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SMOKING AND L U N G CANCER

WILLIAni

L. WATSON,
M.D.,

AND

IDESPREAD INVESTIGATION both here and


abroad has been undertaken in an effort
to determine the extent of, and the reasons for,
the recent increase in the incidence of lung
cancer. R. Doll of the English Medical Research Council, in a conference 'only six years
ago, was skeptical about the reality of an apparent increase in lung cancer, but in 1952 the
International Conference on Lung Cancerll
concluded that a significant and absolute increase in lung-cancer incidence had taken
place.
A recent editorial in the British Medical
Journal1 states that tobacco smoke has been
incriminated as the vehicle conveying an agent
responsible for a large proportion of the cases
of lung cancer and it proposes that intensive
research be carried out in an effort to isolate
the carcinogenic agent in tobacco so that it
may be eliminated and smoking made less
hazardous.
As pointed out by Ochsner, the per 'capita
consumption of cigarettes in the United States
doubled during the decade, 1920 to 1930, and
eighteen years later, 1938 to 1948, the incidence of lung cancer had increased from 4.2 to
11.3 per cent. In this manner he called attention to the fact that an increase in the consumption of tobacco is reflected eighteen to
twenty years later by a significant increase in
the incidence of lung cancer. He believes that,
owing to the increase in cigarette smoking,
bronchogenic carcinoma will soon become
more frequent than other cancer and that by
1970 it will cause 18 per cent of all cancer
deaths.
Although difficult to prove scientifically,
nevertheless a good deal of statistical evidence
has been accumulated to show that heavy smoking over a period of years is much more common in a large group of patients with cancer
of the lung than it is in a comparable control
group of normal persons. Statistics published
recently in the United States19 and in Great
Britain29 9 show that the increase in lung

ALEXANDER
J. CONTE,
M.D.

cancer is real and, in relation to this, it is significant that in the year 1948 at Memorial
Hospital2O there were twice as many admissions
for lung cancer as for stomach cancer.
Evidence to show the carcinogenic potentialities of tar and arsenic in tobacco has been
accumulating rapidly.?*12,16.17 A recent survey
of the content of arsenic of various tobaccos
smoked in North America and Europe3
showed that no direct correlation existed between the amounts of arsenic and lung cancer.
Although American cigarettes were found to
have a much higher arsenic content than Turkish cigarettes, an autopsy series in Istanbul,
where Turkish tobacco is smoked almost exclusively, showed an equally high incidence of
cancer of the lung. Approximately 15 mg. of
arsenic has been found in a pound of tobacco
and the amount of tar taken into the lungs
during a long period of heavy cigarette smoking is amazing, being estimated at about 0.8
quarts per year.'*, 21
Many clinical reports on the relation of
tobacco smoking and lung cancer2. lo, 11, 23. 24
have pointed out that it is rare to find cancer of
the lung in a man who has not been a heavy
smoker for many years. Dungal in Iceland, in
1945, reported the consumption of tobacco to
be at the same level per capita of population as
the consumption was in England in 1920, and
an autopsy series revealed that cancer of the
lung was infrequent at that time in Iceland.
In America, Wynder and Graham22 found a
very small percentage of nonsmokers in a large
group of male patients with cancer of the lung.
There were ten times as many nonsmokers in
a control hospital group. A lag period of one to
two decades was occasionally noted, and 98.7
per cent of the patients with this disease had
smoked more than twenty years. Graham feels
that squamous carcinoma of the bronchus differs greatly from adenocarcinoma of the lung
and that only the increase in epidermoid carcinoma is directly related to the use of tobacco.
In England, in a recent report of 100 cases
of cancer of the lung,13 it was found that one
From the Thoracic Service, Memorial Center for
third of the patients had smoked more than
Cancer and Allied Diseases, New York, New York.
Supported in part by a grant from the American twenty cigarettes daily, while one fifth of the
Cancer Society, Inc., and in part by the Donner controls had smoked such amounts. No statisThoracic Fund.
tical difference was Lound in the exposure to
Received for publication. 0ctol)er 10, 1953.
24 5

246

CANCER
March 1954

to the present writing we can say with conviction that no one knows for certain of any one
specific cause of this disease. If we assume,
however, a number of additive factors working together over a period of years as leading
to neoplastic growth in the lungs, then certainly the evidence to be presented supports
the theory that chronic, heavy tobacco smoking
is one of the responsible factors in a high
percentage of all cases.

TABLE1
COMPARISON OF CONTROL GROUP WITH
CANCER-OF-LUNG GROUP
Cancer of lung
Pt.
Male
Female

No.

Control

Av. age, yr.

265
36
TOTAL301
,

59.1
55.8

No.

Av. age, yr.

287
181

54.2
51.6

58.6

468

52.9

VOl. 7

various dusts and atmospheric fumes. A survey,


MATERIAL
AND METHODS
by Doll and Hill,5 of patients with cancer of
the lung compared with an equal number of
In our series of 2000 cases of lung cancer,
matched controls from various hospitals in many of the earlier records are incomplete
London and rural areas, showed 0.5 per cent regarding the patients' smoking history and
nonsmokers among 1357 males with cancer of not suitable for this statistical survey. With
the lung and in the control group, 4.5 per the financial aid and medical advice of the
cent nonsmokers.
American Cancer Society, we undertook a
It becomes apparent not only that the na- study of the relation of smoking to the inciture of the irritant itself is important but also dence of cancer of the lung in the following
that the chronicity of the irritant is of great fashion. A trained interviewer was coached by
significance in the etiology of lung cancer. Up a psychologist and given full responsibility
for the interviewing of every patient coming
TABLE2
to the Thoracic Clinic at Memorial Hospital
DIFFERENT DIAGNOSES IN CONTROL GROUP regardless of his complaints or nature of his
OF 468 PATIENTS WITHOUT
disease. From 1950 to 1952 a series of 769
CANCER OF LUNG
consecutive patients was studied and, of this
Site
No.
Site
No.
group, 301 were proved to have cancer of the
Head and Neck
GasfrointcsfinalTract.
Ca. of nasooharvnx.. ..... 1
conf'd.. ............... . 87
lung. T h e remaining group was used as a conAdenoma of toigue ...... 3
Stomach
Ca. of alveolar ridge.. ..... 2
trol. So we have, as the basis for study, a large
Ca.. ................ .. 2
Ca. of floor of mouth.. . . . . 3
Colon
Ca. of thyroid.. .......... 2
Ca. of sigmoid.. ...... .. 1 group of patients all in the cancer-of-the-lung
Adenoma of thyroid.. ..... 7
Ca. of rectum. ....... .. 1
age group, all with some problem related to
Ca. of maxillary antrum. .. 3
- Liver
Ca. of hepatic ducts.. . .. 1
the chest, and all seen in one clinic and interTOTAL..
............... 2 1
TOTAL
................. 92 viewed by an unbiased, trained observer. When
Mcdiastinum
Larynx. Trachea. Lungs
Thymoma ............... 4
enough time had elapsed to allow for definite
Ca. of intrinsic larynx.. ... 2
Mediastinal tumors. ...... 1 1
Trachiectasis............. 1
histological diagnoses of the disease, we then
Schwannoma............. 5
Extrinsic larynx tumor. ... 4
Pericardial cyst. .......... 3
separated the true cancer-of-the-lung cases and
Metastatic tumor. ..... ... 10
Neurosarcoma............ 1
Emphysema. .......... ... 9
Hemangioma............. 1
used the remaining group as a control.
Bronchial adenoma.. ... ... 5
Aneurysm.. .............. 4
Bronchitis. ........... ... 7
Chondrosarcoma.......... 2
Diagnosis. A positive histological diagnosis
Bronchiectasis. ........ ... 13
Ostwgenic sarcoma. ...... 1
Pneumonitis. .......... ... 17
Teratoma.. .............. 2
of
cancer of the lung was established by one or
Pulm. tuberculosis. .... ... 31
Hygroma.. .............. 1
Pleural calcification. ... ... 2
Hodgkin's disease.. ....... 7
a combination of the following methods: (1)
Lung abscess.. ........... 10
Reticulum-cell sarcoma.. .. 2
sputum smears; (2) bronchoscopy and biopsy;
Anthracosis.............. 1
Lymphosarcoma.......... 2
Lung Cyst.. .............. 11
Diaphrag. hernia.. ........ 5
(3) bronchoscopy and cytological washings;

.....
.............
...............
.............
.....
..............
-

Pulm. adenomatosis..
1
Metast. tumor, primary
unknown.
I
Pleurisy..
2
Atelectasis..
2
Chronic lung disease.
1
Mesothelioma.. .......... 1
Hamartoma
1
Boeck's sarcoid.. ......... 4

.............
.......

Hiatus hernia
Rhabdomyosarcoma

-1
TOTAL..
............... 57

Breast
Ca. of breast.. ......... 33
Genifal Tracf
Ovarian ca.. ........... 1
Ca. of cervix..
3
Ca. of uterus..
2

Achlasii

.........
.........TOTAL
................. 6
Genitourinary Tract
Ca. of testis.. ............ 2
Ca. of bladder.. .......... 1
Ca. of kidney ............. 4
-

Abscess. .........
1
Congenital short..
2
Diverticulum.. ... ...... 12

TOTAL..
Myocardial disease..
Undiagnosed.
N o disease found.
TOTAL.ALLCASES

.............. ,142

TOTAL..

Gastrointestinal Tract
EBophagus

...............
16
...... 53
............
Ldomyoma. ........... 1
Stricture. ........ ...... 2
cp..

......
......

...............
...... 4771
.............
.........62
......468

TABLE
3
METHODS OF DIAGNOSIS USED
Method

Male

Female

SV *
P and SV
Pt

37

4
12
20

71

157
-

265

36

*SV indicates diagnosis with positive Papanicolaou


smear.
tP represents diagnosis by a positive biopsy as
obtained by the various techniques discussed.

SMOKING
AND LUNG
CANCER

No. 2

(4) aspiration biopsy; (5) exploratory thoracotomy and open biopsy.


Formula. The formula set up for evaluation
of smoking habits of the patients is as follows:
Class 0-Nonsmoker.
Class I-Minimal smoker-less than twenty
cigarettes a day.
Class 11-Moderate smoker-up to twenty cigarettes per day for twenty or more years.
Class 111-Heavy smoker-twenty to sixty cigarettes per day for twenty or more years
with inhalation.
(One pipe equals two and a half cigarettes; one
cigar equals five cigarettes.)
DATA

Watson 6. Conte

247

TABLE
5
MALE PATIENTS WITH
CANCER OF T H E LUNG

Amt. of smoking
Minimal
Moderate
Heavy

TOTAL

Total
Inhalers Noninhalers av. %

6
13
18

1
50
172

223

37

3
24
73

This was a debatable point because patients


interpreted the question differently and most
cigar smokers did not intentionally inhale. It
seemed logical, then, to divide all patients
into three groups, classified as minimal, moderate, or heavy smokers. Table 5 shows that of
all the male patients with cancer of the lung
who smoked, 73 per cent were heavy smokers,
while 24 per cent were moderate, and 3 per
cent were minimal. These figures do not differ
markedly from the previous report except for
an increase in the heavy-smoker group.
The nationality and age of male patients
with cancer of the lung are shown in Table 6.
The youngest male patient was 37 years old
and the oldest, 84. The average age at which
they began to smoke was 19 years and there was
one patient who started at the age of 3.
I n reviewing the nationality of the male
patients, about half were born in the United
States and the remainder were from European
countries. Only two patients came from Turkey, but since all patients lived in the United
States it is assumed that they all smoked the
American type of cigarette, which has a rich
arsenic content. Neither racial nor national

There were 301 patients with histologically


proved cancer of the lung, 265 males and
thirty-six females. In the control group there
were 468 patients of whom 287 were males and
181 females. The number, sex, and average age
of both patients with cancer of the lung and
control patients are shown in Table 1 and
diagnoses in the control group in Table 2. All
the diagnoses in the 301 patients with cancer
of the lung were made by means of positive
histology and/or cytology (Table 3).
Male Patients with Cancer of the Lung. In
studying the 265 male patients with histologically proved cancer of the lung we found that
260 were smokers and five nonsmokers. I n the
male control group 250 were smokers and
twenty-seven nonsmokers. As seen in Table 4,
98.2 per cent of the cancer group were smokers
and 1.8 per cent nonsmokers.
I n comparing these figures with the previous report from this hospital and those pubTABLE
6
lished in England by Doll and Hill, one can AGE AND NATIONALITY OF MALES WITH
CANCER OF T H E LUNG
see that our latest results correspond rather
closely with the English figures for the lungcancer group, but we did find a larger perNO.
Old- Young- Av.age
centage of nonsmokers in our control group.
%
est
est
began
Ca. lung
cases
I n classifying the smoking habits of patients,
Nonsmokers
5
1.89
76
22
we divided them according to whether or not Smokers
260
98.11
84
37
19
they deliberately inhaled the tobacco smoke.
. . . . . . . . . . . . . . . . . . . . .
TABLE
4
SMOKING HABITS OF MALE PATIENTS
WITH LUNG CANCER

% smokers
Lung
cancer

% nonsmokers

Lung
Control cancer

Control

~~

Present series
Watson
Doll and Hill

98.11
95
99

90.3
89
95

1.89
5
0.5

9.7

11
4.5

Nationality

. . . . . . . .
U. S. A.

Italian
Russian
Austrian
Polish
German
Hungarian
Scotch
Greek
Czechoslovakian
Irish

Nationality

NO.

'ii7'
35
29
16
15
9

7
4
4

'

. . .

English
'
Swedish
Spanish
Turkish
Puerto Rican
French
Danish
Venezuelan
Dutch
Finnish
West Indian

Nb.
3
.Z

2
2
2
2
1
1
1
1
1

248

CANCER
Mnrch 1954

Vol. 'I

TABLE7
COMPARISON OF SMOKING HABITS OF CONTROL A N D CANCER-OF-THE-LUNG MALE
PATIENTS

oldest 72 years old. About half the patients


were born in the United States and n o racial
preferences were found (Table 9).
Table 10 indicates the smoking habits of the
Control
Cancer of lung
female group; one can see that only 18 per
cent were smokers and most of them minimal
yo
Av. no. yr. %
Smoking
Av. no. yr.
habits
smoked
smoked
smokers.
Smokers
20
30
There were slightly more than twice the
Minimal
8
3
number
of smokers in the cancer group as comModerate
3.5
24
pared to the controls, and 58 per cent non73
Heavy
57
smokers in the cancer group as compared to
90.3
98.2
TOTAL
the 82 per cent nonsmokers in the controls.
9.7
.~
1.8
Nonsmokers
Although the number of these patients is
relatively small, the influence of smoking in
background seemed to exert any definite the hackground of some patients must be of
influence.
significance.
It is evident that 90.3 per cent of the control
It is worthy of note that the number of cases
group were smokers as compared to 98.2 per of carcinoma of the lung in the female pacent of those with cancer (Table 7). There is a tients i n the last twenty years at Memorial Hosstatistically significant difference in the num- pital has been increasing very slowly, in comber of nonsmoker control males (9.7 per cent) parison with the marked increased incidence
as compared to the number of nonsmoker of this disease in the male. T h e ratio of males
cancer-of-the-lung males (1.8 per cent). Further- to females in this series is more than 7 to 1.
more, there is a much higher proportion of
heavy (class 111) smokers in the male lungDISCUSSION
cancer group (73 per cent) as compared to
Our results parallel the statistics of the
that in the control male group (57 per cent).
This, coupled with the very high incidence of recent literature, i n that a truly significant
smokers in the lung-cancer group, gives strong difference is found in the number of smokers
support to the argument that smoking must in a group of patients with proved cancer of
play a significant role in the background of the lung as compared with a comparable conpatients who develop bronchogenic carcinoma. trol group. It is also shown that the perHowever, the widespread use of tobacco centage of heavy smokers is much greater in
throughout the world makes it very difficult the male group of patients with cancer of the
to find a very large number of controls who lung, while in the female group those with
cancer of the lung were, for the most part,
have not smoked more than twenty years.
Female Patients zuith Cancer of the Lung. minimal to moderate smokers. O u r results
I n studying the thirty-six female patients with point to the important role of tobacco in the
histologically proved cancer of the lung there etiology of lung cancer. It is to be hoped that
were twenty-one nonsmokers (58 per cent) and future research will isolate the specific carcinogen in tobacco smoke so that this factor can
fifteen smokers (42 per cent).
Table 8 shows the smoking habits with relaTABLE9
tion to inhaling in female patients with cancer
AGE
A
N
D
NATIONALITY
OF FEMALES WITH
of the lung. We see that most of the smokers
CANCER OF T H E LUNG
were minimal to moderate in their use of
Age
tobacco. T h e youngest female patient with
cancer of the lung was 31 years old and the
No.
Old- Young- Av.age
Ca. lung
cascs
% est
est
began
TABLE8
FEMALE PATIENTS WITH CANCER OF THE
LUNG
Amt. of
smoking
Minimal
Moderate
Heavy

Nonsmokers
Smokers

Noninhalers Total av. %

8
1

33
59
8

71
72

31
40

21

. . . . . . . . . . . . . . . . . . . . . .

Nationalitv

. . . . . . . . .

Inhalers

58
42

21
15

U. S. A.
Italian
Austrian
Russian
Puerto Rican

NO.

Nationality

. . . . . . . . . .

15
4
6
4
2

N;).

. . .

Irish
Romanian
Hungarian
Polish
Czechoslovakian

1
I
1

I
1

No. 2

SMOKING
A N D LUNG
CANCER*

Watson Q Cotite

249

TABLE10
COMPARISON OF SMOKING HABITS OF CONTROL AND CANCER-OF-THE-LUNG
FEMALE PATIENTS

cinogenic factor in the inception of primary


squamous and epidermoid lung carcinoma.
2. Advances in medical science during the
last fifty years, such as roentgenology, bronControl
Cancer of lung
choscopy, exfoliative cytology, together with
antibiotics, highly trained medical personnel,
Smoking
Av. no. yrs.
Av. no. yrs.
habits
smoked
% smoked
% and improved hospital facilities have helped
to brighten the horizon but have not removed
Smokers
15
20
Minimal
60
33
the prospect of a high morbidity and mortality
Moderate
34
59
from primary lung cancer. Therefore prophyHeavy
6
8
laxis and prevention are essential.
TOTAL
18
42
3. Early diagnosis should lower the morNonsmokers
82
58
tality and lead to a better survival rate. Prevention of the disease, however, depends upon
be eliminated and so lessen the danger of lung a true knowledge of cause and on the identificancer among smokers.
cation and elimination of the carcinogen believed to be in tobacco. This goal can be
SUMMARY
reached with the co-operation of the lay pub1. Our study adds to the growing evidence lic, governmental agencies, commercial organiof the increasing incidence of lung cancer and zatioiis concerned with the production of toadds weight to the premise that cigarette smok- bacco, and trained medical personnel joining
ing (when quantity and chronicity are consid- together in an earnest effort to discover the
ered) probably represents an additional car- causes of lung cancer.
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