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October 7, 1992, Vol 268, No. 13 >
ARTICLE | October 7, 1992

Active and Passive Smoking and Pathological Indicators of Lung Cancer Risk in an Autopsy Study FREE

Dimitrios Trichopoulos, MD; Franco Mollo, MD; Lorenzo Tomatis, MD; Emmanuel Agapitos, MD; Luisa Delsedime, MD; Xenophon Zavitsanos, MD; Anna Kalandidi, MD; Klea Katsouyanni, DrMedSc; Elio Riboli, MD; Rodolfo Saracci, MD
[+] Author Affiliations

Reprint requests to Department of Epidemiology, Harvard School of Public Health, 677 Huntington Ave, Boston, MA 02115 (Dr Trichopoulos).


JAMA. 1992;268(13):1697-1701. doi:10.1001/jama.1992.03490130085035
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References

Objective.  —The association between involuntary smoking and lung cancer has been supported by most epidemiologic studies, but a number of authors and interest groups claim that the possibility of bias has not been excluded. Few autopsy-based studies have explored the role of active smoking and other exposures in lung carcinogenesis, and none has been previously done to examine the role of passive smoking. We have undertaken such an autopsy-based study in Athens, Greece.

Design.  —Lung specimens were taken at autopsy from 400 persons 35 years of age or older, of both genders, who had died within 4 hours from a cause other than respiratory or cancer in Athens or the surrounding area. For each person at least seven tissue blocks were taken from the main and lobar bronchi and at least five blocks from the parenchyma, including an average of about 20 smaller cartilaginous bronchi and membranous bronchioles. The specimens were examined without knowledge of the exposures of the particular subject in Turin, Italy. For 283 (71%) of the subjects the preservation of the bronchial epithelium was satisfactory for pathological examination, and for 206 among them (73%) an interview could be arranged with their next of kin, focusing on smoking habits of the deceased and their spouses, as well as other variables. The interviewers were not aware of the results of the pathological examinations.

Main Outcome Measure.  —Specimens were examined for basal cell hyperplasia, squamous cell metaplasia, cell atypia, and (in membranous bronchioles and bronchiolo-alveolar airways) mucous cell metaplasia, ie, pathological entities that may be lung cancer risk indicators or epithelial, possibly precancerous, lesions (EPPL). The gland and wall thicknesses were also measured and their ratio calculated (Reid Index).

Results.  —In comparison with nonsmokers, EPPL values were significantly higher among current smokers and higher, but not significantly so, among former smokers. Furthermore, EPPL values were significantly higher among deceased nonsmoking women married to smokers rather than to nonsmokers. In this set of data neither occupation nor residence was associated with EPPL, but this could be due to the poor correlation of residential history with exposure to air pollution and the lack of adequate standardization of contemporary Greek occupations. The Reid Index was higher among smokers and former smokers in comparison with non-smokers, among subjects with mainly urban residence in comparison with those with mainly rural residence, and among nonsmoking women married to smokers in comparison with those married to nonsmokers, but none of these differences was statistically significant.

Conclusion.  —These results provide support to the body of evidence linking passive smoking to lung cancer, even though they are based on a study methodologically different from those that have previously examined this association.(JAMA. 1992;268:1697-1701)

REFERENCES

1 +
Trichopoulos D, KalandidiA, Sparos L, MacMahon B.  Lung cancer and passive smoking. Int J Cancer . 1981;;27:1-4.
2 +
Hirayama T.  Non-smoking wives of heavy smokers have a higher risk of lung cancer: a study from Japan. BMJ . 1981;;282:183-185.
3 +
Surgeon General. The Health Consequences of Involuntary Smoking: A Report . Rockville, Md: US Dept of Health and Human Services, Public Health Service, Centers for Disease Control, Center for Health Promotion and Education, Office on Smoking and Health; 1985;. DHHS (CDC) 87-8398:332.
4 +
Tobacco Smoking . Lyon, France: World Health Organization, International Agency for Research on Cancer; 1986;;38. IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans.
5 +
National Research Council, Committee on Passive Smoking. Environmental Tobacco Smoke: Measuring Exposures and Assessing Health Effects . Washington, DC: National Academy Press; 1986;.
6 +
Wald NJ, Nanchahal K, Thompson SG, Cuckle HS.  Does breathing other people's tobacco smoke cause lung cancer? BMJ . 1986;;293:1217-1222.
7 +
Trichopoulos D.  Passive smoking and lung cancer: the Ipsen Lecture 1987. Scand J Soc Med . 1988;;16:75-79.
8 +
Saracci R, Riboli E.  Passive smoking and lung cancer: current evidence and ongoing studies at the International Agency for Research on Cancer. Mutat Res . 1989;;22:117-127.
9 +
Kalandidi A, Katsouyanni K, Voropoulou N, Bastas G, Saracci R, Trichopoulos D.  Passive smoking and diet in the etiology of lung cancer among non-smokers. Cancer Causes Control . 1990;;1:15-21.
10 +
Janerich DT, Thompson DW, Varela LR, et al.  Lung cancer and exposure to tobacco smoke in the household. N Engl J Med . 1990;;323:632-636.
11 +
Riboli E, Preston-Martin S, Saracci R, et al.  Exposure of nonsmoking women to environmental tobacco smoke: a 10-country collaborative study. Cancer Causes Control . 1990;;1:243-252.
12 +
Lee PN.  Passive smoking and lung cancer association: a result of bias? Hum Toxicol . 1987;;6:517-524.
13 +
Lee PN.  Lung cancer and passive smoking: association an artefact due to misclassification of smoking habits? Toxicol Lett . 1987;;35:157-162.
14 +
Everingham R, Woodward S, eds. Tobacco Litigation: AFCO v TI A: The Case Against Passive Smoking . Sydney, Australia: Legal Books; 1991;.
15 +
Agapitos E, Delsedime L, Kalandidi A, et al.  Correlation of early pathological lesions in the bronchial tree with environmental exposures: study objectives and preliminary findings.  In: Riboli E, Delendi M, eds. Autopsy in Epidemiology and Medical Research . Lyon, France: International Agency for Research on Cancer; 1991;:263-268.
16 +
Auerbach O, Petrick T, Stout A, et al.  The anatomical approach to the study of smoking and bronchogenic carcinoma: a preliminary report of forty-one cases. Cancer . 1956;;9:76-83.
17 +
Auerbach O, Gere B, Forman J, et al.  Changes in the bronchial epithelium in relation to smoking and cancer of the lung. N Engl J Med . 1957;;256:97-104.
18 +
Reid L.  Measurement of the bronchial mucous gland layer: a diagnostic yardstick in chronic bronchitis. Thorax . 1960;;15:132-141.
19 +
Carroll R.  Changes in the bronchial epithelium in primary lung cancer. Br J Cancer . 1961;;15:215-219.
20 +
Auerbach O, Stout A, Hammond C, Garfinkel L.  Changes in bronchial epithelium in relation to sex, age, residence, smoking and pneumonia. N Engl J Med . 1962;;267:111-119.
21 +
Auerbach O, Stout A, Hammond C, Garfinkel L.  Bronchial epithelium in former smokers. N Engl J Med . 1962;;267:119-125.
22 +
Field WE, Davey EN, Reid L, Rose FJ.  Bronchial mucus gland hypertrophy: its relation to symptoms and environment. Br J Dis Chest . 1966;;60:66-80.
23 +
Cosio M, Ghezzo H, Hogg J, et al.  The relations between structural changes in small airways and pulmonary-function tests. N Engl J Med . 1977;;298: 1277-1281.
24 +
Auerbach O, Hammond C, Garfinkel L.  Changes in bronchial epithelium in relation to cigarette smoking, 1955-1960 vs. 1970-1977. N Engl J Med . 1979;;300: 381-386.
25 +
Cosio M, Hale K, Niewoehner D.  Morphologic and morphometric effects of prolonged cigarette smoking on the small airways. Am Rev Respir Dis . 1980;;122:265-271.
26 +
Mollo F, Bollati A, Bergia R, Colombo A.  Bronchial mucus gland enlargement in 'healthy' subjects: an autopsy survey on 343 cases of traumatic death, in Turin. Pathologica . 1981;;73:185-192.
27 +
Wright JL, Lawson LM, Paré PD, Kennedy S, Wiggs B, Hogg JC.  The detection of small airways disease. Am Rev Respir Dis . 1984;;129:989-994.
28 +
Mullen JB, Wiggs BR, Wright JL, Hogg JC,  Paré PD. Nonspecific airway reactivity in cigarette smokers. Am Rev Respir Dis . 1986;;133:120-125.
29 +
Whimster WF.  Tracheobronchial submucous gland profiles in smokers and non-smokers. Appl Pathol . 1988;;6:241-246.
30 +
Vine MF, Schoenbach VJ, Hulva BS, Koch GG, Samsa G.  Atypical metaplasia and incidence of bronchogenic carcinoma. Am J Epidemiol . 1990;;131:781-793.
31 +
Bosken CH, Wiggs BR, Paré PD, Hogg JC.  Small airway dimensions in smokers with obstruction to airflow. Am Rev Respir Dis . 1990;;142:563-570.
32 +
Wright JL, Cosio M, Wiggs B, Hogg JC.  A morphologic grading scheme for membranous and respiratory bronchioles. Arch Pathol Lab Med . 1985;;190: 163-165.
33 +
Thurlbeck WM, ed. Pathology of the Lung . New York, NY: Thieme Medical Publishers; 1988;:529-533.
34 +
Tannenbaum A, ed.  Report of the Working Group on Inhalation Carcinogenesis, with special reference to cigarette smoke. Int J Cancer . 1970;;5:282-285.
35 +
Solomon MD, Greenberg DS, Spjut HJ.  Morphology of bronchial epithelium adjacent to adenocarcinoma of the lung. Mod Pathol . 1990;;3:684-687.
36 +
Vutuc C.  Quantitative aspects of passive smoking and lung cancer. Prev Med . 1984;;13:698-704.
37 +
Glantz SA, Parmley WW.  Passive smoking and heart disease: epidemiology, physicology and biochemistry. Circulation . 1991;;83:1-12.
38 +
Wells AJ.  Breast cancer, cigarette smoking and passive smoking. Am J Epidemiol . 1991;;133:208-210.
39 +
Henderson DB, Gordon RJ, Menck H, Soohoo J, Martin SP, Pike MC.  Lung cancer and air pollution in southcentral Los Angeles County. Am J Epidemiol . 1975;;101:477-488.
40 +
Blot WJ, Fraumeni JF.  Geographic patterns of lung cancer: industrial correlations. Am J Epidemiol . 1976;;103:539-550.
41 +
Canvow BW.  The 'urban factor' and lung cancer: cigarette smoking or air pollution? Environ Health Perspect . 1978;;22:17-21.
42 +
Ford AB, Bialic O.  Air pollution and urban factors in relation to cancer mortality. Arch Environ Health . 1980;;35:350-359.
43 +
Hammond EC, Garfinkel L.  General air pollution and cancer in the United States. Prev Med . 1980;;9: 206-211.
44 +
Matanoski GM, Landau E, Tonascia J, et al.  Cancer mortality in an industrial area of Baltimore. Environ Res . 1981;;25:8-28.
45 +
Weinberg GB, Kuller LH, Redmond CK.  The relationship between the geographic distribution of lung cancer incidence and cigarette smoking in Allegheny County, Pennsylvania. Am J Epidemiol . 1982;;115:40-58.
46 +
Vena JE.  Air pollution as a risk factor in lung cancer. Am J Epidemiol . 1982;;116:42-56.
47 +
National Research Council, Committee on the Epidemiology of Air Pollutants, Board on Toxicology and Environmental Health Hazards, Commission on Life Sciences. Epidemiology and Air Pollution . Washington, DC: National Research Council, National Academy Press; 1985;.
48 +
Buffler PA, Cooper SP, Stinnett S, et al.  Air pollution and lung cancer mortality in Harris County, Texas, 1979-1981. Am J Epidemiol . 1988;;128:638-699.
49 +
Zu Z-Y, Blot WJ, Xiao H-P, et al.  Smoking, air pollution, and the high rates of lung cancer in Shenyang, China. J Natl Cancer Inst . 1989;;81:1800-1806.
50 +
Pershagen G, Simonato L.  Epidemiological evidence on air pollution and cancer.  In: Tomatis L, ed. Air Pollution and Human Cancer . New York, NY: Springer-Verlag NY Inc; 1990;:63-74. European School of Oncology Monograph.
51 +
Katsouyanni K, Trichopoulos D, Kalandidi A, Tomos P, Riboli E.  A case-control study of air pollution and tobacco smoking in lung cancer among women in Athens. Prev Med . 1991;;20:271-278.

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

1 +
Trichopoulos D, KalandidiA, Sparos L, MacMahon B.  Lung cancer and passive smoking. Int J Cancer . 1981;;27:1-4.
2 +
Hirayama T.  Non-smoking wives of heavy smokers have a higher risk of lung cancer: a study from Japan. BMJ . 1981;;282:183-185.
3 +
Surgeon General. The Health Consequences of Involuntary Smoking: A Report . Rockville, Md: US Dept of Health and Human Services, Public Health Service, Centers for Disease Control, Center for Health Promotion and Education, Office on Smoking and Health; 1985;. DHHS (CDC) 87-8398:332.
4 +
Tobacco Smoking . Lyon, France: World Health Organization, International Agency for Research on Cancer; 1986;;38. IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans.
5 +
National Research Council, Committee on Passive Smoking. Environmental Tobacco Smoke: Measuring Exposures and Assessing Health Effects . Washington, DC: National Academy Press; 1986;.
6 +
Wald NJ, Nanchahal K, Thompson SG, Cuckle HS.  Does breathing other people's tobacco smoke cause lung cancer? BMJ . 1986;;293:1217-1222.
7 +
Trichopoulos D.  Passive smoking and lung cancer: the Ipsen Lecture 1987. Scand J Soc Med . 1988;;16:75-79.
8 +
Saracci R, Riboli E.  Passive smoking and lung cancer: current evidence and ongoing studies at the International Agency for Research on Cancer. Mutat Res . 1989;;22:117-127.
9 +
Kalandidi A, Katsouyanni K, Voropoulou N, Bastas G, Saracci R, Trichopoulos D.  Passive smoking and diet in the etiology of lung cancer among non-smokers. Cancer Causes Control . 1990;;1:15-21.
10 +
Janerich DT, Thompson DW, Varela LR, et al.  Lung cancer and exposure to tobacco smoke in the household. N Engl J Med . 1990;;323:632-636.
11 +
Riboli E, Preston-Martin S, Saracci R, et al.  Exposure of nonsmoking women to environmental tobacco smoke: a 10-country collaborative study. Cancer Causes Control . 1990;;1:243-252.
12 +
Lee PN.  Passive smoking and lung cancer association: a result of bias? Hum Toxicol . 1987;;6:517-524.
13 +
Lee PN.  Lung cancer and passive smoking: association an artefact due to misclassification of smoking habits? Toxicol Lett . 1987;;35:157-162.
14 +
Everingham R, Woodward S, eds. Tobacco Litigation: AFCO v TI A: The Case Against Passive Smoking . Sydney, Australia: Legal Books; 1991;.
15 +
Agapitos E, Delsedime L, Kalandidi A, et al.  Correlation of early pathological lesions in the bronchial tree with environmental exposures: study objectives and preliminary findings.  In: Riboli E, Delendi M, eds. Autopsy in Epidemiology and Medical Research . Lyon, France: International Agency for Research on Cancer; 1991;:263-268.
16 +
Auerbach O, Petrick T, Stout A, et al.  The anatomical approach to the study of smoking and bronchogenic carcinoma: a preliminary report of forty-one cases. Cancer . 1956;;9:76-83.
17 +
Auerbach O, Gere B, Forman J, et al.  Changes in the bronchial epithelium in relation to smoking and cancer of the lung. N Engl J Med . 1957;;256:97-104.
18 +
Reid L.  Measurement of the bronchial mucous gland layer: a diagnostic yardstick in chronic bronchitis. Thorax . 1960;;15:132-141.
19 +
Carroll R.  Changes in the bronchial epithelium in primary lung cancer. Br J Cancer . 1961;;15:215-219.
20 +
Auerbach O, Stout A, Hammond C, Garfinkel L.  Changes in bronchial epithelium in relation to sex, age, residence, smoking and pneumonia. N Engl J Med . 1962;;267:111-119.
21 +
Auerbach O, Stout A, Hammond C, Garfinkel L.  Bronchial epithelium in former smokers. N Engl J Med . 1962;;267:119-125.
22 +
Field WE, Davey EN, Reid L, Rose FJ.  Bronchial mucus gland hypertrophy: its relation to symptoms and environment. Br J Dis Chest . 1966;;60:66-80.
23 +
Cosio M, Ghezzo H, Hogg J, et al.  The relations between structural changes in small airways and pulmonary-function tests. N Engl J Med . 1977;;298: 1277-1281.
24 +
Auerbach O, Hammond C, Garfinkel L.  Changes in bronchial epithelium in relation to cigarette smoking, 1955-1960 vs. 1970-1977. N Engl J Med . 1979;;300: 381-386.
25 +
Cosio M, Hale K, Niewoehner D.  Morphologic and morphometric effects of prolonged cigarette smoking on the small airways. Am Rev Respir Dis . 1980;;122:265-271.
26 +
Mollo F, Bollati A, Bergia R, Colombo A.  Bronchial mucus gland enlargement in 'healthy' subjects: an autopsy survey on 343 cases of traumatic death, in Turin. Pathologica . 1981;;73:185-192.
27 +
Wright JL, Lawson LM, Paré PD, Kennedy S, Wiggs B, Hogg JC.  The detection of small airways disease. Am Rev Respir Dis . 1984;;129:989-994.
28 +
Mullen JB, Wiggs BR, Wright JL, Hogg JC,  Paré PD. Nonspecific airway reactivity in cigarette smokers. Am Rev Respir Dis . 1986;;133:120-125.
29 +
Whimster WF.  Tracheobronchial submucous gland profiles in smokers and non-smokers. Appl Pathol . 1988;;6:241-246.
30 +
Vine MF, Schoenbach VJ, Hulva BS, Koch GG, Samsa G.  Atypical metaplasia and incidence of bronchogenic carcinoma. Am J Epidemiol . 1990;;131:781-793.
31 +
Bosken CH, Wiggs BR, Paré PD, Hogg JC.  Small airway dimensions in smokers with obstruction to airflow. Am Rev Respir Dis . 1990;;142:563-570.
32 +
Wright JL, Cosio M, Wiggs B, Hogg JC.  A morphologic grading scheme for membranous and respiratory bronchioles. Arch Pathol Lab Med . 1985;;190: 163-165.
33 +
Thurlbeck WM, ed. Pathology of the Lung . New York, NY: Thieme Medical Publishers; 1988;:529-533.
34 +
Tannenbaum A, ed.  Report of the Working Group on Inhalation Carcinogenesis, with special reference to cigarette smoke. Int J Cancer . 1970;;5:282-285.
35 +
Solomon MD, Greenberg DS, Spjut HJ.  Morphology of bronchial epithelium adjacent to adenocarcinoma of the lung. Mod Pathol . 1990;;3:684-687.
36 +
Vutuc C.  Quantitative aspects of passive smoking and lung cancer. Prev Med . 1984;;13:698-704.
37 +
Glantz SA, Parmley WW.  Passive smoking and heart disease: epidemiology, physicology and biochemistry. Circulation . 1991;;83:1-12.
38 +
Wells AJ.  Breast cancer, cigarette smoking and passive smoking. Am J Epidemiol . 1991;;133:208-210.
39 +
Henderson DB, Gordon RJ, Menck H, Soohoo J, Martin SP, Pike MC.  Lung cancer and air pollution in southcentral Los Angeles County. Am J Epidemiol . 1975;;101:477-488.
40 +
Blot WJ, Fraumeni JF.  Geographic patterns of lung cancer: industrial correlations. Am J Epidemiol . 1976;;103:539-550.
41 +
Canvow BW.  The 'urban factor' and lung cancer: cigarette smoking or air pollution? Environ Health Perspect . 1978;;22:17-21.
42 +
Ford AB, Bialic O.  Air pollution and urban factors in relation to cancer mortality. Arch Environ Health . 1980;;35:350-359.
43 +
Hammond EC, Garfinkel L.  General air pollution and cancer in the United States. Prev Med . 1980;;9: 206-211.
44 +
Matanoski GM, Landau E, Tonascia J, et al.  Cancer mortality in an industrial area of Baltimore. Environ Res . 1981;;25:8-28.
45 +
Weinberg GB, Kuller LH, Redmond CK.  The relationship between the geographic distribution of lung cancer incidence and cigarette smoking in Allegheny County, Pennsylvania. Am J Epidemiol . 1982;;115:40-58.
46 +
Vena JE.  Air pollution as a risk factor in lung cancer. Am J Epidemiol . 1982;;116:42-56.
47 +
National Research Council, Committee on the Epidemiology of Air Pollutants, Board on Toxicology and Environmental Health Hazards, Commission on Life Sciences. Epidemiology and Air Pollution . Washington, DC: National Research Council, National Academy Press; 1985;.
48 +
Buffler PA, Cooper SP, Stinnett S, et al.  Air pollution and lung cancer mortality in Harris County, Texas, 1979-1981. Am J Epidemiol . 1988;;128:638-699.
49 +
Zu Z-Y, Blot WJ, Xiao H-P, et al.  Smoking, air pollution, and the high rates of lung cancer in Shenyang, China. J Natl Cancer Inst . 1989;;81:1800-1806.
50 +
Pershagen G, Simonato L.  Epidemiological evidence on air pollution and cancer.  In: Tomatis L, ed. Air Pollution and Human Cancer . New York, NY: Springer-Verlag NY Inc; 1990;:63-74. European School of Oncology Monograph.
51 +
Katsouyanni K, Trichopoulos D, Kalandidi A, Tomos P, Riboli E.  A case-control study of air pollution and tobacco smoking in lung cancer among women in Athens. Prev Med . 1991;;20:271-278.

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