A Study of Six Hundred and Eighty-Four Proved Cases

A Study of Six Hundred and Eighty-Four Proved Cases
St. Louis
General Increase.\p=m-\Thereis rather general agreement
that the incidence of bronchiogenic carcinoma has
greatly increased in the last half-century. Statistical
studies at the Charity Hospital of New Orleans
(Ochsner and DeBakey),1 the St. Louis City Hospital
(Wheeler)2 and the Veterans Administration Hospital
of Hines, Ill. (Avery)3 have revealed that at these
hospitals cancer of the lung is now the most frequent
visceral cancer in men.
Autopsy statistics throughout the world show a
great increase in the incidence of bronchiogenic carcinoma in relation to cancer in general. Kenneway and
Kennewat,4 in a careful statistical study of death
certificates in England and Wales from 1928 to 1945,
have presented undoubted evidence of a great increase
in deaths from cancer of the lung. In this country
statistics compiled by the American Cancer Society
show a similar trend during the past two decades.5
Tobacco as a Possible Cause of Increase.\p=m-\Thesuggestion that smoking, and in particular cigaret smoking,
may be important in the production of bronchiogenic
carcinoma has been made by many writers on the sub¬
ject even though well controlled and large scale clinical
studies are lacking. Adler °
in 1912 was one of the
first to think that tobacco might play some role in this
regard. Tylecote,1 Hoffman,8 McNally,0 Lickint,10
Arkin and Wagner,11 Roffo vl and Maier 13 were just
a few of the workers who thought that there was some
evidence that tobacco was an important factor in the
increase of cancer of the lungs. MidlerJ4 in 1939,
from a careful but limited clinical statistical study,
offered good evidence that heavy smoking is an impor¬
tant etiologic factor. In 1941 Ochsner and DeBakey 15
called attention to the similarity of the curve of increased
sales of cigarets in this country to the greater prevalence
of primary cancer of the lung. They emphasized the
possible etiologic relationship of cigaret smoking to
this condition. In a recent paper Schrek ie concluded
that there is strong circumstantial evidence that cigaret
smoking is an etiologic factor in cancer of the respira¬
tory tract and finds that his data are in agreement with
the results of a preliminary report presented by Wynder
and Graham at the National Cancer Conference in
February 1949.17
Purpose of Study.—The purpose of the present study
was to attempt to determine, so far as possible by clini¬
cal investigations, statistical methods and experimental
studies, the importance of various exogenous factors
that might play a role in the induction of bronchiogenic
carcinoma. In this regard we intended to learn the
relative importance of previous diseases of the lungs,
rural and urban distribution of patients, various occu¬
pations and hereditary background as well as smoking
habits. By obtaining all this information, we hoped to
determine whether any of these factors, either singly
or in combination, have had an effect in increasing the
incidence of bronchiogenic carcinoma.
In the present paper the chief emphasis will be placed
on our findings in regard to smoking.
The results of this study are based on 684 cases of
proved bronchiogenic carcinoma. It should be empha¬
sized that the results in this report have not been
obtained from hospital records since we learned at the
outset of our study that the routine records did not
supply satisfactory answers to our questions. It was
therefore decided to seek the desired information by
special interviews. Six hundred and thirty-four patients
reported on in this paper have been personally inter¬
viewed, and in 33 cases we obtained the information
by mailing a questionnaire.18 In the remaining 17 cases
information for the questionnaire was obtained from a
person who had been intimately acquainted with the
patient throughout his adult life.
From the Department of Surgery, Washington University School of
Medicine and Barnes Hospital. This study has been aided by a grant from the American Cancer Society. Other phases of it will be presented in subsequent publications. 1. Ochsner, A., and DeBakey, M.: Surgical Considerations of Primary Carcinoma of the Lung, Surgery 8:992-1023 (Dec.) 1940.
2. Wheeler, R.: Personal communication to the authors.
3. Avery, E. E.: Personnal communication to the authors.
4. Kenneway, N. M., and Kenneway, E. L. : A Study of the Incidence of Cancer of the Lung and Larynx, J. Hyg. 36:236-267 (June) 1936.
Kenneway, E. L., and Kenneway, N. M.: A Further Study of the Incidence of Cancer of the Lung and Larynx, Brit. J. Cancer 1:260-298
(Sept.) 1947.
5. Statistics on Cancer, New York, American Cancer Society, Statistical Research Division, 1949, p. 19.
6. Adler, I.: Primary Malignant Growths of the Lungs, and Bronchi, New York, Longmans, Green and Co., 1912.
7. Tylecote, F. E.: Cancer of the Lung, Lancet 2:256-257 (July 30)
8. Hoffman, F. L.: Cancer of the Lung, Am. Rev. Tuberc. 19:392\x=req-\
406 (April) 1929.
9. McNally, W. D.: The Tar in Cigarette Smoke and Its Possible
Effects, Am. J. Cancer 16:1502-1514 (Nov.) 1932.
10. Lickint, F.: Der Bronchialkrebs der Raucher, M\l=u”\nchenmed.
Wchnschr. 82:1232-1234 (Aug. 2) 1935.
11. Arkin, A., and Wagner, D. H.: Primary Carcinoma of the Lung, J. A. M. A. 106:587-591 (Feb. 22) 1936.
12. Roffo, A. H.: Der Tabak als Krebserzeugende Agens, Deutsche med.
Wchnschr. 63:1267-1271 (Aug. 13) 1937.
13. Maier, H. C.: Personal communication to the authors.
14. M\l=u”\ller,F. H.: Tabakmissbrauch und Lungencarzinom, Ztschr. f.
Krebsforsch. 49:57-85, 1939.
15. Ochsner, A., and DeBakey, M.: Carcinoma of the Lung, Arch.
Surg. 42:209-258 (Feb.) 1941.
16. Schrek, R.; Baker, C. H.; Ballard, G. P., and Dolgoff, S.: Tobacco
Smoking as an Etiological Factor in Disease: I. Cancer, Cancer Research
10: 49-58 (Jan.) 1950.
17. Wynder, E. L., and Graham, E. A.: Tobacco and Bronchiogenic
Carcinoma: Preliminary report to the National Cancer Conference,
Memphis, February 1949.
18. The questionnaires were sent to male and female patients with
cancer of the lungs from Dr. W. L. Watson’s Thoracic Surgery Service
at Memorial Hospital, New York.
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Through the cooperation of many hospitals and phy¬
sicians throughout all parts of the country who per¬ mitted us to interview their patients, it is felt that a
fairly good cross section of the entire United States
has been obtained. The list of cooperating institutions
and physicians is presented below.19
In order to make this survey as uniform as possible,
each interviewer used the questionnaire shown in
table 1.
In regard to smoking habits, we considered it par¬
ticularly essential to learn how much a patient had
smoked formerly, even though he might not smoke at
all or smoke little at the time of the interview. The
reason for this is the well known existence of a time
lag between the exposure to a carcinogenic substance
and the appearance of cancer. Many patients coming
into the hospital with chronic disease of the lungs had
stopped smoking months, or even years, previously.
We therefore asked the patients to estimate the average
use of tobacco during the last twenty years of their
smoking period. The control patients were questioned
in an identical manner ;
thus any possible error lying
in this method of estimating smoking habits was
In questioning patients about occupations, we
attempted to learn all the occupations of a given
patient, the years during which he had held these jobs
and to what type of dusts or fumes he had been exposed.
Similar details were obtained in regard to other possible
exposures, such as those a patient might have had in
connection with certain hobbies.
Classification of Smoking.—In order to facilitate a
statistical analysis of the results, the arbitrary classifi¬
cation of smoking habits given in table 2 was established.
If a patient smoked for less than twenty years, his
amount of smoking was adjusted to a twenty year
period. Thus a patient smoking 20 cigarets for ten
years only was classified as smoking 10 cigarets daily
(class 2). Such adjustments were rarely necessary,
since only a few patients had smoked for less than
twenty years.
If a man smoked habitually more than one type of
tobacco during the last twenty years, the various types
were added together to make up his classification. Thus
a man who smoked 1 package of cigarets daily, as well as
2 cigars, was classified as a class IV, or an excessive,
Histologie Types.—To insure an undoubted diag¬
nosis, microscopic confirmation of the presence of carci¬
noma was obtained in all cases. Some difficulty arose
in the histologie classification because of the variation
of terms employed by pathologists in the different hos¬
pitals who examined the specimens. For example, what
some pathologists would designate as an adenocarcinoma others would classify as an undifferentiated
carcinoma. Likewise, the term oat cell or round cell
carcinoma was at times used, a designation which is
Table 1.—Etiologic Survey
Name :.Age:
1. Have you ever had a lung disease? If so, state time, duration and
site of disease:
Pneumonia Asthma Tuberculosis Bronchiectasis
Influenza Lung Abscess Chest Injuries Others
2. Do you or did you ever smoke? Yes No Q
3. At what age did you begin to smoke?
4. At what age did you stop smoking?
5. How much tobacco did you average per day during the past 20 years of your smoking?
6. Do you inhale the smoke? Yes No
7. Do you have a chronic cough which you attribute to your smoking.
especially upon first smoking in the morning? If so, for how long?
Yes P No D
8. Do you smoke before or after breakfast? Before D After D
9. Name the brand or brands, and dates, if any given brand has been
smoked exclusively for more than five years.
Change frequently? Q
First brand—from 19_to 19_
Second brand—from 19. ..
to 19.
. .
10. What kind of jobs have you held? Have you been exposed to dust or
fumes while working there? (Use back of page for detailed descrip¬
tion of possible exposure)
From To Position Dust or Fumes
11. Have you ever been exposed to irritative dusts or fumes outside of
your job? In particular have you ever used insecticide spray exces¬
sively? If so, state time and duration.
Yes No Type.Duration.
12. How much alcohol do you or have you averaged per day? State time
and duration in years.
13. Where were you born and where have you lived most of your life?
State the approximate time span you have lived in a certain locality.
Up to what grade did you attend school?
14. State the cause of death of your parents, and of brothers and sisters
if any.
15. Site of Lesion Microscopic Diagnosis Papanicolaou Class
Etiotogical Class
not recognized by some pathologists. In some cases
pathologists called a lesion, from biopsy section, merely
a carcinoma, unclassified. It may be said, however, that
in general by far the most prevalent histologie types
were the epidermoid or squamous carcinoma and its
variant the undifferentiated carcinoma. These are the
most common types found in males. In females the
adenocarcinoma has so far been nearly as common as the
other types. It is unquestionably the epidermoid and
undifferentiated carcinomas which have shown the
19. California: Private patients of Drs. L. Brewer, Daniels, F. Dolley, D. Dugan, H. Garland, E. Holman, J. Jones, W. Rogers, P. Samson, B. Stephens. Hospitals: Birmingham General, French, Good Samaritan, Letterman General, Los Angeles County, Southern Pacific General, Stanford, United States Marine, United States Naval, University of California, Wadsworth General. Colorado: Private patients of Drs. A. Brown, F. Condon, J. Grow, F. Harper, M. Peck. Hospitals: Colorado General, Denver General, Fitzsimmons, Fort Logan Veterans, General Rose, St. Lukes. District of Columbia: Private patients of Drs.
B. Blades, E. Davis. Hospitals: Georgetown, George Washington, Walter
Reed. Illinois: Hospitals: Cook County, Veterans Administration, Hines, Ill. Maryland: Hospitals: Johns Hopkins, United States Naval.
Massachusetts: Private patients of Drs. D. Harken, R. Overholt. Hospitals: Boston City, Massachusetts General, New England Deaconess.
Michigan: Hospitals: Dearborn Veterans. Missouri: Private patients of Drs. J. Fiance, A. Goldman, R. Smith. Hospitals: Jefferson Barracks
Veterans, Jewish, St. Louis City, St. Louis County. New Jersey: Hospitals: Berthold S. Pollack, Newark City. New York: Private patients of
Drs. W. Cahan, H. Maier, J. Pool, W. Watson. Hospitals: Bellevue, Veterans Administration, Brooklyn Cancer Institute, Kings County Memorial, Montefiore, New York City Cancer Institute, New York Hospital, Presbyterian, Roswell Park Memorial Institute. Ohio: Hospitals: Veterans Administration. Pennsylvania: Private patients of Dr. J. Johnson. Hospitals: Jefferson Medical College, Temple University, University of Pennsylvania. Utah: Private patients of Drs. W. Rumel, Cutler.
Hospitals: Holy Cross, St. Marks, Salt Lake County General, Veterans
Administration, Dr. W. H. Groves, Latter-Day Saints.
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greatest increase in recent years. For this reason we
were particularly interested in studying these types
separately from the adenocarcinomas. The present
report includes 605 male and 25 female patients with
epidermoid, undifferentiated and unclassified carcinomas
and 39 male and 15 female patients with adenocarcinoma. In order to determine possible sex variations in
the etiology of cancer of the lung, results in men and
women are reported separately.
Control Study I.—To check all possible bias on the
part of the interviewers who saw only patients believed
to have bronchiogenic carcinoma, it was deemed advisa¬
ble to conduct a control study in which a nonmedical
investigator would interview every patient admitted to
the Chest Service of Barnes Hospital without knowing
the diagnosis in advance. Two interviewers -”
used for this purpose. When the final diagnosis was
determined, all cases of cancer of the lungs (75 men)
were separated from the other cases (132). Control
patients under the age of 30 were excluded since there
were no cases of cancer in this age group. Seventeen
male patients for whom no definitive diagnosis could
be made were also omitted.
In addition these interviewers interrogated patients
with cancer of the lung at other St. Louis hospitals,21
also without previous knowledge of diagnosis. Here the
interviewers were given the names of several patients
with diseases of the chest in a comparable age group,
of whom at least 1 was suspected to have bronchiogenic
carcinoma. The patients with proved cancer of the lung
(25 men) and the other patients (54 men) were added
to the Barnes Hospital groups, thus collectively making
up control study I.
To determine the smoking habits, as well as the other
data contained in the questionnaire of our study of
other hospital patients, the nonmedical investigators
also questioned patients without cancer of the lungs
on the general surgical and medical services at Barnes
Hospital, the Jefferson Barracks Veterans Hospital and
the St. Louis City Hospital. This group, called “gen¬
eral hospital population,” consists of 780 patients. Also
a total of 552 female patients without cancer of the
lungs have been interviewed as control patients on our
surgical and medical services.
Two objects were to be realized by this control study.
One was to learn of possible exposures to exogenous
irritants of a large group of patients without cancer of
the lung and the other to test the validity of the inter¬
views made by those who knew the suspected diagnosis
in a given case in advance.
Age Distribution in Control Cases : For proper
statistical evaluation of a study of this kind it is obvious
that the age distribution should be the same in the con¬
trol cases as in the cases of cancer of the lungs. Since
no patients with cancer of the lungs below 30 or above
80 years of age were seen, no controls beyond these
ages have been included. The controls comprised the
unselected patients as they entered the Barnes Hospital
and other St. Louis hospitals. For that reason their
age distribution is not identical with that of the patients
with cancer. In order to be able to evaluate the cases
without cancer on the basis,of the same age distribution
as that found in the cases of cancer, the following adjust¬
ments were made :
The combined results include data on 780 cases with¬
out cancer. Among these there is the following age
distribution: 30 to 39, 18.7 per cent; 40 to 49, 21 per
cent; 50 to 59, 26.9 per cent; 60 to 69, 20.5 per cent,
and 70 to 79, 12.8 per cent. (For the age distribution
in the 605 cases of cancer see table 5.)
The smoking classifications of the control cases have
been made proportional to the age distribution among
the cases of cancer by multiplying the percentage value
of each smoking classification for each age group of the
controls by the proportion of cases of cancer in that
age group. For example, in the age group 30 to 39 of
the controls there were 146 (18.7 per cent) patients, of
whom 20 (13.6 per cent) were nonsmokers. However,
since of the patients with cancer only 2.3 per cent fell
into this age group, the value of 13.6 per cent was made
proportional to the age distribution in the cases of cancer
(2.3 per cent).-2 In a similar manner the smoking
values for the control group aged 40 to 49 were made
proportional to 17.4 per cent. Finally, the quotients of
the smoking classifications in each age group were added
to make the percentage values shown in figure 3. The
detailed data which compare the smoking classifications
of the two groups according to age are shown in table 6.
It was from those data that the proportional values
were obtained.
Table 2.—Classification of Smoking Habits
Group 0. Nonsmokers (Less tlian 1 cigaret per day foi’
more than 20 years) *
i. Light smokers (From 1 to 9 cigarets per day
for more than 20 years) »
Moderately heavy smokers (From 10 to 15
cigarets per day for more than 20 years) *
Heavy smokers (From H> to 20 cigarets per
day for more than 20 years) *
Excessive smokers (From 21 to .14 cigarets per
day for more than 20 years) *
Chain smokers (35 cigarets or more per day
for at least 20 years) *
Pipe and cigar smokers have been included by arbitrarily counting
1 cigar as ö cigarets and 1 pipeful as 2^ cigarets.
t Includes minimal smokers (from 1 to 4 cigarets a day, or the
equivalent in pipes or cigars for more than 20 years).
The 100 cases of cancer and the 186 cases of control
study I were made proportional in the same manner.
Control Study II.—In addition to the control study
just cited, it was thought to be valuable to have other
physicians carry out similar interviews using our ques¬
tionnaire. It was thought that the results would serve
as an effective control for the cases collected under our
own supervision.
At this time we are reporting preliminary results
based on 83 patients interviewed at the Bellevue Hos¬
pital, Columbia University Division (New York), by
Dr. H. G. Turner23; at the Boston City Hospital by
Dr. G. W. Ware24 ; at the Crile Veterans Hospital
(Cleveland, Ohio) by Dr. C. T. Surington, and at the
Veterans Administration Hospital, Hines, 111., by Dr.
E. J. Shabart.
The first data to be presented are based on 605 proved
cases of bronchiogenic carcinoma in men, other than
adenocarcinoma. Five hundred and ninety-five of these
cases have been diagnosed on the basis of tissue biopsy,
Betty G. Proctor, A.B., and Adele B. Croninger, M.A.
City Hospital, Jewish Hospital and Veterans Administration Hos22. 13.6 \m=x\2.3
0.312 This is the quotient which, added to the others
100 .
determined in the same manner, makes the data
shown in figure 3.
23. Of the service of Dr. James B. Amberson.
24. Of the service of Dr. John W. Strieder.
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9 on the basis of examination of sputum and 1 on the
basis of study of the pleural fluid.25
Comparison of Independent Studies.—Before the
smoking habits of the 605 patients with cancer of the
lungs are compared with those of the general hospital
population, it might be well to compare the results in the
two control studies and the group of 422 patients
(study III) interviewed and collected by one of us
Fig. 1.—Control study I. Amount of smoking in percentage among 100 male patients with cancer of the lungs (solid bars) and 186 male
patients with other chest diseases (lined bars) having the same age and
economic distribution.
(E. L. W.) to determine any possible bias in cases in
which the suspected diagnosis was known in advance
and whether the data are sufficiently similar to warrant
their discussion as a group.
Control Study I : This group consists of 100 patients
with cancer of the lungs and 186 with diseases of the
chest other than cancer interviewed by two nonmedical
investigators who had no previous knowledge of the
diagnosis in a given case. The data show no nonsmokers ( fig. 1 ) among the cancer group, while there
are 14.1 per cent nonsmokers among the patients with
other thoracic diseases. Ninety-five per cent of the
patients with cancer are in the classification of moder¬
ately heavy to chain smokers and 53 per cent are
excessive and chain smokers, while among the patients
without career, 75.3 and 23 per cent, respectively, fell
among these smoking groups.
Control Study II : The data in table 3 cover 83 male
patients with cancer of the lungs interviewed inde¬
pendently by physicians in other cities. Among each
small group of cases some variation is, of course, to be
expected. In each of the individual groups nearly half
or more of the patients are excessive or chain smokers.
Grouping the data of the four independent investigators
together, we find 2.4 per cent nonsmokers and 93.9 per
cent moderately heavy to chain smokers (fig. 2), while
Fig. 2.—Control study II. Percentages for amount of smoking in 83
cases of cancer of the lungs collected independently by Dr. E. J. Shabart
(Chicago), Dr. C. T. Surington (Cleveland), Dr. H. G. Turner (New
York) and Dr. G. W. Ware (Boston).
59 per cent are excessive and chain smokers. The
results of the two control studies correspond closely to
one another as well as to the results of study III
(table 4).
The results in relation to the areas or hospitals
where the cases were observed show uniformity. Small
differences between the ‘groups may well be explained
on the basis of the small size of each series. The
mountain state series includes 13 patients of Mor¬
mon faith. Mormons in general were found to smoke
much less than our general hospital population. Among
the Mormon patients with cancer of the lung, however,
there was only 1 nonsmoker (72 years old). The others
were long-time users of tobacco.
Comparing the three studies, we note little difference.
For example, nonsmokers account for 0.0 per cent in
control study I, 2.4 per cent in control study II and
1.4 per cent in study III. The percentage of heavy to
chain smokers in these three groups is 88, 86.7 and
85.2 respectively, while the percentage of excessive and
chain smokers totals 53, 59 and 49 respectively.
Since we thus have not been able to determine any
essential difference in the amount of smoking in the
three studies, we shall from here on refer to the total
results of 605 cases.
Age Distribution.—The age distribution of cancer of
the lungs in the present series shows 2.3 per cent of the
patients to be under 40 years of age, while 79.3 per cent
were 50 years or older (table 5). This distribution
readily shows that it would be of little value to study
the smoking habits of the younger age groups for the
Table 3.—Control Study II: Amount of Smoking in 83 Cases
of Proved Cancer of the Lung as Determined by Investi¬
gators Using the Same Questionnaire as that Used
in the Cases of this Study
Amount of Smoking:
Moderately heavy.
* Minimal smoker. (For definition
see previous classification of
purpose of control studies, since in them, for reasons
still unknown to us, cancer of the lungs is a rare
Combined Data on Amount of Smoking.—The data
on the amount of smoking among 605 patients with
cancer of the lungs and 780 male patients with other
diseases reflect the results of the individual studies
reported. It may also be noted that there is no essen¬
tial difference in the amount of smoking between the
general hospital population and patients with diseases
of the chest who do not have cancer. The total results
show that whereas there are 14.6 per cent nonsmokers
among the male general population there are 1.3 per cent
nonsmokers among the male patients with cancer of the
lungs ; and while there are 54.7 per cent heavy to chain
smokers and 19.1 per cent excessive and chain smokers
among the general hospital group there are 86.4 and
51.2 per cent, respectively, among the patients with
cancer. All these differences seem highly significant.
The results on the amount of smoking according to
age groups (table 6) show that in general the patients
with cancer of the lungs in their forties and early fifties
have smoked more heavily than the older patients with
this disease. This observation does not seem to apply
to the few patients in their thirties. The age group
70 to 79 has the greatest percentage of light and moder¬
ately heavy smokers.
25. Eight of these cases were diagnosed in Dr. Papanicolaou’s laboratory
on conclusive evidence of carcinoma. One sputum and one pleural fluid
examination were made at the Boston City Hospital.
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The frequency of nonsmokers in the age groups
shown for the patients without cancer is significantly
different from that among patients with cancer in the
same age groups. However, in the 30 to 39 age group the smoking habits of the patient with cancer are diffi¬
cult to evaluate since too few patients of this age have
been seen.
Table 4.—Study III: Amount of Smoking Among Male
Patients With Cancer of the Lang in Relation to Area or
Hospital Where Cases Were Observed (Wynder)*
Smoking Classification, %
Areas or Hospitals. V IV III II I 0 Age
Barnes (76). 18.1 31.5 43.4 5.3 0.0 1.8 54.8
Los Angeles (50). 12.0 32.0 12.0 12.0 0.0 4.0 59.5
San Francisco (50). 20-0 28.0 36.0 14.0 2.0 0.0 54.9
Mountain states (50). 14.0 20.0 30.0 18.0 4.0t 2.0 60.1
St. Louis (25). 20.0 36.0 32.0 12.0 0.0 0.0 58.2
Eastern and northern
States (50). 10.3 23.6 40.0 20.0 0.0 0.0 56.1
New York City (66). 20.0 40.0 32.3 7.7 0.0 0.0 55.8
Memorial Hospital (55)…. 23.0 27.3 29.1 10.9 5.5f 3.0 57.6
Total (422). 18.2 30.8 36.7 11.4 1.4 1.4 56.7
This table does not include any cases represented in control studies
I and II.
t Includes 1 minimal smoker.
Table 5.—Age Distribution in 605 Cases of Cancer
of the Lung in Men
Age Groups of Cases
Table 6.—Percentage Distribution of Amount of Smoking in
Respect to Age Groups Among 780 Men in the General
Hospital Population and 605 Men with Cancer
of the Lungs *
Age Groups
30-39 40-49 50-59 60-09 70-79
No. of Cases. (140) (14) (164) (105) (210) (258) (100) (187) (100) (41)
Amount of smoking;
class: 0. 13.0 7.1 9.7 0.0 14.8 1.6 14.3 1.1 25.0 2.4
1. 5.5 7.1 9.7 1.9 7.1 1.0 18.7 1.1 13.0 12.2
2. 17.1 14.3 18.9 3.8 17.0 7.4 20.6 13.6 21.0 24.4
3. 41.0 42.9 37.1 29.5 43.3 30.0 28.7 38.0 16.0 29.3
4. 14.3 28.6 14.0 28.6 10.5 34.1 10.6 30.5 15.0 17.1
5. 8.2 0.0 10.3 36.2 6.7 19.4 6.8 15.5 10.0 14.6
The percentages for the general male hospital population are given
in the left hand columns.
In comparing the amount of smoking among the
various age groups, one must also consider the type
of tobacco used, which has undergone a marked shift
particularly when the youngest and oldest age groups
are considered.
Statistical Analysis of Data.—The statistical analysis
of these data has been carried out by Dr. Paul R. Rider,
professor of mathematics at Washington University,
and H. David Hartstein, M.A., instructor of statistics
at Washington University.
On the assumption that smoking has no effect on the
induction of cancer of the lungs, the probability (p) of
a deviation from expectation as great or greater than
that observed is as follows :
Control Study I : Class O, p is 0.0002 ; class O plus
class I, p is 0.0002 ;
classes 3 to 5 inclusive, p is 0.0226,
class 4 plus class 5, p is 0.0002; class 4, p is 0.0046,
and class 5, p is 0.0016.
Combined Results ; The values for the combined
results of 605 patients with cancer of the lung as com¬
pared with 780 men in the general hospital population
are as follows: class O, class O plus class 1, classes 3
to 5 inclusive, class 4 plus class 5, class 4 and class 5
have p values which are in all cases less than 0.0001.
Their conclusion is as follows : “On the basis of the
«statistical data for both the control study I and the
combined results, when the nonsmokers and the total of
the high smoking classes of patients with lung cancer
are compared with patients who have other diseases,
we can reject the null hypothesis that smoking has no
effect on the induction of cancer of the lungs. If smok¬
ing does not have anything to do with the induction of
cancer of the lungs, then the observed deviation could
occur only with the probability (p) as shown above.”
Miscellaneous Data.—Nearly all (98.7 per cent) the
cigaret smokers of the cancer group, but fewer pipe
(62.5 per cent) and cigar (18 per cent) smokers, stated
that they inhaled consciously. Seventy-eight and a half
per cent of cancer patients interviewed stated that they
usually began to smoke before breakfast.
Type of Tobacco : Among the general hospital popu¬
lation pipes and cigars were smoked most prominently
Fig. 3.—Percentages for amount of smoking among 605 male patients
with cancer of the lungs (solid bars) and 780 men in the general hospital
population without cancer (lined bars) with the same age and economic
in the older age groups. For example, only 4.3 per
cent of the smokers in the age group 30 to 39 used
chiefly pipes or cigars, 11.0 per cent in the age group
40 to 49, 12.9 per cent in the age group 50 to 59, 30 per
cent in the age group 60 to 69 and 38 per cent in the
age group 70 to 79. Only those patients were tabulated
as either pipe or cigar smokers who smoked a given type
of tobacco predominantly over the last twenty years of
their smoking period. Among the age-adjusted general
hospital population we find 12.4 per cent pipe smokers
and 7.8 per cent cigar smokers and among the patients
with cancer 4.0 per cent and 3.5 per cent respectively
(fig. 4). The average age of the pipe smokers with cancer of
the lung was 60.5, with a range of 52 to 78, and the
average age of the cigar smokers with cancer of the
lung was 63.1, the range being from 53 to 76. The
average number of pipes smoked by the cancer patients
was 15.6 and the average number of cigars 6.8 per day
for the last twenty years of their smoking history. This
amount of smoking is decidedly higher than that found
among the general cigar and pipe smokers.
Duration of Smoking: The duration of smoking in
years dates to the first time the patient began smoking
habitually to any degree. Of 605 patients with cancer
in our series, 96.1 per cent had smoked for twenty
years or more, 85.4 per cent for thirty years or more,
68.2 per cent for thirty-five years or more and 50.2 per
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cent for forty years or more. One patient with epi¬
dermoid cancer began to smoke at 45 (20 cigarets a
day), and clinical symptoms of cancer of the lungs
developed at 50 (class I smoker). He had no other
exposure to irritants. Only three of the patients with
bronchiogenic cancer began to smoke after the age
of 25 (fig. 5).
Fig. 4. Smoking habits and type of tobacco smoked (in percentages) in 605 cases of cancer of the lungs (solid bars) and 780 men in the
general hospital population (lined bars) witli a similar age and economic
Adenocarcinoma in Men : Among 39 men 2e with
adenocarcinoma there were 4 nonsmokers (10.3 per
cent), a percentage higher than that found for the
other types of bronchiogenic carcinoma. There were
7 chain smokers (18 per cent), significantly more than
in the general male hospital population. Ten and
three-tenths per cent were excessive, 38.5 per cent
heavy. 15.4 per cent moderately heavy and 7.7 per cent
light smokers. Among the latter there were 2 minimal
Data on Women;-7 Among 13 women with adeno¬
carcinoma and 2 designated as having terminal bronchiolar carcinoma there was not 1 heavy smoker.
Thirteen were nonsmokers and 2 light smokers. Among
25 patients with epidermoid and undifferentiated carci¬
noma, however, there were 15 smokers of many years’
duration as well as 10 nonsmokers. Among those who
smoked there were 1 light, 4 moderately heavy, 6 heavy,
2 excessive and 2 chain smokers.
4 15 19 20-24 25-29 5034 35-59 40-44 45-49 50 5d 55-59 60 64 65 69
Fig. 5.—Percentages for duration of smoking in years, starting with
the time when the patient first began to smoke habitually, in 605 cases of
cancer of the lungs.
To determine the smoking habits among women in the
general hospital population 552 patients without cancer
of the lung have been interviewed at this hospital.
The data resulting from this study show that but few
women in the cancer age have been heavy smokers for
many years and that most of the heavy smokers are
young women. On the basis of our arbitrary smoking
classification, we found 79.6 per cent of the women to be
nonsmokers while 11.3 per cent were moderately heavy
to chain smokers, and only 1.2 per cent of the controls
in the cancer age 28 were excessive or chain smokers for
at least twenty years (fig. 6).
Universal Increase.—If one feels that the greatly
increased incidence of cancer of the lungs is real and
that this increase is most marked in men, one may
theorize that the change has been due to an external
factor, or group of factors, nationally prevalent but
applicable to men more and over a longer period than
to women.
Influence of Tobacco.—Since in a small percentage
of cases cancer of the lungs occurs in nonsmokers and
minimal smokers and since it obviously does not develop
in every person who has been a heavy smoker for a
long time, it is apparent that smoking cannot be the
only etiologic factor in the induction of the disease.
From the evidence presented, however, the temptation
is strong to incriminate excessive smoking, and in
particular cigaret smoking, over a
long period as at least
one important factor in the striking increase of bron¬
chiogenic carcinoma for the following reasons: (1) it
Fig. 6.—Amount of smoking in percentage among 780 male patients (vertically lined bars) and 552 female patients (horizontally lined bars) of
the general hospital population with the same age and economic distribution
as found among cases of cancer of the lungs.
is rare to find a case of epidermoid or undifferentiated
carcinoma in a male patient who has not been at least
a moderately heavy smoker for many years; (2) the
use of cigarets is much greater among patients with
cancer of the lungs than among other patients of the
same age and economic groups ; (3) the sex distribution
of cancer of the lungs roughly corresponds to the ratio
of long-term smoking habits of the two sexes (see sec¬
tion on “Duration of Smoking”) ; (4) the enormous
increase in the sale of cigarets in this country approxi¬
mately parallels the increase of bronchiogenic carci¬
Amount of Smoking.—The data have clearly shown
that the average patient with cancer of the lungs smokes
much more heavily than the average patient of the
same age and economic group with some other disease.
This contrast becomes even greater if our observation
of Mormons is considered, who as a group smoke far
less than the general hospital population; Mormons
with cancer of the lung were, with one exception, con¬
siderable smokers.
26. Includes 3 cases of Dr. C. T. Surington and 1 case of Dr. H. G.
27. Includes 4 cases of Dr. H. G. Turner and 3 cases of Dr. G. W.
28. See table 5.
29. It is taken for granted, of course, that by itself such parallelism would mean little since similar curves could be drawn for many other
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The fact that patients with bronchiogenic cancer in
their forties and fifties had smoked more heavily than
those in whom the cancer developed at a later age may
indicate that the greater the irritation the sooner will
cancer develop in a susceptible person. Such an obser¬
vation obviously does not apply to the individual case
but rather to the age groups taken collectively. Too
few patients below the age of 40 have been seen in
order to evaluate this age group.
In general it appears that the less a person smokes
the less are the chances of cancer of the lung developing
and, conversely, the more heavily a person smokes the
greater are his chances of becoming affected with this
Type of Tobacco.—The majority of patients with
cancer of the lungs are cigaret smokers rather than pipe
or cigar smokers, the ratio being over and above that
found in the general population. This fact may be due
to one of the following reasons :
1. Cigaret smoke is more frequently inhaled than is
that of either pipes or cigars. Obviously the lungs
of an inhaler are exposed to a greater concentration of
smoke than those of a person who does not consciously
2. Because of the greater physical and economic con¬
venience, more persons are heavy smokers of cigarets
than of either pipes or cigars. Among the latter one
finds more minimal and light smokers than among the
3. Certain irritative substances may be present in
cigarets in greater amounts than in pipes or cigars. The
role of paper, the use of insecticides during the growth
of the tobacco and other ingredients warrant further
research in this regard.
Duration of Smoking.—One of the chief reasons
many investigators have thought that tobacco has no
effect on the development of cancer of the lungs has been
their belief that women today smoke as much as men
and that if tobacco plays a role the sex ratio of the
disease should be about equal. The data presented
demonstrate that it makes little difference how many
women smoke today or have smoked for the past ten
years, since results have shown that over 96 per cent
of patients with cancer of the lungs have smoked for
more than twenty years and that over 80 per cent have
smoked for more than thirty years.
It is, of course, difficult to tell whether the impor¬
tant point in this regard is the fact that these persons
have smoked for many years or that they have been
heavy smokers for a brief period, because we have noted
that also among the general male hospital population
nearly all smokers have been smoking since their youth.
For this reason it is difficult to evaluate the one case in
our study in which the patient smoked only from his
forty-fifth to his fiftieth year, at which time clinical signs
of cancer developed. If one may judge from control data
on women, it would appear that a long duration of
smoking is at least one important factor in the induction
of cancer of the lungs. The relatively low incidence of
the condition in women might be explained by the
fact that few women in the cancer age have smoked
for an extensive period.
On the basis of a twenty year period of smoking, it
may be of interest to note that, while only 1.2 per cent
of the women were excessive or chain smokers, by
contrast 19.1 per cent of the male controls were in those
smoking groups, a ratio which points in the same
direction as the sex ratio of lung cancer.
Lag Period.—If smoking is to be regarded as an
important etiologic factor in the development of cancer
of the lungs, apparently a time lag exists for this dis¬
ease as well as for carcinoma of the bladder, known to
occur years after cessation of exposure to aniline. We
have now seen 3 cases in which clinical signs of cancer
of the lung appeared ten years or more after the patient
stopped smoking. The 3 patients had smoked for thirty
years or more, and none gave a history of occupational
or other irritative exposures. Two of them had stopped
smoking because of a bothersome chronic cough and
1 because of concomitant heart disease. In 1 of the
patients, a 67 year old warehouse clerk, clinical symp¬
toms of cancer developed thirteen years after the cessa¬
tion of smoking. The phenomenon of the lag period
is of course well known in cancer research.
Adenocarcinoma in Men.—Since the great increase
in cancer of the lungs has mostly involved the epi¬
dermoid and undifferentiated carcinomas, it would
appear that the exogenous factors possibly affecting
these types of cancer play a lesser role, if any, in the
induction of adenocarcinomas of the lung in men. As
yet we have not seen a sufficient number of cases of
this type of cancer to warrant definitive conclusions. It
appears, however, that on the basis of present data one
is more likely to find nonsmokers or minimal smokers
with this type of cancer than with the other types.
At the same time, however, the percentage of chain
smokers among men with adenocarcinomas of the lung
is greater than among the general hospital population.
It seems, therefore, that tobacco smoke has also some
influence on the induction of adenocarcinoma in men,
even though, as judged from the incidence, the influence
on this type is much less marked than on the other
types of bronchiogenic carcinoma.
Cancer of the Lungs in Women.—Many observers
have commented on the fact that bronchiogenic carci¬
noma, while on the increase among both men and
women, is increasing more rapidly among men. In
100 consecutive cases collected by Lindskog 30 in 1938
to 1943 the ratio was 4.5 to 1, and in another series
collected in 1947 and 1948 the ratio had reached 24
to 1.31 At Barnes Hospital the ratio in our last 150 cases
has been 18.5 to 1. This’shift in ratio has been noted
in varying proportions throughout the country. Such
a radical change warrants a careful analysis.
The insufficient number of cases of cancer of the
lungs in women in our survey does not allow definite
conclusions at this time. So far, however, smoking
seems to have had no apparent effect on the incidence
of adenocarcinoma in women. It is of great interest
that we have observed 10 cases of epidermoid and
undifferentiated carcinoma of the lungs of women who
were nonsmokers with no history of occupational or
other irritative exposure. This percentage of nonsmokers in women with cancer of the lung is much
higher than that found among men. Proper expla¬
nations for this finding remains to be advanced. At
the same time it appears strongly suggestive that heavy
smoking plays a significant role in the induction of
epidermoid and undifferentiated carcinoma of the lungs
in women, since the percentage of heavy smokers is
considerably higher in the cancer group than in the
general hospital control group.
30. Lindskog, G. F.: Bronchiogenic Carcinoma, Ann. Surg. 124:667\x=req-\
674 (Oct.) 1946.
31. Lindskog, G. F., and Bloomer, W. D.: Bronchiogenic Carcinoma,
Cancer 1:234=237 (July) 1948.
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1. Excessive and prolonged use of tobacco, especially
cigarets, seems to be an important factor in the induc¬
tion of bronchiogenic carcinoma.
2. Among 605 men with bronchiogenic carcinoma,
other than adenocarcinoma, 96.5 per cent were moder¬
ately heavy to chain smokers for many years, compared
with 73.7 per cent among the general male hospital
population without cancer. Among the cancer group
51.2 per cent were excessive or chain smokers com¬
pared to 19.1 per cent in the general hospital group
without cancer.
3. The occurrence of carcinoma of the lung in a male
nonsmoker or minimal smoker is a rare phenomenon
(2.0 per cent).
4. Tobacco seems at this time to play a similar but
somewhat less evident role in the induction of epi¬
dermoid and undifferentiated carcinoma in women.
Among this group a greater percentage of nonsmokers
will be found than among the men, with 10 of 25
being nonsmokers.
5. Ninety-six and one-tenth per cent of patients with
cancer of the lungs who had a history of smoking had
smoked for over twenty years. Few women have
smoked for such a length of time, and this is believed
to be one of the reasons for the greater incidence of
the disease among men today.
6. There may lie a lag period of ten years or more
between the cessation oí smoking tobacco and the occur¬
rence of clinical symptoms of cancer.
7. Ninety-four and one-tenth per cent of male
patients with cancer of the lungs were found to be
cigaret smokers, 4.0 per cent pipe smokers and 3.5 per
cent cigar smokers. This prevalence of cigaret smok¬
ing is greater than among the general hospital popu¬
lation of the same age group. The greater practice of
inhalation among cigaret smokers is believed to be a
factor in the increased incidence of the disease.
8. The influence of tobacco on the development of
adenocarcinoma seems much less than on the other
types of bronchiogenic carcinoma.
9. Three independent studies have resulted in data
so uniform that one may deduce the same conclusions
from each of them.
Since the data presented in this paper were tabulated,
45 additional interviews of male patients with epider¬
moid or undifferentiated cancer of the lung have been
obtained. Eight of these patients have been interviewed
by Dr. J. L. Ehrenhaft from the University of Iowa
Hospital, 9 were given our questionnaire by Lt. Col.
J. M. Salyer from Fitzsimons General Hospital and 7
were reported on by Dr. E. J. Shabart from the Vet¬
erans Administration Hospital, Hines, 111. Among
these 24 cases there were no nonsmokers or light
smokers, 7 heavy smokers, 13 excessive smokers and 4
chain smokers. Twenty-one additional patients have
been interviewed by Miss Croninger on the Barnes
Hospital Chest Service. Among these there were 1
nonsmoker (a 72 year old blacksmith), 10 heavy
smokers, 6 excessive smokers and 4 chain smokers.
These 45 cases, which include reports independently
made at two additional centers (University of Iowa and
Fitzsimons General Hospital), show the same trend
noted in the larger series.
A Preliminary Report
Albany, N. Y.
The published literature on use of tobacco and its
possible association with human cancer fails to show
clearcut consistent observations. Reviews of the literature for the past twenty years reveals that it is often
conflicting and that it consists for the most part of
studies which are inconclusive because of lack of adequate samples, lack of random selection, lack of proper
controls or failure to age-standardize the data. Potter
and Tully1 have reported a higher proportion of
smokers in patients with cancer of the “buccal cavity”
and “respiratory tract” among males “over the age of
40” who were seen at Massachusetts cancer clinics.
Since 1938 a history of tobacco usage has been
obtained routinely from all patients admitted to the
Roswell Park Memorial Institute, Buffalo. These hisPercentage of patients who had ever smoked by type of smoking.
tories are part of the regular clinical history and are
taken before the final diagnosis has been established.
This procedure is considered especially important from
the standpoint of excluding bias. Approximately half
the patients admitted to the institute are subsequently
found not to have cancer. Special attention with respect
to the history of smoking has not been paid to any single
group of conditions, so that these records may be pre¬
sumed to be free from bias which might result from
preconceived ideas as to relation between smoking and
a particular form of cancer.
The histories record the date smoking began, dura¬
tion, type of smoking and amount per day. The relia¬
bility of the quantitative aspects of smoking obtained
by a history is of course highly variable. It is presumed,
however, that such errors are not selective with respect
to presence or absence of cancer, especially since only
patients suspected by their physicians of having cancer
are admitted to the Institute.
With technical assistance of Elizabeth Brezee and David Robbins.
From the Bureau of Cancer Control, Division of Medical Services, New
York State Department of Health.
Dr. Louis C. Kress, Dr. Joseph G. Hoffman and Miss Olive C.
Ralston, of the staff of the Roswell Park Memorial Institute, assisted
by making available the records of the institute and by making suggestions as to the planning of the study.
1. Potter, E. A., and Tully, M. R.: The Statistical Approach to the
Cancer Problem in Massachusetts, Am. J. Pub. Health 35:485-490, 1945.
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