Tobacco Smoking, Motor Exhaust Fumes, and General Air ... · atmospheres (2, 8, 9, 12, 13, 19),...

Tobacco Smoking, Motor Exhaust Fumes, and General AirPollution in Relation to Lung Cancer Incidence

CLARENCEA. MILLSANDMARJORIEMILLSPORTER

(Department of Experimental Medicine, University of Cincinnati, and Laboratoryfor Experimental Medicine,Cincinnati, Ohio)

The rapidly rising incidence and death ratesfrom lung cancer have now brought this diseaseinto the pandemic category (3) and have renderedimperative a searching evaluation of all majorcausative factors. Amelioration or removal of suchcausative factors seems necessary for control of thedisease's advance, since only in a minor percent

age of cases is diagnosis made early enough forsurgery to be curative. The survey results herepresented represent a limited effort at a separateevaluation of the major factors most closely associated with the disease incidence and indicate thelikelihood of a contributing role for motor exhaustfumes.

The finger of suspicion has now been pointed atthree types of pollution: cigarette smoke, motorexhaust fumes, and general urban air pollution.Certain occupational dusts and fumes have beenshown to be closely associated with lung cancerin exposed workers, but the total of all such occupational cancers is insignificant amid the widespread prevalence of the disease today. On theother hand, cigarette smokers seem definitely moreprone than do nonsmokers to develop this typeof cancer; and its over-all prevalence among industrialized urban populationsâ€”more exposed tomotor exhaust fumes and general urban air pollutionâ€”is fourfold higher than among rural residents. It is most unfortunate that many proponents of tobacco smoking etiology have disregarded the possibility that all factors work in synergyto pyramid the disease incidence in areas of atmospheric pollution and in the more exposed sex(males being more exposed to all factors).

In reporting our 1946 studies (14, 16) showinglung cancer to be twice as prevalent among menliving in polluted industrialized areas as in theclean suburbs of Chicago and Cincinnati, we remarked: "One would be inclined to look elsewhere

for a factor which is working synergistically withoutdoor air pollution to affect the respiratorytracts of men in particular. One at once thinks of

Received for publication May 20, 1957.

tobacco smoke in this connection, for the percentage of men who smoke is almost three times asgreat as that of women. ... It is therefore quitepossible that the really alarming respiratoryhazard men face in urban areas of heavy air pollution may be due to the combined and cumulativeeffects of such pollution in conjunction with thechronic irritational action of tobacco smoke."

Stocks later reported (20) a direct relationshipof the prevalence of lung cancer to the size of thecity and to urban population density in Britain,remarking: "The facts . . . seem to fit in with the

hypothesis that atmospheric pollution by smokeis an important factor on which tobaccosmoking isinterposed. . . . This would mean, in effect, thatsmoking is more dangerous to a town dweller thanto a country dweller."

Materials clearly carcinogenic for experimentalanimals have been isolated from polluted cityatmospheres (2, 8, 9, 12, 13, 19), from tobaccosmoke (6, 18), from motor exhaust fumes (10, 11),and from the smoky burning of a large variety oforganic materials. Thus, when statistical studiesshow a direct parallelism between lung cancerprevalence in men and the degree of air pollutionprevailing in the air they breathe, there wouldseem to be grounds for a strong suspicion thatthese known cancerigenic agents in the air areworking slowly through the years. In Chicago, forinstance, lung cancer death rates were found inmen to reach their peak a full decade earlier inlife among those men living in the city's most

polluted districts than among those living in itscleaner suburbs (14, 16).

World-wide attention has now been focused recently upon the tobacco smoking aspects of lungcancer causation by two publications, one inAmerica (7) and one in Britain (5). These two publications set forth the result of the most extensivesmoking-cancer surveys yet conducted, with results generally verifying the more limited previoussurveys of many other investigators. All agree inindicating lung cancer to be sharply more preva-

981

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982 Cancer Research

lent among smokers than nonsmokers. Unfortunately, however, all share also a common failureto consider the part other forms of air pollutionmay have played in the lung cancer causationunder study by them. Their surveys in every casewere carried out quite devoid of controls whichmight have segregated (in part at least) the tobacco smoking and the polluted air factors in the disease causation. All smoking-lung cancer surveysmade to date have dealt with nonrepresentative,specially selected groups of subjects and have beenseverely criticized by Berkson (1) as inadequatefor the drawing of valid conclusions of a generalnature.

obtained entirely by house-to-house visitation inthe Basin districts and by a combination of housevisitation and telephone calls in the suburban andcountry districts where almost all householdershave telephones. In all survey districts, well overhalf the family survey information was providedby the housewife, the adult male members of thehousehold being away at work during the interrogator's working hours. Evening telephone calls

provided contact with most of the householdershaving no informant available during the workingday. A housewife's brutal murder by a door-to-

door itinerant during the later course of the Basinsurvey gave rise to a general suspicion of all un-

OHIO URBAN-RURAL TOBACCO SMOKING SURVEY

Being conducted by the University of Cincinnati College of Medicine in a sincere effort tofind out just what part tobacco smoking and urban air pollution play in the rapidly risinglung cancer death rates. This is purely a fact-finding survey in the interests of human health,â€”it is in no way concerned with the Tobacco Industry or an Anti-Smoking Crusade.

Name Address..Street Zone City

(date) (Â«Re) (Â»ex) (color) (location of home, if different from above)

Place ofResidenceOccupationSmokingâ€”

aCigarettesCigarsPipeful:Estimate

of1955verage

nurrmiles

trave195419531952195119501949194819471946her

of cigarettes, cigars, or pipefuls perday.led

per pear by mutt>r vehiclecar, bus, 1ruck, etc.)

Smoking before 1946: what ; How much ; No. of years.

CHAKT1.â€”Questionaire tonn used in survey

OHIO URBAN-RURAL SURVEY

In planning a survey which would incorporatecontrols for a separate evaluation of the majorfactors and would be representative of the generalpopulation, we designed it to cover three contrasting Ohio population groupsâ€”the dirtier, Basindistricts of Cincinnati, the city's cleaner suburbs,

and rural populations living in the cleaner countryair of the state's rural counties. Items of informa

tion covered in the survey included sex, age, color,place and duration of residence, occupation, tobacco smoking history, and an estimate of annualmotor travel mileage (Chart 1).

Survey information on living populations was

known doorbell-ringers and temporarily curtailedthis section of the survey somewhat short of itsintended scope.

Although there will be those who object to ouruse of family survey information obtained solargely from the housewife, its accuracy is probably about as great as could have been obtaineddirectly from each family adult, as long as it concerns memory reporting of long-past events. Thealternative, a forward-progressing written daily logkept by each surveyed individual, also allows astrong possibility of bias by its daily emphasis ona given environmental factor such as tobaccosmoking through the necessary months or years.



MILLSANDPORTERâ€”TobaccoSmoke, Motor Exhaust Fumes, and Lung Cancer 983

Careful checking by the interrogators wheneverpossible indicated a reasonably close agreementbetween the housewife's estimate of the husband's

smoking and his own estimate.Although unable to carry out a purely random

sampling of smoking and driving habits in theliving population groups under study, we achievedwhat seemed the best compromise within ourmeans. The Cincinnati Basin area comprises theOhio River and Millcreek low-lying bottoms wheregeneral urban air pollution sources are greatestand natural ventilation poorest. Night-time windless weather periods of temperature inversionusually hold the pollution blanket down aroundthese Basin residents as the air they must perforcebreathe. Since our survey dealt with only thewhite population, it did not include the city's

worst slum areas. For convenience we chose themajor white population tenement area boundedon the west by Elm Street, on the north by CliftonAvenue, on the east by Sycamore Street, and onthe south by Twelfth Street. Within this area anapartment-to-apartment canvass was made ofwhite residents age 20 years or over. With regardto housing, economic status, and generally prevailing air pollution, this district is fairly representative of the entire Basin area inhabited by whiteresidents.

Since the lung cancer death cases subjected tosurvey represented all such occurring in the totalarea populations for a 9-year period, it was necessary that our living-person survey be related to thetotal living area populations of the Basin and suburban areas if we were to apply valid significancetests to any area differences found. Our suburbansurvey included one white man aged 40+ yearsfor each 65.2 men in the total living population,so we extended our Basin survey until we also hadone such person for each 65.2 in the Basin livingpopulation. In thus extending our Basin survey(previously curtailed by the housewife's murder)

we chose four discrete Basin neighborhoods wellaway from the previously described major centralarea (Worth Street in the East End, and portionsof Camp Washington, Cumminsville, and Fair-

view).The suburban living-person survey covered

every fourth household with listed telephone onapproximately 40 streets of the city's cleaner areas

in Price Hill, Westwood, and Cheviot. No significant differences were noted in the over-all smokinghabits of the Basin and suburban men set forthin Table 1.

Final tabulations presented in Table 2 includeonly those with at least 10 years' residence in the

given area. For the age groups of the white males

from 40 years upwards, for instance, this meantdisregarding only 4 per cent from the suburbansurvey, 6 per cent from the Basin, and 9 per centfrom the rural.

Information on residents dying of respiratorytract cancer during the 9-year period (1947-1955)

was obtained directly from the death certificates,from hospital records, and from near relatives orclose friends. Survey histories were obtained for76 per cent of all white resident cancer victims inthe urban districts and about 28 per cent in therural districts. All proved to be long-term (over10 years) residents of the given survey areas, although not always of the particular street address.Throughout this article, the term "lung cancer" is

loosely used to denote all primary cancers of therespiratory tract (#161-4 of the InternationalList of Causes of Death). Histological diagnosiswas not available in a majority of cases and wasnot recorded in our survey.

TABLE 1

SUMMARYOFSMOKINGHABITSOFWHITEMALESSURVEYED

BasinSuburbanRuralNon-smokers(percent)23.321.537.2Pipe

andcigars(per

cÂ«Dt)15.115

615.9Ciga

rettes(percent)61.662.946.9Total(percent)100.0100.0100.0

Table 2 in its upper third summarizes thesurvey findings for white men of Cincinnati's

cleaner areas (Census tracts 45-59, 62-5, 73, 75,79-85, 93-102, 105-9). By restricting the tabula

tion in Table 1 to age decades from 40 years upward, we were able to deal mainly with stabilizedsmoking experiences of 15 years or more. Any individual who had quit smoking less than 10 yearspreviously was listed according to his earlier smoking habits. Smoking combinations including cigarettes were listed always under the appropriatecigarette category. For those smokers "rollingtheir own," one bag of tobacco was considered as

the equivalent of one pack of ready-made cigarettes.

The middle third of Table 2 carries the sum-mated data on white males of Cincinnati's morepolluted Basin districts (Census tracts 1-29, 43-4,60-1, 74, 76-8, 86-7, 90-1, 103-4.

The final third of Table 2 carries the surveydata on white males of eighteen Ohio rural counties located at least 40 miles from sizeable industrialized urban centers (Adams, Brown, Coshoc-ton, Darke, Defiance, Geauga, Highland, Hocking,Holmes, Mercer, Monroe, Morgan, Noble, Paul-ding, Perry, Van Wert, Vinton, Williams). The



984 Cancer Research

rural living-population survey was limited toresidents of Brown county lying 40-60 mileseast of Cincinnati and with no city of as much as2500 population. To obtain even minimal numbersof lung cancer deaths in the rural survey, a listof all such recorded deaths for the 9-year period,1947-1955, was first obtained from the StateVital Statistics Section, names of victims and nextof kin from county records as far as possible fordirect questioning, with final recourse to the

survey lack of adequate numbers reduces theChi-square value to a questionable probabilitylevel (Table 3).

Cigarette smoking, when compared with nonsmoking, is also associated with an increased frequency of lung cancer deaths to a significant degree in all population groups. Application of thetest for a regression of the proportion of deaths onthe daily numbers of cigarettes smoked indicatedalso a significant association (4) (Table 4).

TABLE2NUMBERSOFWHITEMALESSURVEYED,*BYAGE,SMOKINGHABITS,ANDANNUALMILEAGESDRIVEN

POP.OB.Cincin

natisubur

banCincin

natiBubâ€¢miOhioruralareas1950POP.12,38011,84711,76185,48810,5448,99812,07881,665Â«4,78722,04834,95081,780AGE40-4950-5960+40+40-4950-5960+40+40-4950-5960+40+ANNUALMILEAGEDRIVENTotal<1Â«,000>

14,000Total<12,000>

12,000Total<

12,000>12,000Total<12,000>

12,000Total<12,000>

12,000Total<

12,000>12,000Total<

12,000>12,000Total<12,000>

12,000Total<

12,000>12,000Total<12,000>12,000Total<12,000>

12,000Total<12,000>

12, 000NoSMOKINGLiv-

Ca.ingdead8402608

043

38716

240

1434126

2117

17971320427

22512

124

12212

062

1061101

0118

IS108125

144

0ÃŽ7017046

035011

0118

111041014

1208

111661042

1PIPE

ANDCIGARSIJv-

Ca.ingdead1311112

02251953

0502642248

Â«853272SOIS27

0700

017

S1631

049

1946174

2732268

205215

31114

228

118010146

63967

089

1068721

8<15

CIO/BULiv

io*to173UtstcetoI8780710829721817187Â»*S88Â«41181tau4088*11188t/SÃ•TCa.dead2204tÂ»141CC201840004401414018180110110i2044015-35CIG/DATLiv-Ca.ingdeadISO9106524489

327524148S6

4680S36

13255

872116244

25121

898523361

4154847

749

4749380

9231

9620177301962

337125235

722513221

1816156

3118

28752143

7>

35CIG/IULiv

ing118ita48802011â€¢10â€¢1141CC770872881587187858C8318UorCa.dead58C14882S18s422713181C418117se28488311542C73278118133TOTALSLIT-Ca.ingdead208

17(8)t1661142

6185

58(24)1568829

20151

123(36)1299922

24544

198(6.1)45114893

50175

26(6)1471828

8125

67(18)1115314

14185

122(30)1791076

15485

215(55)43717848

37HZ

11(8)107565

6157

16(45)1051152

6230

44(128)2008930

5559

71(181)41255147

16*Including only men with 10+ years' residence in givenarea.t

Numbers in parentheses represent deaths without survey contact.

records of practicing physicians in the countieslisted. This phase of the rural survey will not becompleted for quite some time, but the results already at hand seem worthy of presentation at thistime.

In consultation with two Cincinnati biometri-cians, the following statistical analysis of the datapresented in Table 2 was carried out.

Pipe and cigar smoking, when compared withnonsmoking, is associated with an increased frequency of lung cancer deaths to a significant degree. This finding holds true for Cincinnati Basinand suburban white men, but in the Ohio rural

Significant degrees of association were alsofound to exist between cigarette smoking and increased lung cancer death frequency when separate calculations were made for those men drivingless than 12,000 miles per year in urban traffic andfor those driving more than this mileage (Table 5).

The graded character of this significant association of cigarette smoking with increased frequency of lung cancer deaths is shown in Chart2, in which lung cancer deaths included in thesurvey are expressed as a percentage of totalliving and dead surveyed populations in the various areas. An added point of significance, shown



MILLSANDPORTERâ€”TobaccoSmoke, Motor Exhaust Fumes, and Lung Cancer 985

in Chart 2, is the heightening of lung cancer deathpercentages among nonsmokers and both categories of cigarette smokers in association withdriving mileages above 12,000 mi/yr among bothurban population groups.

TABLE3COMPARISONOFPUPEANDCIGARSMOKINGWITHNON

SMOKINGAMONGWHITEMALESSURVEYED

Cincinnati Basin men, 40+ yrs.:LivingCancer deaths

TotalsXÂ»= 6.791 (D.F.* = 1)

.01>P>.001

Cincinnati suburban men,40+yrs.:

LivingCancer deaths

TotalsX!= 8.627 (D.F. = 1)

.01>P>.001

Ohio rural men, 40+yrs.:LivingCancer deaths

TotalsX2= 2.922(D.F. = 1)

.1>P>.05* D.F. = degrees of freedom.

Non-smokers

11313

126

11717

134

20811

219

Pipeand

cigars

7322

96

8532

117

8910

99

Total

18635

221

20249

251

29721

318

Driving mileages above 12,000 mi/yr as compared with lesser driving mileages are associatedto a significant degree with increased lung cancerdeath frequency among both urban survey populations but not among the rural (Table 6).

General urban air pollution, to which Basin residents are exposed much more than residents ofcleaner suburban areas, on the basis of the dataat hand seems associated with a heightening oflung cancer death frequency to a degree of questionable significance if all ages above 40 years areincluded in the calculation. The association becomes more clear and of significant degree, however, if the calculation is limited only to men ofages 40-59 years when driving habits are moresharply delineated (Table 7). It is fully realized, inmaking these calculations, that the lack of randomsampling in the area surveys enters a degree ofdoubt as to the validity of any conclusions to bedrawn.

Survey data similar to those presented in Table2 were also collected on white women of the threeareas (Table 8). Lung cancer frequency among thewomen was at levels too low for the application ofvalid significance testing of differences. There is asyet no evidence (from our survey data) of a tendency of lung cancer frequency in women to rise in association with cigarette smoking. It is of interestthat urban nonsmoking men exhibit lung cancerfrequencies not greatly different from those exhib-

TABLE4COMPARISONOFCIGARETTESMOKINGWITHNONSMOKINGAMONGWHITEMALESSURVEYED

Cin. suburban men, 40+yr.:LivingCancer deaths

TotalsSource

TotalLinear regressionQuadratic regression

Cin. Basin men, 40+yr.:LivingCancer deaths

TotalsSource


Ohio rural men, 40+yr.:LivingCancer deaths

TotalsSource


Non-smokers

11717

134

11313

126

20811

219

1-35cig/day

322107

429

268114

382

22932

261

>S5cig/day

2042

62

3166

97

S318

51

Totals

459166

625

412193

605

47061

531

D.F.

67.50036.14131.859

75.34675.833

- 0.487

87.25322.01015.243

<.001<.001<.001

<.001<.001

<.001<.001<.001



986 Cancer Research

ited by the women, suggesting the lack of anypurely sex factor in the disease incidence.

One point not answered by the data thus farpresented is whether tobacco smoking per se isassociated with a "triggering off" of lung cancer

development, or whether a basic biological factormay be leading to both tobacco smoking and cancerdevelopment. The latter is a conceivable possibility,but it is not reasonably conceivable that this relationship would involve cancers of the bronchialmucosa and not those of tissues not directly exposed to air-borne irritants or carcinogens.

In attempting to explore this point in our Cincinnati survey, we considered it wise to excludefrom consideration cancers of the digestive and

excretory systems and to limit ourselves entirelyto primary malignant tumors of the pancreas,prostate, central nervous system, and bones (#157,177, 193, and 196, International List of Causes ofDeath). Cincinnati resident deaths from thesecauses for 4 years (1952-55) were listed, and survey contact was obtained for 26 white males aged50-59 and for 28 aged 60-69. The percentages ofthese falling into the various smoking categoriesare shown in Table 9 and compared with analogouspercentages for the combined Cincinnati suburbanand basin living populations and lung cancerdeaths.

Men dying of these special types of cancer (pancreas, etc.) exhibited smoking habits essentially

TABLE5CLASSIFICATIONOFCIGARF.TTESMOKINGONBASISOFANNUALAUTOMOBILEMILEAGE

< 12,000m/ruCin.

suburban men,40+yr.TotalLinear

regressionQuadraticregressionCin.

Basin men,40+yr.:TotalLinear

regressionQuadraticregressionCin.

rural men,40+yr.:TotalLinear

regressionQuadraticregressionDJ.

xÂ«2

46.000130.857115.1432

67.941159.4461

84952

32.749117.3221

15.427P

DJ<.001

2<.0011<.0011<.001

2<0011.OK.

0011<

.0012<.0011<.001

1>

12,000MI/Ã•Kx1P10.898

.OK.00110651

.OK.0010.247.7<.512185

<00110.495<.0011.690.2<.l5.669

.1<.054.328.02<.051.341

.3 <2White

Men,age 40 +yrs.8OiAll drivingmileages70

A60jy//50//40//30

Jtf /^ 30i

^^jÂ¿/20 -^<"^ /2Â°'IOS^â€”

---or'^10-Ol

n0Mo 35>35Number

of cigarettessmokedâ€¢/,daily

80-1 80i<I2000mi/yr.60-

AT6050

/50-40-/ S>403Â°-

^/201

-Â¿Â¿-^S20'10*^---*10-0

1 0-Ã®a

BasinaSuburbanO

Rural^^^^-oCigar

apipesmokingA>I2000

mi/yr.//*////y^

,r^r

o^_r_OHÃ’35 >35 "O HÃ“35>35Number

of cigarettes smoked Number of cigarettessmokeddailydoilyCHART

2.â€”Surveyed lung cancer dead as percentageofotalliving and dead surveyed.TABLE

6RELATION

OFDRIVINGMILEAGETOLUNGCANCERDEATHSAMONGCincinnati

Basinmen,40+yrs.:LivingCancer

deathsTotalsX*=7.477(D.F.

=1).01>P>.001Cincinnati

suburbanmen40+yrs.:LivingCancer

deathsTotalsXt

= 6.162(D.F. =l).02>P>.01Ohio

rural men,40+yrs.juiving

CancerdeathsTotalsX2

= 0.477(D.F. =1)5>P>.3WHITE

MALESSURVEYED<12,000>12,000mi/yr

mi/yr437

4817837615

85451

9S14850599

143Aia

1*7r1 -ut55

16467

168TotalÂ»485215700-)44198742;55971630



MILLS AND PORTERâ€”Tobacco Smoke, Motor Exhaust Fumes, and Lung Cancer 987

similar to those of the living population controls,in sharp contrast to the much higher cigarettesmoking percentages of those dying of lung cancer.Application of x2 tests to the observed frequenciesindicated no significant differences between thesmoking habits of the special-type cancer victimsand the living populations, but it showed a sharplysignificant diffÃ©rencebetween the lung cancer victims and those succumbing to the special-typecancers having no polluted air contact (Table 10).

We cannot, therefore, entertain the hypothesisof a basic biological factor as possibly responsiblefor both the smoking and heightened lung cancerincidence in the smokers. These findings strengthenthe likelihood of real significance residing in theobserved relationships. Tobacco smoking wouldthus seem significantly related to the developmentof lung cancer, and this smoking-cancer relationship seems further heightened for those with highurban motor driving mileages and perhaps stillfurther for those residing in Cincinnati's polluted

Basin districts.The data here presented will make it difficult

for Kotin (or any other member of the ScientificAdvisory Board of the Tobacco Industry ResearchCommittee) to continue holding that there is"... no convincing evidence that tobacco pos

sesses the necessary qualifications for the initiationand promotion of lung cancer . . . ," or that theuse of tobacco is ". . . capable of playing only a

secondary role in the increase in lung cancerrates" (8). It would now seem most likely, rather,

that the heavy dosing of the respiratory mucosawith tobacco smoke for many hours each day actsas the dominant etiologic factor in much of today's

lung cancer, with motor exhaust fumes and general urban air pollution as yet perhaps serving onlyto aggravate the tobacco-smoking effects.

The only other survey approaching this one incomplete coverage of all major factors associatedwith lung cancer incidence is that of Stocks et al.(20) in England. It is unfortunate that Stocks andhis co-workers used hospital and clinic patients asrepresentative of the urban and rural populations,instead of making actual house-to-house surveysas we have now done. The errors of expecting hospital or clinic patients to represent the generalpopulations from which they derived have alreadybeen emphasized (17).

DISCUSSIONMost timely and of great significance in today's

serious lung cancer situation is Otto Warburg'srecent paper "On The Origin of Cancer Cells"

(22). In it Warburg presents the case for nonspecific and irreversible damage to intracellular

enzymatic systems of the mitochondria as the firststep in the change from a normal to a cancer cell.Such changes in the mitochondrial metabolismhave been shown to hold indefinitely throughmany successive cellular generations and to become progressively greater with repetition of thedamaging episodes. Labile sulfhydryl and oxidant-sensitive linkages make the epithelial tissues liningthe air passages very vulnerable indeed to suchintracellular damage from polluting materials inthe air breathed.

Herein lies a possible and very disturbing ex-

TABLE7DRIVINGMILEAGEANDLUNGCANCERDEATHSAMONG

ALLWHITEMALESSURVEYEDANDAMONGTHOSE40-59YEARSOLD

Baain Suburban TotalsBasin vs. suburban men,

40+yrs.:<12,000 mi/yr

888326

LivingCancerdeaths

437178

451148

TotalX2= 2.749(D.F. = 1

.1>P>.05

>12,000mi/yr.LivingCancer deaths

TotalX2= 1.683(D.F.= 1

All mileagesLivingCancer deaths

TotalX2= 2.857(D.F. = 1)

.1>P>.05Basin vs. suburban men, age

40-59 years only:<12,000mi/yr.

LivingCancer deaths

TotalX2= 8.579(D.F. = 1)

.01>P>.001

>12,pOOmi/yrLiving

Cancer deaths

TotalX2= 1.040(D.F. = 1)

.5>P>.3

All mileagesLivingCancer deaths

TotalXÂ»= 7.920(D.F. = 1)

.01>P>.001

615

50

143

485215

700

599

4837

85

544198

742

1214

14187

228

1029413

1442

25871

329

4222

64

30093

393

32249

371

7126

97

75

468

580120

700

11348

161

693168

861



988 Cancer Research

planation for the significant associations nowshown to exist between the various forms of airpollution and the rising lung cancer incidence.The urbanization and motorized mechanizationupon which today's civilization is based thus

seems to be encountering health hazards of considerable magnitude. Before the days of effectiveantibiotics and chemotherapy, pneumonia andtuberculosis exhibited the same close relationshipto polluted air as is found for lung cancer. Today,lung cancer is the greatest killer among respira-

are immediately associated with an excess of some350 respiratory and cardiac deaths each year, ascompared with the year's least smoggy days (15),

and yet still more importance is perhaps to beattached even there to the more chronic types ofpollution damage slowly leading on to the initiation of cancer and perhaps emphysema.

We must now consider the possibility that eachnonfatal exposure to polluted air damage mayproduce irreversible and irreparable cell damage inthe respiratory system which could accumulate

TABLE8NUMBERSOFWHITEFEMALESSURVEYED,*BYAGE,SMOKINGHABITS,ANDANNUALMILEAGESDRIVEN

GROUPCincin

nati!'Cincin

natiHasinareaaOhioruralareas1950POP.14,10412,79015,76642,66010,4929,07913,39032,961Â«3,88422,16335,62691,671AGE40-4950-5960+40+40-4950-5960+40+40-4950-5960+40

+ANNUALMILEAGEDRIVENTotal<

12,000>12,000Total<12,000>

12,000Total<

12,000>12,000Total<12,000>

12,000Total<

12,000>12,000Total<12,000>

12,000Total<12,000>

12,000Total<12,000>

12,000Total<12,000>

12,000Total<

12,000>12,000Total<

12,000>12,000Total<12,000>

12, 000No

SMOKINGLiv

ing12a12321SS129416316304214166686718Â»85017617603293281146144213212842352323Â«13Â«049Ca.dead660330ISIS0Â«42401103301717021210110{S0Â«7*70S3330<15

CIG/DAYLiv

ing66660SO300981IOS10413232024240212107777040391191811010069672Ca.dead0000003303300000000000000000u000000015-35

CIO/DATLiv-iag393812121011061601484804040013IS0101101024322990tS038362Ca.deadt20220000-140000ii0220S30220000000220>15-35CIO/DATLiv

ing000000000000220110110440440000000440Ca.dead1100000001102200000002Â«0110000000ii0TOTALSLiving230227318418041731721Â£87Â«7981501491ito15002112110anÂ«101214209S160IMS200247862461113Ca.dead9(l)t908(0)S018(8)18032(9)3208(1)S04(4)4019(4)19026(9)2604(5)05(1-1)S027(59)27036(77)360

* Including only those with 10+ years' residence in given area,

t Numbers in parentheses represent deaths without survey contact.

tory diseases and is rapidly growing in stature asa health problem. Other forms of chronic, non-fatal damage from breathing polluted air (emphysema, for instance) perhaps carry a muchgreater over-all hazard than does lung cancer butare more difficult of quantitation because they areless clear-cut and do not directly kill.

Air pollution's mass killing episodes (Belgium,

1930; Donora, 1948; London, 1948, 1952, and1956) are more dramatic but also perhaps of lessover-all importance than this slower damage to theair passages and lungs. Los Angeles' smoggy days

through the years with repetition of the exposureepisodes. This community health problem maythus differ sharply from those associated with infectious disease where tissue recovery is usuallycomplete following each damaging episode. Thispossibility of irreversible and accumulative damage from breathing polluted air renders imperative an entirely new evaluation of pollution levelssafely allowable for exposed persons. Immediatedamaging effects in the respiratory system mayperhaps no longer serve as the criterion of safetyâ€”wemust now consider the possibility that re-



MILLS AND PORTERâ€”Tobacco Smoke, Motor Exhaust Fumes, and Lung Cancer 989

peated but isolated exposure may eventually leadto accumulated cellular changes of serious importance.

SUMMARY AND CONCLUSIONSDetails are presented of a survey covering resi

dence, smoking and driving habits of living populations and those dying of lung cancer in the basin

TABLE9SMOKING

HABITSANDDEATHSFROMLUNGCANCERANDOTHERCANCERS*Surveyed

populationLivingwhitemalesCancerdeaths(pancreas,etc.)Cancer

deaths(lung)Living

whitemalesCancerdeaths(pancreas,etc.)Cancer

deaths (lung)Age50-59**U60-69uItNon-smokers(percent)22.023.13.230.925.08.6Pipeandcigar(percent)12.67.76.422.728.67.9Ciga

retteÂ«(percent)65.469.290.446.846.486.5

* These include primary malignant tumors of the pancreas, prostate,central nervous system, and bones.

and suburban areas of Cincinnati and in Ohiorural areas. The findings in this survey give riseto the following deductions and conclusions :

1. Tobacco smoking was found to be significantly related to lung cancer incidence in the subjects of this study, whether or not there was inaddition heavy exposure in urban motor traffic orto general urban air pollution.

2. Annual driving mileages above 12,000 milesper year, as compared with lesser driving mileages,are significantly related to lung cancer incidenceamong urban men, except for those in the heavysmoking category.

3. Lung cancer death frequencies were foundsignificantly higher among Cincinnati's Basin men

than among suburban men in this survey.4. Lung cancer rates in nonsmoking men, urban

or rural, did not differ significantly from the lowrates found prevailing in women of all groups.

5. Finally, it is suggested that the alarmingrise in lung cancer incidence is predominantly ahazard pertaining to urban tobacco smoking, buta hazard intensified for those urban smokers withheavy exposure also in urban traffic.

TABLE 10

RELATIONOFSMOKINGHABITSTODEATHSFROMLUNGCANCERANDCERTAIN

OTHERCANCERSNon- Cigarette

smokers smokersLiving 117 275Cancer deaths (pancreas, etc.) 13 31

Totals 130 306X2=.001 (D.F. = 1)

P=.98

Cancer of lungs 16 230Cancer of pancreas, etc. 13 31

Totals 29 261XÂ»= 22.018(D.F. = 1)

P<.001

LivingCancer (pancreas,

etc.)Totalsx'

=.461 (D.F.=.5>P>.3Non-smokers117131302)Pipe

andcigars69

1079Ciga

retteÂ»275

31306

Cancer (lungs) 16Cancer (pancreas,

etc.) 13

Totalsx' = 24.510(D.F. =

P<.001

29

19

10

29

230

31

261

Totals392

44

436

24644

290

Totals

461

54

515

265

54

319

REFERENCES

1. BERKSON, J. The Statistical Study of Association betweenSmoking and Lung Cancer. Proc. Staff Meeting MayoClinic, 30:319-48, 1955.

2. CAMPBELL, J. A. Cancerigenic Agents Present in Atmosphere and Incidence of Primary Lung Tumors in Mice.Brit. J. Exper. Path., 20:122-32, 1939.

3. CLEMMENSEN, J. Bronchial Carcinomaâ€”A Pandemic.Danish Med. Bull., 1:37-46, 1954.

4. COCHHAN, W. G. Some Methods for Strengthening theCommon x* Tests. Biometries, 10:417-51, 1954.

5. DOLL, R., and HILL, A. B. The Mortality of Doctors inRelation to Their Smoking Habits. Brit. M. J., pp. 1451-

55, 1954.6. ESSENBEHG, J. M. Cigarette Smoke and the Incidence of

Primary Neoplasm of the Lung in the Albino Mouse.Science, 116:561-62, 1952.

7. HAMMOND,E. C., and HORN, D. The Relationship betweenHuman Smoking Habits and Death Rates. J.A.M.A.,166:1316-28, 1954.

8. KOTIN, P. The Role of Atmospheric Pollution in Patho-genesis of Pulmonary Cancer: A Reriew. Cancer Research,16:375-93, 1956.

9. KOTIN, P.; FALK, H. L.; MADER, P.; and THOMAS, M.Aromatic Hydrocarbons: I. Presence in the Los AngelesAtmosphere and the Carcinogenicity of AtmosphericExtracts. A.M.A. Arch. Indust. Hyg. & Occup. Med.,9:153-63, 1954.

10. KOTIN, P.; FALK, H. L.; and THOMAS, M. Aromatic Hydrocarbons: II. Presence in the Particulate Phase of Gasoline Engine Exhaust and the Carcinogenicity of ExhaustExtracts. A.M.A. Arch. Indust. Hyg. & Occup. Med.,9:164-77, 1954.

11. . Aromatic Hydrocarbons: III. Presence in theParticulate Phase of Diesel Engine Exhausts and theCarcinogenicity of Exhaust Extracts. Ibid., 11:113-20,

1955.



990 Cancer Research

12. LEITER,J., and SBEAB,M. J. Production of Tumors inMice with Tars from City Air Dusts. J. Nat. Cancer Inst.,3:167-74, 1942^3.

18. LEITER,J.; SHIMKIN,M. B.; and SHEAR,M. J. Productionof Subcutaneous Sarcomas in Mice with Tars Extractedfrom Atmospheric Dusts. Jour. Nat. Cancer Inst., 3:155-65, 1942-43.

14. MILLS,C. A. Air Pollution and Community Health. Boston: Christopher Pub. House, 1954.

15. . Respiratory and Cardiac Deaths in Los AngelesSmogs. Am. J. Med. Sc., 233:379-86, 1957.

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J. Nat. Cancer Inst., 13:1283-98, 1953.18. ROFFO,A. H. Krebserzeugendes Benzpyren gewonnen aus

Tabakteer. Ztschr. Krebsforsch., 49:588-97, 1939.19. SEELIG,M. G., and BENIQNUS,E. L. Coal Smoke, Soot,

and Tumors of the Lung in Mice. Am. J. Cancer, 28:96-111, 1936.

20. STOCKS,P. Epidemiology of Cancer of the Lungs in England and Wales. Brit. J. Cancer, 6:99-111, 1952.

21. STOCKS,P., and CAMPBELL,W. Lung Cancer Death RateÂ»among Nonsmokers and Pipe and Cigarette Smokers, anEvaluation, in Relation to Air Pollution by Benzpyreneand Other Substances. Brit. M. J., pp. 929-34, 1955.

22. WABBURG,O. On the Origin of Cancer Cells. Science, 123:309-16, 1956.



1957;17:981-990. Cancer Res Clarence A. Mills and Marjorie Mills Porter Pollution in Relation to Lung Cancer IncidenceTobacco Smoking, Motor Exhaust Fumes, and General Air

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