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Environmental Tobacco Smoke and Lung Cancer in Nonsmoking Women: Title and subTitle BreakA Multicenter Study FREE

Elizabeth T. H. Fontham, DrPH; Pelayo Correa, MD; Peggy Reynolds, PhD; Anna Wu-Williams, PhD; Patricia A. Buffler, PhD; Raymond S. Greenberg, MD, PhD; Vivien W. Chen, PhD; Toni Alterman, PhD; Peggy Boyd, PhD; Donald F. Austin, MD; Jonathan Liff, PhD
[+] Author Affiliations

Reprint requests to Louisiana State University Medical Center, Department of Pathology, 1901 Perdido St, New Orleans, LA 70112-1393 (Dr Fontham).


JAMA. 1994;271(22):1752-1759. doi:10.1001/jama.1994.03510460044031
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Published online

Objective.  —To determine the relative risk (RR) of lung cancer in lifetime never smokers associated with environmental tobacco smoke (ETS) exposure.

Design.  —Multicenter population-based case-control study.

Setting.  —Five metropolitan areas in the United States: Atlanta, Ga, Houston, Tex, Los Angeles, Calif, New Orleans, La, and the San Francisco Bay Area, Calif.

Patients or Other Participants.  —Female lifetime never smokers: 653 cases with histologically confirmed lung cancer and 1253 controls selected by random digit dialing and random sampling from the Health Care Financing Administration files for women aged 65 years and older.

Main Outcome Measure.  —The RR of lung cancer, estimated by adjusted odds ratio (OR) with 95% confidence interval (CI), associated with ETS exposure.

Results.  —Tobacco use by spouse(s) was associated with a 30% excess risk of lung cancer: all types of primary lung carcinoma (adjusted OR=1.29; P<.05), pulmonary adenocarcinoma (adjusted OR=1.28; P<.05), and other primary carcinomas of the lung (adjusted OR=1.37; P=.18). An increasing RR of lung cancer was observed with increasing pack-years of spousal ETS exposure (trend P=.03), such that an 80% excess risk of lung cancer was observed for subjects with 80 or more pack-years of exposure from a spouse (adjusted OR=1.79; 95% CI=0.99 to 3.25). The excess risk of lung cancer among women ever exposed to ETS during adult life in the household was 24%; in the workplace, 39%; and in social settings, 50%. When these sources were considered jointly, an increasing risk of lung cancer with increasing duration of exposure was observed (trend P=.001). At the highest level of exposure, there was a 75% increased risk. No significant association was found between exposure during childhood to household ETS exposure from mother, father, or other household members; however, women who were exposed during childhood had higher RRs associated with adult-life ETS exposures than women with no childhood exposure. At the highest level of adult smoke-years of exposure, the ORs for women with and without childhood exposures were 3.25 (95% CI, 2.42 to 7.46) and 1.77 (95% CI, 0.98 to 3.19), respectively.

Conclusion.  —Exposure to ETS during adult life increases risk of lung cancer in lifetime nonsmokers.(JAMA. 1994;271:1752-1759)

REFERENCES

Office of Health and Environmental Assessment, Office of Research and Development. Respiratory Health Effects of Passive Smoking: Lung Cancer and Other Disorders . Washington, DC: US Environmental Protection Agency; 1992;.
Fontham ETH, Correa P, Wu-Williams A, et al.  Lung cancer in nonsmoking women: a multicenter case-control study. Cancer Epidemiol Biomarkers Prev . 1991;;1:35-43.
Akiba JD, Kato H, Blot WJ.  Passive smoking and lung cancer among Japanese women. Cancer Res . 1986;;46:4804-4807.
Brownson RD, Reif JS, Keefe TJ, Ferguson SW, Pritzl JA.  Risk factors for adenocarcinoma of the lung. Am J Epidemiol . 1987;;125:25-34.
Buffler PA, Pickle LW, Mason TJ, Contant C.  The causes of lung cancer in Texas.  In: Mizell M, Correa P, eds. Lung Cancer: Causes and Prevention . New York, NY: Verlag Chemie International Inc; 1984;:83-99.
Chan WD, Fung SC.  Lung cancer in nonsmokers in Hong Kong.  In: Grundmann E, ed. Cancer Campaign, VI: Cancer Epidemiology . Stuttgart, Germany: Gustav Fischer Verlag; 1982;:199-202.
Correa P, Fontham E, Pickle L, Lin Y, Haenszel W.  Passive smoking and lung cancer. Lancet . 1983;; 2:595-597.
Gao Y, Blot WJ, Zheng W, et al.  Lung cancer among Chinese women. Int J Cancer . 1987;;40:604-609.
Garfinkel L, Auerbach O, Joubert L.  Involuntary smoking and lung cancer: a case-control study. J Natl Cancer Inst . 1985;;75:463-469.
Geng G, Liang ZH, Zhang GL.  On the relationship between smoking and female lung cancer.  In: Aoki M, Hisamichi S, Tominaga S, eds. Smoking and Health . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;:483-486.
Humble CG, Samet JM, Pathak DR.  Marriage to a smoker and lung cancer risk. Am J Public Health . 1987;;77:598-602.
Inoue R, Hirayama T.  Passive smoking and lung cancer in women.  In: Aoki M, Hisamichi S, Tominaga S, eds. Smoking and Health . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;:283-285.
Janerich DT, Thompson WD, Varela LR, et al.  Lung cancer and exposure to tobacco smoke in the household. N Engl J Med . 1990;;323:632-636.
Kabat GC, Wynder EL.  Lung cancer in nonsmokers. Cancer . 1984;;53:1214-1221.
Kalandidi A, Katsouyanni K, Volopoulou N, et al.  Passive smoking and diet in the etiology of lung cancer among nonsmokers. Cancer Causes Control . 1990;; 1:15-21.
Koo LC, Ho JH, Saw D, Ho CY.  Measurements of passive smoking and estimates of lung cancer risk among nonsmoking Chinese females. Int J Cancer . 1987;;39:162-169.
Lam TH, Kung ITM, Wong CM, et al.  Smoking, passive smoking, and histological types in lung cancer in Hong Kong Chinese women. Br J Cancer . 1987;;6: 673-678.
Lam WK. A Clinical and Epidemiological Study of Carcinoma of the Lung in Hong Kong . Hong Kong: University of Hong Kong; 1985;. Thesis.
Lee PN, Chamberlain J, Alderson MR.  Relationship of passive smoking to risk of lung cancer and other smoking-associated diseases. Br J Cancer . 1986;;54:97-105.
Liu Z, He X, Chapman RS.  Smoking and other risk factors for lung cancer in Xuanwei, China. Int J Epidemiol . 1991;;20:26-31.
Pershagen G, Hrubec Z, Svensson C.  Passive smoking and lung cancer in Swedish women. Am J Epidemiol . 1987;;125:17-24.
Shimizu H, Morishita M, Mizuno K, et al.  A case-control study of lung cancer in nonsmoking women. Tohoku J Exp Med . 1988;;154:389-397.
Sobue T, Suzuki R, Nakayama N, et al.  Passive smoking among nonsmoking women and the relationship between indoor air pollution and lung cancer incidence. Gan No Rinsho . 1990;;36:329-333.
Svensson C, Pershagen G, Klominek J.  Smoking and passive smoking in relation to lung cancer in women. Acta Oncol . 1989;;28:623-629.
Trichopoulos D, Kalandidi A, Sparros L.  Lung cancer and passive smoking. Lancet . 1983;;2:667-668.
Wu AH, Henderson BE, Pike MD, Yu MC.  Smoking and other risk factors for lung cancer in women. J Natl Cancer Inst . 1985;;74:747-751.
Wu-Williams AH, Samet JH.  Environmental tobacco smoke: exposure-response relationships in epidemiologic studies. Risk Anal . 1990;;10:39-48.
Butler TL. The Relationship of Passive Smoking to Various Health Outcomes Among Seventh-Day Adventists in California . Los Angeles: University of California—Los Angeles; 1988;. Thesis.
Garfinkel L.  Time trends in lung cancer mortality among nonsmokers and a note on passive smoking. J Natl Cancer Inst . 1981;;6:1061-1066.
Hirayama T.  Cancer mortality in nonsmoking women with smoking husbands based on a large-scale cohort study in Japan. Prev Med . 1984;;13:680-690.
Hole DJ, Gillis CR, Chopra C, Hawthorne VM.  Passive smoking and cardiorespiratory health in a general population in the west of Scotland. BMJ . 1989;;299:423-427.
Brownson RC, Alavanja MC, Hock ET, Loy TS.  Passive smoking and lung cancer in nonsmoking women. Am J Public Health . 1992;;82:1525-1530.
Stockwell HG, Goldman AL, Lyman GH, et al.  Environmental tobacco smoke and lung cancer risk in nonsmoking women. J Natl Cancer Inst . 1992;;84:1417-1422.
Haley NJ, Axelrad CM, Tilton KA.  Validation of self-reported smoking behavior: biochemical analysis of cotinine and thiocyanate. Am J Public Health . 1983;;73:1204-1207.
Langone JJ, Gjika HB, Van Vunakis H.  Nicotine and its metabolites: radioimmunoassays for nicotine and cotinine. Biochemistry . 1973;;12:5025-5030.
Riboli E, Preston-Martin S, Saracci R, et al.  Exposure of nonsmoking women to environmental tobacco smoke: a ten country collaborative study. Cancer Causes Control . 1990;;1:243-262.
Jarvis MJ, Turnstall-Pedoe H, Feyerabend C, Vesey C, Saloojee Y.  Comparison of tests used to distinguish smokers from nonsmokers. Am J Public Health . 1987;;77:1435-1438.
Haley NJ, Colosimo SG, Axelrad CM, Harris R, Sepkovic DW.  Biochemical validation of self-reported exposure to environmental tobacco smoke. Environ Research . 1989;;49:127-135.
Hoffmann DW, Haley NJ, Adams JW, Brunneman KD.  Tobacco sidestream smoke: uptake by nonsmokers. Prev Med . 1984;;13:608-617.
Mattsen ME, Boyd G, Boyd D, et al.  Passive smoking on commercial airline flights. JAMA . 1989;; 261:867-872.
Schlesselmann JJ. Case-Control Studies: Design, Conduct, Analysis . New York, NY: Oxford University Press; 1982;.
Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods . Belmont, Calif: Lifetime Learning Publications; 1982;.
Ries LAG, Hankey BF, Miller BA, Hartman AM, Edwards BK. Cancer Statistics Review 1973-88 . Bethesda, Md: National Cancer Institute; 1991;: I52-VI23. NIH publication 91-2789.
Committee on Passive Smoking, Board on Environmental Studies and Toxicology, National Research Council. Environmental Tobacco Smoke: Measuring Exposures and Assessing Health Effects . Washington, DC: National Academy Press; 1986;.
Wynder EL, Goodman MT.  Smoking and lung cancer some unresolved issues. Epidemiol Rev . 1983;; 5:177-207.
Pron GE, Burch JB, Howe GR, Miller AB.  The reliability of passive smoking histories reported in a case-control study of lung cancer. Am J Epidemiol . 1988;;127:267-273.
Coultas DB, Peake GT, Samet JM.  Questionnaire assessment of lifetime and recent exposure to environmental tobacco smoke. Am J Epidemiol . 1989;;130:338-347.
LeMarchand L, Wilkins LR, Hankin JH, Haley NJ.  Dietary patterns of female nonsmokers with and without exposure to environmental tobacco smoke. Cancer Causes Control . 1991;;2:11-16.
Coultas DB, Samet JM, McCarthy JF, Spengler JD.  A personal monitoring study to assess workplace exposure to environmental tobacco smoke. Am J Public Health . 1990;;80:988-990.
Brunnemann KD, Cox JE, Hoffmann D.  Analysis of tobacco-specific N'-nitrosamines in indoor air. Carcinogenesis . 1992;;13:2415-2418.

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Office of Health and Environmental Assessment, Office of Research and Development. Respiratory Health Effects of Passive Smoking: Lung Cancer and Other Disorders . Washington, DC: US Environmental Protection Agency; 1992;.
Fontham ETH, Correa P, Wu-Williams A, et al.  Lung cancer in nonsmoking women: a multicenter case-control study. Cancer Epidemiol Biomarkers Prev . 1991;;1:35-43.
Akiba JD, Kato H, Blot WJ.  Passive smoking and lung cancer among Japanese women. Cancer Res . 1986;;46:4804-4807.
Brownson RD, Reif JS, Keefe TJ, Ferguson SW, Pritzl JA.  Risk factors for adenocarcinoma of the lung. Am J Epidemiol . 1987;;125:25-34.
Buffler PA, Pickle LW, Mason TJ, Contant C.  The causes of lung cancer in Texas.  In: Mizell M, Correa P, eds. Lung Cancer: Causes and Prevention . New York, NY: Verlag Chemie International Inc; 1984;:83-99.
Chan WD, Fung SC.  Lung cancer in nonsmokers in Hong Kong.  In: Grundmann E, ed. Cancer Campaign, VI: Cancer Epidemiology . Stuttgart, Germany: Gustav Fischer Verlag; 1982;:199-202.
Correa P, Fontham E, Pickle L, Lin Y, Haenszel W.  Passive smoking and lung cancer. Lancet . 1983;; 2:595-597.
Gao Y, Blot WJ, Zheng W, et al.  Lung cancer among Chinese women. Int J Cancer . 1987;;40:604-609.
Garfinkel L, Auerbach O, Joubert L.  Involuntary smoking and lung cancer: a case-control study. J Natl Cancer Inst . 1985;;75:463-469.
Geng G, Liang ZH, Zhang GL.  On the relationship between smoking and female lung cancer.  In: Aoki M, Hisamichi S, Tominaga S, eds. Smoking and Health . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;:483-486.
Humble CG, Samet JM, Pathak DR.  Marriage to a smoker and lung cancer risk. Am J Public Health . 1987;;77:598-602.
Inoue R, Hirayama T.  Passive smoking and lung cancer in women.  In: Aoki M, Hisamichi S, Tominaga S, eds. Smoking and Health . Amsterdam, the Netherlands: Elsevier Science Publishers; 1988;:283-285.
Janerich DT, Thompson WD, Varela LR, et al.  Lung cancer and exposure to tobacco smoke in the household. N Engl J Med . 1990;;323:632-636.
Kabat GC, Wynder EL.  Lung cancer in nonsmokers. Cancer . 1984;;53:1214-1221.
Kalandidi A, Katsouyanni K, Volopoulou N, et al.  Passive smoking and diet in the etiology of lung cancer among nonsmokers. Cancer Causes Control . 1990;; 1:15-21.
Koo LC, Ho JH, Saw D, Ho CY.  Measurements of passive smoking and estimates of lung cancer risk among nonsmoking Chinese females. Int J Cancer . 1987;;39:162-169.
Lam TH, Kung ITM, Wong CM, et al.  Smoking, passive smoking, and histological types in lung cancer in Hong Kong Chinese women. Br J Cancer . 1987;;6: 673-678.
Lam WK. A Clinical and Epidemiological Study of Carcinoma of the Lung in Hong Kong . Hong Kong: University of Hong Kong; 1985;. Thesis.
Lee PN, Chamberlain J, Alderson MR.  Relationship of passive smoking to risk of lung cancer and other smoking-associated diseases. Br J Cancer . 1986;;54:97-105.
Liu Z, He X, Chapman RS.  Smoking and other risk factors for lung cancer in Xuanwei, China. Int J Epidemiol . 1991;;20:26-31.
Pershagen G, Hrubec Z, Svensson C.  Passive smoking and lung cancer in Swedish women. Am J Epidemiol . 1987;;125:17-24.
Shimizu H, Morishita M, Mizuno K, et al.  A case-control study of lung cancer in nonsmoking women. Tohoku J Exp Med . 1988;;154:389-397.
Sobue T, Suzuki R, Nakayama N, et al.  Passive smoking among nonsmoking women and the relationship between indoor air pollution and lung cancer incidence. Gan No Rinsho . 1990;;36:329-333.
Svensson C, Pershagen G, Klominek J.  Smoking and passive smoking in relation to lung cancer in women. Acta Oncol . 1989;;28:623-629.
Trichopoulos D, Kalandidi A, Sparros L.  Lung cancer and passive smoking. Lancet . 1983;;2:667-668.
Wu AH, Henderson BE, Pike MD, Yu MC.  Smoking and other risk factors for lung cancer in women. J Natl Cancer Inst . 1985;;74:747-751.
Wu-Williams AH, Samet JH.  Environmental tobacco smoke: exposure-response relationships in epidemiologic studies. Risk Anal . 1990;;10:39-48.
Butler TL. The Relationship of Passive Smoking to Various Health Outcomes Among Seventh-Day Adventists in California . Los Angeles: University of California—Los Angeles; 1988;. Thesis.
Garfinkel L.  Time trends in lung cancer mortality among nonsmokers and a note on passive smoking. J Natl Cancer Inst . 1981;;6:1061-1066.
Hirayama T.  Cancer mortality in nonsmoking women with smoking husbands based on a large-scale cohort study in Japan. Prev Med . 1984;;13:680-690.
Hole DJ, Gillis CR, Chopra C, Hawthorne VM.  Passive smoking and cardiorespiratory health in a general population in the west of Scotland. BMJ . 1989;;299:423-427.
Brownson RC, Alavanja MC, Hock ET, Loy TS.  Passive smoking and lung cancer in nonsmoking women. Am J Public Health . 1992;;82:1525-1530.
Stockwell HG, Goldman AL, Lyman GH, et al.  Environmental tobacco smoke and lung cancer risk in nonsmoking women. J Natl Cancer Inst . 1992;;84:1417-1422.
Haley NJ, Axelrad CM, Tilton KA.  Validation of self-reported smoking behavior: biochemical analysis of cotinine and thiocyanate. Am J Public Health . 1983;;73:1204-1207.
Langone JJ, Gjika HB, Van Vunakis H.  Nicotine and its metabolites: radioimmunoassays for nicotine and cotinine. Biochemistry . 1973;;12:5025-5030.
Riboli E, Preston-Martin S, Saracci R, et al.  Exposure of nonsmoking women to environmental tobacco smoke: a ten country collaborative study. Cancer Causes Control . 1990;;1:243-262.
Jarvis MJ, Turnstall-Pedoe H, Feyerabend C, Vesey C, Saloojee Y.  Comparison of tests used to distinguish smokers from nonsmokers. Am J Public Health . 1987;;77:1435-1438.
Haley NJ, Colosimo SG, Axelrad CM, Harris R, Sepkovic DW.  Biochemical validation of self-reported exposure to environmental tobacco smoke. Environ Research . 1989;;49:127-135.
Hoffmann DW, Haley NJ, Adams JW, Brunneman KD.  Tobacco sidestream smoke: uptake by nonsmokers. Prev Med . 1984;;13:608-617.
Mattsen ME, Boyd G, Boyd D, et al.  Passive smoking on commercial airline flights. JAMA . 1989;; 261:867-872.
Schlesselmann JJ. Case-Control Studies: Design, Conduct, Analysis . New York, NY: Oxford University Press; 1982;.
Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods . Belmont, Calif: Lifetime Learning Publications; 1982;.
Ries LAG, Hankey BF, Miller BA, Hartman AM, Edwards BK. Cancer Statistics Review 1973-88 . Bethesda, Md: National Cancer Institute; 1991;: I52-VI23. NIH publication 91-2789.
Committee on Passive Smoking, Board on Environmental Studies and Toxicology, National Research Council. Environmental Tobacco Smoke: Measuring Exposures and Assessing Health Effects . Washington, DC: National Academy Press; 1986;.
Wynder EL, Goodman MT.  Smoking and lung cancer some unresolved issues. Epidemiol Rev . 1983;; 5:177-207.
Pron GE, Burch JB, Howe GR, Miller AB.  The reliability of passive smoking histories reported in a case-control study of lung cancer. Am J Epidemiol . 1988;;127:267-273.
Coultas DB, Peake GT, Samet JM.  Questionnaire assessment of lifetime and recent exposure to environmental tobacco smoke. Am J Epidemiol . 1989;;130:338-347.
LeMarchand L, Wilkins LR, Hankin JH, Haley NJ.  Dietary patterns of female nonsmokers with and without exposure to environmental tobacco smoke. Cancer Causes Control . 1991;;2:11-16.
Coultas DB, Samet JM, McCarthy JF, Spengler JD.  A personal monitoring study to assess workplace exposure to environmental tobacco smoke. Am J Public Health . 1990;;80:988-990.
Brunnemann KD, Cox JE, Hoffmann D.  Analysis of tobacco-specific N'-nitrosamines in indoor air. Carcinogenesis . 1992;;13:2415-2418.
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