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t'J lnt. J. concer: 27. 1-4 (J980 LUNG CANCER AND PASSIVE SMOKING Dimitrios TRICHOPOL'LOS', Anna KALAtiDID11. Loukas SPARROS' andBrian MACM,AHON='3 ' Dcpactmrnt of Hygiene and Epidemiology. Universiq• of Athens School of Medicinr„ Athens. Grrrcr =Deparrment of Epidcmiology, Harvard School of Public Health, 677 Huntington Avenue, Boston. MA 02115„ USA. ".tins women with ItMtg cancer and 167 ottw hw. phal patients wsn k+tsr.iswsd r+rjarding the smokig Nabits of tAcrrrsl.as and their ht+sbv+dt- Fortr of the lun= cancer taass and 149 of the atiwer Patisnts wsre non.unok.rs. Amonit the non-smokkt= women there was a ststisticatly .ignificant diHsr.ncs t4.twssn the cancer tasss and the otlttr patients with rsspsct en tiislr AuabanA' smoklng habits. Estimates of the r.laeirs rYk of AwK cancer as.ociat.d with having a Ntrbard who snwksa were 14 for a t.rrwksr of ktsa than ons pack and 3.4 for women wtw.e husbands tmok.d more Mvt ons Pack of cigarettes per day. The Itlnkations of the data are sxarninsd; It b evident that further kwsstlption of th's ioue it warranted. Acute and chronic effects on lung function and the cardiovascular svstem have been noted in non-smok- ers involuntarily or passively exposed to the ciga- rette smoke of others (Aronow, 1978; Lenfant and Liu, 1980). We report observations suggesting that the effects of such exposure may includ'e the most notorious health consequence of smoking among smokers themselves - carcinoma of the lung. MATERIAL AND U¢THODS This is a case-control study: The cases were all of the female. Caucasian patients, registered as resi- dents of Athens, who were admitted to any of three large hospitals in Athens, between September 1978 and June 1980, with~a finalidiagnosis of lung cancer other than adenocarcinoma or terminal bronchial (alveolar) carcinoma. The hospitals were the largest chest hospital of Athens ("Sotiria"), the largest cancer hospital ("Agios savas") and the only other hospital exclusively for cancer patients ("Agii Anar- gyri"). Of the 51 cases identified, 14 .rere histologi- cally and 19 cytologically confirmed, while in 18 the diagnosis was based on clinical and radiological evi- dence. Diagnosis of adenocarcinoma can confidently be excluded in the 14 histologically confirmed ases. it tsposstble that some adenocarcinomas are in- cluded among the 19 cytologically diagnosed cases and probable that there are some among the 18 clini- cally diagnosed patients. However, even in un- selected clinical series of lung cancerr cases among women in Cmcrce, adenocarcinotnas and alveolar carcinotnas do not represent more than one-third of cases (Papacharalampous, personal commuttica- tion): the number in our series is tkrefore not likely to be more than seven or eight. Comparison patients (controls) were hospitalized during the same time period in the Athens Hospital for Orthopedic Disorders (KAT). This hospital is located in the same area of Athens as those which were the sources of the cases. The hospitals from which the cases came were considered unsuitable as sources of controls because of the high proportion of patients with other diseases of the lungs and other smoking-related diseases: we did not wish to have the interviewer judge. on a case-by-case basis. the suitability ofa patient for control purposes. Six times during the time-period of the study, the same physir cian who interviewed the cases visited the Hospital for tJrthopedic Disorders and interviewed all the av- ailable adult women patients in two departments of the hospital. Non-Caucasian patients and patients not registered as residents of Athens were not in- cluded. Of the 163 controls so ascertained, 108 were being treated for fractures, 18 for osteoarthrosis and 37 for other bone and joint diseases. All cases and comparison patients (controls) were interviewedby the same physician. They were asked about the smoking habits of themselves and their husbands. Specifically, they were asked when they started smoking. if and when they stopped and what was the average number of' cigarettes smoked daily; the same questions were asked about, their hus- bands. Those who had stopped smoking 5-20 years before the interview were classified as ex-smokers; those who had stopped smoking within 5 years of the interview were considered as current smokers; and those who stopped smoking more than 20 years pre- viously were classified as non-smokers. For the com- putation of the total'number of cigarettes smoked byy her husband, a woman's exposure was considered to start with her marriage and to end when she was divorced'„ or when the husband died or stopped smoking. A change of htuband was considered as a change in the husband's smoking habits (if the two were in fact different), and singleness was consi- dered the equivalent oT rnarriage to a non-srnoker. Statistical significance is assessed by the X= for linear trend in proportions, as described by Armit- age (1971). asstrLis Demographic characteristics of the cases and con- trols are compared in Table 1. The groups are similar in age, as indicated by the distributions in Table I and tneans of 61.7 for cases and 62.1 for controls. Duration of marriage, occupation, sodoeconomic status (as measured by years of schooling) and re- cent residence are not notably or signi6cantly diffe- tent between txses and controls. It is, therefore, not necessary to stratify for these variables in the analy- sis particularly since none is significantly associated -'To whom reprint requests should be addrested. Received: October 15, 1980.

2 TRJCHOPOULOSET AL TABLE I 1.umhcr Penzntyr. Clunnersm Cnn Conoroh Cases Gciatroh Total number 51 163 100.0 100.0 Age: <50 years 7 21 13.7 129 5U-69 years 30 98 58.8 60.1 70+ years 14 44 21.5 27.0 Never married 1 15 2.0 9.2 Duration of marriage': <20iyears 8 33 16.0 22.3 20=39 years 31 70 62:0 47.3 40!years 11 45 22.0 30.4. Occupation Housewife 32' 96 62.7 58.9 Agriculture or labor 12 44 23.5 27.0 Schooling of 6+ years 19 71 37.3 43.6 Recent residena': Urban 34 101 66.7 62.0 Semi,urban 3 13 , 5.9 8.01 Rural 14 49 27.5 30!1. ' Percenuges of the samed. -° All pauents ryere repstered as.resrdent m Atliens. bui some hadchanted resdence recertmn.. perNpe m connecvoe .tih theu oeedlor medical nre. Clusified acmrdm6 to:e+andardeLulfscusono of the GreekKauonal Statrtical Servrce. with smoking in these data. The duration of sehool- ing of the husband was slightly longer in controls than in cases (65:0 °k 6 years or more, compared to 54.9 9c ) but again was not related to smoking habit. Among the 51 women with lung cancer, 11 were smokers, whereas among the 163 control women J4 were smokers, giving a relative risk associated with smoking of 2.9. These 25 women, were excluded from the following analysis. The mean age of the remaining 40 lung cancer patients was 62.8years and of the 149 remaining control women 62.3 years. Among non-smokers, control women were of onlyy slightly higher socioeconomic status than the cancer patients - 63 °k of their husbands had finished prim- ary school, compared to 5896 amotig the controls. Table II shows the distribution of non-smoking women with lung cancer and of non-smoking control women according to current imoking habits of their husbands. Tbere is a-statistially significant associa iti- on betwaen the 6usband"s smoking and a woman' Mmg cancer nsk. A>,on-smokia= woman whose hus- DEMOGRAPHIC CHARAC7ERISTICS OF THE CASE AND CONTROL PATIENTS band is a regular smoker has a risk of developing lung cancer which is twice as high as that of a non-~ 1smoking woman married'to a non-smoker. Table III' shows the distribution of non•stnoking women with lung cancer, and of non-smoking control women according to the estimated total number of cigarettes smoked by their husbands by the time of the interview. It may be noted thatihere are only 64 women in the "zero" category since the husbands of three women with lung cancer and of 15 controls died',,or divorced their wives, or stopped smoking, more than 20 years ago and thus were classified among the non-smokers in Table II. There is a statis- tically significant association ~ between total number of cigarettes smoked by the husband and a woman's lung cancer risk. The aisociation between husband's smoking habits and wife's lung canoer risk was ex- amined separately for patients with or without cy- tological confirmation of the cancer. The slope of the linear trend was praeticaUy idential in the two groups. TABLE n SMOKING HABITS OF HUSDANOS OF NON-SMOKING WOMEN wITH LUNG CANCER AND OF NON-SMOICDdG COlP17tOL MOMEN' I~~c s~a N6eqmotns. E.s400oter. Cyesnas PaA.y. (otmmt awi.n) Lung cancer 11 6 Controls 71 22 RR' 1.0 1.8 1-10 ~ r1-20 21-30 31+ TeW 2 13 4 4 40 9 32 6 9 149 „~- 2.4 3.4 ' ReLtm rnk - the rati6 of the rst' of tiuy wKSr amoo .oexn rtfoae husbandl belong lo a puncvlu raotm9 otepry to tlsat .®o06 .amea, rhose husbaadt are noa-emoken. - Xs (lisrar trend) m 6.~~. a(2-tail) <0.02.

LUNG CANCER AND~~MSS~~IVE SMOKIhG~, 3~ It was noted above that the proportion of never- married women is lower among the cases than among the controls, andl since single women have been classified with those whose husbands were non- smokers, the associations in Tables ll and ILI are stronger than would have been observed if concern were limited to ever-married women, In Athens, in the age-groups involved in this study. never-married women tend:to have the traditional values and habits associated with singleness in elderly women and for this reason are, we believe, correctly classified in the extretrx group of.+omen never having been exposed to a husband's cigarette smoking. However, if the single women are excluded, the association remains significant (X2 - 4.6; p=0j03) and relative risks of 1.5, 2.0 and 3.0 are observed for the three categories 'of husband's smoking for which relative risks are shown in Table 11. unusual i opportunity to investigate this issue. Until about 20 years ago, smoking was unusual among wo- men. whereas it was already quite common among meni('Cireek Cancer Society. 1978). It is therefore easier to discover an effect of passive smoking among Greek women than among men or, womemin other Western populations, since in the latter groups the overwhelming effects of active smoking, to- gether with the high correlation between smoking habits of spouses. will confound and conceal the les- ser effects of passive smoking. Ir is, omfinr curnideration, strange that the rela- tive risk associated with passive smoking in this study (2.4 for all categories of smokers combined) is only slightly lower than the figure of 2.9 associated with active smoking by the women themselves. However, the numbers are small and the confidence TABLE lIl DISTRIBLTION OF tiOt; SMOKIyG wOMEw wITH LUNG CAI:CER AND OF NON-SMOKING COK-RtOL WOMEN ACC"ORDrNG TO THE ESTIMATED TOTXL hUMBER OF CIGwRETrES SMOKED BY THEIR HUSBA.NDS BY TFM TIME OF TtM INTERVIEw n'Y"tK Toaal num6er of ryarma ~(mM rAaa.nds) ~. poup 0 1-99. 100-14D. 7DQ0.p9. Ji06-)9'9. a00+~. Teol Lung cancer 8' 4 6 9 6 7 40 Controls 56 21 26 16 12 IB 149 RR' 1.0 1.3 2.5 ~-----•---r 3 - .0 "See foornote to Tab1eI X' (tancar trend7.- 6.50. p(2-ud)~<0.02 DISCUSSION This study has obvious limitations and is offered principally to suggest that further investigation of this issue should be pressed. Most seriously,, jhe numbers of cases are small, Nevertheless, the associ- ation is in the direction expected - if any association were to be expected - and is unlikely to be due to chance. There is a high percentage (35 °k) of cases lacking cytology, but the association existed both in those with and in those without cytologic diagnosis. That the comparison group was taken from a diffe- rent hospital from those of the cases may also raise questions. However, the ratio of smokers among the cases themselves to that among the comparison pa- tients is about as expected from previous studies of smoking and lung cancer in women (Hammond, 1966; Doll rro1:, 1980), and Do rtujor demographic difference between cases and cantrols was found, other than in the proportion of single women. The difference in the proportion of single women is eon- sistenv with the hypothesis of a meaningful associa- tion between lung cancer risk and husband's smok- ing, but in any event cannot explain the difference observed within the group of, married women. Against the limitations of the study must be put the fact that the Greek setting provides a somewhat limits of the latter figure are broad (95%, 1.3-6.8). In the only other controlled'study of this matter in Greece (Kanellakis et cl:, 1976), smokers of kss than one pack of cigarettes a day had a 5-fold and' smokers of more than one pack per day a 200.fold increase in lung cancer relative to non-smokers. These are the risks appropriately compared with our estimates of 2.4 and 3.4 associated with husband's smoking of similar amounts. Further, active "smok- ing" does not have the same connotation in men and women. Women smokers tend to smoke less heavily than male smokers but have lower relative risks of lung cancer even for a given level of smoking (Ham- mond, 1972). 7he explanation appears to I'se in the facts that duration of smoking is an important deter- minant of risk, women in the current lung txncer ages commenced smoking at a later age than tnen of similar age and have therefore been smoking for shorter periods, and substantially smaller propor- tions of women than men inhale (Wald, 19'78; Doll er 01., 1980). These factors complicate a comparison of the risks associated with active and passive smoking, but at least one of them - the frequency of inhalation - seems likely to operate in favor of a relatively larger effect for passive than for active smoking, other components of the exposure being equal. Fi, nally, it has been observed that smokers tend to clus-

4. TRICIiOrOU1.OS ET AL ter together socially (Reeder. 1977)„and the smok- ing habits of a woman's husband may be an index of a broader exposure to cigarette smoke than thar whichemanates from the husband himself. ACKKOw1EDGEME`.TS This work was supponed by, grants fTom the Greek Ministry of Social Ser^vices and the U.S. Na- tional Cancer institute (5 PO1 CA 06373). REiERENCEs Aro.trrwcE. P.. Stanmca/ nsrrhods in ntedical rtseanch. Blsck• well Scientific.,Oidord (19711. Arto:ow, W.S.. Etfect of passive smoking on anpnapectoris. N. Engf: J. Med.'. 2l9, 21-24 (1978):.. Dott. R., GnAV, R., HArr>ftt. B., and Psro, R.. Mortality in relatbn to smoking 22 years' observation on femak British doaors. Bnt. nted. J, l0.967-976 (1980). G%EEx CAr+cEn Socgn. Research on tAe.Qinida of the prDlic towords cancer, pp. 48-51, Cancer Society. Athens (1978) (In Greek). Hwaaor.m E.C.. Smoking habits and'air polhnion in relation to lung cancer. /n D.H.K. Lee (ed. ), Environmenml factors in nrspirotorJ• diuau. pp. 177-199, Academic Press, New York (1972): HAw+tor,v. E.C:. Srnoking in relation to the death tates o( one million men and'wonxn. In. W. Haettsrrl (bd:), Na. Camcer Itxr Monogr. No. l'!, pp, 127-204. Superitttendent of Docv- tnents, Washington, D.C. (1966). K..rjEtLUUS, A.. Tnicuorout;os. D, MrcttAiAxoroucos, N., MARAGOVDASIS. S.. KANELLA1t1. K.. XIROUCMAKI, E., and. KA>_arontwrcI. V.. The relationship betweenstnokin` of Greek eiprettes and~ the development of lung cancer. Mareria Med.' Grrca. 4,3514355 (1976) (In Greek. with an English sumtnaryp. UwAxr. C.. and LrL. B.M.. (Passive) smokers versus (volun, tary)~senokers. N. Engl. J. Mi•d.. 302, 742-743 (198U): Reenea. L.G.. Soeioeultural f.cton in the etiobgy of smoking behavior: an assessment. In. M:E. Jarvik. J.W: Cullen. E.R'. Gritz, T.M. Vogt, and L.J. West (ed!), Research on smoking behavior. Nanonal /nrnrute an Drug Abuse Research Monogr; 17. DHEW' Publication No. (ADM) 78-581, pp, 186-200, Superintendent of Documents. Washington D.C:,(1977):, WAtD: N.J.. Smoking as a cause of disease.Jn: A.E. Bennett (ed): Recenr advances in communirv rnedinne. pp 73-96. Churchill Li4in(stone, New York (1978),.