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American Journal of Epidemiodogy Vol 137. No 2 Copyright C 1993 by The Johns Hopkins University School of Hygiene and Public HeaR^ Pnnted in U S A AA rights reserved indoor Air Pollution and Lung Cancer in Guangzhou, People's Republic of China Qing Liu,'•Z Annie J. Sasco,2.3 Elio Riboli,2 and Meng Xuan Hu' A case-control study comprising 224 male and 92 female incident lung cancer cases and the same number of individually matched hospital controls was conducted from June 1983 to June 1984 in Guangzhou, People's Repubbc of China, to evaluate the association between indoor air pollution and lung cancer risk. Guangzhou residents were exposed to several sources of pollution in their homes, most importantly to cooking fumes. Increased risks were found among subjects living in a house without a separate kitchen (the exposure odds ratio was 2.4 (95% confidence interval (Cl) 1.4- 4.2) for men and 5.9 (95% Cl 2.1-16.0) for women). Simiiariy, living in a house with poor air circulation was associated with an exposure odds ratio of 2.1 (95% Cl 1.2- 3.8) for men and 3.6 (95% CI 1.4-9.3) for women. A trend in the association between lung cancer risk and factors pertaining to house and kitchen ventilation was observed, and a decreasing risk of lung cancer was observed for several variables indicating better ventilation, even after adjustment for potential confounders such as education, occu- pation, living area, smoking, and history of chronic respiratory diseases. No statistically significant differences were found between cases and controls for frequency of cooking at home, presence of a chimney in the kitchen, or type of cooking fuel. Smoking was clearly related to risk of lung cancer in both men and women, and among nonsmoking women, exposure to tobacco smoke from their spouses was also associated with an increased risk. These results suggest that, in addition to smoking, indoor air pollution may be a risk factor for lung cancer. Am J Epidemiol 1993;137:145-54. air pollutants, environmental; lung neoplasms; smoking; tobacco smoke pollution; ventilation Lung cancer is the major cause of cancer death for both men and women in Guang- zhou, the main city in the Guangdong prov= ince of the People's Republic of China, rep- resenting about one fourth of all cancer deaths in that city. During the period 1981- 1984, the crude mortality rates for lung can- cer in the Guangzhou metropolitan area Received for publication March 18, 1991, and in final form August 17, 1992. Abbreviation: Cl, confidence interval. ' Department of Medical Statistics, Sun Yat-Sen Univer- sity of Medical Sciences, Guangzhou 510089, People's Republic of China. 2 Unit of Analytical Epidemiology, International Agency for Research on Cancer, 150 cours Albert Thomas, 69372 Lyon Cedex 08. France. ' tnstdut National de la Sante et de la Recherche Medi- cate (INSERM), Lyon, France. 145 were, respectively. 45 male deaths and 24 female deaths per 100,000 person-years (1). Although smoking is the most important cause of lung cancer (2-4), smoking behav- ior cannot fully explain the epidemiology of lung cancer in Chinese women, in whom there is a rather high incidence of lung cancer, predominantly adenocarcinoma, de- Reprint requests to Dr. Annie J. Sasco, Unit of Analytical Epidemiology, Wiernational Agency for Research on Can- cer, 150 cours AJbert Thomas, 69372 Lyon Cedex 08, France. Dr. Qing Liu was supported by a Research Training Fellowship awarded by the International Agency for Re- search on Cancer. The authors are grateful to Dr. Jing Yuan, Dr. Hao-Ran Guo, and Jiu-Lan Zhang for conducting the interviews and to the staffs of the Guangzhou hospitals who gave ;nvaJu• able access to ttieir patients and records. 25a11g6987

1-FO ....u U. spite relatively low smoking rates (5-12). The male:female ratio of lung cancer inci- dence is about 2 in China (1, 13), even though there is a much bigger difference than that in smoking rates between men and women. In contrast, this ratio varies from 4 to 10 in Western Europe and is about 2 in the United States (13), but with a much higher prevalence of current and former smokers among American women. During the last decade, increasing atten- tion has been paid to the health effects of the indoor microenvironment. Some studies have shown a positive relation of passive smoking to lung cancer risk (14-18), as well as an association with exposure to radon and its decay products (19-25). However, re- search results for other sources of indoor air pollution, such as cooking and heating, have been rather elusive and inconclusive (26- 29). The goal of this study was to evaluate whether there is any relation between indoor air pollution resulting from domestic cook- ing practices and lung cancer occurrence. MATERIALS AND METHODS Newly diagnosed cases of primary lung cancer (International Classification of Dis- eases, Ninth Revision, code 162) were se- lected from eight major hospitals covering most of Guangzhou from June 1983 to June 1984. All cases occurred in permanent resi- dents of the city of Guangzhou. A total of 327 lung cancer cases were identified from the medical records of these eight hospitals during that year. It was possible to complete an interview for 316 cases (224 men and 92 women; 96.6 percent). Eleven cases were excluded because either they were too ill to answer the interview, they could not be traced, or they had already died. Fifty-five percent of cases were diagnosed by means of repeated chest radiographic examinations and clinical examination; 13 percent were diagnosed by bronchoscopy alone; and 32 percent of the cases had cytologic or histo- logic confirmation. Controls who were also permanent resi- dents of the city of Guangzhou were individ- uallv matched to cases on age (to within 2 vears), sex. residential district (Liwan. Yuexiu, Haizhu, or Dongshan), and date of diagnosis or hospital admission. Controls were selected according to the matching cri- teria among inpatients of the surgery de- partments at six of the same eight major hospitals. No controls were chosen from either the Tumor Hospital or the Chest Hos- pital. Patients who had been admitted for chronic obstructive diseases of the lung, pul- monary tuberculosis, malignant tumors. and coronary heart disease were excluded. Each control was to be interviewed during the 2 months following the interview of his/her matched case. In most instances, the first selected patient control was interviewed; only for 26 subjects were second-choice con- trols chosen because of an inability to trace the subject or because an individual was found to be inadequate regarding one or several of the matching variables. No subject refused the interview. The interview was carried out at the sub- ject's home by trained epidemiologic work- ers using a structured questionnaire. All cases and controls were interviewed in per- son. The interviewers obtained extensive in- formation about the subject's general de- mographic characteristics, occupational his- tory, history of respiratory diseases, family cancer history, smoking habits, spouse's smoking habits, cooking practices (including domestic fuel use), and residence history. After completing the questionnaire, the in- terviewer measured the size of the windows and doors that opened onto the outside of the building, thereby providing an estima- tion of ventilation capacity. The ventilation capacity of the kitchen was analyzed sepa- rately from that of the rest of the dwelling, hereafter designated the living area. If the subject had lived in his or her present home for less than 20 years, the interviewer asked similar questions regarding the preceding residences and their ventilation conditions. In the latter case, given that no measure- ments were available, the ventilation condi- tions of previous residences were simply ranked as poor, average, or good based on the questionnaire data. Data on up to three residences were collected; however, since the 2501196988

Indoor Air Pollution and Lung Cancer 147 (Liwan, t1d date of Controls ;ching cri- irgery de- :ht major isen from 'hest Hos- nitted for lung, pul- mors, and ,ied. Each -ing the 2 )f his/her the first erviewed; ioice con- v to trace idual was g one or 4o subject l,ohulation of the People's Republic of' ('hina is relatively stable. ven• few subjects f1ad mo%ed more than twice. E\posure odds ratios. their 95 percent confidence intervals. and significance levels %%ere computed using a matched-pair analy- sis method (30). A conditional logistic regression model was used to estimate ex- posure odds ratios for multiple class vari- ables and to adjust for confounding factors. The SAS (31) and EGRET (32) software packages were used for the analysis. RESULTS Table I presents the demographic char- acteristics of lung cancer cases and controls. The ages of cases ranged from 28 years to 83 vears. hut the majority of cases were in their fifties or sitties. The median ages of male and female cases were 62 years and 60.5 years. respectively. The median ages of male and female controls were 62 and 61.5. Almost all subjects were of Han nationality. and most subjects had been born in the province of Guangdong. Marital status. ed- ucational level. dialect, occupation, and liv- ing area did not differ significantly between cases and controls. although cases had a lower educational level and a smaller aver- age living area than controls. Thus, we con- trolled for education. occupation, and living area when we analyzed other variables. t the sub- ,gic work- iaire. All =d in per- ensive in- neral de- ional his- a, family spouse's including = history. e, the in- windows ,utside of 1 estima- •ntilation ~ed sepa- dwelling, •a. If the mt home ~er asked )receding nditions. measure- in condi- ° simply )ased on to three since the TABLE 1. Demographic characteristics of lung cancer cases and controls, Guangzhou, People's Republic of China, 1983-1984 Men Women Characteristic No. of cases No. of controls No. of cases °° No. of controls % Age (years) <40 2 0.9 3 1.3 1 1.1 1 1.1 40-49 13 5.8 12 5.4 9 9.8 10 10.9 50-59 76 33.9 80 35.7 33 35.9 33 35.9 60-69 90 40.2 84 37.5 24 26.1 23 25.0 >70 43 19.2 45 20.1 25 27.2 25 27.2 Marital status Married 193 86.2 194 86.6 56 60.9 53 57.6 Widowed 27 12.1 24 10.7 36 39.1 33 35.9 Divorced 3 1.3 4 1.8 0 0.0 0 0.0 Single 1 0.4 2 0.9 0 0.0 6 6.5 Years of education <1 22 9.8 10 4.5 40 43.5 41 44.6 1-6 139 62.1 134 59.8 35 38.0 '35 38.0 7-12 50 22.3 60 26.8 17 18.5 16 17.4 >13 13 5.8 20 8.9 0 0.0 0 0.0 Province of birth Guangdong 207 92.4 206 92.0 8'0 87.0 83 90.2 Other 17 7.6 18 8.0 12' 13.0 9 9.8 Occupation Worker 152 67.8 153 68.3 59 64.1 55 59.8 Other 70 31.3 67 29.9 11 12.0 13 14.1 None 2 0.9 4 1.8 22 23.9 24 26.1 Living area (m2 per person) <2.00 11 4.9 6 2.7 2 2.2 2 2.2 2.00-3.99 56 25.0 42 18.7 27 29.3 15 16.3 4.00-7.99 100 44.6 109 48.7 38 41.3 42 45.6 _8.00 57 25.5 67 29.9 25 27.2 33 35.9 2501196989

I TABLE 2. History of occupational exposure and personal and familial history of selected diseases among lung cancer cases and controFs, Guangzhou, People's Republic of China, 1983-1984 Men Women Exposure ~ controls EOR,• EOR2' 95°~6 Cl' ~~tr~ EOR, EORz 95% CI History of occupational ex- posure Nonet 151 184 1.0 1.0 69 78 1.0 1.0 Dust 20 8 2.6 2.2 0.78-62 13 4 4.3 8.8 1.6-46.6 Srnoke 23 12 2.1 2.1 0.89-5.1 1 2 0.74 0.57 0.00-73.4 Other 30 20 1.7 1.6 0.72-3.5 9 8 1.5 1.0 0.26-4.2 History of puimonary tuber- culosis Not 137 176 1.0 1.0 78 85 1.0 1.0 Yes 87 48 2.8 2.4 1.3-4.6 14 7 2.2 1.3 0.39-4.3 History of ctronic bronchitis Not 125 185 1.0 1.0 63 79 1.0 1.0 Yes 99 39 3.9 3.0 1.6-5.5 29 13 2.6 0.90 0.36-2.4 Family history of cancer Not 203 216 1.0 1.0 83 86 1.0 1.0 Yes 21 8 2.9 0.90 0.62-1.3 9 6 1.5 0.94 0.54-1.6 ' EOR,, matched exposure odds ratio: EOR2, matched logistic exposure odds ratio, adjusted for education, occupation, Iiving area, and smoicing; tq, confidence intaval. t Referent. As expected, the subjects with lung cancer showed increased frequencies of occupa- tional exposure to hazardous working envi- ronments, a history of pulmonary tubercu- losis, and a historv of chronic bronchitis in both sex groups (table 2). When education, occupation, living area, and smoking were controlled for. the associations of lung can- cer with the above risk factors were not substantially modified among men, but they were attenuated or even disappeared among women, except for exposure to dust. In con- trast, the increased risk of lung cancer asso- ciated with a family history of cancer, found in univariate analysis, disappeared for both men and women when we controlled for the same variables. Smoking was strongly re- lated in a dose-response manner to the risk of lung cancer in both men and women (table 3). Ninety-five percent of male cases and 59 percent of female cases had ever smoked, compared with 80 percent and 25 percent of male and female controls, respec- tively. The exposure odds ratios for lung cancer were 6.3 (95 percent confidence in- terval (CI) 2.7-15.0) and 4.9 (95 percent CI 2.3-10.4) among male and female smokers. respectively. An increased risk of lung cancer was also observed among nonsmoking women who lived with a husband who smoked the equivalent of 20 or more ciga- rettes per day (table 3). Table 4 presents information on the cook- ing practices of lung cancer cases and con- trols. Results showed that women bore the primary burden of cooking in the family. The majority of families cooked three times per day at home, and coal was the basic cooking fuel used. Questions were asked on the type of fuel used during three historical periods (1949-1957. 1958-1976, and 1977 to the present). Since cooking fuel is rationed by the government, there was little variation in fuel usage among families in Guangzhou. Before 1958, most families used wood and charcoal. From 1958 to 1976, they gradually turned to coal, and gas was used only after 1976. Results are presented for the most recent period, which is the only one in which differences between cases and controls could be distinguished. The history of coal use in Guangzhou was usually longer than 20 vears. and only in the past 3-5 years had a small proportion of families changed to pe' troleum gas as a domestic fuel. Very fQw families used mainlv electricity or kerosene 2501 1 96990

Indoor Air Pollution and Lung Cancer 149 •ases among 2 95% Ci 1.6-46.6 0.00-73.4 0.26-4.2 0.39-4.3 0.36-2.4 0.54-1.6 ;cupation, living .)nsmoking •band who more ciga- n the cook- s and con- n bore the he familv. hree times the basic e asked on : historical and 1977 is rationed variation uangzhou. wood and gradually onlv after the most e in which .rols could oal use in than 20 :ars had a ;ed to pe- Ver-v few kerosene TABLE 3. Exposure to smoking among lung cancer cases and controls, Guangzhou, People's Republic of China, 1983-1984 ~ Exposure No of No of EOR' 95°° Ct' cases controls Actrve smoking (cigarette equivalents smoked per day) among men Never smokert 12 44 1.0 1-19 21 93 1.2 0 43-3 5 20-29 97 66 7.1 2.6-19.5 ~30 94 21 21.4 7.1-64 0 x 2 for trend = 99.6 p < 0.001 Active smoking (cigarette equivalents smoked per day) among women Never smokert 38 69 1.0 1-9 8 10 1.8 0.57-5.9 10-19 16 9 3.5 1.2-9.8 a20 30 4 17.9 4 0-80.6 x2 for trend = 28.0 P < 0.001 Passive smoking among nonsmoking women (cigarette equiva- lents smoked per day by husband)$ Not exposedt 13 32 1.0 1-19 6 21 0.7 0.23-2.2 ?20 19 16 2.9 1.2-7.3 x= for trend = 4.5 p = 0.034 ` EOR, matched logistic exposure odds ratio. adjusted for education, occupation, and living area, comparing never smokers to present and former smokers combined; CI, confidence interval. t Referent. # Unmatdhed method was used. for cooking. In the kitchens of more than 60 percent of families, there was no chimne} or other apparatus for extracting fumes. No significant case-control differences were as- sociated with the above variables. -- Information on the use of cooking oil was not formallv included in our study. In the People's Republic of China, cooking oil is rationed by the government-controlled food and oil company, and in Guangzhou. the main cooking oil used is peanut oil (for a short time it was bean oil). Rapeseed oil was not widely available, and we did not expect to find any differences in the types of oil being used, because all Guangzhou residents are dependent on the same government sup- ply. Analysis of the effect of ventilation con- ditions on lung cancer risk was conducted for housing at the time of diagnosis and interview, as well as housing where subjects had lived the longest: finally, data were sum- marized over all residences. The results of these analyses were similar (data not shown): therefore, this paper presents only the results of the analysis for current ventilation con- ditions. In addition, the proportions of cases and controls who had moved during the past 10 or 20 years did not differ significantly. and duration of residence in the current housing was similar for cases and controls. For most subjects. the current residence was also the longest residence. Table 5 shows that after adjustment for education, occupation, occupational ex- posure, pulmonary tuberculosis history, chronic bronchitis history, family cancer his- tory, amount of smoking per day, and living area, as well as passive smoking (for women only), several variables pertaining to venti- lation conditions were strongly associated with lung cancer risk. There was increased risk associated with having a window or door opening from the kitchen directly into the living area or bedroom, and for cooking in the living area or bedroom. For cooking in the living area or bedroom, the exposure odds ratio was 2.4 (95 percent CI 1.4-4.2) for men and 5.9 (95 percent CI 2.1-16.0) for women. Having windows or doors that opened in different directions so that indoor air could circulate also significantly influ- enced the risk of lung cancm The relative risk for lung cancer tended to decrease with increasing size of ventilation openings in living areas and kitchens. For the best ven- tilated living area as compared with the least ventilated. the e.xposure odds ratio for lung cancer was reduced to only 0.14 (95 percent CI 0.04-0.5 1) for men and 0.02 (95 percent CI 0.00-0.? 1) for women. The exposure odds ratios for kitchen ventilation were 0. 15 (95 percent CI 0.05-0.44) for men and 0.06 (95 percent Cl 0.01-0.32) for women, re- spectively. The differences were statistically significant. A similar trend was found for the ceiling height throughout the apartment. but no clear trend was seen for the floor on 2501196991

" 150 ' l.iu et al. TABLE 4. Cooking practices of lung cancer cases and controls, Guangzhou, People's Republic of China, 1983-1984 Men Women Cooking practice No. of cases No. of controls EOR,* EOR2* 95% CI* No. of No. of cases controls EOR, EORz 95% Ct Frequency of cooking at home Rarelyt 107 100 1.0 1.0 4 5 1.0 Occasionally 45 63 0.65 0.52 0.25-1.1 8 8 1.2 1.2 0.17-9.2 Frequently 72 61 1.1 1.1 0.69-1.9 80 79 1.3 1.1 0.19-6.1 Having a chimney in kitchen (years) No chimneyt 160 147 1.0 1.0 56 54 1.0 1.0 1-9 33 37 0.80 0.55 0.22-1.6 16 10 1.7 3.6 0.72-17.5 >10 31 40 0.70 0.80 0.34-1.9 20 28 0.77 1.1 0.40-3.0 Cooking fuel Coalt 200 193 1.0 1.0 81 79 1.0 1.0 Gas 14 22 0.59 0.48 0.15-1.6 8 9 0.90 0.90 0.24-3.3 Wood 8 9 0.79 0.57 0.11-3.0 3 4 0.67 0.67 0.04-11.7 Other 2 0 0 0 No. of ineals prepared at home per day 0-1 t 18 26 1.0 1.0 2 3 1.0 1.0 2 26 33 1.2 0.83 0.27-2.6 7 12 0.67 0.48 0.03-8.8 3 180 165 1.7 1.3 0.50-3.3 83 77 1.5 1.5 0.12-17.7 * EOR,, matched exposure odds ratio; EOR2, matched logistic exposure odds ratio, adjusted for education, occupation, occupational exposure, history of tuberculosis, chronic bronchitis, family history of cancer, smoking, and living area; Cl, confidence interval; EOR3, matched logistic exposure odds ratio, adjusted for passive smoking in addition to all of the variables listed above. t Referent. which the subject lived, with the exception of a higher risk for people living on the ground floor as opposed to a higher floor. When we analyzed the effect of floor by district of residence and by sex, we found the higher risk for persons living on the ground floor in three out of four districts for women and in two out four districts for men (data not shown). DISCUSSION Usually, hospital controls are selected from the same hospitals as the cases, but in this study some of the controls were not chosen from the same hospital as their matched cases because two of the hospitals that were sources of cases were deliberatelv excluded as sources of controls. We did this to avoid selection of subjects with diseases that could potentially be linked to smoking and/or air pollution. To reduce potential bias in the control selection procedure, we matched cases and controls on district of residence, thereby controlling for the referral pattern of patients. Most importantly, this matching also controlled for atmospheric air pollution. Results of environmental surveil- lance were only available at the district level, as were lung cancer mortality rates. One district, Liwan, has the highest levels for all indexes of air pollution (falling dust, benzo(a)pyrene, total suspended particulate matter, sulfur dioxide, nitrogen oxide, and _carbon monoxide), whereas_the other three districts do not differ from one another ap- preciably (33). The highest age-standardized (world standard population) lung cancer mortality rates for women are recorded in Liwan at ??.2 deaths per 100,000 woman- years, compared with the lowest rate for the district of Dongshan at 18.3. For men, the highest mortality rate is in Yuexiu at 51.8, versus the lowest rate in Dongshan at 40.9. All of the pairs of cases and controls lived in the same residential district, in an area of about 10 km'. They were exposed to ap- proximately similar levels of outdoor air pollution, although variations may have oc- curred within districts. No data were avail- 2501196992

Indoor Air Pollution and Lung Cancer 151 of China, ' 95% CI 0.17-9.2 0.19-6.1 0.72-17.5 0.40-3.0 0.24-3.3 0.04-11.7 0 03-8.8 0.12-17.7 occupation, :1, confidence ;ted above. ntly. this pheric air .1 surveil- rict level, ,tes. One ,Is for all lg dust, irticulate .ide. and ier three )ther ap- dardized cancer lyded in ~%,oman- e for the nen. the at 5 1.8, at 40.9. As lived i area of I to ap- loor air lave oc- •e avail- TABLE 5. Ventilation conditions in the homes of lung cancer cases and controls, Guangzhou, People's Aepublic of China, 1983-1984 Men Women Ventdation factor No. of No. of EOR,' EORz' 95% Cl' No. of No. of EOR, EOR,' 95% Cl cases controls cases controls $eparate kitchen Yest 72 113 1.0 1.0 29 52 1.0 1.0 No 152 111 2.0 2.4 1.4-4.2 63 40 3.1 5_9 2.1-16.0 C,Ood air circulation Yest 90 120 1.0 1.0 38 60 1.0 1.0 No 134 104 1.7 2.1 1.2-3.8 54 32 3.0 3.6 1.4-9.3 Size of ventilation openings in living area (m2 per per- son) 0.0-0.4t 7 8 .0 .0 6 6 .0 1.0 0.5-0.9 86 69 0.53 0.39 0.14-1.1 36 23 0.69 0.36 0.09-1.5 1.0-1.9 38 53 0.33 0.30 0.10-0.91 22 24 0.40 0.25 0.05-1.1 2.0-3.9 22 30 0.33 0.24 0.06-0.90 9 13 0.24 0.14 0.02-0.89 >4.0 31 24 0.28 0.14 0.04-0.51 9 26 0.11 0.02 0.00-0.21 X' for trend 14.5 (p < 0.001) 18.0(p < 0.001) Size of ventilation openings in kitchen (m2 per family) 0.0-0.4t 79 41 1.0 1.0 22 8 1 0 1.0 0.5-0.9 58 52 0.55 0.77 0.36-1.7 27 25 0.29 0.11 0.02-0.60 1.0-1.4 48 59 0.38 0.23 0.10-0.56 24 22 0.31 0.13 0.02-0.74 1.5-1.9 19 31 0.28 0.49 0.16-1.5 7 13 0.15 0.09 0.01-0.63 _2.0 20 41 0.20 0.15 0.05-0.44 12 24 0.16 0.06 0.01-0.32 x2 for trend 25.7 (p < 0.001) 10.3 (P < 0.001) Height of room (m) Q.8t 61 45 1.0 1.0 22 12 1.0 1.0 2.8-3.1 72 71 0.77 0.91 0.41-2.0 30 26 0.62 0.54 0.09-1.3 _3.2 91 108 0.65 0.64 0.31-1.3 40 54 0.39 023 0.06-0.84 xZ for trend 3.5(p=0.06) 5.5 (p = 0.02) Floor of apartment Groundt 106 92 1.0 1.0 50 32 1.0 1.0 1 77 78 0.85 0.79 0.40-1.5 23 34 0.30 0.12 0.03-0.46 2-3 27 34 0.66 0.88 0.36-2.1 14 22 0.29 0.11 0.02-0.54 >4 14 20 0.59 0.62 0.20-1.9 5 4 0.56 0.72 0.07-7.01 X2 for trend 3.0 (p = 0.08) 5.0 (p = 0.02) * EOR,, matched exposure odds ratio: EOR2, matched logistic exposure odds ratio, adjusted for education, occupation, occupational exposure, history of tuberculosis, chronic bronchitis, family history of cancer, smoking, and living area: Cl, confidence interval: EOR3, matched logistic exposure odds ratio, adjusted for passive smoking in addition to all of the variabres listed above. t Referent. able on a scale smaller than the district. We knew that separation of the effects of out- door air pollution from those of indoor air pollution might be difficult. This led us to match on residence as a proxy for matching on outdoor air pollution level. In addition, our results, demonstrating a clear reduction in risk of lung cancer for living in a house with large openings onto the outside, indi- cate that outdoor air pollution is unlikely to explain or confound the association found between lung cancer risk and indoor sources of air pollution. Our results showed that comparability be- tween cases and controls with regard to basic demographic variables was good, suggesting that these demographic variables might not have a major confounding effect. Further- more, education and occupation, which were considered good representative vari- 2501196993

I 152 Liu et al. ables of social class, were also controlled for in the analysis. Since the number of cases in each histo- logic category was limited, a separate analy- sis could not be carried out for the associa- tion of indoor air pollution with specific histologic types of lung cancer. Some diag- nostic error mav also have occurred. How- ever. undifferential misclassification of cases and controls usually leads only to a bias toward the null and cannot explain the ob- served results. It is possible that some social class differ- ences between cases and controls could ac- count for part of the difference in ventilation conditions. The finding of a higher risk of lung cancer among subjects living at street level could be explained by a higher concen- tration of both indoor and outdoor air pol- lutants on the ground floor as opposed to higher floors, where natural ventilation is usually better. Social class, which is closely linked with housing conditions in China, was nevertheless more strongly associated with the total surface of the living area than was the specific measure of ventilation. Al- though cases had smaller living areas than controls, the difference was not substantial. After adjustment for education, occupation, and living area, the relation between venti- lation conditions and lung cancer risk re- mained. This means that any bias linked to social status cannot be a major confounder of the observed association. Recall bias can affect most retrospective studies; however, in this study, the size of ventilation openings was objectively measured, so the association bctwLen ventilation conditions and lung cancer risk cannot be an artifact of recall bias. Smoking was the major cause of lung cancer in both sex groups, and a clear dose- response relation was observed between the amount of tobacco smoked and lung cancer risk. High smoking rates were observed in both male and female groups. These rates ,were higher than those obtained from a case- control study of lung cancer carried out among Shanghai Chinese women (11) but similar to rates from other studies (6, 10, 18. 34). The subjects of this study belonged to an older population and had relatively low social status (a low educational level and the major occupation of worker). These two fac- tors are known to be associated with high smoking rates (35). Furthermore, the defi- nition of a smoker in this study included both ever and current smokers. For instance, if we had counted only current smokers, the smoking rate would have been reduced to 14 percent in female controls. Passive smok- ing may also account for some excess risk, although increased risk was only observed in the women living with husbands who smoked heavily. No effect was seen for women married to light smokers. This may be explained by the reduced sample size and by the imprecise quantification of passive smoking. The results of other studies in Chinese women have suggested that passive smoking contributes to a slight increase in lung cancer risk (11. 18). Several reports of environmental moni- toring showed that the concentrations of nitrogen oxide, sulfur dioxide, benzo(a)- pyrene, and total suspended particulate mat- ter in Guangzhou were higher in dwellings than in the outdoor atmosphere and varied according to time of day and season (36). Three peaks of pollutant concentrations dur- ing the day were correlated with cooking activities. Results of studies also showed that there were higher concentrations of sus- pended dust and suspended benzo(a)pyrene in the rooms and urinary benzo(a)pyrene in housewives in households where coal was used as a cooking fuel compared with house- holds where petroleum gas was used (36, 37). Results of a study conducted in the north of China showed that use of coal for heating elevated the risk of lung cancer in comparison with use of gas. Cooking in the bedroom was also related to an excess risk (34). High mortality from female lung can- cer in Xuan Wei County. Yunnan Province, was also associated with the combustion of smoky coal at home (38). These results in- dicated that home cooking practices were a major source of indoor air pollutants and that coal produced more severe air pollution than other kinds of domestic fuel. Evidence also comes from the evaluation 2501196994

Indoor Air Pollution and Lung Cancer 153 ativelv low vel and the ~se two fac- with high the defi- ~ included )r instance, iokers, the reduced to 3ive smok- xcess risk, observed ands who seen for This may le size and .)f passive studies in at passi ve icrease in tal moni- ations of benzo(a)- date mat- dwellings .td varied son (36). ions dur- cooki ng ,wed that of sus- a)pyrene )yrene in :oal was h house- sed (36, 1 in the coal for incer in .g in the :ess risk ,ng can- rovince, stion of :ults in- were a -tts and Alution luation of occupational exposure to coal burning. $teel, gas. and coke oven workers have an elev ated risk of lung cancer (39-45). The results of animal experiments have demon- strated that some components of coal fumes are carcinogenic or mutagenic (38, 46, 47). Since coal use, frequent home cooking, and lack of an apparatus for extracting fumes are universal in Guangzhou, it was difficult to find a significant difference between any population groups. However, this indicates that severe indoor air pollution exists for most families in Guangzhou, where people live in comparatively overcrowded condi- tions with poor ventilation. Better ventila- tion of houses could thus play a key role in improvement of the indoor microenviron- ment, and dissimilar ventilation conditions could be responsible for different exposure levels of lung cancer cases and controls. During the study period, there was in most houses no artificial ventilation such as air conditioning, so the indoor microenviron- mental conditions depended mainly on nat- ural ventilation. The area of ventilation (as defined by the area of openings to the out- side) was a good representative measure of ventilation conditions. This is in agreement with other studies on indoor air pollution showing that the concentrations of pollu- tants are greatly affected by ventilation (19, 34). 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