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I I I I I I I I I I THE ETIOLOGY OF LUNG CANCER IN NONSMOKSNG FEMALES IN HARBIN, CHINA Dai Xu-dong, Lin Chun-yan, Sun Xi-wei, Shi Yu-bo and Lin Ying-ji Cancer Research Institute, Harbin Medical University Harbin, China Introduction Lung cancer is one of the most important types of malignancy in males, and is becoming increasingly common among females. A considerable amount of research conducted in different countries has focussed on studying the etiology of lung cancer. A number of epidemiological studies, conducted since the 1950s, have reported a close relationship between smoking and the incidence of lung cancer. Such an association, however, seems more directly applicable to males than females. Because Chinese women have a relatively low smoking prevalence yet have a higher incidence of lung cancer than might be anticipated, it seems possible that in females, some other risk factors are responsible for the increasing rate of lung cancer and may be more important than smoking. This report summarizes the results of a 1:1 population-based, case-control epidemiological study of nonsmoking females with lung adenocarcinoma, conducted in Harbin, China, designed to investigate the etiologic risk factors for lung cancer in nonsmoking females. Materials and Methods I I I I Information analyzed in this report came from the data bank collected over the last several years by the Department of Cancer Epidemiology, Cancer Research Institute, Harbin Medical University. To be included as a subject for the study, a patient had to reside in the city of Harbin for more than 10 years, be between 30 and 69 years of age, never have smoked more than 100 cigarettes, and be diagnosed with primary lung cancer, with confirmation by pathology, between January 1, 1992 and December 31, 1993. For each subject, a population control was also selected. Control subjects were randomly selected from the city of Harbin, matched 1:1 with cases by age (± 5 years) and by nonsmoking status. The field staff conducted face-to-face interviews in the hospital or at home. An unconditional logistic regression model was used for data analysis. The administered questionnaire covered such parameters as education, marital status, residence history, income, fuel use, diets, cooking and heating practices, exposure to passive smoke, individual tumor history, and family tumor history. Results 1. According to data obtained in different countries, smoking prevalence is lower in female than in male lung cancer subjects. Many reports show that the smoking prevalence for males exceeds 90 %; we found a somewhat lower rate of 88 % in Harbin. The smoking prevalence in female lung cancer subjects in Harbin is 45.4%, which is slightly higher than the 35.1'Y reported for Shanghai. I

I 2. A significant difference in worldwide lung cancer mortality rates has been observed for nonsmoking females. The lowest is 3.3/100,000, found in Bombay, India, and the highest is around 14.3/100,000, found in Chinese women in Hong Kong, Hawaii and Harbin. Time trends in the mortality rates for female lung cancer are very striking. In Hong Kong, where two-thirds of the female lung cancer cases are not attributable to smoking, the lung cancer mortality rate rose from 7.7 in 1961 to 29.3/100,000 in 1985. Likewise in Shanghai and Harbin, in which three-fourths of the female lung cancer cases are not attributable to smoking, the lung cancer mortality rate has also increased significantly over the years. 3. Previous studies have suggested that analysis of the histological types of lung cancer may provide clues to their etiology. Accordingly, the distribution of lung cancer histological types among nonsmoking females was determined in the present investigation. Our study found adenocarcinoma to account for 77% of lung cancer in nonsmoking females in Harbin, which is certainly consistent with several previously published findings and appears to be substantially higher than the 60% reported for Shanghai. 4. In order to examine the potential etiological factors for nonsmoking female lung cancer, a population-based, case-control study was conducted in Harbin, using 120 cases of nonsmoking female lung adenocarcinoma and the same number of nonsmoking female controls. An unconditional logistic regression model was used to analyze potential risk and protective factors. The results show the risk factors to be: period of coal stove use in the bedroom; period of heating by coal; exposure to coal dust for more than 10 years; practicing fried and deep fried cooking more than 5 times per month; and a history of cancer in the family. The protective factors are: personal income of more than 50 Yuan per month; average personal residence area of more than 6W in the last 20 years; carrot consumption of more than 65 times per year. Discussion The relationship between smoking and lung cancer has always been emphasized by epidemiologists. Many studies have shown an association between smoking and squamous cell carcinoma in males. Since in females the prevalence of smoking is relatively low, and because adenocarcinoma is the primary histological type in female lung cancer, it seems possible that risk factors exist for females which potentially play a more important role than smoking as the major cause of female lung cancer. I I I I I I I I I I I ~ ~ Based on data generated from epidemiological and experimental studies, several risk factors have been identified in the etiology of lung cancer in nonsmoking females. Koo and co-workers from Hong Kong indicate that the etiological factors for lung cancer in Chinese women may be related to some i unidentified environmental factors. Gao et al. from Shanghai point out the association between cookin g oil smoke and female lung cancer. Studies performed in Xuanwei, Yunnan Province, provide evidence for a relationship between smoke from indoor coal burning and the high rate of female lung cancer. Our ~ studies from Harbin, China, indicate that indoor air pollution from coal burning as well as lack o f vitamins are risk factors for female lung cancer. Additional studies are in progress to further analyze N these and other factors in order to fully expound the high rate of lung cancer in Chinese women. ~~ tp ~ -4 00 W , 2- Q CA ? I

i I I I I I I I I I I I I I References 1. Gao, Y-T; Blot, W.J., etal. Lung cancer among Chinese women. Int. J. Cancer 1987; 40:604 2. Hinds, M.W., et al. Differences in lung cancer risk from smoking among Japanese, Chinese and Hawaiian women in Hawaii. Int. J. Cancer 1981; 27:297 3. Koo, L.C. et al. An analysis of some risk factors for lung cancer in Hong-Kong. Int. J. Cancer 1985; 35:149 4. Koo L.C. and Ho J. H-C. Worldwide Epidemiological patterns of lung cancer in nonsmokers. Int. J. Eoidemiol. 1990, 19 Supplement 1, 514-523 5. Mumford, J.L., et al. Lung cancer and indoor air pollution in Xuanwei, China. Science 1987; 235:217 6. Byers, T., et al. Dietary vitamin A and lung cancer risk. Amer. J. Epidemiol. 1987; 125:351 7. Lubin, J.H. and Blot, W.J. Assessment of lung cancer risk factors by histological category. L Natl. Cancer Inst. 1984; 73:383 8. Lam, T.H., et al. Smoking passive smoking and histological types in lung cancer in Hong Kong Chinese women. Br. J. Cancer 1987; 56:673 9. Koo, L.C. Dietary habits and lung cancer risk among Chinese females in Hong Kong who never smoked. Nutr. Cancer 1988; 11:155 10. Hirayama, T. Diet and cancer. Nutr. Cancer 1979; 1:67 11. Enstrom, J.E. Rising lung cancer mortality among nonsmokers. J. Natl. Cancer Inst. 1979; 62:755 i -4 O W 3_ O Clt Gf I

I I Table 1. Smoking Prevalence for Male Lung Cancer Patients Place England Hong Kong New York City San Francisco, White Singapore, Chinese San Francisco, Chinese Shanghai Aichi, Japan Malaysia Harbin Norway Study 99.5 99.0 98.1 98.1 96.6 92.8 92.0 91.4 89.0 88.0 87.9 Doll et al. 1952 Chan et al. 1979 Kabat et al. 1984 Green et al. 1982 MacLennan et al. 1977 Green et al. 1982 Gao et al. 1987 Shimizu et al. 1984 Menon et al. 1979 Dai et al. 1988 Kvale et al. 1983 Table 2. Incidence Rates and Smoking Prevalence for Female Lung Cancer Patients Place Hawaii, Hawaiians Harbin San Francisco, Chinese San Francisco, White Hawaii, Chinese Hong Kong Singapore, Chinese Shanghai Hawaii, Japanese India France Age-adjusted incidence rates '' Smoking prevalence 40.5 27.2 25.1 24.7 23.6 23.4 19.8 18.1 11.5 4.0 3.5 84.5 45.4 43.9 91.9 22.4 56.0 52.3 35.1 46.0 5.6 47.9 -4- I I I I I I I r I 0 NOo I I I I

I 1 I I I I 1 I I I I I I I I I I I Table 3. Age-Adjusted Lung Cancer Mortality Rates Among Nonsmoking Women Place Bombay, India 1979 Hawaii, Japanese 1982 Japan 1985 Hawaii, Hawaiians 1982 USA, White 1964 Hong Kong, Chinese 1983 Hawaii, Chinese 1982 Harbin 1987 Rate Source 3.3 Jussawalla et al. 1979 4.7 Hinds 1982 5.3 Tominaga 1987 6.2 Hinds 1982 9.4 Haenszel et al. 1964 13.8 Koo etal. 1985 14.1 Hinds 1982 14.8 Dai 1988 Table 4. Temporal Changes in Lung Cancer Mortality Rates in Females PAR' of Place Smoking eriod.' Age-Adjusted Average:.Increase Rate Rates Japan 13 % Harbin 24% I Shanghai 24% ° Population Attributable Risk 1950-1985 1986-1990 1963-1980 0.80-6.10 20.93-29.19 11.10-18.40 6.16 11.72% 3.21 Table 5. Percentage of Nonsmoking Female Lung Cancer Patients With Adenocarcinoma Place Harbin Hong Kong, Chinese Shanghai Patients . %. with adenocarcinoma 190 454 152 77.0 67.2 61.0 -5- I

I Table 6. Logistic Regression Analysis for 120 Nonsmoking Female Lung Patients With Adenocarcinoma Factor B ~ OR . 05% CI . ~ Personal income per month in 1980 > =50 Average personal residcnce area > =6W Period of coal stove use in the bedroom 1-19 years > =30 years Period of heating by coal 1-24 years 25-34 years Exposure to coal dust > 10 years Fried and deep fried cooking >5 times per month Carrot consumption in 1980 >=65 times/year History of cancer in family -1.2523 0.286 0.090-0.903 0.0329 -1.7107 0.181 0.062-0.531 0.0019 1.4940 4.455 1.609-12.335 0.0040 2.9314 18.753 3.937-29.320 0.0002 1.7600 5.812 1.671-20.218 0.0057 1.5469 4.697 1.284-17,185 0.0194 0.9803 2.665 1.089-6.523 0.0318 2.2917 9.205 1.533-55.277 0.0152 -2.5954 0.075 0.018-0.307 0.0003 1.7646 5.839 1.581-21.568 0.0081 N O O j ~ 00 W O -6- ~ I I I I I I I I I I I I I I