KSOEM
Articles
- Page Path
- HOME > Ann Occup Environ Med > Volume 36; 2024 > Article
- Original Article Cooking oil fume exposure and Lung-RADS distribution among school cafeteria workers of South Korea
-
Minjun Kim1
, Yangho Kim1, A Ram Kim1, Woon Jung Kwon2, Soyeoun Lim2, Woojin Kim1, Cheolin Yoo1 -
Annals of Occupational and Environmental Medicine 2024;36:e2.
DOI: https://doi.org/10.35371/aoem.2024.36.e2
Published online: January 31, 2024
1Department of Occupational and Environmental Medicine, Ulsan University Hospital, Ulsan University School of Medicine, Ulsan, Korea.
2Department of Diagnostic Radiology, Ulsan University Hospital, Ulsan University School of Medicine, Ulsan, Korea.
- Correspondence: Cheolin Yoo. Department of Occupational and Environmental Medicine, Ulsan University Hospital, University of Ulsan College of Medicine, 879 Bangeojinsunhwando-ro, Dong-gu, Ulsan 44033, Korea. 0722863@uuh.ulsan.kr
• Received: August 8, 2023 • Revised: September 29, 2023 • Accepted: January 3, 2024
Copyright © 2024 Korean Society of Occupational & Environmental Medicine
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
- 841 Views
- 105 Download
- 1 Web of Science
Abstract
-
Background Cooking oil fumes (COFs) from cooking with hot oil may contribute to the pathogenesis of lung cancer. Since 2021, occupational lung cancer for individual cafeteria workers has been recognized in South Korea. In this study, we aimed to identify the distribution of lung-imaging reporting and data system (Lung-RADS) among cafeteria workers and to determine factors related to Lung-RADS distribution.
-
Methods We included 203 female participants who underwent low-dose computed tomography (LDCT) screening at a university hospital and examined the following variables: age, smoking status, second-hand smoke, height, weight, and years of service, mask use, cooking time, heat source, and ventilation. We divided all participants into culinary and non-culinary workers. Binomial logistic regression was conducted to determine the risk factors on LDCT of Category ≥ 3, separately for the overall group and the culinary group.
-
Results In this study, Lung-RADS-positive occurred in 17 (8.4%) individuals, all of whom were culinary workers. Binary logistic regression analyses were performed and no variables were found to have a significant impact on Lung-RADS results. In the subgroup analysis, the Lung-RADS-positive, and -negative groups differed only in ventilation. Binary logistic regression showed that the adjusted odds ratio (aOR) of the Lung-RADS-positive group for inappropriate ventilation at the workplace was 14.89 (95% confidence interval [CI]: 3.296–67.231) compared to appropriate ventilation as the reference, and the aOR for electric appliances at home was 4.59 (95% CI: 1.061–19.890) using liquid fuel as the reference.
-
Conclusions The rate of Lung-RADS-positive was significantly higher among culinary workers who performed actual cooking tasks than among nonculinary workers. In addition, appropriate ventilation at the workplace made the LDCT results differ. More research is needed to identify factors that might influence LDCT findings among culinary workers, including those in other occupations.
BACKGROUND
Lung cancer has high morbidity and mortality rates worldwide, with 2.2 million new diagnoses and 1.79 million deaths per year.1 According to the 2020 Cancer Registration Statistics, 28,949 new cases of lung cancer were diagnosed in Korea, of which 19,657 were men and 9,292 were women.2 In a national survey of Korea, the incidence of lung cancer among female and non-smokers is gradually increasing, and high-temperature cooking has been identified as potential causes of lung cancer in these groups.3,4 Lung cancer is a malignant tumor caused by uncontrolled cell growth in the lungs. If not treated early, it can spread to surrounding tissues and organs. Primary lung cancer includes small cell lung carcinoma (SCLC) and non-small cell lung cancer (NSCLC). Of these, NSCLC accounts for 85% of cases and is divided into 3 main pathologic subtypes: squamous cell carcinoma, large cell carcinoma, and adenocarcinoma (ADC).
To date, low-dose computed tomography (LDCT) is the only test recommended for lung cancer screening. In South Korea, LDCT is annually recommended for high-risk individuals aged 55–74 years.5 Although smoking is a major risk factor for lung cancer,6 about 25% cases occur in nonsmokers.7,8
Recently, the number of smokers has been decreasing due to smoking cessation programs, and cooking oil fumes (COFs) have been cited as a major risk factor for lung cancer besides occupational exposure.7 In nonsmokers, SCLC is rarely observed, and ADC is the most common. ADC, accompanied by epidermal growth factor receptor (EGFR) mutations, is more common among Asians (50% of NSCLC) than in Westerners (20% of NSCLC).9 Early diagnosis is necessary as targeted therapies increase survival rates.10,11
Cooking with high-temperature frying, stir-frying, and grilling recipes produces COFs, a form of adsorption of polycyclic aromatic hydrocarbons (PAHs), volatile organic compounds (VOCs), and formaldehyde onto particulate matter (PM). The International Agency for Research on Cancer has listed frying, emissions from high-temperature as group 2A carcinogen.12 Due to eating-out culture, COFs have become a major source of indoor air pollution, especially for female workers, and various studies have been conducted.4,13,14
Since 2021, occupational lung cancer among cafeteria workers has been recognized in South Korea. This study, we aimed to identify the distribution of lung-imaging reporting and data system (Lung-RADS) in food service workers aged ≥ 55 years or had been working for ≥ 10 years using LDCT and determine factors related to Lung-RADS distribution in cooks and kitchen assistants in charge of actual cooking and nutrition teachers who do not participate in actual cooking.
METHODS
Overall, 217 participants undergo LDCT screening at Ulsan University Hospital between June 2022 and August 2022. People aged ≥ 55 and those who had been working for ≥ 10 years were selected. Cooks and kitchen assistants were in the exposed group while nutrition teachers were in the unexposed group. The participants in the exposed group, culinary workers, were responsible for cooking, serving, transporting, and maintaining food service equipment and utensils. Those in the nonexposed group, nonculinary workers, were responsible for supervising cooks and performing administrative and supervisory tasks including meal planning and distribution. All 217 participants were female, and individuals with tuberculosis, asthma, or cancer other than lung cancer before screening (n = 14) were excluded from the study. Patients diagnosed with lung cancer 3 months before screening and underwent LDCT were regarded as 4X. Finally, 203 participants (167 exposed and 36 unexposed) were selected for data analyses.
Data were collected using a self-reported questionnaire before LDCT screening for individuals who agreed to participate in the study (Supplementary Data 1). The questionnaire included questions on the participant’s age, smoking status, passive smoking, height, weight, service years, use of masks when cooking, cooking time at home, heat source at home, and home ventilation for both exposed and unexposed individuals. The exposed group was further questioned about the proportion of cooking duties at work, number of recipes they cooked, amount of heat exposure per week, main ingredients, and ventilation conditions at the workplace.
We categorized the extent to which cooking dominates the workday into 4 levels: i) most of the time, ii) more than half, iii) less than half, and iv) others, with the highest level being defined as high proportion of cooking tasks. For cooking (grilling, boiling, stir-frying, frying, and others), we classified respondents doing all the frying, stir-frying, and grilling as being exposed to recipes that use a lot of fat or oil. For recipes using heat, a response was classified as follows: i) at every meal, ii) more than half, iii) less than half, and iv) others, and a response of daily was considered high exposure. For frequently used ingredients (vegetables, meat, fish, others), high-exposure group were those who responded that they mainly use both meat and fish. Workplace ventilation was classified as follows: i) open window only, ii) open windows and turn on fans, iii) fans only, and iv) no special ventilation, respondents were considered to have better ventilation if they reported using both windows and fans.
Cooking time at home was classified as high exposure when exceeded 2 hours, and for the heat source at home, electric fuel was considered low exposure. For ventilation at home, we defined better ventilation as the use of both windows and fans, same as at the workplace.
The American College of Radiology’s (ACR) Lung Cancer Screening Registry uses the Lung-RADS categories and updated Lung-RADS ver1.1 (Supplementary Table 1) produced by the ACR in 2019.15 Lung-RADS, which is administered to lung cancer high-risk group aged 55–74 years with a smoking history of ≥ 30 pack-years, was adapted, and used for screening subjects who were all nonsmokers. Of these, Category ≥ 3 requiring follow-up within 6 months was defined as Lung-RADS-positive.
Lung-RADS version 1.1
Category 1: Negative and definitely benign nodules.
Category 2: Benign appearance and a likelihood to be malignant < 1%.
Category 2b: Nodules that may correspond to categories 3 or 4 but are highly suspected to be benign considering the high tuberculosis prevalence in Korea.
Category 3: Probably benign but with a likelihood of ≥ 1% to be malignant, requiring 6 months of LDCT follow-up.
Category 4A: Suspicious nodules suspected to be lung cancer with a likelihood of 5%–15% to be malignant, requiring 3 months of LDCT follow-up or positron emission tomography-computed tomography (PET-CT) or bronchoscopy.
Category 4B, 4X: very suspicious nodules suspected to be lung cancer with a likelihood of > 15% to be malignant, requiring Chest CT, PET-CT, or tissue sampling.
LDCT was performed using SIMENS SOMATOM go.TOP (Siemens Medical Solutions, Forchheim, Germany), and the protocol was as follows: tube voltage: 110 kVP; tube current: 14 mAs; rotation: 0.33 seconds; collimation: 0.6 mm; pitch: 1.5 for 16-channel scanners or higher. Images were read by a specially trained radiologist.
The work environment measurements were monitored by the Environmental Health Team of the Occupational Health Center of the city where the schools are located. Acetaldehyde, formaldehyde, acrylamide, benzene, ozone, respirable PM, carbon monoxide (CO), noise, and high temperature were measured in 6 schools from July 13 to July 26 in 2022, using personal and regional samples.
Continuous variables were presented as mean values and standard deviations; categorical variables were presented as frequencies and percentages. All participants were divided into culinary and nonculinary workers, and characteristics of each group were compared using the χ2 test or Fisher’s exact test and the independent-sample t-test. We defined culinary workers as a subgroup of participants who are expected to have high exposure to COFs. Subgroup analyses were performed using the same method. LDCT findings were categorized using Lung-RADS version 1.1, and Category ≥ 3 requiring follow-up within 6 months was defined as Lung-RADS-positive, and groups were compared using the χ2 test. To adjust for confounding variables and analyze the effect of each variable on Lung-RADS, we performed binomial logistic regression analyses for the overall group and culinary group. All p-values < 0.05 were considered statistically significant. All statistical analyses were performed using SPSS Statistics version 24 (IBM Corp., Armonk, NY, USA).
The present study protocol was reviewed and approved by the Institutional Review Board (IRB) of Ulsan Hospital (IRB No. UMC 2023-03-013).
RESULTS
Of 203 participants, 167 and 36 were in the exposed and unexposed groups, respectively. The mean age was 55.87 ± 3.58 and 48.19 ± 6.39 years in the exposed and unexposed groups, respectively, and it was significantly higher for the culinary workers (Table 1, p = 0.000). The participants were all female nonsmokers, and no statistically significant differences were observed between the 2 groups for passive smoking. Those in both groups worked for a mean period of 18.37 ± 4.91 and 20.97 ± 8.33 years, respectively, in food service, although no statistically significant exists (p = 0.079). The participants in the exposed group were more likely to wear masks before the pandemic than those in the unexposed group (p = 0.004). The proportion of participants who cooked at home for ≥ 2 hours was also higher in the exposed group (75; 44.9%) than in the unexposed group (2; 5.6%) (p = 0.000). For heat sources used at home, the culinary workers relied significantly more on liquefied gas, with 154 (92.2%) participants in the exposed group and 27 (75.0%) participants in the unexposed group (p = 0.005). For home ventilation, both groups used at least one method of ventilation, and the exposed group was found to be more thoroughly ventilated with 155 (92.8%) participants adopting both methods compared to 28 (77.8%) participants in the unexposed group.
Table 1
Baseline characteristics of participants according to work
Values are presented as number (%) or mean ± standard deviation. The p-values were calculated using the χ2 test and the independent t-test. The p-values were analyzed by Fisher’s exact test (passive smoking, heat source in the house, ventilation in the house).
BMI: body mass index.
*p < 0.05; **p < 0.01; ***p < 0.001.
Chi-square analyses of Lung-RADS distribution in the exposed and unexposed groups revealed 17 participants to be Lung-RADS-positive, with all of them being in the exposed group, culinary workers. This was statistically significant (Table 2, p = 0.031). In the exposed group, 111 (65.5%) participants had Lung-RADS Category 1, 36 (21.6%) had Category 2, 3 (1.8%) had Category 2b, 8 (4.8%) had Category 3, 4 (2.4%) had Category 4A, 1 (0.6%) had Category 4B, and 4 (2.4%) had Category 4X. In the nonexposed group, there were 27 (75.0%) participants with Lung-RADS Category 1, 8 (22.2%) with Category 2, and 1 (2.8%) with Category 2b, with no participant having Category ≥ 3. Binomial logistic regression analyses of body mass index (BMI), passive smoking, age, years of work experience, mask use, time spent cooking at home, heat source at home, ventilation status, and occupation did not identify any variables that significantly affected Lung-RADS results.
Table 2
Lung-RADS distribution of participants according to work classification
| Lung-RADS | Total (n = 203) | p-value | |
|---|---|---|---|
| Exposed (n = 167) | Unexposed (n = 36) | ||
| Negative | 150 (89.8) | 36 (100.0) | 0.031* |
| Positive | 17 (10.2) | 0 (0.0) | |
Subgroup analyses were performed on the exposure group where many Lung-RADS-positive participants were observed. In subgroup analysis, 17 (10.2%) Lung-RADS-positive and 150 (89.8%) Lung-RADS-negative individuals were analyzed out of a total of 167 exposed individuals. Only workplace ventilation differed between the Lung-RADS-positive group (12, 70.6%) and Lung-RADS-negative group (141, 94.0%), and this difference was statistically significant (Table 3, p = 0.007). Binomial logistic regression analyses performed after adjusting for age, passive smoking, BMI, years of work, mask-wearing, cooking time at home, cooking time at work, favorite recipes, heat exposure during cooking, and favorite ingredients showed that the odds ratio (OR) for Lung-RADS-positive days was 14.89, and the p-value was significant when thorough ventilation was used as the reference (Table 4, p = 0.000). For household heat sources, the OR was 4.59 and p-value was significant when liquid fuel use was used as the reference (p = 0.041).
Table 3
Baseline of characteristics of subgroup (culinary workers)
The p-values were calculated using the χ2 test and the independent t-test. The p-values were analyzed using Fisher’s exact test (passive smoking, heat sources at the home, ventilation at the home, ventilation at the workplace).
Lung-RADS: lung-imaging reporting and data system; BMI: body mass index.
**p < 0.01.
Table 4
The adjusted odds ratios and 95% confidence intervals for the associations between different variables with lung-imaging reporting and data system-positive in subgroup analyses
Bold fonts refer to statistically significant results. The adjusted odds ratio was calculated via binomial logistic regression analyses (Model 1: adjusted for passive smoking, age, BMI, employment period, wearing a mask before COVID-19, recipe, ingredient, cooking hours at the home, cooking at the workplace, recipe with heat). There is no statistical significance in binomial logistic regression analyses of the entire study population (passive smoking, age, BMI, employment period, wearing a mask before COVID-19, cooking hours at the home, heat source at the home, ventilation at the home, work classification).
BMI: body mass index; COVID-19: coronavirus disease 2019.
*p < 0.05; **p < 0.01; ***p < 0.001.
Six schools in the city (4 elementary schools, one middle school, and one high school) were surveyed from July 13 to July 26 in 2022. Measurements were conducted for acetaldehyde, formaldehyde, acrylamide, benzene, ozone, respirable PM, CO, noise, and high temperature (Table 5). Underground (C), newly established school on the ground floor (D), semi-basement but fully equipped with electricity (E), ozone was measured higher than the exposure standard of 0.08 ppm.; 8-hour total weight average (8hr-TWA) 0.0954 ppm (C, personal sample), 0.0911 ppm (C, regional sample) 0.0872 ppm (D, personal sample), and 0.1106 ppm (E, regional sample), respectively. The temperature was measured above the exposure standard of 30.0°C in a newly established school on the ground floor (D); 31.9°C (D, regional sample). No values exceeding exposure limits were found for acetaldehyde, formaldehyde, acrylamide, benzene, respirable PM, CO, and noise. For CO, 28 ppm and 20 ppm were measured in local samples for 3 hours in (D) but 10.5 ppm and 7.5 ppm were measured in the 8hr-TWA, which were below the standard, and in the school (F) where fried meals were cooked on the day of measurement, the CO concentration was confirmed to be 48 ppm and 5 ppm for 3 hours of exposure but 18 ppm and 5 ppm were measured in the 8hr-TWA, which were below the standard.
Table 5
Workplace environmental monitoring results by school
Semi-basement (A), Newly established cafeteria in the semi-basement (B), Underground (C), Newly established school on the ground floor (D), Semi-basement, but fully equipped with electricity (E), Mainly prepared a fried food menu on the day of measurement (F).
PM: particulate matter; CO: carbon monoxide.
DISCUSSION
The study aimed to determine the LDCT results among school cafeteria workers and explore risk factors for its. The number of culinary workers who was identified as Lung-RADS-positive was 17 (10.2%), furthermore Category 4A, 4B and 4X were 4 (2.4%), 1 (0.6%) and 4 (2.4%). In a subgroup analysis of culinary workers, the use of electric plates and appliances as a heat source at home and poor ventilation at workplace increased the likelihood of Lung-RADS-positive. EGFR mutations are found in 50% of nonsquamous cell carcinomas in Asian populations and EGFR-targeted therapies are more effective in women, ADC, nonsmokers, and East Asians, thereby necessitating early detection.9,10,11 In a large descriptive study conducted at a single institution in South Korea, the incidence rates of interval cancer (94.6%), surgery (96.4%), and early-stage lung cancer (Stage 1 and Stage 2, 92.7%) among nonsmokers were significantly higher than those among smokers.16 To date, LDCT is the only screening test recommended for lung cancer screening. The National Lung Screening Trial (NLST), a large-scale randomized controlled trial conducted in the United States, provides evidence to support LDCT use for screening. The NLST trial compared lung cancer screening in Americans with a smoking history of at least 30 pack-years and no more than 15 years of smoking cessation in an LDCT screening group (26,713) and chest X-ray control group (26,722), and demonstrated a significant reduction in lung cancer mortality and overall mortality in the LDCT group.17 The Dutch-Belgian Randomized Lung Cancer Screening Trial, published in 2018, also demonstrated a reduction in lung cancer mortality.18
In 1997, the National Institute of Occupational Safety and Health estimated that occupational cancer accounted for 4% of all cancer-related deaths, and lung cancer accounted for 10% of all occupational cancer-related deaths.19 Occupations with a higher risk of lung cancer include welding, painting, foundry work, and mining.20 In about 25% of cases, lung cancer occurs in nonsmokers, and its causes include chronic inflammation, infections, family history, environmental exposure, and occupational exposures to substances such as asbestos, arsenic, and chromium.7,8,21
Cooking with high-temperature frying, stir-frying, and grilling recipes can produce COFs, which are adsorbed PAHs, VOCs, and formaldehyde on PM and ultra-fine particles (UFP).12 Previous reports have indicate that the chemical compositions of COFs can vary depending on the type of oil used, type of ingredient, and cooking method.14 Although the toxic mechanisms of COF remain unknown, a recent study demonstrated that oxidative stress and endoplasmic reticulum stress interact to cause lung injury in female rats.22
A study of the relationship between cooking fumes and lung cancer in Chinese women found a dose-response relationship with cooking time-years,13 and a study conducted on Norwegian cooks found that the incidence of respiratory symptoms was proportional to the extent to which frying was performed.23 When comparing the eating habits, it was found that the proportion of stir-fried dishes was low in Korea compared to China and Taiwan but the proportion of grilled or fried dishes was relatively high. The situation of food service workers in Korea is not considered to differ significantly from that of populations identified as being at high risk in epidemiologic studies conducted in Taiwan and China.24
In women, COFs are a risk factor for lung cancer, regardless of the individual’s smoking status, and the risk varies with the extent of ventilation.25 In this study, we also found a significant reduction in LDCT positive with both mechanical and window ventilation in a subgroup analysis of culinary workers. When validating ventilation facilities of school cafeteria in Ulsan, 30 schools showed 13 cases of inadequate hardware management of rooftop blowers (broken facilities, insufficient capacity, and non-injected lubricant oil) and 5 cases of poor software maintenance of facilities (poor cleaning and non-operation of ventilation facilities). Meta-analyses conducted in China have reported an increased risk of lung cancer when fume extractors are not used or ventilation is inadequate,4,25 and a study in Taiwan found that the long-term use of fume extractors reduced the risk of lung cancer by ≥ 50% in female nonsmokers, with the effect being greater with a higher frequency of cooking.13
Previous studies have shown that gas combustion in commercial settings has high concentrations of PM2.5, PM10, or VOC, NO, and CO than electricity.26,27,28 Nevertheless, in our study, there were significantly more LDCT-positive participants when electric induction was used at home; however, this may be due to the ventilation system, ingredients used during cooking, or recall bias. In other studies, UFP concentration is higher in gas combustion than in electricity in most cases when cooking for 5 minutes; however, it was found that electricity also produces a large amount of UFP, especially when cooking fatty foods, and the UFP is higher than that in gas combustion.29 This shows that fatty foods and oils are associated with the occurrence of UFP, and the UFP size is also affected by them. Per our findings, the difference in the total concentrations of PM10 and VOCs between heating sources varied depending on whether the cooking was done at home or in a restaurant, and that the concentration of PM10 was not affected by the heating source when home and restaurant cooking were combined.26
COFs generated during cooking are mixtures of a variety of compounds, including PAHs, formaldehyde, acetaldehyde, acrylamide, and acrolein. In this study, the working environment in the cafeteria of 6 schools was tested, and it was found that ozone and high-temperature work exceeded the standard. However, these 2 factors are not associated with lung cancer development, and values below the threshold were found for acetaldehyde, formaldehyde, acrylamide, benzene, respirable PM, CO, and noise; therefore, it was impossible to determine which of the compounds COFs influenced the lung cancer screening results. Workplace measurements in the cafeterias of 24 South Korean schools showed that while usual concentrations did not constitute a problem, cooking with oil-intensive recipes temporarily increased concentrations of formaldehyde, PAHs, acrolein, PM2.5, and CO.30 Previous reports have identified short-term, high-dose exposures, which is likely because the compositions and concentrations of COFs can vary depending on the type of oil used, cooking method, cooking temperature, and type of food.14 Despite the high cost and difficulty of conducting workplace studies, large-scale workplace measurements of cooking workers are required to access short-term exposures and the types and concentrations of COF components based on the type of work, ingredients used, cooking method, and time required.
This study has certain limitations. First, it is a cross-sectional study, which makes it difficult to establish causality; thus, well-controlled research such as cohort study is required. Second, the results are based on self-reported questionnaire, this may be subjected to recall biases. Third, monitoring in the same region did not identify any substances that contribute to lung cancer. Fourth, it does not take into account environmental exposures such as radon, asbestos, and exposure from nearby industrial facilities. Fifth, it was impossible to determine what level of protective mask was worn by study participants. Additionally, we categorized nutrition teachers as nonculinary workers who are more likely to be exposed to COFs than general office workers, whereas they should have been studied as a more appropriate comparison group. And due to limited sample size of the study, the CIs in the multivariate analysis were wide and the results may not be generalized.
Further research is required to investigate the number of meals or frequency of foods that can generate large amount of COFs. These factors are also taken into account when evaluating work-related lung cancer in Korea. Studies have reported associations between foods, oil, cooking methods, and number of meals with lung cancer.31,32 Irritants in COFs can induce respiratory symptoms such as nasal congestion, chronic cough, and breathing difficulty.33 According to a study, having ocular irritation symptoms is associated with an increased risk of lung cancer.32 So complaining symptoms, such as ocular or respiratory symptoms, should be further analyzed.
To the best of our knowledge, this is the first study to analyze LDCT findings in Korean culinary workers. When compared to nonculinary workers, we found a significantly higher number of Lung-RADS-positive individuals in the culinary group, with 4X being observed in 4 of them, and 2 of them were ADC. Retrospective cohort study of 4,365 nonsmoking women aged 40–74 years in South Korea, the initial LDCT positive rate was 6.8%, and in a study conducted in Taiwan, it was 3.6% (64 out of 1,763 asymptomatic men and women aged ≥ 40 years), which is lower than 8.4% in the entire study population and 10.2% among the culinary workers of this study.34,35 When comparing initial Lung-RADS results in this study with those of Korean cohort studies conducted on nonsmokers, despite differences in age and disease history, culinary workers in this study had a higher rate of Lung-RADS-positive than the rates found in both studies (Supplementary Table 2).16,34 The exposed group worked for a mean duration of 18.37 ± 4.91 years, whereas the unexposed group worked for longer. Other studies have suggested that the risk of lung cancer increases with the duration of cooking36; however, in this study, no lung cancer cases were diagnosed at the 6-month follow-up appointment, except for a 57-year-old woman with 17 years of cooking experience diagnosed with right upper lung ADC and underwent video-assisted thoracic surgery lobectomy 6 months before LDCT and a 57-year-old woman with 16 years of cooking experience who fell into Category 4X at screening and was later confirmed to have ADC via histology. Nonsmokers with lung cancer are more likely to have previously detected nodules that progress to cancer than to experience new interval cancer that was not initially detected.16 It is necessary to check not only LDCT-positive results but also the actual lung cancer incidence through follow-up examinations and conduct screening examinations for cooking workers who are not included in the screening population due to retirement or leaves of absence, and also to confirm the association between LDCT results and lung cancer incidence and duration of cooking work to confirm the dose-response relationship and confirm the association with lung cancer.
Besides COFs, culinary workers are exposed to heat, noise, musculoskeletal demands, and are at risk not only in the cafeteria but also in other areas of the workplace.37,38,39 Most of the research conducted on cooking and COFs so far has been conducted in China and Taiwan, and it is known that improper cooking conditions and combustion appliances are the problem.4,13,25 Studies of culinary workers in other large-scale cooking facilities such as hospitals and military bases, as well as smaller catering establishments with outdated equipment, should be conducted to identify appropriate lung cancer risk groups and maximize the cost-effectiveness of screening.
CONCLUSIONS
Although the workplace measures in this study did not identify factors that could influence Lung-RADS findings, there was a significantly higher rate of Lung-RADS-positive among culinary workers who performed actual cooking tasks compared to nonculinary workers. We analyzed lung cancer screening test results by occupation and found that occupational exposure to COFs can affect the development of lung cancer and that ventilation affects lung cancer screening results. If further analyses confirm the dose-response relationship between cooking fume exposure and Lung-RADS findings, including not only cafeteria workers but also other cooking workers, it will provide a basis for future work environment improvement measures for cooking workers and health promotion policies through specialized health examinations.
Acknowledgments
The authors thank Ms. Nang Jung Kim, from Occupational and Environmental Health Center in Ulsan University Hospital, for her informational assistance for this study.
-
Competing interests: The authors declare that they have no competing interests.
-
Author Contributions:
Abbreviations
ACR
American College of Radiology
ADC
adenocarcinoma
aOR
adjusted odds ratio
BMI
body mass index
CI
confidence interval
CO
carbon monoxide
COF
cooking oil fume
EGFR
epidermal growth factor receptor
GGN
ground glass nodule
LDCT
low-dose computed tomography
Lung-RADS
lung-imaging reporting and data system
NLST
National Lung Screening Trial
PAH
polycyclic aromatic hydrocarbon
PET-CT
positron emission tomography-computed tomography
PM
particulate matter
SCLC
small cell lung carcinoma
UFP
ultra-fine particles
VOC
volatile organic compound
8hr-TWA
8-hour total weight average
SUPPLEMENTARY MATERIALS
Supplementary Table 2
Comparing initial Lung-RADS results with those of a cohort study conducted on non-smokers in Korea
- 1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71(3):209–249. 33538338.ArticlePubMedPDF
- 2. Korean Central Cancer Registry. Annual Report of Cancer Statics in Korea in 2020. 16th ed. Ilsan, Korea: National Cancer Center; 2020.
- 3. Kim YC, Won YJ. The development of the Korean Lung Cancer Registry (KALC-R). Tuberc Respir Dis 2019;82(2):91–93.ArticlePubMedPMCPDF
- 4. Xue Y, Jiang Y, Jin S, Li Y. Association between cooking oil fume exposure and lung cancer among Chinese nonsmoking women: a meta-analysis. Onco Targets Ther 2016;9:2987–2992. 27284248.ArticlePubMedPMC
- 5. Jang SH, Sheen S, Kim HY, Yim HW, Park BY, Kim JW, et al. The Korean guideline for lung cancer screening. J Korean Med Assoc 2015;58(4):291–301.
- 6. Doll R, Hill AB. Smoking and carcinoma of the lung. Preliminary report.. Bull World Health Organ 1999;77(1):84–93. 10063665.PubMedPMC
- 7. Pallis AG, Syrigos KN. Lung cancer in never smokers: disease characteristics and risk factors. Crit Rev Oncol Hematol 2013;88(3):494–503. 23921082.ArticlePubMed
- 8. Corrales L, Rosell R, Cardona AF, Martín C, Zatarain-Barrón ZL, Arrieta O. Lung cancer in never smokers: the role of different risk factors other than tobacco smoking. Crit Rev Oncol Hematol 2020;148:102895. 32062313.ArticlePubMed
- 9. Bonanno L, Favaretto A, Rugge M, Taron M, Rosell R. Role of genotyping in non-small cell lung cancer treatment: current status. Drugs 2011;71(17):2231–2246. 22085382.ArticlePubMed
- 10. Thatcher N, Chang A, Parikh P, Rodrigues Pereira J, Ciuleanu T, von Pawel J, et al. Gefitinib plus best supportive care in previously treated patients with refractory advanced non-small-cell lung cancer: results from a randomised, placebo-controlled, multicentre study (Iressa Survival Evaluation in Lung Cancer). Lancet 2005;366(9496):1527–1537. 16257339.ArticlePubMed
- 11. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, Tan EH, Hirsh V, Thongprasert S, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 2005;353(2):123–132. 16014882.ArticlePubMed
- 12. International Agency for Research on Cancer. List of Classifications by Cancer Sites With Sufficient or Limited Evidence in Humans IARC Monographs Volumes 1-132a. Lyon, France: International Agency for Research on Cancer; 2022, 4–5.
- 13. Chen TY, Fang YH, Chen HL, Chang CH, Huang H, Chen YS, et al. Impact of cooking oil fume exposure and fume extractor use on lung cancer risk in non-smoking Han Chinese women. Sci Rep 2020;10(1):6774. 32317677.ArticlePubMedPMCPDF
- 14. Peng CY, Lan CH, Lin PC, Kuo YC. Effects of cooking method, cooking oil, and food type on aldehyde emissions in cooking oil fumes. J Hazard Mater 2017;324(Pt B):160–167. 27780622.ArticlePubMed
- 15. Chelala L, Hossain R, Kazerooni EA, Christensen JD, Dyer DS, White CS. Lung-RADS. version 1.1: challenges and a look ahead, from the AJR special series on radiology reporting and data systems. AJR Am J Roentgenol 2021;216(6):1411–1422. 33470834.PubMed
- 16. Kang HR, Cho JY, Lee SH, Lee YJ, Park JS, Cho YJ, et al. Role of low-dose computerized tomography in lung cancer screening among never-smokers. J Thorac Oncol 2019;14(3):436–444. 30445189.ArticlePubMed
- 17. Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, Fagerstrom RM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365(5):395–409. 21714641.ArticlePubMedPMC
- 18. De Koning H, Van Der Aalst C, Ten Haaf K, Oudkerk M. PL02. 05 Effects of volume CT lung cancer screening: mortality results of the nelson randomised-controlled population based trial. J Thorac Oncol 2018;13(10):S185.Article
- 19. Kang SK, Ahn YS, Chung HK. Occupational cancer in Korea in the 1990s. Korean J Occup Environ Med 2001;13(4):351–359.ArticlePDF
- 20. Consonni D, De Matteis S, Lubin JH, Wacholder S, Tucker M, Pesatori AC, et al. Lung cancer and occupation in a population-based case-control study. Am J Epidemiol 2010;171(3):323–333. 20047975.ArticlePubMedPMC
- 21. Riudavets M, Garcia de Herreros M, Besse B, Mezquita L. Radon and lung cancer: current trends and future perspectives. Cancers (Basel) 2022;14(13):3142. 35804914.ArticlePubMedPMC
- 22. Deng L, Ma Y, Ma P, Wu Y, Yang X, Deng Q. Toxic effect of cooking oil fume (COF) on lungs: evidence of endoplasmic reticulum stress in rat. Ecotoxicol Environ Saf 2021;221:112463. 34198188.ArticlePubMed
- 23. Svedahl SR, Hilt B, Svendsen K. Work environment factors and respiratory complaints in Norwegian cooks. Int Arch Occup Environ Health 2020;93(2):205–212. 31531780.ArticlePubMedPDF
- 24. Baek HY, Kim JS, Wen Y, Joung HJ, Li SJ. Comparative study on dietary patterns of Korean - Chinese and Koreans. Korean J Diet Cult 2001;16(4):341–353.
- 25. Jia PL, Zhang C, Yu JJ, Xu C, Tang L, Sun X. The risk of lung cancer among cooking adults: a meta-analysis of 23 observational studies. J Cancer Res Clin Oncol 2018;144(2):229–240. 29164315.ArticlePubMedPDF
- 26. To WM, Yeung LL. Effect of fuels on cooking fume emissions. Indoor Built Environ 2011;20(5):555–563.ArticlePDF
- 27. Wong TW, Wong AH, Lee FS, Qiu H. Respiratory health and lung function in Chinese restaurant kitchen workers. Occup Environ Med 2011;68(10):746–752. 21297152.ArticlePubMed
- 28. Zhao Y, Zhao B. Emissions of air pollutants from Chinese cooking: a literature review. Build Simul 2018;11(5):977–995.ArticlePDF
- 29. Dennekamp M, Howarth S, Dick CA, Cherrie JW, Donaldson K, Seaton A. Ultrafine particles and nitrogen oxides generated by gas and electric cooking. Occup Environ Med 2001;58(8):511–516. 11452045.ArticlePubMedPMC
- 30. Lee IJ, Lee SG, Choi BH, Seo HK, Choi JH. Hazard levels of cooking fumes in republic of Korea schools. Saf Health Work 2022;13(2):227–234. 35664910.ArticlePubMedPMC
- 31. Metayer C, Wang Z, Kleinerman RA, Wang L, Brenner AV, Cui H, et al. Cooking oil fumes and risk of lung cancer in women in rural Gansu, China. Lung Cancer 2002;35(2):111–117. 11804682.ArticlePubMed
- 32. Ko YC, Cheng LS, Lee CH, Huang JJ, Huang MS, Kao EL, et al. Chinese food cooking and lung cancer in women nonsmokers. Am J Epidemiol 2000;151(2):140–147. 10645816.ArticlePubMed
- 33. Juntarawijit Y, Juntarawijit C. Cooking smoke exposure and respiratory symptoms among those responsible for household cooking: a study in Phitsanulok, Thailand. Heliyon 2019;5(5):e01706. 31193378.ArticlePubMedPMC
- 34. Kim HY, Jung KW, Lim KY, Lee SH, Jun JK, Kim J, et al. Lung cancer screening with low-dose CT in female never smokers: retrospective cohort study with long-term national data follow-up. Cancer Res Treat 2018;50(3):748–756. 28724283.ArticlePubMedPMCPDF
- 35. Wu FZ, Huang YL, Wu CC, Tang EK, Chen CS, Mar GY, et al. Assessment of selection criteria for low-dose lung screening CT among Asian ethnic groups in Taiwan: from mass screening to specific risk-based screening for non-smoker lung cancer. Clin Lung Cancer 2016;17(5):e45–e56. 27133540.ArticlePubMed
- 36. Yu IT, Chiu YL, Au JS, Wong TW, Tang JL. Dose-response relationship between cooking fumes exposures and lung cancer among Chinese nonsmoking women. Cancer Res 2006;66(9):4961–4967. 16651454.ArticlePubMedPDF
- 37. Niu JW, Zheng XH, Zhang L, Xu SY, Li X, Guo SS, et al. Investigation of ergonomics in Chinese university cafeterias’ working situation at peak hours using jack. Proceeding of 2011 IEEE 18th International Conference on Industrial Engineering and Engineering Management; 2011 September 3–5; Changchun. New York, NY, USA: IEEE; 2011;p. 595–599.
- 38. Zhao K, Zhou X, Zhao B. Cooking generated particles’ impact on indoor air quality of university cafeteria. Build Simul 2010;3(1):15–23.ArticlePDF
- 39. Ierardi AM, Pavilonis B. Heat stress risk among New York City public school kitchen workers: a quantitative exposure assessment. J Occup Environ Hyg 2020;17(7-8):353–363. 32552608.ArticlePubMed
References
Figure & Data
REFERENCES
Citations
Citations to this article as recorded by 
PubReader
ePub Link
Cite
XML DownloadCooking oil fume exposure and Lung-RADS distribution among school cafeteria workers of South Korea
Cooking oil fume exposure and Lung-RADS distribution among school cafeteria workers of South Korea
| Characteristics | Exposed (n = 167) | Unexposed (n = 36) | ||
|---|---|---|---|---|
| Sex | ||||
| Female | 167 (100.0) | 36 (100.0) | ||
| Smoke | ||||
| Never-smoker | 167 (100.0) | 36 (100.0) | ||
| Passive smoking | 0.215 | |||
| Non-exposure | 153 (91.6) | 35 (97.2) | ||
| Exposure | 14 (8.4) | 1 (2.8) | ||
| Age (years) | 55.87 ± 3.58 | 48.19 ± 6.39 | 0.000*** | |
| BMI (kg/m2) | 23.57 ± 2.28 | 22.51 ± 2.77 | 0.015* | |
| Employment period (years) | 18.37 ± 4.91 | 20.97 ± 8.33 | 0.079 | |
| Mask-wearing | 0.004** | |||
| No | 47 (28.1) | 19 (52.8) | ||
| Yes | 120 (71.9) | 17 (47.2) | ||
| Cooking hour at home | 0.000*** | |||
| Less than 2 hours | 92 (55.1) | 34 (94.4) | ||
| More than 2 hours | 75 (44.9) | 2 (5.6) | ||
| Heat source at home | 0.006** | |||
| Gas combustion | 154 (92.2) | 27 (75.0) | ||
| Electric plates and appliance | 13 (7.8) | 9 (25.0) | ||
| Ventilation at home | 0.012* | |||
| Only a fan or a window | 12 (7.2) | 8 (22.2) | ||
| Both a fan and a window | 155 (92.8) | 28 (77.8) | ||
| Lung-RADS | Total (n = 203) | ||
|---|---|---|---|
| Exposed (n = 167) | Unexposed (n = 36) | ||
| Negative | 150 (89.8) | 36 (100.0) | 0.031* |
| Positive | 17 (10.2) | 0 (0.0) | |
| Characteristics | Lung-RADS- positive (n = 17) | Lung-RADS-negative (n = 150) | ||
|---|---|---|---|---|
| Passive smoking | 0.570 | |||
| Non-exposure | 16 (94.1) | 137 (91.3) | ||
| Exposure | 1 (5.9) | 13 (8.7) | ||
| Age (years) | 56.47 ± 3.36 | 55.81 ± 3.61 | 0.475 | |
| BMI (kg/m2) | 24.22 ± 1.94 | 23.50 ± 2.31 | 0.215 | |
| Employment period | 18.78 ± 5.96 | 18.33 ± 4.79 | 0.719 | |
| Mask wearing | 0.551 | |||
| No | 5 (29.4) | 42 (28.0) | ||
| Yes | 12 (70.6) | 108 (72.0) | ||
| Recipe | 0.538 | |||
| Oil-intensive recipes | 9 (52.9) | 91 (60.7) | ||
| Oil-free recipes | 8 (47.1) | 59 (39.3) | ||
| Ingredient | 0.892 | |||
| Fatty food (both fish and meat) | 9 (52.9) | 82 (54.7) | ||
| Low fatty food | 8 (47.1) | 68 (45.3) | ||
| Cooking hours at home | 0.400 | |||
| Less than 2 hours | 11 (64.7) | 81 (54.0) | ||
| More than 2 hours | 6 (35.3) | 69 (46.0) | ||
| Heat source at home | 0.132 | |||
| Gas combustion | 14 (82.4) | 140 (93.3) | ||
| Electric plates or appliance | 3 (17.6) | 10 (6.7) | ||
| Ventilation at home | 0.649 | |||
| Only a fan or a window | 1 (5.9) | 11 (7.3) | ||
| Both a fan and a window | 16 (94.1) | 139 (92.7) | ||
| Cooking at the workplace | 0.411 | |||
| Only cooking | 7 (41.2) | 47 (31.3) | ||
| With other work | 10 (58.8) | 103 (68.7) | ||
| Recipe with heat | 0.612 | |||
| Every day | 9 (52.9) | 89 (59.3) | ||
| Not every day | 8 (47.1) | 61 (40.7) | ||
| Ventilation at the workplace | 0.007** | |||
| Only a fan or a window | 5 (29.4) | 9 (6.0) | ||
| Both a fan and a window | 12 (70.6) | 141 (94.0) | ||
| Variables (Classification) | Crude model | Model 1 | |
|---|---|---|---|
| Heat source at home | |||
| Gas combustion | 1.00 (reference) | 1.00 (reference) | |
| Electric plates and appliance | 3.00 (0.738–12.194) | 4.59* (1.061–19.890) | |
| Ventilation at home | |||
| Both a fan and a window | 1.00 (reference) | 1.00 (reference) | |
| Only a fan or a window | 0.79 (0.096–6.524) | 0.17 (0.015–1.863) | |
| Ventilation at the workplace | |||
| Both a fan and a window | 1.00 (reference) | 1.00 (reference) | |
| Only a fan or a window | 6.53** (1.885–22.602) | 14.89*** (3.296–67.231) | |
| Place | Acetaldehyde | Formaldehyde | Acrylamide | Benzene | Ozone | PM | Heat | CO | Noise |
|---|---|---|---|---|---|---|---|---|---|
| (A) | - | 0.0063 | - | - | 0.0471 | 0.0755 | 27.9 | - | 73.0 |
| (B) | - | 0.005 | - | - | 0.0768 | 0.1971 | 23.8 | - | 79.7 |
| (C) | - | 0.0234 | - | - | 0.0954 | 0.1999 | 23.4 | - | 74.9 |
| (D) | - | 0.0015 | - | 0.01475 | 0.0872 | 0.1614 | 31.9 | 10.5 | 70.5 |
| (E) | 0.0094 | 0.0016 | - | 0.1521 | 0.1106 | 0.1707 | 21.9 | - | 74.2 |
| (F) | 0.0135 | 0.0028 | - | - | - | 0.0631 | 26.9 | 18 | 67.0 |
Table 1 Baseline characteristics of participants according to work
Values are presented as number (%) or mean ± standard deviation. The
BMI: body mass index.
*
Table 2 Lung-RADS distribution of participants according to work classification
Values are presented as number (%). The
Lung-RADS: lung-imaging reporting and data system.
*
Table 3 Baseline of characteristics of subgroup (culinary workers)
The
Lung-RADS: lung-imaging reporting and data system; BMI: body mass index.
**
Table 4 The adjusted odds ratios and 95% confidence intervals for the associations between different variables with lung-imaging reporting and data system-positive in subgroup analyses
Bold fonts refer to statistically significant results. The adjusted odds ratio was calculated via binomial logistic regression analyses (Model 1: adjusted for passive smoking, age, BMI, employment period, wearing a mask before COVID-19, recipe, ingredient, cooking hours at the home, cooking at the workplace, recipe with heat). There is no statistical significance in binomial logistic regression analyses of the entire study population (passive smoking, age, BMI, employment period, wearing a mask before COVID-19, cooking hours at the home, heat source at the home, ventilation at the home, work classification).
BMI: body mass index; COVID-19: coronavirus disease 2019.
*
Table 5 Workplace environmental monitoring results by school
Semi-basement (A), Newly established cafeteria in the semi-basement (B), Underground (C), Newly established school on the ground floor (D), Semi-basement, but fully equipped with electricity (E), Mainly prepared a fried food menu on the day of measurement (F).
PM: particulate matter; CO: carbon monoxide.
