Risk assessment of personal exposure to polycyclic aromatic hydrocarbons and aldehydes in three commercial cooking workplaces

Cooking-related emissions are associated with environmental pollution and adverse health effects. Of the various chemical species emitted during cooking, polycyclic aromatic hydrocarbons (PAHs) and aldehydes are two chemical species with carcinogenic or tumor promoting characteristics. Although PAH exposure has been studied in commercial kitchen workers, few studies have investigated simultaneous exposure to PAHs and aldehydes in these workers. The aims of this study were to compare personal concentrations of PAH and aldehyde in three commercial cooking workplaces and to estimate their corresponding cancer risks. The three cooking workplaces included western fast food restaurant kitchens, Chinese cafeteria kitchens, and street food carts. Comparisons showed that workers in western fast food restaurant kitchens and Chinese cafeteria kitchens tended to have lower personal concentrations of these pollutants compared to workers in street food carts. The geometric mean (95% CI) cancer risks in the three workplaces were, from lowest to highest, 1.36 (1.12–1.67) × 10−5 for western fast food restaurant kitchens, 1.52 (1.01–2.28) × 10−5 for Chinese cafeteria kitchens, and 3.14 (2.45–4.01) × 10−5 for street food carts. The percentage contributions of aldehyde species to cancer risk were very high (74.9–99.7%). Street food cart workers had high personal exposure to aldehyde probably due to lack of effective exhaust systems. Thus, their cancer risk was significantly higher than those of workers in western fast food restaurant kitchens (p < 0.001) and Chinese cafeteria kitchens (p = 0.013).


Results
Area air concentrations. The geometric mean (GM) concentration of total PAH was substantially higher in the street food cart group (8790.2 ng/m 3 ) compared to the Chinese cafeteria kitchen and western fast food restaurant kitchen groups (3721.1 and 3171.0 ng/m 3 , respectively). Most PAHs were 2-ring or 3-ring PAHs, which have lower toxic equivalent factors compared to other PAHs. The most potent carcinogen, benzo(a)pyrene, was only detected in the barbecue stand and in the popcorn chicken stand. Analyses of total aldehyde revealed GM concentrations of 163.6, 222.8, and 233.7 μg/m 3 in western fast food restaurant kitchens, Chinese cafeteria kitchens and street food carts, respectively ( Table 1). The aldehyde analyses showed that the three workplaces had similar aldehyde concentration profiles. The most abundant aldehydes were hexaldehyde and nonanal ( Supplementary  Fig. S1).
Personal exposure concentrations. In the western fast food restaurant kitchens and Chinese cafeteria kitchens, half of the participants were female. In the street food carts, however, only one participant was female. No fume extractors were used in street food carts. The prevalence of personal protective equipment and fume extractors differed among the three working environments. The number of working years was shorter in the western fast food restaurant kitchen group compared to the other two groups ( Table 2). Table 3 shows personal exposure results. In western fast food restaurant kitchens, Chinese cafeteria kitchens and street food carts, the respective GM concentrations of total PAH were 558.5, 4943.1, and 4576.1 ng/m 3 , and the respective GM concentrations of total aldehyde were 67.6, 62.1 and 165.3 μg/m 3 . In terms of PAH ring number wise distribution, the most frequently detected in the three workplaces were two-ring PAHs (78.2-92.3%) followed by three-ring PAHs (6.7-21.3%) and four-ring PAHs (0.4-1.8%) ( Supplementary Fig. S2). The three workplaces significantly differed in personal exposure to naphthalene, acenaphthylene, fluorene, anthracene, total PAH, and total BaP eq (p-values 0.006, <0.001, <0.001, 0.020, 0.002, and <0.001 respectively, Supplementary Table S1). In post hoc analysis, the largest differences in PAH concentrations were observed in comparisons between western fast food restaurant kitchens and Chinese cafeteria kitchens and between western fast food restaurant kitchens and street food carts. The aldehyde analyses showed that the three workplace types significantly differed in formaldehyde, acrolein, crotonaldehyde, valeraldehyde, hexaldehyde, t-2-heptenal, t,t-2,4-DDE, nonanal and total aldehyde (p-value range < 0.001-0.018, Supplementary Table S1). Post hoc analysis showed that the largest differences in aldehyde concentrations were observed in comparisons between western fast food restaurant kitchens and street food carts and between Chinese cafeteria kitchens and street food carts. Personal exposure to aldehyde was higher in the street food cart group compared to the other two groups.

Discussion
Exposure concentrations and cooking methods. Workplace selection was based on cooking methods which generate substantial air pollutants, such as frying or barbecuing. Several studies reported these two cooking methods produced more pollutants than the other cooking methods did. For example, Yao, et al. 7 reported that deep frying generates more PAHs compared to pan frying because deep frying uses oil at a hotter temperature and in a larger amount. In Zhao, et al. 2 study, a comparison of night market stalls revealed that total PAH levels were highest in a barbecue food stall (43.145 μg/m 3 ). The low indirect heat from burning charcoals used for barbecue cooking can result in incomplete combustion, which is the main mechanism of PAH formation 22 .
The BBQ stand was the only workplace using charcoal as its cooking fuel. Several studies reported that solid fuel use is a significant source of particulate matters and PAHs 10,23,24 . Our findings confirmed the results from the previous studies and showed that the BBQ stand had the highest PAH levels of the investigated workplaces; while its aldehyde level was moderate (Table S3). The highest personal aldehyde levels were found in the popcorn chicken and chicken steak stands which used deep frying as their cooking method. Our findings of aldehyde emissions were similar to those found in Ho et al. study 25

Comparison between area and personal concentrations. Correlation coefficients between area and
personal GMs for individual workplace measurements were 0.650 (p = 0.058) and 0.383 (p = 0.308) for total PAH and total aldehyde, respectively (Table S3). PAH results showed a moderate correlation with a marginal trend toward significance, while aldehyde results showed no association. A possible explanation for marginal or no associations between area and personal measurements shows as follows. Area measurements were based on samples taken at fixed sites near the stoves whereas personal measurements were based on samples taken from workers who tended to move among various locations throughout the workday. For example, a single worker  may have been sampled while in the cooking area, in the preparation area, in the dish-washing station, or in the rest area. Therefore, the carcinogenic risk estimation from personal sampling was more representative compared to those from area samples, which were often used to assess the carcinogenic potencies of cooking emissions in previous studies 10,26,27 . Area concentrations. Table 4 32 . Notably, some studies have also reported PAH concentrations in terms of BaP eq concentrations to evaluate their carcinogenic potencies. The range of BaP eq concentrations measured in the current study was 0.001-0.372 μg/m 3 whereas previous studies have reported ranges of 0.041-0.233 μg/m 3 for cooking emissions from five family kitchens in Taiwan 9 , 0.023 μg/m 3 for ion casting emissions in a foundry plant 31 , and 0.20-10.87 μg/m 3 in emissions from coke plants 30 . Table 1 shows that the range of total aldehyde concentrations in the three cooking workplaces was 18.7-946.0 μg/m 3 . Concentrations reported in the literature include 159-3095 μg/m 3 for 13 aldehydes in commercial kitchens 25 , mean concentrations of 185-241 μg/m 3 for six aldehydes in residential kitchens 33 , and 21-170 μg/m 3 for 18 carbonyl compounds in five commercial kitchens 27 . Thus, our data were again consistent with the literature. The aldehyde profile in this study showed high concentrations of hexaldehyde, t,t-2,4-DDE and nonanal detected in COFs, which was consistent with that reported in Peng et al. 34 .
Personal concentrations. Personal concentrations of total PAH measured in the 22 workers in the three commercial cooking workplaces investigated in this study ranged from 0.06 to 14.6 μg/m 3 (Table 4). Zhao, et al. 2 reported total PAH in a range of 23.4-44.2 μg/m 3 in cooks at Taiwan night markets ( Table 4). As expected, our data for the street food cart workers were consistent with those reported for night market workers due to their similar cooking conditions. In earlier studies of occupational exposure, mean personal concentrations of total PAH were 0.99 and 6.95 μg/m 3 for side-oven workers and topside-oven workers in a coke plant 35 , respectively, and 5.05 μg/m 3 for traffic policemen 36 (Table 4). However, the PAHs measured in our study and for traffic policemen were predominantly 2-ring and 3-ring PAHs whereas PAHs measured in coke oven plants were predominantly 5-ring and 6-ring PAHs, which have a higher toxicity and potency. Mean total BaP eq was also assessed to account for the different toxicities and potencies of PAHs. Mean total BaP eq concentration were 0.004 μg/m 3 in the current study. In contrast, the BaP eq concentrations reported previously were 0.18 μg/m 3 for coke side-oven workers, 1.57 μg/m 3 for coke topside-oven workers, and 0.082 μg/m 3 for traffic policemen. Therefore, both total PAH and BaP eq concentrations should be investigated and compared to clarify their sources and toxic potencies.
Personal concentrations of the 13 aldehydes measured in this study ranged from 37.7 μg/m 3 to 322.2 μg/m 3 . In contrast with many studies of personal exposure to PAHs, studies of personal exposure to aldehydes are rare. One example is Svendsen, et al. 37 , who reported total personal concentrations of formaldehyde, acetaldehyde and acrolein ranging from 8-186 μg/m 3 in restaurant kitchens in Norway. Another study of three restaurant kitchens Incremental lifetime cancer risk. The ILCR from exposure to cooking emissions ranged from 8.04 × 10 −6 to 3.60 × 10 −5 (Table S4). Eighteen (18/22 = 82%) workers in this study had an ILCR higher than 1 × 10 −5 . The percentage contribution to cancer risk was much higher for aldehydes (range, 74.9-99.7%) than for total PAH (range, 0.3-25.1%). The three commercial cooking workplace types had similarity in cooking method (frying) and cooking oil (palm oil and soybean oil). Emissions from western fast food restaurant kitchens and Chinese cafeteria kitchens were regulated by Taiwan's Air Pollution Control Act 39 . Under the Act, these kitchens needed to install air pollution control devices, maintain the devices under workable conditions, clean the devices regularly, and meet the emission standards. Street food carts had an exception from the Taiwan's Air Pollution Control Act due to their small scale (capital investment < NT$ 100,000, and workplace area < 100 m 2 ). This lead to air pollutants from street food carts uncontrolled. This could be the reason that workers in the street food cart group had significantly higher overall ILCRs compared to workers in the other two groups. One of the notable differences of these three types was exhaust systems. There was no effective mechanical exhaust systems in the street food    37 found that concentrations of fat aerosols and aldehyde concentrations were highest in kitchens with insufficient exhaust systems; another study by Yu, et al. 9 similarly reported high PAH concentrations in kitchens with poor ventilation. Although the open air environment of street food carts enables rapid dispersal of pollutants, cooking emissions were higher in the street food cart group compared to the other two groups probably because street food carts are rarely equipped with fume extractors or other exhaust systems for collecting and removing pollutants from breathing zones. Additionally, other factors, such as equipment type, maintenance, cooking space etc. may be potential contributors for high PAH and aldehyde concentrations of street food cart workers. In the literature, reported ranges of estimated cancer risk related to cooking emissions include 2.5 × 10 −6 -1.4 × 10 −5 for household cooking emissions 9  Aldehyde species are dominant chemical species in cooking-related emissions. The low carbon number aldehydes formaldehyde and acetaldehyde are confirmed and probable carcinogens, respectively 6 . Some high carbon number aldehydes also showed carcinogenic effects. For example, Wu, et al. 21 reported that some high carbon number aldehydes (e.g., t,t-2,4-DDE, t,t-2,4-nonadienal, t-2-decenal and t-2-undecenal) were potent mutagens. The aldehyde t,t-2,4-DDE promotes cancer by inducing cancer cell proliferation and by inhibiting anti-oxidant enzyme activities 19,[42][43][44] . However, data are insufficient for their classification as probable or possible carcinogens. High carbon number aldehydes were not be able to include in the risk analyses in the current study. Notably, the cancer risk might be even higher than the estimated values.
Limitations and strengths. This study has several limitations. First, since the street food carts were located on the roadside, vehicular emissions may have resulted in overestimated cooking emissions. On the other hand, the street food carts analyzed in this study were located on a street with a low traffic volume of ~5600 vehicles per day (Directorate General of Highways, 2014) 45 . The estimated total PAH emission of this traffic volume was 0.232 μg/m 3 based on Ho, et al. 46 findings which indicated total PAH emission of 2.211 μg/m 3 at the traffic volume of 53000 vehicles per day. Therefore, the influence of automobile exhaust on these workplaces was probably limited. Nevertheless, future studies should recognize and control for the effects of traffic emissions when investigating cooking workplaces located on or near the roadside. Second, the findings of this study cannot be generalized to all commercial cooking workplaces because the analysis was limited to small or medium sized workplaces in which the primary cooking method was frying or barbecuing. For a comprehensive study of the PAH and aldehyde levels in cooking workplaces and for estimates of cancer risks in populations with high exposure to cooking-related emissions, future studies should include analysis of large-sized cooking workplaces, which may differ in terms of number and type of cooking activities, and in terms of the number of workers. Third, the small sample size precluded assessment of other contributing factors in exposure to PAH and aldehyde (e.g., cigarette smoking and cooking oil type). The small sample size also precluded assessment of gender-specific exposure and gender-specific cancer risk in the three groups. Further gender-specific analyses are needed because COF exposure associated with lung cancer in nonsmoking women. Despite the small sample size, however, this study demonstrated a significantly higher cancer risk in street food cart workers compared to workers in the other two groups. This study is the first to estimate the cancer risk of personal exposure to both PAHs and aldehydes in cooking workplaces. The estimation was more representative of human exposure compared to previous studies that have used area samples to assess the carcinogenic potencies of cooking emissions 10,26,27 . This study investigated occupational exposure to cooking-related emissions and revealed that workers in the street food cart group had the highest ILCRs. Notably, aldehyde species were the main contributors to cancer risk. Although the street food cart group belongs to the small-scaled workplaces, it accounts for one third of all cooking workplaces, and the cooking emissions from street food carts affect not only workers, but also people in nearby areas. The considerable emissions generated from street food carts is problematic not only in Taiwan, but in many countries throughout the world. The data in this study suggest that cooking emissions and exposure from street food carts can be effectively controlled by installing mechanical exhaust systems and maintaining them in good condition.

Methods
Workplace selection and sampling strategy. The three commercial cooking workplace types analyzed in this study were kitchens in western fast food restaurant chains (main product: fried chicken), kitchens in cafeteria-style Chinese restaurant chains, and street food carts. These workplace types were selected for analysis because the cooking methods that they use (frying or barbecuing) are known to generate substantial air pollutants 23,34 . Additionally, western fast food restaurant kitchens, cafeteria-style Chinese restaurant kitchens, and street food carts account for most of the commercial cooking workplaces in Taiwan (10%, 21%, and 32% of respectively) 47 . These cooking workplaces are associated with high personal exposure to cooking-related emissions. Table 5 shows the characteristics and sample sizes of the three cooking workplace types. The analysis included three restaurants or vendors in each of the three groups. All western fast food restaurant kitchens and Chinese cafeteria kitchens analyzed in this study followed Taiwan's Air Pollution Control Act 39 ; which regulated COFs of commercial kitchens by installing exhaust ventilation systems (hoods, ducts, air cleaning devices, and fans) above the frying units or stoves (Supplementary Fig. S3), maintaining the exhaust systems under workable conditions, and cleaning the system regularly. Street food carts were not obligated to install air pollution control devices due to their small scale in terms of capital investment and working counter area (1.5-3.0 m 2 ), while some used  wall-mounted fans to increase general ventilation ( Supplementary Fig. S4). The room inside the cart was used for storage and to house the cooking machinery. Workers stood outside of the carts to prepare food. Between September 4, 2014 and November 1, 2014, area and personal samples were collected to determine concentrations of PAHs and aldehydes ( Supplementary Fig. S5). For each restaurant or vendor, all samples were collected for 8 h on the same day. Area samples were collected in the kitchen area or other working area at a height of 1.5 m to represent the breathing zone of a worker in a standing position. One to three area samples were taken at each restaurant or vendor; thus, five, six and seven samples were taken in western fast food restaurant kitchens, Chinese cafeteria kitchens, and street food carts. Personal samples were taken from workers who were responsible for cooking. The recruited workers included twelve western fast food restaurant kitchen workers, six Chinese cafeteria kitchen workers, and four street food cart workers (Table 5). All subjects gave written informed consent to participate before the study was performed. Each participating worker wore two personal samplers (one for PAHs and one for aldehydes) and completed questionnaires regarding personal demographic data and characteristics pertinent to this study, including lifestyle (e.g., tobacco and alcohol consumption), occupational history (e.g., work history, periods of employment, cooking method used, and protective equipment used), and health status (e.g., chronic disease, respiratory disease). The study protocol (IRB number: KMUH-IRB-990191) received ethical approval by the Institutional Review Board of Kaohsiung Medical University Hospital (IRB-KMUH). The study was performed in accordance with the guidelines and regulations of the IRB-KMUH. Names and other personal information that could be used to identify participants were excluded from the manuscript, including Supplementary Information. Sampling and analysis methods. This study targeted the 16 PAHs prioritized for control by the United States Environmental Protection Agency (Supplementary Table S5) due to their high toxicity and high potential for human exposure. Particulate matter was collected with a Teflon filter (25 mm × 2 μm pore size, Pall Corporation, Port Washington, New York, USA) in an IOM (Institute of Occupational Medicine, Edinburgh, U.K.) sampler, and gaseous PAHs were collected with a polyurethane foam cartridge (ORBO ™ 1000, 22 mm (OD) × 7.6 cm (L), Supelco, Bellefonte, Pennsylvania, USA). Particulate-and gas-phase PAHs were simultaneously collected with a specially designed single-pump sampling train. The IOM sampler had a Teflon filter in the front section of the sampling train. One tube was connected to a polyurethane foam cartridge, and another tube was connected to a flow regulator. The two tubes converged at a tee fitting connected to a pump 34 ( Supplementary  Fig. S6). The flow regulator was adjusted to obtain the flow rates required by the particulate-and gas-phase sampling devices (2 L/min and 1 L/min, respectively). The flowrates were measured and confirmed by an air flow calibrator (Defender 510, Mesa Laboratories, Inc., Butler, NJ, USA). Collected samples were extracted using a 1:1 mixture of acetone and hexane in a microwave extraction system (START E, Milestone, Shelton, CT, USA) 24,48 . After extraction, the samples were analyzed by a gas chromatograph/mass spectrometer (Trace GC Ultra/DSQ II MS, Thermo Fisher Scientific, Waltham, Massachusetts, USA). The PAHs were separated with a capillary gas chromatography column (Equity ® -5, 30 m × 0.25 mm × 0.25 μm, Supelco, Bellefonte, Pennsylvania, USA) with a temperature program. The analytical quality controls for the 16 PAHs are shown in Supplementary Table S5.
The thirteen aldehydes selected for analysis in this study (Supplementary Table S6) were targeted because they have raised health concerns (e.g., formaldehyde and acetaldehyde) or because their chemical characteristics are representative of COFs 34 (e.g., nonanal and t,t-2,4-DDE). The sampling train used to collect aldehydes was identical to that used to collect PAHs, i.e., an IOM sampler with a DNPH-coated glass fiber filter (  pore size, Supelco, Bellefonte, Pennsylvania, USA) and a 2,4-DNPH cartridge (Supelco, Bellefonte, Pennsylvania, USA) were connected in series for particulate-and gaseous-phase aldehyde sampling. After sample collection, the samplers were stored at 4 °C in sealed aluminum bags until extraction. Samples were extracted by acetonitrile and then analyzed with a high performance liquid chromatograph (PU-2089, Jasco, Japan) equipped with an ultraviolet detector operated at 360 nm (Varian ProStar 320, Varian, USA). A reverse phase column (Ascentis ® RP-Amide Column, 5 μm, 250 × 4.6 mm, Supelco, Bellefonte, Pennsylvania, USA) with a gradient mobile phase of acetonitrile/water was used to separate aldehydes. The gradient program was performed at a flowrate of 1.2 ml/ min as follows: start with an acetonitrile/water ratio of 40/60 for 1 min, increase acetonitrile from 40% to 90% within 49 min, hold for 3 min, and decrease acetonitrile from 90% to 40% within 12 min. The analytical quality controls for the 13 aldehydes are shown in Supplementary Table S6