women groups (NX and EX), we
obtain a 42 to I lung cancer ratio for the smoker
compared with the totally nonexposed indicating
that passive smoking may be worse than reported.
These data attribute a higher incidence of lung
cancer to both active and passive smoking. There-
fore, if smoking and other environmental pollut-
ants that are causative factors are eliminated, lung
cancer may once again become a rare disease.t8
ACKNOWLEDGMENTS
The author would like to thank the following
individuals for their assistance in the preparation
of this manuscript: Dr. Marvin A. Schneiderman
of the National Research Council, Washington,
D.C.; Dr. A. Judson Wells of the American Lung
Association, Kennett Square, PA; Dr. Thomas
Novotny of the Office of Smoking and Health,
Atlanta, GA; Dr. James P. Campbell of Humana
Hospital, St. Petersburg, FL; Dr. Lisa A. Nemec of
the Women's Medical Center, St. Petersburg, FL;
and Dr. Robert H. Depue, Jr., Washington, D.C.
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