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IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Household Use of Solid Fuels and High-temperature Frying. Lyon (FR): International Agency for Research on Cancer; 2010. (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, No. 95.)

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Household Use of Solid Fuels and High-temperature Frying.

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2Studies of Cancer in Humans

2.1. Introduction

Since the 1970s, a total of 17 case–control studies have explored the relationship between exposure to cooking fumes and the risk for lung cancer. These studies were conducted in Chinese populations residing in China (including Taiwan and Hong Kong Special Administrative Region) and Singapore. While active tobacco smoking is a well-established major cause of lung cancer in Chinese men and women, a relatively high proportion of lung cancer in Chinese women, many of whom are nonsmokers, can not be explained by active smoking. Thus, one motivation for these studies was to investigate the role of other lifestyle factors, including indoor air pollution from cooking oil fumes, in the etiology of lung cancer in Chinese women.

Exposure assessment of cooking practices and cooking oil fumes varied substantially (Tables 2.1 and 2.2). Two aspects related to cooking oil fumes have been investigated: (i) the types of oil used and practices of high-temperature cooking, including frequency, stir-frying, deep-frying and pan-frying, and (ii) cooking practices, including the availability of a separate kitchen, ventilation in the kitchen based on the number and size of windows, the use of a fume extractor, personal assessment of ventilation, such as frequency of eye irritation during cooking and smokiness in the kitchen, duration of exposure (years of cooking) and susceptible time of exposure (age started to cook). In four studies (Lan et al., 1993; Dai et al., 1996; Shen et al., 1996; Wang et al., 1996), results were based on a single variable that represented some aspect of cooking practices. In contrast, exposure assessment was more comprehensive in seven studies (Gao et al., 1987; Ko et al., 1997; Zhong et al., 1999; Ko et al., 2000; Lee et al., 2001; Metayer et al., 2002; Yu et al., 2006). In several studies, the authors specified that past cooking practices or those experienced earlier in life (Seow et al., 2000) or at a particular age or time period in life (Ko et al., 1997, 2000; Lee et al., 2001) were investigated. Behaviours related to the type of cooking oil used most often and the frequency of high-temperature cooking (stir-frying, pan-frying, deep-frying) were also frequently examined. However, in most of the studies, no discussion was included regarding the timing of exposure or whether the information collected was related to current, usual or past cooking practices. Other factors included frequency of eye irritation during cooking, frequency of smokiness in the house, location of the kitchen, windows in the kitchen and the presence of fume extractors; these are viewed as indirect measures to assess the severity of exposure to cooking fumes and general household ventilation. Greater attention was paid to the measures of exposure that were considered to be more objective and whether duration, frequency and intensity of exposure to cooking oil fumes were assessed.

Table 2.1. Assessment of cooking practices/fumes included in the published case–control studies of lung cancer.

Table 2.1

Assessment of cooking practices/fumes included in the published case–control studies of lung cancer.

Table 2.2. Assessment of cooking practices/fumes by type of oil, type of frying and type of fuel included in the published case–control studies of lung cancer.

Table 2.2

Assessment of cooking practices/fumes by type of oil, type of frying and type of fuel included in the published case–control studies of lung cancer.

Of the 17 case–control studies that have investigated the relationship of exposure to cooking oil fumes and lung cancer, one was a study of lung cancer mortality (Lei et al., 1996); the other studies included six population-based (Gao et al., 1987; Xu et al., 1989; Wu-Williams et al., 1990; Lan et al.., 1993; Zhong et al., 1999; Metayer et al., 2002) and 10 hospital-/clinic-based studies of incident lung cancers (Ger et al., 1993; Dai et al., 1996; Shen et al., 1996; Wang et al., 1996; Ko et al., 1997, 2000; Seow et al., 2000; Zhou et al., 2000; Lee et al., 2001; Yu et al., 2006). Twelve studies included only women (Gao et al., 1987, Wu-Williams et al., 1990; Lan et al., 1993; Dai et al., 1996; Wang et al., 1996; Ko et al., 1997; Zhong et al., 1999; Ko et al., 2000; Seow et al., 2000; Zhou et al., 2000; Metayer et al., 2002; Yu et al., 2006), seven of which studied only nonsmokers (Lan et al., 1993; Dai et al., 1996; Wang et al., 1996; Ko et al., 1997; Zhong et al., 1999; Ko et al., 2000; Yu et al., 2006). Men and women, smokers and nonsmokers were included in the other five studies (Xu et al., 1989; Ger et al., 1993; Lei et al., 1996; Shen et al., 1996, Lee et al., 2001).

These studies used heterogeneous methodologies and included different sources of cases, types of controls, methods of data collection and use of surrogate respondents; the degree of pathological confirmation of lung cancer diagnoses also differed. Relevant information regarding each of the case–control studies (i.e. study population, study period, sources of cases and controls, number of cases and controls, response rate, number of proxy interviews, percentage of pathologically/cytologically confirmed cases) and selected results are shown in Table 2.3.

Table 2.3. Case–control studies of cooking practices/fumes and lung cancer in China.

Table 2.3

Case–control studies of cooking practices/fumes and lung cancer in China.

2.2. Case–control studies

2.2.1. Northern China

Two large population-based case–control studies carried out in industrial areas in northern China during the late 1980s provided information on cooking practices and the risk for lung cancer. The main objectives of these two studies were to examine the role of active and passive smoking, and pollution from industrial and domestic sources. Xu et al. (1989) studied men and women who had lung cancer in Shenyang while Wu-Williams et al. (1990) examined the pattern of risk for lung cancer among women in Harbin and Shenyang.

The study in Shenyang included 1249 lung cancer cases (729 men, 520 women) and 1345 population-based controls (788 men, 557 women); 86% of male cases and 70% of male controls were smokers; the corresponding figures in women were 55% of cases and 35% of controls (Xu et al., 1989). Nearly 80% (85.1% in men, 75.0% in women) of the lung cancers were pathologically/cytologically confirmed; 31% of these were adenocarcinoma of the lung. After adjusting for age, education and active smoking, the risk for lung cancer was higher when cooking took place in the bedroom or entry corridor to the bedroom than in a separate kitchen or elsewhere in the house. In men, the adjusted odds ratios were 1.0, 1.2 and 2.1 in relation to cooking in the bedroom for 0, 1–29 and ≥30 years, respectively (p trend <0.05); the corresponding adjusted odds ratios in women were 1.0, 1.5 and 1.8 (p trend <0.05).

The report by Wu-Williams et al. (1990) was based on 965 female lung cancer cases in northern China (445 in Harbin, 520 in Shenyang) and 959 female controls (404 in Harbin, 555 in Shenyang); 417 cases and 602 controls were nonsmokers. Seventy-four per cent (714/965) of the lung cancers were histologically/cytologically confirmed of which 44% were adenocarcinoma of the lung. Cases and controls were compared in terms of deep-frying practices. Compared with no deep-frying, the adjusted odds ratios were 1.2, 2.1 and 1.9 for deep frying once, twice and more than three times per month, respectively. Cases reported that their homes became smoky during cooking more often than controls and that they had irritated eyes more frequently during cooking. Compared with women who never or rarely experienced eye irritation during cooking, the risk was increased among those who occasionally (odds ratio, 1.6; 95% CI, 1.2–1.8) or frequently (odds ratio, 1.8; 95% CI, 1.3–2.6) reported such irritation. The authors noted that results were similar for squamous-/oat-cell cancers and adenocarcinomas and for smokers and nonsmokers. Pollution from coal burning for heating was a major risk factor in this area in northern China; in a multivariate analysis, deep-frying and eye irritation remained significant risk factors after adjusting for active smoking, previous lung diseases and coal burning (i.e. use of kangs). [The Working Group noted that, although coal heating was adjusted for in the multivariate analysis, the risk associated with frequent eye irritation may be due to fuel smoke and cooking smoke. The assessment of cooking practices was relatively limited in these two studies.]

Two small studies were conducted in Harbin (Dai et al., 1996) and Shenyang during the early 1990s (Wang et al., 1996; Zhou et al., 2000). The study by Dai et al. (1996) included 120 nonsmoking women who had adenocarcinoma of the lung and an equal number of nonsmoking controls; all were long-term (at least 10 years) residents of Harbin. The risk for adenocarcinoma of the lung was significantly influenced by frequency of frying food; women who pan-fried and deep-fried more than five times per month experienced a more than ninefold increased risk (adjusted odds ratio, 9.20; 95% CI, 1.53–55.28) after adjustment for various covariates including exposure to coal burning. [The Working Group noted that the prevalence of frying was not presented; the wide confidence interval is a concern. It is unclear whether these questions related to current or usual frying practices and whether other questions on cooking practices were asked. One Chinese study by Lin et al. (1996) evaluated the exposure to cooking oil fumes and the risk of lung adenocarcinoma among female nonsmokers. An age-adjusted increased risk of lung cancer (odds ratio, 3.0; 95% CI, 1.35–6.69) was observed for those who reported to fry food more than 3 times per month.

In a hospital-based study conducted in Shenyang, Wang et al. (1996) compared the experiences of 135 female lifetime nonsmokers who had been diagnosed with primary lung cancer and an equal number of nonsmoking female population controls. Of the lung cancers included, 57.2% were diagnosed pathologically or cytologically, 54.5% of which were adenocarcinoma. The risk for lung cancer increased significantly in association with some or frequent exposure to cooking fumes (odds ratio, 3.79; 95% CI, 2.29–6.27). In a multivariate analysis, exposure to cooking fumes remained a significant risk factor (adjusted odds ratio, 4.02; 95% CI, 2.38–6.78) after adjusting for exposure to coal smoke and other factors. [The Working Group noted that this study was small and the exposure was limited to dichotomized (no/yes) assessment. The specific variables that were included in the multivariate analysis were not described. Coal use and exposure to coal smoke were reported in this study and may confound the findings related to cooking fumes. The validity of a diagnosis of adenocarcinoma is questionable because the authors stated that determination of the histological cell type was based on relevant medical record, chest X-rays, CT films and cytological and histological slides.]

Zhou et al. (2000) published another report on a subset of women from the hospital-based study in Shenyang (Wang et al., 1996). Specifically, 72 women (52 nonsmokers) who had been diagnosed with adenocarcinoma of the lung between 1991 and 1995 were compared with an equal number of control women (49 nonsmokers). A nonsignificant increased risk was observed in relation to deep-frying; the crude odds ratio was 1.68 (95% CI, 0.45–6.84) for deep-frying two or more times per week compared with none or once a week. The risk for adenocarcinoma increased significantly among women who reported that they experienced medium/heavy exposure to cooking fumes (crude odds ratio, 4.53; 95% CI, 2.09–9.94) or had frequent eye irritation and exposure to smoke during cooking. The risk for lung cancer was not significantly associated with whether cooking was carried out in a separate kitchen or in the living-room or bedroom. In a multivariate regression analysis, frequent eye irritation from smoke had an independent impact on risk. Compared with women who reported no eye irritation from smoke, those who reported slight, medium and heavy eye irritation showed elevated risks; the respective adjusted odds ratios were 1.58, 11.45 and 3.41 for (p for trend=0.002). [The Working Group noted that most of the lung cancer cases and controls included in the analysis by Zhou et al. (2000) represented a select subgroup of subjects reported by Wang et al. (1996) and the selection criteria were not described. This study was small and the confidence intervals were very wide.]

2.2.2. Other parts of China and Singapore

One of the first studies of exposure to cooking oil fumes and the risk for lung cancer was a large population-based case–control study conducted in the mid-1980s in Shanghai that was designed to examine lifestyle factors and lung cancer (Gao et al., 1987). The study included 672 women who had lung cancer and 735 population controls, of whom 436 cases and 605 controls were nonsmokers. Eighty-one per cent (542/672) of the lung cancers were diagnosed histologically or cytologically. Questions on cooking practices included type of oil used most often, frequency of frying, smokiness in the kitchen during cooking and frequency of eye irritation during cooking. Several measures of cooking practices were associated with an increased risk for lung cancer after adjusting for age, education and tobacco smoking. Compared with women who most frequently used soya bean oil, those who used rapeseed oil had an increased risk for lung cancer (adjusted odds ratio, 1.4; 95% confidence interval [CI], 1.1–1.8). The increased risk associated with the use of rapeseed oil existed at each level of reported frequency of eye irritation when cooking. However, the increased risk associated with frequent eye irritation when cooking was found among both women who used soya bean oil and those who used rapeseed oil, although the highest risk was found in women who used rapeseed oil and frequently experienced eye irritation (adjusted odds ratio, 2.8; 95% CI, 1.8–4.3). There was a stepwise increase in risk associated with smokiness in the house. Specifically, women who reported occasional/frequent eye irritation and a considerable amount of smokiness in the house showed a more than twofold increased risk (adjusted odds ratio, 2.6; 95% CI, 1.8–3.7). Risk increased with increasing number of dishes prepared by stir-frying (adjusted odds ratios, 1.0, 1.2, 1.2 and 2.6 for ≤20, 20–24, 25–29 and ≥30 times per week, respectively) and deep-frying (adjusted odds ratios, 1.0, 1.5, 1.6 and 1.9 for 0, 1, 2 and ≥3 times per week, respectively). The risk patterns were similar for adenocarcinoma and squamous-cell/oat-cell carcinoma of the lung. [The Working Group noted that this was one of the first well-conducted population-based studies on this topic and had many strengths. The Working Group also noted that the increased risk was found with increasing number of dishes prepared by boiling food. Since it should produce less oil vapour than stir-frying and deep-frying, the comparably high odds ratios associated with boiling food were unexpected, although the authors suggested that oil was also added during boiling.]

In the 1990s, Zhong et al. (1999) conducted another study in Shanghai that used study methods similar to those used by Gao et al. (1987) and included a total of 649 women who had been diagnosed with incident lung cancer during 1992–94 and 675 population controls. Subjects who had smoked at least one cigarette a day for at least 6 months (145 cases, 74 controls) were excluded from the analyses. Thus, results on cooking practices were based on 504 cases and 601 controls who were lifetime nonsmokers. Seventy-seven per cent (387/504) of the lung cancers were diagnosed histologically or cytologically; 76.5% (296/387) of these were adenocarcinoma. Women who did not cook in a separate kitchen experienced a small increased risk (adjusted odds ratio, 1.28; 95% CI, 0.98–1.68). Risk for lung cancer was higher among those who had used rapeseed oil most frequently compared with those who had used soya bean oil (adjusted odds ratio, 1.84; 95% CI, 1.12–3.02). However, the risk was not elevated when both types of oil had been used (adjusted odds ratio, 0.92; 95% CI, 0.37–2.28). Risk also increased with higher frequency of frying. Compared with women who deep-fried once a week or less often, those who deep-fried more than once a week had a nearly twofold increased risk (adjusted odds ratio, 1.88; 95% CI, 1.06–3.32). Similarly, compared with women who pan-fried food once a week or less often, those who pan-fried food more than once a week had a significantly increased risk (adjusted odds ratio, 2.09; 95% CI, 1.14–3.84). However, the risk pattern in relation to stir-frying was less consistent. Compared with stir-frying less than seven times a week, women who stir-fried seven times a week had a reduced risk (adjusted odds ratio, 0.38; 95% CI, 0.19–0.75), but those who stir-fried more than seven times a week showed an increased risk (adjusted odds ratio, 2.33; 95% CI, 0.68–7.95). Women exposed to visible fumes from high-temperature frying had an increased risk (adjusted odds ratio, 1.64; 95% CI, 1.24–2.17). This risk more than doubled for women who reported considerable smokiness (i.e. smokiness affected vision during cooking) from ‘cooking oil or fumes’ (adjusted odds ratio, 2.38; 95% CI, 1.58–3.57) compared with those who reported no smokiness. There was also a trend of increasing risk with increasing frequency of self-reported eye irritation; the adjusted odds ratio was 1.68 (95% CI, 1.02–2.78) for women who reported frequent (≥5 times per week) eye irritation compared with those who reported no eye irritation. Risk patterns related to Chinese-style cooking were generally similar in analyses that were restricted to all self-respondents (400 cases, 581 controls) or to self-respondents with histologically confirmed lung cancer (308 cases, 581 controls). Results were also comparable for women who had adenocarcinomas (296 cases), non-adenocarcinomas (91 cases) or unknown cell type (i.e. diagnosed clinically/radiologically) of lung cancer (117 cases). In a multivariate regression analysis, cooking temperature, smokiness in the kitchen during cooking, type of cooking oil and the frequency of stir-frying and of pan-frying displayed independent effects on the risk for lung cancer after adjustment for variables on ventilation (e.g. area of windows, cooking in a separate kitchen). Frequency of eye irritation and frequency of deep-frying were correlated with the other variables and did not exhibit independent effects on risk. [The Working Group noted several strengths in this population-based study: it was conducted among lifetime nonsmokers, the assessment of cooking practices was comprehensive and the analyses were thorough. Results were generally consistent across various subgroup analyses by histological and respondent type. The type of fuel used for cooking (coal, gas) was not significantly associated with risk and was not adjusted for in the multivariate analysis. It should be noted that the distribution of stir-frying was skewed and the confidence intervals were wide for stir-frying. The prevalence of use of rapeseed oil was 7.2% among controls in this study compared with 47.2% in Shanghai in the mid-1980s. The reason for the large differences in the pattern of use of rapeseed oil was not discussed but may be due to differences in the questions asked in the two studies.]

Two other studies were conducted in urban areas of China to examine the relationship between exposure to cooking oil fumes and risk for lung cancer. Shen et al. (1996) investigated potential risk factors for lung cancer among long-term (at least 20 years) residents of Nanjing in a hospital-based, case–control study that included 263 cases of lung cancer and an equal number of population controls. Only histologically confirmed lung cancers were studied (83 squamous-cell carcinomas, 180 adenocarcinomas). Exposure to cooking fumes was associated with an increased risk for squamous-cell carcinoma (adjusted odds ratio, 3.81; 95% CI, 1.06–13.73) and adenocarcinoma (adjusted odds ratio, 2.99; 95% CI, 1.68–5.34) of the lung. [The Working Group noted that the study had serious limitations. The report lacked details regarding the study design (e.g. response rate) and characteristics of the study population (e.g. gender distribution, active smoking history). The source of information on exposures was not presented. Only significant results were presented; risk patterns in relation to the amount of oil used in cooking and frequency of cooking per week were not presented.]

Cooking practices and lung cancer mortality were investigated in a case–control study in Guangzhou (Lei et al., 1996). Using registered deaths that occurred in this city in 1986, the analysis was based on 792 (562 men, 229 women) lung cancer deaths reported in long-term (at least 10 years) Guangzhou residents. The comparison group included other registered decedents who were matched to cases on gender, age (±5 years) and residence and whose cause of death was unrelated to cancer or respiratory disease. A standardized interview administered to spouses or cohabiting relatives of the decedents collected information on active smoking, exposure to secondhand smoke, living conditions, cooking facilities, exposure to coal dust and dietary habits. In analyses conducted separately in men and women, cases and controls did not differ significantly in their preference of frying, years of cooking (infrequent, ≤20, 20–40, >40 years) or size the of kitchen (<1, 1–2, ≥2 m2 per household). Similarly, living conditions (type of building, location of residence, interior dimensions of residence) and average size of the living area did not differ significantly between lung cancer cases and controls. [The Working Group noted that the study had several deficiencies. The quality of information on cooking practices obtained from next of kin is questionable; a considerable amount of information was missing; the data analysis was confined to crude analysis; and the accuracy of lung cancer diagnosis based on reviewed death records is not known for China.]

In addition to the above-mentioned studies that were conducted largely in urban areas of China, two studies were conducted in more rural parts of China: one in Xuan Wei County, Yunnan Province (Lan et al., 1993), an area where mortality rates for lung cancer are very high among women, and one in Gansu Province, a rural area in northwestern China (Metayer et al., 2002).

The study in Xuan Wei County, Yunnan Province, investigated the use of rapeseed oil in the study population and was based on 139 incident female lung cancers that were diagnosed between 1988 and 1990 and 139 age-matched controls (Lan et al., 1993). Of the lung cancer cases, 55 (39.6%) were diagnosed cytologically/pathologically. All cases and controls were nonsmokers. Compared with women who never used rapeseed oil, those who used it occasionally or frequently showed an increased risk; the respective adjusted odds ratios were 1.26 (95% CI, 0.68–2.63) and 4.58 (95% CI, 0.56–37.08) after adjusting for age, length of menstrual cycle, age at menopause and family history of lung cancer. [The Working Group noted that coal use was prevalent in this study population and was not considered in the analysis on cooking oil. In addition, the definition of occasional or frequent use of rapeseed oil was not provided. Few subjects (2.2% of controls) were frequent users of rapeseed oil and the confidence limits were wide. It is unclear whether other questions related to cooking practices were asked.]

Metayer et al. (2002) conducted a population-based case–control study that was designed to examine the association between cooking oil fumes and other sources of indoor air pollution and lung cancer in Gansu Province. The study included 233 female lung cancer cases and 459 control subjects; 206 cases and 411 controls were nonsmokers. Thirty-seven per cent of the cases were cytologically or histologically confirmed. Smokers (27 cases, 47 controls) were included in the analysis on cooking practices. Compared with women who only used linseed oil, an elevated risk was associated with the use of rapeseed oil alone (adjusted odds ratio, 1.65; 95% CI, 0.8–3.2), rapeseed and linseed oil in combination (adjusted odds ratio, 1.70; 95% CI, 1.0–2.5) and perilla/hempseed oil (adjusted odds ratio, 3.25; 95% CI, 0.8–14.0). The risk for lung cancer was unrelated to the frequency of deep-frying (adjusted odds ratio, 1.0, 0.82 and 0.83 for never/less than once a month, 1–2 times per month and ≥3 times per month, respectively). However, there was a significant exposure–response of increased risk with increasing frequency of stir-frying (adjusted odds ratios, 1.00, 1.96, 1.73 and 2.24, for stir-frying <15, 15–29, 30 and ≥31 times per month; p for trend=0.03). Risk tended to increase with decreasing age when started to cook (adjusted odds ratio, 0.69 for started cooking at age ≥17 versus ≤13 years), with increasing number of meals cooked per day (adjusted odds ratio, 1.36 for ≥3 meals versus ≤2 meals) and with increasing years of cooking (adjusted odds ratio, 1.0, 1.26, 2.51 and 2.46 for ≤29, 30–39, 40–49 and ≥50 years) (p for trend <0.09). Although women who reported frequent eye–throat irritation showed a significantly increased risk (adjusted odds ratio, 2.82; 95% CI, 1.6–5.0) compared with those who never experienced such irritation (p trend <0.01), the general level of indoor smokiness was unrelated to risk. Risk for lung cancer was not elevated among women who reported considerable home smokiness (odds ratio, 0.76; 95% CI, 0.4–1.6) compared with those who reported no smokiness. The authors hypothesized that, as underground cave dwellings in Gansu Province reported high ventilation rates as measured by air exchanges per hour, this may explain the lack of any risk associated with general smokiness. The positive associations with stir-frying, years of cooking and eye irritation were found in women who cooked with linseed oil only (80 cases, 247 controls) and in those who cooked with rapeseed oil (148 cases, 205 controls). In addition, the authors reported that the results were generally similar when the analyses were restricted to self-respondents or to histologically confirmed lung cancer cases. [The Working Group noted that this study included a comprehensive assessment of cooking practices and conditions. Coal use for heating/cooking was not significantly associated with lung cancer risk in this population. Although coal use was not considered in the analysis on cooking practices, it is unlikely to confound the findings. The results suggest that fumes from all types of oil may have deleterious effect. This study is limited by a relatively large number of only clinically/radiologically diagnosed lung cancers and because interviews were conducted with next-of-kin respondents for 123 cases (53%) and 20 controls (4%).]

Shi et al. (2005) conducted a case–control study that included nonsmoking women who had been newly diagnosed with lung cancer between June 2000 and December 2002 in city hospitals of urban Shenyang. Eighty-four per cent of cases were diagnosed pathologically or cytologically. Controls were randomly selected from the general female population of urban areas and matched on age (within ±2 years). Information on demographic factors, exposure to cooking oil smoke, types of fuel used, exposure to coal smoke, use of heated kangs, passive smoking, history of lung disease and other factors was obtained. Risk for lung cancer increased significantly in association with exposure to cooking oil smoke (odds ratio, 3.18; 95% CI, 2.55–3.97) and fuel smoke (odds ratio, 2.56; 95% CI, 1.83–4.55) after adjusting for education and social class. Risk was unrelated to the use of kangs (odds ratio, 1.12; 95% CI, 0.91–1.39). In a multivariate analysis, the increased risk associated with cooking oil smoke remained statistically significant (adjusted odds ratio, 4.11; 95% CI, 2.14–7.89) but the risk associated with fuel smoke was no longer statistically significant. [The Working Group noted that, although the finding on cooking oil smoke was adjusted for fuel smoke, it is difficult to rule out residual confounding in this study.]

Seven studies on cooking practices and the risk for lung cancer have been conducted in other parts of China, including one study in Hong Kong Special Administrative Region (Yu et al., 2006), four in Taiwan (Ger et al., 1993; Ko et al., 1997, 2000; Lee et al., 2001) and two in Singapore (MacLennan et al., 1977; Seow et al., 2000).

(a) Hong Kong Special Administrative Region

Chan-Yeung et al. (2003) conducted a case–control study in Hong Kong Special Administrative Region during the late 1990s which included 331 Chinese residents (212 men, 119 women) who had been diagnosed with a histologically confirmed primary lung cancer in a large teaching hospital. An equal number of age- and gender-matched residents identified from the same hospital who had non-malignant respiratory diseases were used as controls. Most of the women were nonsmokers (106 cases, 113 controls) while many of the men were smokers (160 cases, 116 controls). All cases and controls were interviewed by one interviewer and were asked about regular exposure to cooking fumes from frying in the house. Years of regular exposure to frying food was not significantly related to the risk for lung cancer in men or women. For women with no or less than 2 years of exposure, the respective odds ratios associated with <3.5 years, ≥3.5–≤7 and >7 years of exposure to frying food were 1.08 (95% CI, 0.50–2.32), 1.05 (95% CI, 0.46–2.42) and 1.54 (95% CI, 0.57–4.13) after adjustment for demographic factors and smoking habits. The corresponding risk estimates in men were 0.69 (95% CI, 0.32–1.49), 0.83 (95% CI, 0.38–1.80) and 1.22 (95% CI, 0.38–3.99). [The Working Group noted that this study included a single measure of exposure to frying in the house. Control subjects had non-malignant respiratory diseases and may have had risk factor profiles that are more similar to the lung cancer patients than control subjects selected from the general population. Thus, estimates of risk associated with exposure to frying may be underestimated.]

Yu et al. (2006) conducted a case–control study in Hong Kong Special Administrative Region during the early 2000s that included 200 nonsmoking Chinese women who had been diagnosed with a histologically confirmed primary lung cancer in a large oncology centre and 285 population controls. All but 12 participants (six cases, six controls) were interviewed in person using a standardized structured questionnaire that asked extensive questions about lifetime cooking habits since childhood and included number of years of cooking, the frequencies of stir-frying, pan-frying and deep-frying, the types of cooking oils used, the use of a fume extractor or exhaust fans and the habit of heating up a wok to high temperatures. The risk for lung cancer increased significantly with increasing total cooking ‘dish–years’, a composite index that was constructed to account for both the frequency and the duration of cooking. The odds ratios were 1.00, 1.31, 2.80, 3.09 and 8.09, respectively, for ≤50, 51–100, 101–150, 151–200 and ≥200 ‘total frying dish–years’ after adjusting for age, education, employment status, previous lung disease and family history of lung cancer. The results remained significant after further adjustment for factors that may contribute to indoor air pollution (e.g. radon, exposure to environmental tobacco smoke, use of kerosene, use of firewood, burning of incense and use of mosquito coils) and dietary factors. In addition, a trend of increasing risk with heating a wok to high temperature was observed; the odds ratio was 1.0, 1.02 and 1.97 in relation to never/seldom, occasionally and always engaging in such cooking habits. Risk (per 10 dish–years) was highest for deep-frying (odds ratio, 2.56; 95% CI, 1.31–5), intermediate for pan-frying (odds ratio, 1.47; 95% CI, 1.27–1.69) and lowest for stir-frying (odds ratio, 1.12; 95% CI, 1.07–1.18). However, risk was not significantly associated with the use of a particular type of oil (peanut oil, corn oil, canola oil) for cooking or with using a fume extractor. A pattern of risk associated with total cooking dish–years was observed for adenocarcinoma and for non-adenocarcinoma, although the results were stronger for adenocarcinoma of the lung, which represented 69% of the lung cancer cases included in this study. [The Working Group noted that this study included a comprehensive assessment of lifetime cooking habits. Duration and frequency of exposure was captured by a composite index, ‘total cooking dish–years’, which permitted a quantitative assessment of cumulative exposure. While the confidence interval for the highest exposure category (>200 dish–years) was wide, there was a monotonic increase in risk with increasing exposure. It should be noted that this index was computed based on the number of dishes cooked by the three cooking methods (stir-frying, pan-frying and deep-frying). Although the response rate among controls was modest (∼50%), few differences between cases and controls were noted for demographic factors except for a higher rate of employment among controls (88%) compared with cases. Elevated risks associated with moderate to high levels of cooking (>100 dish–years) remained after further adjustment for employment status.]

(b) Taiwan (China)

Four hospital-based case–control studies of lung cancer from Taiwan investigated the role of cooking practices. The main type of oil used in Taiwan is vegetable oil (mainly peanut or soya bean oil).

Ger et al. (1993) conducted a hospital-based case–control study in Taipei, Taiwan, that included 131 primary lung cancers (92 men, 39 women) identified between 1990 and 1991. All were histologically confirmed. Two control groups were interviewed; 262 hospital controls were matched to cases on sex, date of birth (±5 years), date of interview (±4 weeks) and insurance status and 262 neighbourhood controls were matched to cases on age, sex and residence of case at the time of diagnosis. In total, 48 cases and 229 controls (111 hospital controls, 118 neighbourhood controls) were nonsmokers. Risk for adenocarcinoma and squamous-/small-cell cancers in men and women combined was unrelated to cooking style; cases and controls did not differ in pan-frying, stir-frying, deep-frying or boiling practices after adjusting for active smoking and other covariates. Risk for adenocarcinoma increased significantly in persons who reported that they were professional cooks (adjusted odds ratio, 5.54; 95% CI, 1.49–20.65); no increased risk was found for squamous-cell cancer (adjusted odds ratio, 1.16; 95% CI, 0.32–422). [The Working Group noted that this study included few female lung cancer patients. Results were based on dichotomized cooking variables (e.g. no/yes frying) that were not defined.]

Three hospital-based case–control studies were conducted in Kaohsiung, a heavily industrialized city in Taiwan (Ko et al., 1997, 2000; Lee et al., 2001). The designs of these studies were similar. The first study included 117 female lung cancer cases identified between 1992 and 1993 who were compared with 117 hospital controls who were admitted for a health check-up (55 controls) or for eye diseases (62 controls) (Ko et al., 1997). Active smokers (11 cases, three controls) were excluded so that the analysis was based on 105 case–control pairs who were nonsmokers. In a univariate analysis, risk for lung cancer increased with increased frequency of stir-frying (odds ratio, 2.4; 95% CI, 1.1–5.2 for ≥5 versus 0–4 times per week), pan-frying (odds ratio, 2.3; 95% CI, 1.2–4.6 for ≥5 versus 0–4 times per week) but not with deep-frying (odds ratio, 0.9; 95% CI, 0.5–1.9 for ≥5 versus 0–4 times per month). Risk also increased with younger age when started to cook (odds ratio, 1.6; 95% CI, 0.8–3.0 for started at ages 7–20 versus after age 21 years). Risk for lung cancer was elevated in women who cooked in a kitchen without a fume extractor; this was found at different ages of cooking including before age 20 years (odds ratio, 5.3; 95% CI, 1.1–25.6), between the ages of 20 and 40 years (odds ratio, 6.4; 95% CI, 2.9–14.1) or after 40 years of age (odds ratio, 2.3; 95% CI, 1.1–5.1). The risk for lung cancer was not significantly related to types of cooking oil (lard versus vegetable oil). In a multivariate analysis, use of a fume extractor during cooking between the ages of 20 and 40 years remained statistically significant (adjusted odds ratio, 8.3; 95% CI, 3.1–22.7). [The Working Group noted that, while there was no increased risk associated with cooking with coal, the risk increased significantly in relation to cooking with wood or charcoal before 20 years of age and between the ages of 20 and 40 years. These investigators examined the combined effects of frying and use of fume extractors between the ages of 20 and 40 years. The increased risks associated with stir-frying and pan-frying remained regardless of use of fume extractors.]

A second study conducted by the same group of investigators was based on 131 lung cancer cases identified between 1993 and 1996, 252 hospital controls and 262 community controls; all participants were nonsmokers (Ko et al., 2000). All lung cancers were histologically confirmed; 63% were adenocarcinoma of the lung. Of the more than 10 variables related to cooking practices that were investigated, risk for lung cancer was associated with five. There was a significant trend of increasing risk with number of meals cooked per day (adjusted odds ratios, 1.0, 3.1 and 3.4 for cooking 1, 2 and 3 meals per day, respectively). Risk was also elevated for women who cooked between the ages of 20 and 40 years without a fume extractor (adjusted odds ratio, 2.2; 95% CI, 1.3–3.8). In addition, women who reported frequent eye irritation (odds ratio, 2.1; 95% CI, 1.3–3.5) showed significantly elevated risks. Subjects who usually waited until fumes were emitted from the oil and then stir-fried, pan-fried or deep-fried also experienced about a twofold increased risk that was statistically significant. In contrast, years of cooking at home, general ventilation in the kitchen, number of windows in kitchen (<2 versus ≥2) and size of openings (windows) to the outside did not differ between cases and controls. The risk estimates presented above were obtained when cases were compared with community controls, and risk patterns were generally similar when lung cancer cases were compared with hospital controls. [The Working Group noted that use of coal and wood/charcoal was not reported. However, since this study overlapped with the earlier study (Ko et al., 1997), the same comments relating to cooking fuel are applicable.]

A further expansion of the previous two studies included lung cancer patients diagnosed between 1993 and 1999 (Lee et al., 2001). Women who had been diagnosed with squamous-/small-cell (84 cases) cancer or adenocarcinoma of the lung (162 cases) and 407 corresponding controls were included in the analysis. Women who had other lung cancer cell types (45 cases) and men who had lung cancer were excluded from the analysis of cooking practices. Prevalence of smoking in female controls was not presented but, among female cases, 96.9% of those with adenocarcinoma of the lung and 81.6% of those with squamous-/small-cell lung cancer were nonsmokers. Risk was significantly higher for those who cooked in a kitchen without a fume extractor; the adjusted odds ratio was 3.0 (95% CI, 1.3–7.1) for squamous-/small-cell cancer and 3.9 (95% CI, 2.3–6.6) for adenocarcinoma of the lung. Women who stir-fried, pan-fried or deep-fried only when fumes were emitted from the oil showed significantly higher risk for adenocarcinoma (respective odds ratios, 2.0, 2.6 and 1.6) but not for squamous-/small-cell cancer of the lung (respective odds ratios, 0.9, 0.8 and 1.0). Risk for either cell type of lung cancer was not significantly influenced by age when first started to cook (>20 versus ≤20 years) or type of cooking oils (lard versus vegetable oils). In a multivariate regression analysis, cooking in a kitchen that was not equipped with a fume extractor remained a significant risk factor for both squamous-/small-cell lung cancer and adenocarcinoma of the lung; the respective adjusted odds ratios were 3.3 (95% CI, 1.2–9.2) and 3.8 (95% CI, 2.1–6.8). In addition, waiting to fry until the cooking oil has reached a high temperature was associated with an increased risk for adenocarcinoma of the lung (adjusted odds ratio, 2.1; 95% CI, 1.1–3.0) but not for squamous-/small-cell lung cancer. [The Working Group noted that there was an overlap of cases and controls in the three reports by Ko and colleagues. An advantage of the second report (Ko et al., 2000) is that a group of population controls was also included and most of the risk patterns were similar compared with both control groups. It should be noted that use of wood/charcoal, a significant risk factor for both cell types of lung cancer, was not adjusted for in the analysis on cooking practices.]

(c) Singapore

Seow et al. (2000) conducted a hospital-based case–control study in Singapore during the late 1990s; 303 women who had been diagnosed with a pathologically confirmed primary lung cancer (56% were adenocarcinoma of the lung) and 765 hospital controls were compared. Analyses were conducted separately for smokers (former and current smokers combined; 127 cases, 100 controls) and lifetime nonsmokers (176 cases, 663 controls). All participants were interviewed in person using a standardized questionnaire that asked extensive questions on diet, reproductive history, exposure to secondhand smoke and cooking practices. Specifically, questions included the frequency of stir-frying, types of oil used and usual cooking practice 20–30 years before diagnosis. Subjects were also asked how often the air in their kitchen became filled with oily ‘smoke’ during frying. For each of these cooking exposures, there were six possible responses ranging from never/less than yearly, less than monthly, to daily and more than once a day. Among smokers, the risk for lung cancer doubled in association with daily stir-frying (adjusted odds ratio, 2.0; 95% CI, 1.0–3.8) after adjusting for a large number of potential confounders. This increase in risk was confined to those who stir-fried meat on a daily basis (adjusted odds ratio, 2.7; 95% CI, 1.3–5.5). Compared with smokers who stir-fried meat less frequently than daily, risk was intermediate for those who stir-fried meat less than daily in a fume-filled kitchen (adjusted odds ratio, 1.7; 95% CI, 0.7–3.9) and was highest for those who stir-fried daily and reported a smoke-filled kitchen (adjusted odds ratio, 3.5; 95% CI, 1.8–6.9). Women who stir-fried meat daily and primarily used unsaturated oils had the highest risk (adjusted odds ratio, 4.6; 95% CI, 1.6–13.0), while risk was intermediate for those who stir-fried daily but did not use unsaturated oils exclusively (adjusted odds ratio, 2.2; 95% CI, 1.2–4.2). In contrast, the risk for lung cancer in nonsmokers was unrelated to stir-frying (adjusted odds ratio, 1.0; 95% CI, 0.7–1.5) or stir-frying meat daily (adjusted odds ratio, 0.9; 95% CI, 0.6–1.4). Risk for lung cancer in nonsmokers was not affected by smokiness of kitchen or types of oil used. [The Working Group noted that this study presented no data on pan-frying or deep-frying. Although fuel use was not considered in this analysis, it is unlikely to be an important confounder because gas/kerosene is usually used (MacLennan et al., 1977). However, this was one of the few studies that described the questions that were asked regarding cooking practices and that specifically addressed cooking practices during the period 20–30 years before cancer diagnosis/interview. Reasons for the differences in findings by smoking status are not apparent but the sample size of smokers was modest. The risk estimates presented in the tables were slightly different from the numbers presented in the text; the numbers presented in the tables are those given in this Monograph.]

2.3. Meta-analysis

Feng & Ling (2003) carried out a meta-analysis on case–control studies among nonsmoking women that were published between 1992 and 2002 in the English and Chinese literature and examined the relationship between exposure to cooking oil fumes and lung cancer. Six studies (two in English and four in Chinese) were conducted in mainland China and two (in English) in Taiwan. All studies reported significantly increased odds ratios ranging from 2.10 to 9.20. The combined odds ratio using a fixed effects model was 2.94 (95% CI, 2.43–3.56). [The Working Group noted that the two studies in Taiwan had some overlap in their study subjects. Two reports by the same group of authors in China (Wang et al., 1996), one in English and one in Chinese, essentially overlap one another. The exposure metrics were not uniform and the rationale for selecting certain odds ratios out of a range in each paper was not entirely clear.

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©International Agency for Research on Cancer, 2010.
Bookshelf ID: NBK385513

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