Chinese Food Cooking and Lung Cancer in Women Nonsmokers

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1 American Jurnal f Epidemilgy Cpyright 2000 by The Jhns Hpkins University Schl f Hygiene and Public Health All rights reserved Vl.151,. 2 Printed In U.S.A. Chinese Fd Cking and Lung Cancer in Wmen nsmkers Ying-Chin K, 1-2 Li Shu-Chuan Cheng, 3 Chien-Hung Lee, u Jhi-Jhu Huang, 4 Ming-Shyan Huang, 4 Eing-Lng Ka, 5 Hwei-Zu Wang, 6 and Hsiang-Ju Lin 7 Cigarette smking cannt fully explain the epidemilgic characteristics f lung cancer in Taiwanese wmen, wh smke rarely but have lung cancer relatively ften. In a previus study, the authrs suspected that expsure t fumes frm cking ils was an imprtant risk factr fr lung cancer in Taiwanese wmen nnsmkers in the Republic f China. In a new case-cntrl study cnducted in , they further explred the assciatin f il fumes with lung cancer in wmen. Tw sets f were used cncurrently. The subjects were 131 nnsmking incident cases with newly diagnsed and histlgically cnfirmed primary carcinma f the lung, 252 hspital hspitalized fr causes unrelated t diseases f smking, and 262 cmmunity ; all were wmen nnsmkers matched by age and date f interview. Details n cking cnditins and habits were cllected, in additin t ther epidemilgic data. Lung cancer risk increased with the number f meals per day t abut threefld fr wmen wh cked these meals each day. The risk was als greater if wmen usually waited until fumes were emitted frm the cking il befre they began cking (adjusted dds ratis = ) and if they did nt use a fume extractr (adjusted dds ratis = ). These results suggest that a prprtin f lung cancer may be attributable t the habit f waiting until the cking il has been heated t a high temperature befre cking the fd. Am J Epidemil 2000;151: lung neplasms; mutagens; ils; risk factrs; temperature; wmen Lung cancer has been the leading cause f cancer death amng wmen in Taiwan, Republic f China, since Althugh cigarette smking is cnsidered the mst imprtant cause f lung cancer, it cannt fully explain the epidemilgic characteristics f lung cancer in Taiwanese wmen (1), wh smke rarely but have lung cancer relatively ften, as d Chinese wmen in the United States (2), Australia (3), Hng Kng (4), Singapre (5), Malaysia (6), Japan (7), and sme cities n mainland China (8). The prevalence f cigarette smking amng adults in Taiwan is percent fr men but nly 3-4 percent fr wmen. The Received fr publicatin vember 3, 1998, and accepted fr publicatin April 14, Abbreviatins: Cl, cnfidence interval; OR, dds rati. 1 1nstitute f Medicine, Schl f Medicine, Kahsiung Medical University, Kahsiung, Taiwan, Republic f China. 2 Schl f Public Health, Kahsiung Medical University, Kahsiung, Taiwan, Republic f China. 3 Center fr Health Sciences, SRI Internatinal, Menl Park, CA. 4 Department f Internal Medicine, Kahsiung Medical University Hspital, Kahsiung, Taiwan, Republic f China. 5 Department f Surgery Medicine, Kahsiung Medical University Hspital, Kahsiung, Taiwan, Republic f China. 6 Department f Ophthalmlgy, Kahsiung Medical University Hspital, Kahsiung, Taiwan, Republic f China. 7 Department f Pathlgy, Kahsiung Medical University Hspital, Kahsiung, Taiwan, Republic f China. Reprint requests t Dr. Ying-Chin K, Schl f Public Health, Kahsiung Medical University,. 100 Shih-Chuan 1st Rad, Kahsiung, Taiwan, Republic f China. reprted rates f smking fr Chinese wmen with lung cancer are lwer (frm 22 percent in Hawaii t 56 percent in Hng Kng) than thse fr all wmen with lung cancer in Eurpe and America (70-90 percent) (9). hi Taiwan, the rate f smking is even lwer; nly 10 percent f female lung cancer patients smke, whereas 86 percent f male lung cancer patients have a histry f smking. What causes wmen nnsmkers in Taiwan t be affected needs further investigatin. In additin t smking, ccupatinal expsure t carcingens (10-13) is anther well-established risk factr fr lung cancer, but it is limited t specific grups. Fr female lung cancer patients in general, varius ptential factrs have been reprted t be assciated with lung cancer, including envirnmental tbacc smke (14), ambient air pllutants (15, 16), diet (17-20), cking fuels (21, 22), indr air pllutin (23), and a family histry f lung cancer (24, 25). Chinese cking invlves frying ingredients in il, which prduces ample il fumes t which the ck is expsed. In ur previus case-cntrl study (1), we suspected that expsure t fumes emitted frm cking ils, when nt reduced by an extractr such as a fume hd, appeared t be an imprtant risk factr fr lung cancer in Taiwanese wmen nnsmkers. The purpse f the present study was t further explre the rle f 011 fumes fr wmen lung cancer patients wh ck. 140

2 Fd Cking and Lung Cancer 141 We used tw sets f (hspital and cmmunity ) cncurrently t increase sample size and reduce hspital selectin bias. MATERIALS AND METHODS Study samples This study used a case-cntrl design. Subjects were residents f the greater Kahsiung area f Taiwan, which includes a city and sme suburban and rural cmmunities. Each case was matched by age and date f interview t tw types f (hspital and cmmunity ). The cases and hspital were drawn frm Kahsiung Medical University Hspital, a leading teaching hspital in suthern Taiwan. The cases were nnsmking incident patients with newly diagnsed and histlgically cnfirmed primary carcinma f the lung (Internatinal Classificatin f Diseases, Ninth Revisin cde 162). A ttal f 148 eligible lung cancer cases were identified between 1993 and Excluded frm this analysis were thse wh had died (n = 6), thse wh were t sick (n = 5), and thse wh refused t participate (n = 6), leaving 131 cases fr analysis. Amng these cases, 26 (19.8 percent) had squamus cell carcinma, 82 (62.6 percent) had adencarcinma, 18 (13.7 percent) had small cell carcinma, 3 (2.3 percent) had large cell carcinma, and 2 (1.5 percent) had unclassified carcinma. The hspital were new female patients hspitalized fr causes unrelated t diseases f smking. Amng them, 77 percent had eye prblems (cataract r glaucma) and 23 percent had bne fractures. These were drawn frm the same gegraphic areas as the cases, were selected within 3 weeks after the case had been identified, and were matched t cases n age (within 2 years) and smking status. A ttal f 281 hspital were available, and 252 agreed t participate in the study. The cmmunity were selected randmly frm a cmputerized ppulatin database f the greater Kahsiung area. We first chse 18 cmmunities frm a ttal f 82. We then selected 641 husehlds in these cmmunities. Infrmatin regarding smking status was btained and the ages f the selected subjects were verified thrugh telephne interviews. A ttal f 1,240 wmen wh were lder than age 40 years and were lifetime nnsmkers were eligible t be. Once a case was identified, tw cmmunity matched by age (within 2 years) were selected n the basis f their sequence n the list. If the selected wman refused t participate in the study, the next eligible wman n the list was chsen until tw healthy had been recruited. Thirtytw healthy wmen refused t r culd nt participate Am J Epidemil Vl. 151,. 2, 2000 in the study. The reasns given were that they were t busy fr the interview, were ut f twn, r were mving ut f the study area and culd nt be lcated. A ttal f 262 age-matched cmmunity participated in the study. Data specificatin Tw trained interviewers cnducted persnal interviews t cllect epidemilgic data. A structured questinnaire had been develped t btain infrmatin n demgraphic characteristics, sciecnmic status, smking histry, passive smke expsure, histry f lung diseases, ccupatin, dietary habits, lifetime residence, general air pllutin inside the hme, and ventilatin cnditins as well as cking habits. Details f the data specificatin are described elsewhere (1). A nnsmker was defined as a wman wh had never smked ne cigarette during her lifetime. Subjects wh lived r wrked with a smker during their childhd and adulthd, such as a parent, husband, chabitant, r cwrker, were cnsidered passive smkers. A detailed smking histry fr smkers was cllected, including the year in which smking started, the year in which smking stpped (if applicable), and hw many cigarettes they had smked during their lifetime. The number f smker-years, calculated as the number f years expsed t smkers multiplied by the number f smkers t whm the subject had been expsed, was used as the indicatr f passive smking. Chrnic brnchitis, emphysema, asthma, and tuberculsis were included in the histry f lung diseases. The ccupatinal histry prtin f the questinnaire listed all types f jbs divided int five categries: administratin, hazardus industry, farmer, husewife, and chef. Subjects were asked t list all jbs they had held fr at least 1 year. Hazardus industry included irn, petrleum, chemical, and cement prductin facilities; chefs usually have restaurants and wrk in their hmes, accrding t Taiwanese custm. Infrmatin n daily dietary habits was cllected regarding 12 fd items, and subjects were asked abut the frequency and quantity f cnsumptin f meat, vegetables, fruit, smked fd, and pickles, fr example. The place in which the subject had resided fr the lngest perid f time was cnsidered her main residence (average duratin, 46.3 (standard deviatin, 17.2) years fr cases and 45.2 (standard deviatin, 18.0) years fr ). If this place was within 1 km f a majr industrial site, the subject was classified as living adjacent t an industrial district. Air pllutin factrs inside the hme were als assessed. Infrmatin included the types f incense used (e.g., Taiwanese yellw and black incense) and the duratin and frequency f burning Chinese incense and msquit cils.

3 142 Ketal. Furthermre, the interviewers asked each husewife wh had t ck fr her family abut the types f cking fuel and cking ils she used, her preferred cking methd, the number f windws in the kitchen, the sizes f penings t the utside, and ventilatin cnditins (a dichtmus variable) and the use f a fume extractr in the hme kitchen. Because stir frying, frying, and deep frying are three types f cking techniques that invlve frying fd in il and are usually used t prepare Chinese fd, we als measured hw frequently husewives used each technique. We als asked abut their regular cking habits, such as whether they waited fr fumes t be emitted frm cking ils befre they began t ck. Accrding t the cncepts f traditinal Chinese cking, quick frying in ils that have been heated t reach high temperatures keeps fd as fresh as pssible. Age at which cking started was determined t be a husewife's age when she started t ck daily. Statistical analysis In this case-cntrl study, dds ratis and their 95 percent cnfidence intervals were used as estimates f relative risk. Univariate cnditinal lgistic regressin was applied t test the ptential risk factrs mentined abve. The significant risk factrs identified as a result f this univariate analysis were ccupatin, previus lung disease, and passive smking (table 1). All multivariate lgistic regressin mdels were adjusted fr these variables and sciecnmic status, which is prbably related t the use f a fume extractr in the kitchen. RESULTS All demgraphic data fr the cases and the tw grups f are shwn in table 1. Age, residential area, ethnicity, religin, educatin, and sciecnmic status f the cases were well matched t bth grups f. There were mre chefs amng the cases than the (6.9 percent f cases versus 1.2 and 3.1 percent f hspital and cmmunity, respectively). Mre cases als had preexisting lung disease (18.3 percent f cases versus 6.8 and 8.4 percent f, respectively) and expsure t passive smking (78.6 percent f cases had ever been expsed t passive smking versus 65.9 and 59.5 percent f, respectively). Almst all subjects cked daily, which is cnsistent with the practice f traditinal Chinese wmen (table 2). The dds rati fr cking was nt significantly related t the develpment f lung cancer. The age at which cking started and the number f years spent cking at hme did nt differ between the cases and TABLE 1. Distributins f demgraphic and cnfunding factrs (%t) amng Taiwanese wmen nnsmkers, Republic f China, Age (years) < >70 Factr Residential area Urban Suburban Rural Ethnicity Fuklenese Mainlander Other Religin Buddhism Taism Flk Other Educatin (years) ne 1-9 >9 Sciecnmic status Lw Median High Occupatin* Administratin Hazardus industry Farmer Husewife Chef Previus lung disease* F"asstve smking (smkeryears)* ^ >60 CjtKAR OUEWO (n= 131) Hspital (n = 252) Cmmunity (n = 262) * p < 0.05 fr bth cmparisns with hspital and cmmunity. t Sme percentages d nt ttal 100 because f runding. either grup f. Hwever, number f meals per day was significantly assciated with lung cancer and reflected a dse-respnse trend: wmen wh cked three meals per day had an almst threefld increased risk f lung cancer (dds rati (OR) = 2.8,95 percent cnfidence interval (Cl): 1.2, 6.3 cmpared Am J Epidemil Vl. 151,. 2, 2000

4 Fd Cking and Lung Cancer 143 TABLE 2. Adjusted dds ratis (OR) and 95% cnfidence intervals (Cl) f lung cancer assciated with cking and ventilatin cnditins In the hme kitchens f Taiwanese wmen nnsmkers, Republic f China, Daily cking Age cking started (years) >20 20 Years spent cking at hme >40 Meals per day Windws in kitchen <2 Size f penings t the utside Small r mderate Large Ventilatin In the kitchen Pr Gd. f cases with hspital ; OR = 3.4, 95 percent Cl: 1.6, 7.0 cmpared with cmmunity ). Cking tw meals per day was assciated with a significantly higher risk f lung cancer when cases were cmpared with cmmunity (OR = 3.1, 95 percent Cl: 1.6, 6.2), but the risk was nly marginally higher when they were cmpared with hspital (OR = 1.9, 95 percent Cl: 0.9, 4.0). In additin, as shwn in table 2, there was n difference in the ventilatin cnditins in the hme kitchens f cases and. Because a large prprtin f husewives cked less frequently after age 40 years (when their daughters r daughters-in-law tk charge f the cking) and sme started t ck befre age 20 years, these age cutpints (i.e., 20, 40 years) were used t analyze the rle f a fume extractr in the kitchen. As shwn in table 3, subjects wh cked when they were years f age (the main ages fr cking amng Taiwanese husewives) withut using a fume extractr had a significantly higher risk f lung cancer than the hspital (OR = 5.4, 95 percent Cl: 2.7, 10.8) and the cmmunity (OR = 2.2, 95 percent Cl: 1.3, 3.8). The assciatin f lung cancer with the use f a fume extractr befre age 20 and after age 40 Hspital OR (95% Cl) 1.9(0.2, 18.1) (0.6, 1.7) (0.5, 1.8) 1.2(0.4, 3.4) 1.9(0.9,4.0) 2.8(1.2,6.3) 0.9(0.5, 1.3) 1.1 (0.6,2.0) 0.9(0.6, 1.4) Cmmunity OR (95% Cl) 5.9 (0.7, 53.6) 1.5 (0.9, 2.4) 1.3(0.6,2.6) (0.4,2.9) 3.1 (1.6, 6.2) 3.4(1.6,7.0) 1.3(0.8,2.1) 0.9(0.5, 1.5) 0.9(0.6, 1.4) years was nt significant, but a 1.3-fld significant increased risk f lung cancer was fund in cmparisn with hspital. We further examined hw wmen habitually cked the fd. The purpse was t investigate whether the risk f lung cancer was assciated with the temperature f the cking il when the wmen placed the fd int the frying pan. As shwn in table 4, eye irritatin when cking was significantly assciated with lung cancer (OR = 2.2, 95 percent Cl: 1.3, 3.8 cmpared with hspital ; OR = 2.1, 95 percent Cl: 1.3, 3.5 cmpared with cmmunity ), indicating that sme hazardus, irritating substance frm the cking il may spread t the air during cking. Subjects wh were frequently expsed t cking fumes had a higher risk f lung cancer (OR = 1.7, 95 percent Cl:, 2.9 cmpared with hspital ; OR = 2.5, 95 percent Cl: 1.4, 4.3 cmpared with cmmunity ). Furthermre, subjects wh usually waited until fumes were emitted frm the il and then stir fried, fried, and deep fried had a significantly higher risk f lung cancer, althugh, when cmpared with cmmunity, the significance was nly marginal fr the deepfrying prcedure (table 4). These significantly higher Am J Epidemil Vl. 151,. 2, 2000

5 144 Ketal. E CO c 1 CO c c 8 _3 "5 I 8 a O 57 #1 «ii UJ A m 3. :" i i p C\J ^ eg in S q T^ C\j r-~ in in > in LU risks were als bserved fr each cking methd, even when the frequency f cking was taken int accunt (data nt shwn). We als tested whether there was an interactin between cking habits and use f fume extractrs (table 5). We fund that wmen wh did nt use a fume extractr and waited fr the cking il t reach a high temperature befre beginning t ck (adding the fd when the il fumes were emitted cnsistently) had cnsistently higher risks f lung cancer (OR = ) than either hspital r cmmunity. Subjects wh did nt use a fume extractr and did nt wait until the il was ht befre they cked the fd als had significantly higher risks f lung cancer in cmparisn with hspital (OR = ); the risk was higher but nt statistically significant when cmpared with cmmunity. The risk f lung cancer was marginally higher fr subjects wh cked when the pan and cking il were ht and did use a fume extractr, indicating that the fumes released int the air frm evaprating, high-temperature il culd nt be cleaned cmpletely by the fume extractr. In additin, n interactin was fund between expsure t cking fumes and passive smking. DISCUSSION This study presents evidence that cking habits are assciated with lung cancer in Taiwanese wmen nnsmkers. As shwn in this and ur earlier study (1), wmen wh d nt use fume extractrs during cking are at high risk f develping lung cancer. Furthermre, wmen wh wait until the il has reached a high temperature befre cking the fd (stir frying, frying, and deep frying) and d nt use a fume extractr have a cnsistently higher risk f lung cancer when cmpared with bth hspital and cmmunity. We used tw sets f cncurrently t explre the study gals. The purpse f such a design is t reduce ptential bias frm the use f either the hspital-based r cmmunity-based apprach and t secure the study findings, especially when results frm tw grups f are cnsistent. Our results frm bth cmparisns were quite cnsistent, althugh the estimates f dds ratis were smewhat different. Because subjects did nt knw the hypthesis f the present study, recall bias, if existent, shuld have been Limited and shuld nt have influenced ur cnclusins. All patients were newly diagnsed cases, and were matched by date f interview; therefre, the survival effect was nt very likely. Althugh a small prprtin f ptential subjects were excluded because they had died, were t sick, r refused t participate, these subjects were nt related t the mea- Am J Epidemil Vl. 151,. 2, 2000

6 Fd Cking and Lung Cancer 145 TABLE 4. Adjusted dds ratis (OR) and 95% cnfidence intervals (Cl) f lung cancer assciated with the cking habits f Taiwanese wmen nnsmkers, Republic f China, f cases. Hspital OR (95% Cl) Cmmunity OR (95% Cl) Eye irritatin when cking Rarely Frequently (1.3, 3.8) (1.3,3.5) Smkiness when cking Rarely Frequently (,2.9) (1.4,4.3) Stir frying after fumes emitted (1.1,3.7) (1.4,4.2) Frying after fumes emitted (1.1,3.8) (1.4,4.9) Deep frying after fumes emitted (1.3,3.5) (0.9, 2.4) surement f expsures f interest and hence shuld nt have substantially biased ur results. The assciatin f cking habits, fume extractr use, and lung cancer is bilgically plausible because the substances emitted frm il fumes have prven t be mutagenic; we identified ply cyclic armatic hydrcarbn carcingens in three different cmmercial cking ils frequently used in Taiwan (26). It als has been reprted that tw f these hydrcarbns (benzene and frmaldehyde) were identified in rapeseed il fumes (27, 28), althugh rapeseed il was never used in Taiwan. Restaurant cks nt nly in Asian cuntries (29) but als in western cuntries (30-32) als have been reprted t have higher risks f lung cancer. One study snwed that this ccupatin was assciated with lung cancer, the cases included mre prfessinal chefs than either grup f. We have suggested that a prprtin f lung cancer may be attributable t the carcingens emitted frm the fumes f high-temperature cking il. These fumes are generated nt nly in Asian cuntries but als in western cuntries when husewives r cks fry fd and d nt use efficient fume extractrs. Thse wmen wh used a fume extractr but waited t ck the fd until the il was very ht als had a higher risk f lung cancer, indicating that the fume TABLE 5. Interactin effects f lung cancer assciated with cking habits and use f a fume extractr In the kitchens f Taiwanese wmen nnsmkers, Republic f China, Using fume extractr t using fume extractr Using fume extractr t using fume extractr Cking habit. f cases/ hspital OR' (95% Cl*). f cases/ hspital OR (95% Cl). f cases/ cmmunity OR (95% Cl). f cases/ cmmunity OR (95% Cl) Stir frying after fumes emitted 14/70 71/ (1.1,4.1) 8/9 37/22 5.9(1.5,23.3) 12.2(4.5,33.1) 14/77 71/ (1.3, 4.9) 8/10 37/35 2.8(0.8, 10.0) 5.0(2.2, 1) Frying after fumes emitted 12/61 73/ (0.9,3.7) 5/7 40/ (0.8, 16.2) 10.5(3.9,28.4) 12/68 73/ (1.3,5.5) 5/5 40/ (0.8, 13.2) 5.3 (2.2, 12.3) Deep frying after fumes emitted 22/103 63/ (1.2,3.9) 9/10 36/21 7.6(2.1,26.9) 9.5 (3.9, 23.3) 22/77 63/ (0.9,3.1) 9/9 36/ (0.9, 8.5) 3.2(1.4,7.3) * OR, dds rati; Cl, cnfidence interval. Am J Epidemil Vl. 151,. 2, 2000

7 146 Ketal. extractr did nt cmpletely clean the hazardus substance frm the air in the kitchen. We have hypthesized that the fume extractr might have been psitined t high abve the il surface t capture the fumes cmpletely. This hypthesis was recently tested in ur study grup (33); we fund that fume samples were mutagenic when the fume extractr was lcated 70 cm abve the il surface, whereas the samples were nt mutagenic r weakly mutagenic when the distance was 50 cm r less. Interestingly, wmen wh did nt wait t ck until the il was very ht and did nt use a fume extractr als had a marginally higher risk. It may be that, althugh there were n visible fumes frm the cking il, sme invisible substance was emitted and was nt cleaned by the fume extractr. Over 96 percent f the wmen nnsmkers wh participated in the present study stated that they regularly cked the family meals. Epidemilgic studies have shwn that lung cancer risk increases with the number f meals cked per day (22, 23). These results prvide the first clue that factrs related t cking are assciated with lung cancer. In the present study, we fund that wmen wh cked withut using a fume extractr and usually waited until fumes were emitted frm the il develped cancer because f lng-term expsure t cking il fumes. Therefre, we suggest that sme prprtin f lung cancer in wmen shuld be preventable. Fr example, changing cking habits r cking at lwer temperatures and installing a welldesigned fume extractr in the hme kitchen shuld be encuraged. Althugh mst western wmen d nt ck at hme as ften as Chinese wmen d, the pssibility f a cumulative txic effect cannt be ignred. Since the use f fume extractrs is nw very ppular in Taiwan, ne culd questin why mrtality frm lung cancer remains steady and has nt been reduced significantly in cmparisn with earlier decades. Pssible explanatins are that the fume extractrs are nt psitined apprpriately, as described abve, and that ventilatin is nt efficient because mdern husing is small; mst Taiwanese peple live in small apartments in high-rises, especially in big cities such as Kahsiung. Anther imprtant explanatin is that mst mdem Taiwanese wmen, like westerners, use vegetable il rather than lard il because it is lw in chlesterl. In Taiwan, the market fr vegetable il increased frm less than 50 percent t 85 percent between 1950 and Hwever, vegetable il cntaining unsaturated fatty acids was fund t be mre unstable than lard il at higher temperatures and culd emit benzapyrene, which was nt fund in lard il fumes (26). Other reasns may include a chrt effect, lnger life expectancies (peple in the early decades f life may die yung befre they have a chance t develp cancer), and ther risk factrs such as smking, passive smking, air pllutin, and the pssible effects f the interactin between the mutagenicity f cking il fumes and these factrs. In summary, we fund that wmen nnsmkers were at higher risk fr lung cancer if they were expsed t cking il fumes emitted at high temperatures and that the risks were strengthened when the fumes were nt reduced by an extractr. ACKNOWLEDGMENTS This wrk was supprted in part by a grant frm the Natinal Science Cuncil (NSC B , NSC l-b ). REFERENCES 1. K YC, Lee CH, Chen MJ, et al. Risk factrs fr primary lung cancer amng nn-smking wmen in Taiwan. Int J Epidemil 1997;26: King H, Lcke FB. Cancer mrtality amng Chinese in the United States. J Nad Cancer Inst 1980:65: Grulich AE, McCredie M, Cates MS. Cancer incidence in Asian migrants t New Suth Wales, Australia. 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