Abstract
In the present study, the concentration of 13PAHs and the six indicator PCBs was determined through GC-MS/MS in 36 grilled and fried fish products. The study is unique in terms of the simultaneous determination of two types of persistent organic pollutants in grilled and fried fish products. The concentration of ∑13PAHs and ∑6PCBs in these samples varied from 20.80 ± 2.06–947.65 ± 40.85 µg kg−1 and 2.86 ± 0.16–46.52 ± 0.46 µg kg−1, respectively. Dietary exposure and human health risks due to the consumption of fried and grilled fish products for flexitarians, fish-eating population and the entire population were assessed. The incremental lifetime cancer risk (ILCR) estimates for the flexitarians, the entire population, and fish-eating population associated with dietary intake of these products ranged from 4.68 × 10−5 to 1.32 × 10−3, 1.06 × 10−3 to 2.97 × 10−2 and 1.46 × 10−3 to 4.12 × 10−2 respectively. Furthermore, the cancer risk of grilled and fried fish products assessed for the fish-eating population was compared with the cancer risk of raw fish calculated based on the peer-reviewed Indian literature. The mitigation strategies for reduction of PAHs and PCBs in defined fish products have been recommended in the study. The study also highlights the need for in-depth research on PAHs and PCBs formation in grilled and fried fish products.
Keywords: PAHs, PCBs, GC-MS/MS, Incremental lifetime cancer risk (ILCR), Hazard Index (HI)
Graphical Abstract
Highlights
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Grilled & fried fish samples were compared for PAHs and PCBs contamination levels.
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Coal grilled fish samples showed highest levels of PAHs.
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Levels of BaP in all the samples were found to exceed the EU limit (2 µg kg−1).
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The ILCR for fish eating population ranged from 1.46 × 10−3 to 4.12 × 10−2.
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HI of PCBs for fish eating population was found exceeded (>1) in 66.67 % samples.
1. Introduction
Fish and fish product consumption is vital for many health benefits due to their high-quality proteins and essential amino acids. However, fish (wild as well as farmed fish) are exposed to a number of contaminants like polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) present in the water during growth [10], [64], [8], [86]. Polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) are two different kinds of bio-accumulative, persistent organic pollutants (POPs) having carcinogenic and toxic properties [31].
PAHs, ubiquitous pollutants, are produced when organic materials burn incompletely during both natural and man-made activities like volcanic eruptions, forest fires, waste and biomass burning, vehicle use, coke production, and thermal industrial processes [70]. There are hundreds of PAHs present in nature. However, the United States Environmental Protection Agency (USEPA) has listed sixteen of them as the most priority ones to be analyzed and monitored in environmental matrices due to their potential nature of carcinogenicity, immunotoxicity, mutability, teratogenic and endocrine-disrupting property [23], [35], [37], [52], [78]. The listed sixteen PAHs (priority PAHs) are benzo[a]anthracene (BaA), benzo[b]fluoranthene (BbF), benzo[k]fluoranthene (BkF), benzo[a]pyrene (BaP), benzo[ghi]perylene (BghiP), dibenz[a,h]anthracene (DahA), indeno[1,2,3-cd]pyrene (IcdP), chrysene (Chry), naphthalene (Nap), acenaphthylene (Acy), acenaphthene (Ace), fluorene (Fl), phenanthrene (Phe), anthracene (Ant), fluoranthene (Flu), and pyrene (Pyr). The EPA listed these sixteen PAHs in the 1970s [78], [98]. Among sixteen PAHs, benzo[a]pyrene was considered as a marker of carcinogenic PAHs in food for a long time [81]. However, PAH4 (BaP, BbF, Chry, and BaA) and PAH8 (PAH4 in addition to BkF, BghiP, DahA, and IcdP), defined by the European Food Safety Authority (EFSA), are more accurate indicators than considering BaP alone [100], [20]. PAH4 and PAH8 both are now generally used as appropriate indicators to monitor the occurrence and carcinogenic potency of PAHs in food [87]. The European Union (EU) has set maximum tolerable levels (MLs) for BaP as 2 µg kg−1 and for 4PAHs as 12 µg kg−1 [25]. However, FSSAI has set the maximum tolerable levels for BaP as 5 µg kg−1for smoked fishery products [29].
PCBs are not formed during cooking practices [57]. The surface of aquatic bodies is an important route for the deposition of these compounds and further concentration in the food chain. The minerals and organic particles/sediments in aquatic bodies absorb these compounds due to their hydrophobic nature, from where PCBs are consumed by fishes via gills with food. These contaminated fishes are mainly responsible for dietary exposure to PCBs in humans [50]. Mainly, seafood and dairy products are responsible for greater than 90 % of PCB exposure in humans [19], [39]. There are total 209 congeners of PCBs categorized as dioxin-like PCBs (DL-PCBs) and non-dioxin-like PCBs (NDL-PCBs) [3]. Both categories are potential food contaminants. Seven congeners (ΣPCB7-PCBs 118, 138, 153, 28, 52, 101, and 180) among 209 congeners identified by the International Commission for the Exploration of the Seas (ICES) and the European Commission [26] are commonly known to determine the total PCB burden in environmental as well as tissue and food samples [71]. The sum of six indicator PCBs (138, 153, 28, 52, 101, and 180) comprises about 50 % of the total NDL-PCBs present in food. These six indicator PCBs (ΣPCB-6) are appropriate indicators of human exposure to NDL-PCBs [21]. The presence of PCBs in food is primarily responsible for many human health abnormalities due to their reprotoxic, endocrine, neurotoxic, immunotoxic, and carcinogenic nature [4], [48]. The EU has set maximum tolerable levels (MLs) for ΣPCB-6 as 75 ng g−1 wet weight in the fish muscle meat and fishery products [26]. However, FSSAI has set the maximum tolerable levels for six indicator PCBs in inland and migratory fish as 2.0 mg kg−1 and 0.5 mg kg−1 in marine fish [29].
Fish must be cooked before consumption by humans. Indeed, cooking practices such as frying and grilling with a perfect blend of cooking ingredients at an optimal temperature and moisture can provide delicious tastes and textures in food ([66], [92]; Lu et al., 2018; [43]; Mubeen et al., 2020; [17]). In contrast, these thermal processing practices of food, such as roasting, smoking, toasting, barbequing, frying, and grilling, are becoming major health concerns in humans due to the formation of high levels of PAHs in food ( [99], [62], [72], [80], [88]).
Most humans consume seafood products, especially fish, due to their high-quality nutritional values [65]. In per capita terms, worldwide food fish consumption rose from 9.0 kg (live weight equivalent) in 1961–20.3 kg in 2017, increasing at an average rate of about 1.5 percent per year [27]. It has doubled in the last 50 years, and dietary recommendations include a significant increase in fish consumption [90]. India is a fast-growing country with a developing economy where people are shifting toward easy and nutritious food. Therefore, the demand for fish is expected to increase in the future. India is the third largest fish-producing country in the world, with 8 % of global production. India has a total fish production of 162.48 lakh tonnes with a 10.34 % annual growth rate. The annual per capita fish consumption for the entire population of India is 8.89 kg, whereas it was found to be 12.33 kg for the fish-eating population [34]. However, as per NSSO surveys in 2011, per capita consumption of fish in the Delhi NCR region was estimated to be 4.04 kg/annum. It was found that fish was more consumed non-vegetarian food items than chicken and mutton. The projected fish consumption (up to 2020) was estimated at 5.11 kg/capita/annum with an annual average growth of 2.26 % [47].
As previously stated, PCBs are synthetic POPs that can accumulate in fish from a contaminated aquatic environment. In contrast, the contamination of PAHs in fish products occurs through aquatic conditions and thermal processing, and they can cause serious issues to human health. Consequently, it is crucial to investigate the levels of PAHs and PCBs in edible fish tissues and effect of thermal processing such as grilling on the levels to ensure food safety for the human population. Based on the peer-reviewed literature, we hypothesize that grilled fish products will have higher levels of PAHs as compared to fried fish products. Consequently, consumers of grilled products will be at a higher risk of exposure to the health hazards of PAHs. However, in case of PCBs, fried products are likely to have higher concentrations and consequent health risk.
Worldwide, most of the published literature reports levels of PAHs or PCBs separately in cooked fish products. In the Indian context, the contamination of PAHs and PCBs has been predominantly documented in unprocessed raw fish samples, and no study has been conducted on the levels of PCBs in processed fish products. However, only a few studies on the contamination of PAHs in Indian processed fish products show a paucity of data in this field. Correspondingly, in the Indian context, the information on the cancer risk associated with consuming fish products is also scanty. To fill this gap, the present study was conducted to determine the levels of PAHs and PCBs simultaneously in grilled and fried fish products. Additionally, the dietary exposure to flexitarians (people who occasionally eat meat or fish), the fish-eating population, and the entire population due to consumption of these products was determined. Furthermore, the incremental lifetime cancer risk was also assessed based on their daily consumption pattern.
2. Material and methods
2.1. Sampling and sample preparation
The present study was undertaken in the Delhi-NCR region, India. The sampling site selection was based on the availability of fish food products at restaurants and street vendors in the study region. From each location, at least 2–3 restaurants and street vendors selling grilled/fried fish products were randomly selected. The samples and sampling locations are depicted in the given map (Fig. 1). The study’s objective was to estimate a typical dietary exposure pattern of PAHs & PCBs through fried and grilled fish products available in Delhi-NCR commercial settings (restaurants and street markets). The selected locations for sampling were chosen because they represented an indicative food environment of such settlements. A questionnaire survey (online and offline) was carried out from October 2022 to April 2023 to estimate the intake level of PAHs and PCBs through fish consumption in the study population. The adults (flexitarians) engaged in fried and grilled fish purchases in these locations were selected as survey participants (N = 74). The selected participants were adults who frequently consume fried and grilled fish only from the market. To assess the exposure to PAHs and PCBs through fish products’ intake across the population groups, the entire population and the fish-eating population were also included for which the per capita consumption rate was taken as reported by the Indian Council of Agricultural Research (ICAR & world fish, 2023). Based on findings of survey and data taken from the ICAR, the risk assessment was carried out.
Fig. 1.
Map of Delhi-NCR sampling locations. Note: Where sample codes having * denote samples from restaurants, in sample codes the first two letters represent fish species, the third letter denotes cooking method, and numbers represent the location and number of samples per location. For example, PBG1 * represents grilled Pangasius bocourti from location 1 and SSF2.1 denotes the first fried Sperata seenghala sample from location 2.
Total 36 samples of commonly available fried and grilled fish products were randomly collected from Delhi-NCR markets. The collected samples were of seven different fish species represented as Basa (Pangasius bocourti), Surmai (Scomberomorus guttatus), Singhara (Sperata seenghala), Barramundi or Bhetki (Lates calcarifer), Sole (Solea solea), Rohu (Labeo rohita), and Tilapia (Oreochromis niloticus). The fish samples were traditionally fried in refined oil on an LPG gas stove and grilled with charcoal. The collected samples were first wrapped in aluminum foil and then packed in a sterile stomacher bag. The packed samples were kept in ice containers and transported to the laboratory, where the edible fish muscle of the samples was ground with a blender until the samples had the consistency of a smooth paste. The well-homogenized samples were then stored in the deep freezer at −20ºC.
2.2. Chemicals
All reagents and chemicals were of analytical grade with the possible highest purity. Acetonitrile of LC-MS grade and Acetone of GC grade were purchased from Merck, Germany. Deionized Milli-Q water used in this study was produced by the Milli-Q system installed in the laboratory. Magnesium sulphate anhydrous and sodium acetate anhydrous, along with cleanup pouch components (PSA & C18), were purchased from Merck, Germany. FAPAS (T0693QC) blank fish, the certified materials for quality control were obtained from FAPAS, Fera Science Ltd. (Fera), Sand Hutton, York. Standard Solution of 7 PCBs mix: PCB 28, 52, 101, 153, 138, 180, and 209, each at 10 µg mL−1 and the 16PAH standard mix: benzo[a]anthracene (BaA), benzo[b]fluoranthene (BbF), benzo[k]fluoranthene (BkF), benzo[a]pyrene (BaP), benzo[ghi]perylene (BghiP), dibenz[a,h]anthracene (DahA), indeno[1,2,3-cd]pyrene (IcdP), chrysene (Chry), naphthalene (Nap), acenaphthylene (Acy), acenaphthene (Ace), fluorene (Fl), phenanthrene (Phe), anthracene (Ant), fluoranthene (Flu), and pyrene (Pyr), each at 1 µg mL−1 was acquired from Supelco, Inc. (Bellefonte, PA, USA). A mix of PAHs internal standards (SV internal standard mix): Acenaphthene d10, Naphthalene d8, Chrysene d12, and Phenanthrene d10 was purchased from Restek, India.
2.3. Extraction of PAHs and PCBs
The QuEChERS (quick, easy, cheap, effective, rugged, and safe) method (AOAC: 2007 buffered method) described by Escarrone et al. [24] was used after slight modifications to extract the PAHs and PCBs from the grilled and fried fish samples. The stored samples (well homogenized, chopped, and kept in a deep freezer) were kept out of the freezer and left for some time for thawing. A quantity of 1 g was taken from each sample into the extraction tube (50 mL centrifuge tubes) having a ceramic homogenizer stone (from Agilent) along with 5 mL Milli-Q water. The samples were mixed well with the help of a vortex for 20–30 seconds. A quantity of 10 mL acetonitrile was added into each extraction tube and vortexed for 20–30 seconds. After the vortex step, the mixture of extraction salts (buffered) named anhydrous magnesium sulfate (6.5 gm) and sodium acetate (1.5 gm) was rapidly mixed with the sample in extraction tubes, which were again vortexed immediately after the addition of extraction salts. Then, the extraction tubes were centrifuged at 5000 RPM for 5 minutes. The supernatant (1 mL) of centrifuged extraction tubes was collected in another polypropylene tube (2 mL micro-centrifuge tubes) containing a cleanup mixture of 150 mg MgSO4, 50 mg PSA, and 50 mg C18. The cleanup tubes were vortexed for 20 s, followed by centrifugation at 5000 rpm for 5 min. The extractable quantity of around 1 mL solution of the supernatant from the cleanup tubes was collected in a 2 mL amber-colored vial with a blue screw cap and spiked with 50 µg kg−1 PAHs internal standards. The vials were then transferred for GC-MS/MS analysis.
2.4. GC-MS/MS analysis
The analysis was performed using an Agilent 7890B GC, coupled with a 7010B triple-quadrupole MS (Agilent Technologies, Santa Clara, CA, USA) and a computer having Mass Hunter software for data acquisition and processing. Separation of compounds was achieved by two identical HP5MS ultra-inert capillary columns (Agilent Technology, 15 m×250 µm×0.25 µm). Sample injection (1 µL) was carried out in split less mode at 310 °C. The column separation was obtained by a temperature gradient starting at 55 ºC for 1 min, increased to 300 ºC at the rate of 20 ºC/min. After each run, a column backflush was used to avoid column contamination. The column head pressure was set up at 9.166 psi with a constant flow rate of 3 mL/min using helium as a carrier gas. The GC runtime was 19.25 min with a 5 min post run time. The mass spectrometer was operated using electron ionization mode (with a high-efficiency source) at an electron energy of 100 eV in MRM mode. Nitrogen was used as collision gas at 1.5 mL/min and helium as quench gas at 4 mL/min for all MS/MS experiments. The MRM transitions (precursor to product ion transition) of each PAH and PCB compound were determined based on collision tests.
2.4.1. Analytical quality control
The method validation was conducted for linearity, the limit of detection (LOD, S/N > 3), the limit of quantification (LOQ, S/N > 10), accuracy (%), precision (%), and recovery (%) on fish samples. Spiked FAPAS blank fish samples (at 20 µg kg−1 & 50 µg kg−1) were analyzed in replicates to evaluate the recovery performance and accuracy of the method. The linearity curve was plotted from the analysis of 16PAH & 6PCB standard mix at 1, 5, 10, 20 µg kg−1, and 50 µg kg−1 IS mixture. These matrix match calibration curves and linearity tests were performed daily for each sample batch. Identification of PAHs & PCBs congeners was done by comparing their retention times and mass-to-charge values to matrix-matched standards analyzed under the same conditions. The chromatogram of 16 PAHs and 6 PCBs is given in Fig. 2. The PAHs and PCBs content were quantified by calculating the relative response from single compounds using calibration curves (peak area or relative response of the same compound in the matrix-matched standards).
Fig. 2.
Chromatogram of 16 PAHs and 6 indicator PCBs spiked in blank matrix from FAPAS (spiked concentration: 20 µg kg−1).
2.5. Human health risk assessment
The human health risk assessment methodology for the calculations of benzo(a)pyrene-equivalent carcinogenicity (BaPTEQ), estimation of dietary intake (EDI), margin of exposure (MOE), incremental lifetime cancer risk (ILCR) due to PAHs, and hazard index of PCBs is given below.
2.5.1. Benzo(a)pyrene-equivalent carcinogenicity (BaPTEQ)
The determination of carcinogenic potency due to the consumption of fried and grilled fish products was conducted by comparison of the carcinogenic toxicity of seven PAH congeners (2B group) with the reference compound BaP. The BaPTEQ of the PAHs was calculated by using the following Eq. 1.
| (1) |
Where BaPTEF represents the toxic equivalency factor for PAH members [5], [60] and Ci denotes the concentration of the individual PAH congener.
2.6. Estimation of dietary intake
The dietary PAHs exposure was estimated using the mean concentration of each toxic compound in fish samples. The estimated daily intake (EDI) was calculated for the adults according to the following equation [36].
| (2) |
Where C represents the concentration of PAHs (EFSA indicators) in fish samples, namely, BaP, 4PAH (Chry, BaP, BaA, and BbF), and 8PAH (PAH4, BkF, BghiP, D[a,h]A, and IcdP,), BWA represents the average body weight. The average body weight for adults is taken 65 kg as per the guidelines recommended by National Institute of Nutrition, India [59].
2.6.1. Margin of exposure (MOE)
The MOE due to the consumption of fried and grilled fish was calculated by using the following equation [36].
| (3) |
Where BMDL10 is the lower bound of a 95 % confidence interval for the benchmark dose (BMD). The BMDL10 values (mg kg-1 bw/day) for BaP, 4PAH and, 8PAH are 0.07, 0.34 and, 0.49 respectively. The calculated MOE values are considered as-a MOE value< 10000 indicates serious adverse health effects, and b) MOE value> 10000 shows no toxic effects to humans [20].
2.6.2. Incremental lifetime cancer risk (ILCR) due to exposure to PAHs
Cancer risk is calculated as the incremental probability of an individual developing cancer over a lifetime as a result of exposure to a potential carcinogen. The ILCR values related to the dietary exposure of carcinogenic PAHs were estimated by the following equation [22].
| (4) |
Where CR: Cancer risk; IngR indicates the average daily intake of cooked fish, EF represents the exposure frequency (24 days/year for the flexitarian; 365 days/year for the fish-eating population and entire population); ED stands for exposure duration, which is taken as 30 years for adults [83]; CF represents the conversion factor, which is 1 × 10−6 kg mg−1; OSF: cancer oral slope factor which is 0.73, 0.73, 0.073, 7.3, 0.73, 7.3, and 0.0073 for the PAHs: BaA, BbF, BkF, BaP, IndP, D[a,h]A, and Chry, respectively. ATca: average time for carcinogenic PAHs (70 years for adults). The cancer risk is considered negligible in case of CR< 10−6, acceptable in case 10−6<CR< 10−4, and unacceptable in case CR> 10−4 [22], [56], [84].
2.6.3. Hazard index for PCBs
Dietary exposure to indicator PCBs was calculated by integrating the levels of indicator PCBs congeners in fried and grilled fish available in Delhi-NCR with their corresponding consumed quantity. To estimate the HI for 6 indicator PCBs, the average daily dose or estimated daily intake (EDI) followed by Hazard Quotients (HQ) for each PCB congener were calculated through the following equations.
| (5) |
| (6) |
| (7) |
Where EDI (ng kg−1 bw day−1) represents daily exposure to indicator PCBs in the adults of Delhi-NCR population. CM represents the measured concentration of PCB congeners in fried and grilled fish samples. TDI represents the tolerable daily intake of PCBs which was taken as 10 ng kg−1 bw day−1 [20], [3], [6].
2.7. Statistical analysis
The results are presented as mean ± standard deviation. The variability among the samples was assessed through performing one-way analysis of variance at statistical significance (p-value<0.05) using the SPSS model version 23.
3. Results and discussion
In this study, market samples of grilled and fried products prepared from seven kinds of fish species were tested for the contamination of 16 PAHs and indicator 6 PCBs. However, among 16PAHs, relative standard deviation (RSD) for LMW PAHs viz. Nap, Acy, and Ace was found to be higher than the prescribed limit of RSD in food (≤20 %). Therefore, we reported only 13 out of 16 PAHs in this study. The focused analytes of the study were 13 PAHs (BaA, BbF, BkF, BaP, BghiP, DahA, IcdP, Chry, Fl, Phe, Ant, Flu, and Pyr) and 6 indicator PCB congeners (138, 153, 28, 52, 101, and 180). Dietary exposure and health risk assessment were conducted based on data of these analyzed contaminants and a questionnaire-based survey.
3.1. Concentrations and profiles of PAHs in fried and grilled fish samples
The mean concentration of ∑13PAHs in all the fish samples ranged from 20.80 ± 2.06–947.65 ± 40.85 µg kg−1 and varied significantly among the samples. The grilled fish samples were found to have higher concentrations of PAHs than the fried samples (supplementary figure SF.1). However, Anova test showed that the concentration of PAHs vary significantly with the cooking method except for the two PAHs (DahA and BghiP). The mean concentration of ∑13PAHs in grilled fish samples was found to vary from 29.38 ± 1.74–947.65 ± 40.85 µg kg−1 whereas it ranged from 20.80 ± 2.06–151.42 ± 1.16 µg kg−1 in fried fish samples. The mean concentrations of ∑13PAHs and individual PAHs in all the samples are presented in supplementary table S1. The highest mean concentration of ∑13PAH (947.65 ± 40.85 µg kg−1) was found in sample SSG6 (grilled Sperata seenghala). Higher concentrations during grilling may be linked to the influential parameters such as types of fuel (i.e., coal, wood) used for grilling, temperature, grilling duration, and the distance between the fish and energy source. During grilling, drippings from the fish are directly exposed to charcoal, which may lead to the formation of high concentrations of PAHs followed by their deposition on the food surface [16], [2], [44], [85], [93]. The studies conducted by Sharifiarab et al. [75] and Wang et al. [87] also reported higher concentrations of PAHs in grilled fish samples than the fried fish samples which is in line with the present study. Similarly, Jahurul et al. [38] investigated the PAHs in fish during different cooking methods and found the trend as grilled fish (40.69 µg kg−1) > boiled fish (9.02 µg kg−1) > deep-fried fish (2.39 µg kg−1). Sahin et al. [73] reported the concentration of 16 PAHs and BaP in grilled fish samples as 7.26 µg kg−1and 0.73 µg kg−1 respectively indicating lower concentrations than found in the present study. Similarly, Masuda et al. [55] also reported the concentration of PAHs in grilled fish lower than the present study.
In the present study, higher concentrations of PAHs were observed in fried fish samples than grilled samples in Lates calcarifer fish. Most of the cooked Lates calcarifer fish samples were purchased from the Chittaranjan Park region of Delhi. At this location, fried fish is more commonly available as street food products than grilled fish. The higher concentration of PAHs in fried fish samples may be the result of repeated frying cycles in the same oil [36]. The increased levels of PAHs are subjected to a series of thermal processes in cooking oil and food material [51], [94]. A study conducted by Manda et al. [53] reported lower concentration of PAH8 in grilled fish (49.81 μg/kg) as compared to fried fish product (101.99 μg/kg). Similarly, Perelló et al. [66] reported the higher concentration of 16 PAHs in fried sardines, hake, and tuna than grilled sardines, hake, and tuna with the following trend: fried fish products (13.30–35.42 µg kg−1) > grilled fish products (3.15–27.93 µg kg−1), with the highest content (35.42 µg kg−1) detected in fried sardine fish samples. The results of the present study also showed higher concentrations of PAHs in fried fish samples than those reported by MASTAN et al. [54].
In this study, marker PAHs (BaP, 4 PAHs, and 8 PAHs) were found higher in grilled fish than in the fried fish samples (Fig. 3). The concentration of BaP was found to be above its maximum permissible limits of 2 µg kg−1 in all the samples. On the other hand, 63.89 % of the samples were found to have PAH4 concentrations higher than their maximum permissible limits of 12 µg kg−1 (supplementary table S3). These limits were set by the European Commission for muscle meat of smoked fish and smoked fishery products [26]. In addition to cooking methods (grilling and frying), pre-existing PAHs in fish resulting from environmental pollution (contaminated soil, water, and air) may also contribute to elevated levels of BaP and other PAHs in grilled and fried fish samples [74].
Fig. 3.
Distribution of EFSA Indicator PAHs and PCBs in grilled and fried fish samples.
In the present study, among all the grilled samples, the highest mean concentrations of BaP, ∑4PAHs, and ∑8PAHs were observed as 46.70 ± 5.62 µg kg−1, 159.30 ± 15.88 µg kg−1 and 413.60 ± 70.97 µg kg−1 respectively, in the grilled Sperata seenghala (SSG6) (supplementary table S3). Similarly, the fried Lates calcarifer (LCF7.2) showed the highest concentration of BaP as 13.81 ± 1.05 µg kg−1, whereas the highest ∑4PAHs and ∑8PAHs, viz., 23.33 ± 1.55 µg kg−1, and 40.82 ± 1.67 µg kg−1 respectively, were found in SSF4 Sperata seenghala among all fried samples. Wang et al. [87] reported the mean concentration of PAH4 and PAH8 as 5.02 µg kg−1 and 6.51 µg kg−1, respectively, in grilled fish, 2.54 µg kg−1 and 3.17 µg kg−1 in fried fish samples, respectively, which is much lower than reported in the present study. Similarly, higher levels of ∑8PAHs (16.86 ± 2.09–413.60 ± 70.97 µg kg−1) were observed in grilled fish samples in the present study than the concentration (6.65–99.09 µg kg−1) reported by Oz et al. [63]. Viegas et al. [85] reported BaP (1.36–4.72 µg kg−1) and ∑8 PAHs (43.32 µg kg−1) concentrations in grilled salmon fish, which are much lower than found in the present study. Sharifiarab et al. [75] reported that average 16 PAHs and 4 PAHs concentrations in fish samples increased from 16.44 ± 4.63 µg kg−1 to 25.41 ± 7.31 µg kg−1 and 3.96 ± 0.92 µg kg−1 to 5.98 ± 1.47 µg kg−1 respectively, after grilling with charcoal. On the other hand, the mean concentrations of 16 PAHs and 4 PAHs were found as 20.28 µg kg−1 and 4.91 µg kg−1 respectively, after frying. An increase in the level of PAHs in fish during cooking might be caused by the transfer of PAHs from coal and frying oil to the fish [32], [75].
The composition of PAHs in grilled and fried fish samples showed the dominance of LMW PAHs (3 rings) over HMW PAHs (4–6 rings) (supplementary table S1). The grilled fish samples were found to have the following composition of PAHs: 3-ring PAHs> 4-ring PAHs> 5-ring PAHs> 6-ring PAHs. However, in fried fish samples, it was as follows: 3-ring PAHs> 5-ring PAHs> 4-ring PAHs> 6-ring PAHs (supplementary figure SF.2). This pattern is different from the results reported by Iwegbue et al. [36] who found that fried fish samples had higher concentrations of HMW PAHs than the LMW PAHs. However, the composition of PAHs in smoked fish was reported as 2–4 ring PAHs (LMW)> 5–6 ring PAHs (HMW), which is in line with the finding of the present study.
3.2. Concentrations and profiles of PCBs in fried and grilled fish samples
The mean concentration of each PCB congener in all the samples was found to vary from not detected (ND) to 11.43 ± 0.23 µg kg−1. The mean concentration of ∑6PCBs in grilled and fried samples ranged from 2.86 ± 0.16 µg kg−1 to 46.52 ± 0.46 µg kg−1 and 10.50 ± 0.47 µg kg−1 to 40.06 ± 0.78 µg kg−1 respectively (supplementary table S3). However, as per the Anova test, the difference in concentration between grilled and fried fish samples was not statistically significant. This could be due to minor or negligible formation/reduction of PCBs during the cooking process. The highest mean concentration of ∑6PCBs was found to be 46.52 ± 0.46 µg kg−1 in grilled Scomberomorus guttatus (SGG1.2 *). However, grilled Lates calcarifer (LCG7) showed the lowest mean concentration of ∑6PCBs as 2.86 ± 0.16 µg kg−1. In general, fried fish samples were found to have a higher concentration of ∑6PCBs than the grilled fish samples (Fig. 3). PCBs are synthetically produced chemicals and are not formed during cooking. However, PCB-contaminated frying oil and multiple frying cycles in the same oil are the major sources of PCBs deposition in food. Multiple frying cycle may concentrate the contaminant in the frying oil thereby leading to raised concentrations in the fried food product. Due to pre-occurrence of PCBs in coal, grilling may also slightly contribute PCBs to the foods. A few studies have been conducted to study the effect of cooking on PCB concentrations in fish products, and inconsistent results have been reported. The mechanism for the change in PCBs concentrations in cooked fish is complex [58], [96]. A study reported the reduced concentration of PCBs in sardines and hake during grilling, whereas the concentration was found to increase very slightly in tuna. Grilling and frying processes could be responsible for reducing the levels of PCBs in fish. The reduction of PCB levels could happen due to the loss of fatty acids during grilling and deep frying into the cooking oil [40]. Frying process can remove more than 50 % PCBs in edible fish tissues [76]. On the other hand, evaporation of water and PCBs from the fish fillets might occur due to the high temperature of the cooking oil [58], [89]. Selection of the total surface area and the thickness of the fillet during cooking could be other influential factors affecting the PCBs levels in fish [67], [76].
3.3. Human health risk assessment
In India, daily fish consumption has risen 66 % (from 20.36 g to 33.78 g) amongst the fish-eating population and 81.43 % (from 13.42 g to 24.37 g) amongst the entire population over the last 15-year timeframe [34]. The conducted survey was aimed at assessing the per capita consumption of fish amongst flexitarians residing in Delhi-NCR. As per our survey, fried fish products are more consumed than grilled fish as street food in the study area. On average, most of the adults (flexitarians) in the study population consume fish 24 times per year (varied place to place as per the availability of the cooked fish products). The consumption rate of a flexitarian was found to be approximately 250 g at a time (per capita daily consumption: 16.44 g). Using this survey data (such as exposure frequency and consumption quantity), four health risk indicators BaPTEQ, margin of exposure (MOE), hazard index (HI), and incremental lifetime cancer risk (ILCR) were calculated and compared for flexitarian, fish-eating populations, and the entire population.
Furthermore, peer-reviewed research studies (from 1990 to 2024) on PAHs in Indian raw fish samples were systematically collected through various academic databases (Table. S8). The assembled database might be crucial for understanding the contribution of the environment to PAHs and PCBs contamination in raw fish samples. The diverse food processing methods such as drying, heating, grilling, frying, and smoking, can introduce the synthesis of carcinogenic polycyclic aromatic hydrocarbons (PAHs) in food products which is a concern of public health [97].
This compilation was subsequently employed to evaluate the cancer risk for the fish-eating population and compare it with the results of the present study. It was observed that the ILCR values of grilled and fried fish products were higher than the raw fish products (Fig. 4.1). The current study examined the six indicator PCB congeners in grilled and fried fish products, and none of the published studies from India have reported these PCBs in raw and processed fish products.
Fig. 4.1.
Incremental Lifetime Cancer Risk for fish eating population associated with consumption of grilled and fried fish (present study); Raw Fish* (calculated based on published data for PAHs in raw fish in India).
3.3.1. BaP toxicity
The BaPTEQ levels were calculated for the 4 PAHs and 7 PAHs (BaP, BaA, BbF, BkF, Chry, IcdP, and DahA) in grilled and fried fish samples. BghiP don’t have potency equivalency factors (PEFs) [5]. Therefore, BaPTEQ was calculated for 7 PAHs instead of 8 PAHs. BaPTEQ is a cancer risk evaluation tool for Public Health Assessment (PHA). Carcinogenicity for various polycyclic aromatic hydrocarbons (PAHs) can be quantified as a benzo(a)pyrene toxic equivalent (BaPTEQ) [5]. In the present study, the BaPTEQ levels in all the grilled and fried fish samples were found to be higher than the screening level of 0.67 μg kg− 1 for the total PAHs in fish for human consumption [84]. The BaPTEQ values ranged from 2.48 to 55.16 µg kg−1, and 2.55–88.61 µg kg−1 respectively. The BaPTEQ for 4 PAH, and 7 PAH in fried and grilled fish samples are shown in supplementary table S3. Generally, the BaPTEQ values were found to be higher in grilled fish samples than fried fish samples. The results of the present study were found similar to the one reported by Wang et al. [87] in which the BaPTEQ values for 4 PAH, 8 PAH, and 15 PAHs were found to be higher for the grilled samples than the fried fish samples. Effiong et al. [18] reported the BaPTEQ values for the commercially available fish samples, which ranged from 0.11 to 182 μg kg−1. On the other hand, Iwegbue et al. [36] reported the BaPTEQ values in fried fish samples to vary from 0.56 to 7.80 μg kg− 1 which was lower than found in the present study.
3.3.2. Daily intakes and margin of exposure for PAHs
The estimated daily intake (EDI) and MOE were calculated based on the concentrations of BaP and the EFSA-suggested markers (4PAH, and 8PAH) in food. As per EFSA, the MOE values of BaP, PAH4, and PAH8 could be more useful in place of BaP alone as markers of the carcinogenicity of carcinogenic PAHs [41]. For MOE calculations, since there is no benchmark-dose (BMDL10) reference value available in the literature that involves all 13 PAHs. Therefore, EDIBaP, EDIPAH4, and EDIPAH8 were used to calculate margins of exposure (MOE) for the flexitarian, fish-eating population, and entire population in the present study. All the values of EDI and MOE are presented in supplementary table S4 and table S5, respectively. In this study, the dietary intakes of indicator PAHs from consumption of fried and grilled fish ranged from 0.54 to 11.82 ng BaP kg− 1bw day− 1, 1.89–40.32 ng PAH4 kg− 1bw day− 1, and 2.08–104.67 ng PAH8 kg− 1bw day− 1 for flexitarian; 1.12–24.27 ng BaP kg− 1bw day− 1, 3.89–82.79 ng PAH4 kg− 1bw day− 1, and 4.26–214.95 ng PAH8 kg− 1bw day− 1 for the fish-eating population; 0.81–17.51 ng BaP kg− 1bw day− 1, 2.80–59.73 ng PAH4 kg− 1bw day− 1, 3.08–155.07 ng PAH8 kg− 1bw day− 1 for the entire population. The flexitarians were found to have higher per-day dietary intakes of PAHs than the other consumers. The present study also showed that the dietary intakes of PAHs are more through the consumption of grilled fish than fried fish. These results suggest that those consumers who eat more grilled fish are more exposed to PAHs. Similarly, a study conducted by Wang et al. [87] reported higher EDI values for PAH4 and PAH8 in the grilled fish samples than the fried samples; however, the EDI value of BaP through grilled fish was almost the same as that of fried fish. Iwegbue et al. [37] reported the daily intake of BaP, 2PAH, 4PAH, and 8PAHs within the ranges of 0–4.9, 0.7–11.3, 1.9–15.3, and 3.7–23.2 ng kg− 1bw day− 1 respectively, through the consumption of some popular fish species in Nigeria. Similarly, Effiong et al. [18] reported the average daily intake values of PAHs through consumption of fish for the respective EFSA indicators BaP, 2PAH, 4PAH, and 8PAHs as 0.72–17.2 ng kg−1 bw day−1, 1.66–35.7 ng kg−1bw day−1, 8.81–66.6 ng kg−1bw day−1 and 28–110 ng kg−1bw day−1. As per the recommendation of the World Health Organization (WHO), the daily exposure to dietary BaP should be below 10 ng kg−1bw day−1. However, in the present study, the EDI value of BaP for only one sample (SSG6) out of 36 fish samples was above 10, indicating high risk to the public’s health. The results of 97.22 % of fish samples in the present study were found in line with studies conducted by Sharifiarab et al. [75] and Bogdanović et al. [7], which reported the EDI values for fish samples below 10 ng kg−1bw day−1.
For the flexitarians, the MOE values of BaP, 4 PAH, and 8 PAH in 97.22 % of samples were found within safe limits (<10000). Whereas MOE values of BaP in 5.56 % of samples for the entire population and 8.33 % of samples for fish-eating population were found to exceed the limits. Similarly, the MOE values for 8 PAHs in 5.56 % of samples for fish-eating population were found to be exceeded. One sample SSG6 (grilled Sperata seenghala) showed all MOE values of BaP, 4 PAH, and 8 PAHs exceeded for the flexitarians, the entire population, and fish-eating population (supplementary table S5). Iwegbue et al. [37] reported the MOE values of BaP, 2 PAHs, 4 PAHs, and 8 PAHs to be greater than 10,000, showing no potential risk for Nigerian consumers. Wang et al. [87] reported the MOE values of BaP, 4 PAHs, and 8 PAHs in fried and grilled fish as > 10,000. Similar results were found in a study conducted by Sahin et al. [73]. Similarly, Bogdanović et al. [7] and Kim et al. [46] reported the values of MOE for 4 PAHs in fish samples as > 10000. Lee et al. [49] reported the 95th percentile MOE values for 4 PAHs and 8 PAHs as 5.2 × 105 and 9.1 × 104 for the adults (age:19–65 years). On the other hand, Akpambang et al., [1] reported the MOE values for BaP and 8PAHs in grilled or smoked fish samples lower than the 10,000, which indicated the potential risk for Nigerian consumers.
3.3.3. Carcinogenic risks of PAHs
The incremental lifetime cancer risk (ILCR) for flexitarians, the entire-population and the fish-eating population arising from the consumption of fried and grilled fish samples ranged from 4.68 × 10−5 to 1.32 × 10−3, 1.06 × 10−3 to 2.97 × 10−2, and 1.46 × 10−3 to 4.12 × 10−2, respectively. All grilled and fried fish samples consumed by the fish-eating population and the entire population exceeded the safe ILCR limits (10−4), resulting in exposure to potential cancer risk. These results emphasize the urgent need for mitigation strategies. On the other hand, 27.78 % of grilled and fried fish consumed by flexitarians resulted in ILCR values within the acceptable range (10−6<CR<10−4). ILCR values for the grilled fish were found to be higher than those for the fried fish (Fig. 4.2). The cancer risk values are presented in supplementary table S7. Iwegbue et al. [36] also reported DahA as a major contributor to the cancer risk from the consumption of the fried fish samples. Wang et al. [87] studied the ILCR values for children, adolescents, the elderly and adults for eating grilled and fried fish. The study found potential health risks associated with the consumption of grilled and fried fish, especially in adults. Forsberg et al. [28] reported the lifetime excess cancer risk due to exposure to carcinogenic PAHs in the range from 8.2 ± 5.2 × 10−4 to 3.4 ± 2.8 × 10−3 (at a consumption rate of 300 g/day) and from 1.4 ± 0.9 × 10−5 to 5.7 ± 4.7 × 10−5 (at a consumption rate of 5 g/day). Similarly, Gao et al. [30] reported the ILCR values for charcoal grilled fish samples higher than the recommended limitations. These results are in line with the results of the present study. Similarly, Duan et al. [15] reported the ILCR value as 6.65 × 10−5 for Chinese urban adults associated with the exposure to PAHs through consumption of grilled and fried fish food products. Effiong et al. [18] reported the ILCR values from 9.5 × 10−5 to 1.29 × 10−4 and from 3.66 × 10−5 to 1.33 × 10−4 for the fishes found in Bonny River and the Cross River, respectively, indicating probable cancer risk from the consumption of these fish products. On the contrary to the present study, Sharifiarab et al. [75] estimated the ILCR for the adults as 2.85 × 10−9 and found that the consumption of grilled and fried fish was safe for human health.
Fig. 4.2.
Incremental Lifetime Cancer Risk due to the exposure of carcinogenic PAHs through consumption of grilled and fried fish.
3.3.4. Dietary Intake and Hazard Index of PCBs
In the present study, the dietary intakes of indicator PCBs from the consumption of fried and grilled fish ranged from 0.72 to 11.77 ng PCB6 kg− 1bw day− 1, 1.07–17.44 ng PCB6 kg− 1bw day− 1, and 1.48–24.18 ng PCB6 kg− 1bw day− 1 for flexitarians, entire population, and fish-eating population, respectively. The study showed that the fish-eating population consumed the highest PCBs as a result of per-day fish consumption. Wirnkor et al. [91] reported the EDI values for PCBs from fish consumption ranging from 2160 to 9690 ng PCB6 kg− 1bw day− 1 for adults, which was much higher than found in the present study. However, Renieri et al. [71] reported that NDL-PCBs dietary exposure to the Greek population due to fish consumption ranged from 2.15 to 3.38 ng PCB6 kg− 1bw day− 1.
The non-carcinogenic risk was estimated in terms of the hazard index (HI) as a result of dietary exposure to indicator 6 PCBs through human consumption of fried and grilled fish. The HI value of 6 PCBs in all the samples ranged from 0.07 to 1.18 for flexitarians, 0.11–1.74 for the entire population, and 0.15–2.42 for fish-eating population (supplementary table S6). For the flexitarians, only two samples, SGG1.2 * and SGF1.2 * , showed the HI values greater than 1. Similarly, the HI values of 6 PCBs in 41.67 % of samples for the entire population and 66.67 % of samples for fish-eating population were found to be higher than 1 (supplementary table S6). The trend of 6 PCBs HI for the different groups of populations was observed as fish-eating populations>entire population>flexitarians (supplementary figure SF.4). These results are similar to the HI values reported by Wirnkor et al. [91], in which all HI values for PCBs were found above 1, indicating the potential non-carcinogenic risk for the fish consumers. Omar, Mahmoud [61] also reported HI values for total PCBs above 1, indicating that fish from up- and downstream of the River Nile were not safe for human consumption. However, Renieri et al. [71] reported HI values for indicator PCBs in farmed and wild fish below 1, indicating no risk for the Greek population through dietary exposure, and similar results were found in the study conducted by Deribe et al. [13].
4. Recommendations of PAHs and PCBs reduction strategies
The consumption of PAHs and PCBs contaminated fish products is an important scientific concern due to human health issues. Therefore, innovative reduction and control strategies should be implemented during grilling and frying practices. The following practices can mitigate PAHs and PCB levels in fish products.
4.1. Reduction of PAHs
-
(i)
Use of white charcoal during grilling practices is reported as a low producer of PAHs as compared to black charcoal [45]. Therefore, the use of white charcoal for grilling the fish can be preferred. Preheating and charring the charcoal until attaining a smokeless flame with a high temperature should be done before grilling or barbecuing the fish, as it reduces the smoke exposure to fish [9]. Meat or fish is directly exposed to smoke during coal grilling and results in more deposition of PAHs. Direct exposure to smoke can be avoided through indirect heating methods such as grilling meat with wrappings and using an electric grill or gas oven instead of a coal grill. The grilling of fish with wrappings also minimizes the fat drippings on the heat source that reduces the PAHs formation. The leaner portion of meat or fish should be used for grilling with a properly maintained distance from the heat source [11], [79].
-
(ii)
Frying has been commonly used as a major cooking method in households as well as commercial settings. Some interventions, such as managing the temperature and time of frying, selecting appropriate cooking oil, and avoiding the reuse of oil for frying, can be effective mitigation strategies for PAHs in fried fish [36]. Use of suitable cooking oils such as sesame oil, sunflower oil, rapeseed oil, and soybean oil can reduce the formation of PAHs in fried fish [77]. In addition, shallow-pan frying instead of deep frying, along with the air-frying technique, is also an effective reduction strategy for PAHs in fried fish [17].
-
(iii)
The thermal processing of food produces free radicals, which has been considered as the key source of PAHs formation in food. The generation of free radicals can be eliminated by incorporation of marinades such as onion, vinegar, garlic, tomato juice, and spices (coriander, black pepper, turmeric, tamarind paste, etc.). These marinades have citric acid, antioxidants, ascorbic acid, phenolic compounds, etc., which inhibit the formation of free radicals produced by the thermal combustion of food [11], [79]. Therefore, use of appropriate marinades before grilling and frying the fish has the potential to reduce PAHs.
-
(iv)
The PAHs can also be reduced in meat by using probiotics and lactic acid bacteria (LAB), which is also a novel eco-friendly mitigation strategy [11].
-
(v)
The packaging materials, such as low-density polyethylene (LDPE), high-density polyethylene (HDPE), polypropylene, and polyethylene terephthalate (PET), can adsorb PAHs from the food [11], [79]. The use of packaging materials might be used as a PAHs reduction strategy. However, these packaging materials are the main source of another emerging food contaminant that is microplastics [42].
4.2. Reduction of PCBs
The effect of cooking on PCB levels in food is quite debatable because studies have been reported for both increase and decrease of PCB levels in fish during cooking practices [12], [14], [33], [57], [58], [67], [68], [69], [82], [95], [96]. For example, Rawn et al. [69] studied the impact of cooking methods on PCB levels in fish and fish products and reported that the PCB levels were slightly changed after cooking with a reduction of 7.9 % in finfish and an increase of 2.9 % in shellfish and other seafood. Frying of finfish also showed the highest reduction of PCBs (12 %) of all cooking methods. However, Sherer & Price [76] reported that frying can remove more than 50 % of PCBs from the fish.
5. Future prospects/challenges
PAHs are formed during frying and grilling because of thermal processing. Whereas PCBs are deposited in the food through environmental matrices and pre-contaminated cooking mediums such as contaminated cooking oil. The PAHs reduction in cooked fish products has been documented with various mitigation strategies. Whereas, the factors that contribute for the increase or decrease of PCBs during cooking practices are complex. Future innovative research is necessary to completely understand the effect of cooking on PCB levels in food and their mitigation strategies.
6. Conclusion
Compared to fried fish samples, the concentration of PAHs in grilled fish samples was found to be significantly higher. The concentrations of benzo[a]pyrene in all the samples and marker ∑4PAHs in 64 % of samples were found to exceed the permissible limit of 2 µg kg−1 and 12 µg kg−1, respectively, set by the European Union. Potential health concerns, indicated by BaPTEQ, were found to be higher than the screening threshold (particularly in grilled samples). Eating fish products contaminated with PAHs increases incremental lifetime cancer risk significantly. The HI values of 6 PCBs exceeded in 5.56 % of samples for flexitarians, 41.67 % of samples for the entire population and 66.67 % of samples for fish-eating population. The present study shows that PAHs and PCBs are present in grilled and fried fish products beyond the acceptable limits. The recommended strategies for the mitigation of PAHs include regulating cooking temperature, duration and distance from heat source, using white charcoal instead of black charcoal, preheating and charring charcoal to minimize smoke, employing wrappings to prevent direct smoke and fat drippings. In addition, opting for suitable cooking methods such as electric grills or gas ovens rather than coal grills, selecting appropriate cooking oils, avoiding the repeated use of frying oil, using appropriate marinades and probiotics, and opting for suitable packaging materials, can also reduce the PAHs formation in food. However, for PCBs, frying is a suitable cooking method to mitigate PCBs in food significantly.
To further enhance our understanding of the formation of PAHs and the mechanism of PCB reduction during the grilling and frying process, as well as the influential factors and mitigation strategies involved, large-scale studies must be conducted.
CRediT authorship contribution statement
Chakkaravarthi S.: Writing – review & editing, Project administration. Agarwal Tripti: Writing – review & editing, Supervision, Resources, Project administration, Funding acquisition, Conceptualization. . Abhishek: Writing – original draft, Visualization, Methodology, Formal analysis, Data curation.
Declaration of Competing Interest
The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Tripti Agarwal reports financial support was provided by India Ministry of Food Processing Industries. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper
Acknowledgement
Funding received from the Ministry of Food Processing Industries, India, through grant number Q-11/3/2021-R&D is acknowledged. Author Mr. Abhishek is thankful to UGC for providing a fellowship for conducting research work. He is also thankful to Dr. Lochan Singh for providing her valuable suggestions for conducting this research work. The NIFTEM publication ID of this manuscript is NIFTEM-P-2024–46.
Handling Editor: Dr. L.H. Lash
Footnotes
Supplementary data associated with this article can be found in the online version at doi:10.1016/j.toxrep.2025.101953.
Appendix A. Supplementary material
Supplementary material
Data availability
Data will be made available on request.
References
- 1.Akpambang V.O.E., Purcaro G., Lajide L., Amoo I.A., Conte L.S., Moret S. Determination of polycyclic aromatic hydrocarbons (PAHs) in commonly consumed Nigerian smoked/grilled fish and meat. Food Addit. Contam.: Part A. 2009;26(7):1096–1103. doi: 10.1080/02652030902855406. [DOI] [PubMed] [Google Scholar]
- 2.Arar S.H., Ikbarieh S.G., Kailani M.H., Alawi M.A. Monitoring of polycyclic aromatic hydrocarbons (PAHs) in smoke of charcoal grilled meat-restaurants in Amman, Jordan. Toxin Rev. 2022;41(1):290–297. doi: 10.1080/15569543.2020.1870498. [DOI] [Google Scholar]
- 3.Arnich, N., Tard, A., Leblanc, J. (2009). Dietary intake of non-dioxin-like PCBs (NDL-PCBs) in France, impact of maximum levels in some foodstuffs. Elsevier. Retrieved July 6, 2022, from 〈https://www.sciencedirect.com/science/article/pii/S0273230009000944〉. [DOI] [PubMed]
- 4.ATSDR, 2014. Polychlorinated Biphenyls (PCBs) | Toxicological Profile. [PubMed]
- 5.ATSDR, 2022. Guidance for Calculating Benzo(a)pyrene Equivalents for Cancer Evaluations of Polycyclic Aromatic Hydrocarbons.
- 6.Baars, A.J., Theelen, R.M.C., Janssen, P.J.C.M., Hesse, J.M., van Apeldoorn, M.V., Meijerink, M.V., Verdam, L. and Zeilmaker, M.J., (2001). Re-evaluation of human-toxicological maximum permissible risk levels.
- 7.Bogdanović T., Pleadin J., Petričević S., Listeš E., Sokolić D., Marković K., Ozogul F., Šimat V. The occurrence of polycyclic aromatic hydrocarbons in fish and meat products of Croatia and dietary exposure. J. Food Compos. Anal. 2019;75:49–60. [Google Scholar]
- 8.Çakiroĝullari G.Ç ., Kiliç D., Uçar Y. Levels of polychlorinated dibenzo-p-dioxins, dibenzo-p-furans and polychlorinated biphenyls in farmed sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata) from Turkey. Food Control. 2010;21(9):1245–1249. doi: 10.1016/J.FOODCONT.2010.02.010. [DOI] [Google Scholar]
- 9.Chaemsai S., Kunanopparat T., Srichumpuang J., Nopharatana M., Tangduangdee C., Siriwattanayotin S. Reduction of the polycyclic aromatic hydrocarbon (PAH) content of charcoal smoke during grilling by charcoal preparation using high carbonisation and a preheating step. Food Addit. Contam.: Part A. 2016;33(3):385–390. doi: 10.1080/19440049.2016.1143124. [DOI] [PubMed] [Google Scholar]
- 10.Costopoulou D., Vassiliadou I., Leondiadis L. PCDDs, PCDFs and PCBs in farmed fish produced in Greece: Levels and human population exposure assessment. Chemosphere. 2016;146:511–518. doi: 10.1016/J.CHEMOSPHERE.2015.12.019. [DOI] [PubMed] [Google Scholar]
- 11.Das A.K., Bhattacharya D., Das A., Nath S., Bandyopadhyay S., Nanda P.K., Gagaoua M. Current innovative approaches in reducing polycyclic aromatic hydrocarbons (PAHs) in processed meat and meat products. Chem. Biol. Technol. Agric. 2023;10(1):109. doi: 10.1186/s40538-023-00483-8. [DOI] [Google Scholar]
- 12.de Boer J., Lammertse N., Koekkoek J., van Hattum B. PCB and organochlorine pesticide concentrations in eel increase after frying. Chemosphere. 2013;90(1):139–142. doi: 10.1016/j.chemosphere.2012.07.042. [DOI] [PubMed] [Google Scholar]
- 13.Deribe E., Rosseland B., Borgstrøm R., Salbu B., Gebremariam Z., Dadebo E., Skipperud L., Eklo O. Organochlorine pesticides and polychlorinated biphenyls in fish from lake awassa in the ethiopian rift valley: human health risks. Bull. Environ. Contam. Toxicol. 2014;93(2):238–244. doi: 10.1007/s00128-014-1314-6. [DOI] [PubMed] [Google Scholar]
- 14.Domingo J.L. Influence of cooking processes on the concentrations of toxic metals and various organic environmental pollutants in food: a review of the published literature. Crit. Rev. Food Sci. Nutr. 2011;51(1):29–37. doi: 10.1080/10408390903044511. [DOI] [PubMed] [Google Scholar]
- 15.Duan X., Shen G., Yang H., Tian J., Wei F., Gong J., Zhang J. Dietary intake polycyclic aromatic hydrocarbons (PAHs) and associated cancer risk in a cohort of Chinese urban adults: inter- and intra-individual variability. Chemosphere. 2016;144:2469–2475. doi: 10.1016/j.chemosphere.2015.11.019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Duedahl-Olesen L., Ionas A.C. Formation and mitigation of PAHs in barbecued meat – a review. Crit. Rev. Food Sci. Nutr. 2022;62(13):3553–3568. doi: 10.1080/10408398.2020.1867056. [DOI] [PubMed] [Google Scholar]
- 17.Dutta K., Shityakov S., Zhu W., Khalifa I. High-risk meat and fish cooking methods of polycyclic aromatic hydrocarbons formation and its avoidance strategies. Food Control. 2022;142 doi: 10.1016/J.FOODCONT.2022.109253. [DOI] [Google Scholar]
- 18.Effiong I.A., Bassey F.I., Iwegbue C.M.A., Ekpa O.D., Williams S.A., Oguntunde F.C., Osabor V.N., Martincigh B.S. Polycyclic aromatic hydrocarbons in three commercially available fish species from the Bonny and Cross River estuaries in the Niger Delta, Nigeria. Environ. Monit. Assess. 2016;188(9):508. doi: 10.1007/s10661-016-5479-9. [DOI] [PubMed] [Google Scholar]
- 19.EFSA Opinion of the scientific committee on a request from EFSA related to A harmonised approach for risk assessment of substances which are both genotoxic and carcinogenic. EFSA J. 2005 〈https://efsa.onlinelibrary.wiley.com/doi/abs/10.2903/j.efsa.2005.282〉 [Google Scholar]
- 20.EFSA Reasoned opinion of EFSA prepared by PRAPeR on MRLs of concern for the active substance vinclozolin. EFSA Sci. Rep. 2008;166:1–36. [Google Scholar]
- 21.EFSA Update of the monitoring of levels of dioxins and PCBs in food and feed. EFSA J. 2012;10(7):2832. doi: 10.2903/j.efsa.2012.2832. [DOI] [Google Scholar]
- 22.EPA, U.S. (1989). Risk assessment guidance for superfund. Volume I: Human health evaluation manual (part a). EPA/540/1-89/002.
- 23.Ergönül P.G., Sánchez S. Evaluation of polycyclic aromatic hydrocarbons content in different types of olive and olive pomace oils produced in Turkey and Spain. Eur. J. Lipid Sci. Technol. 2013;115(9):1078–1084. doi: 10.1002/ejlt.201200398. [DOI] [Google Scholar]
- 24.Escarrone A.L.V., Caldas S.S., Furlong E.B., Meneghetti V.L., Fagundes C.A.A., Arias J.L.O., Primel E.G. Polycyclic aromatic hydrocarbons in rice grain dried by different processes: Evaluation of a quick, easy, cheap, effective, rugged and safe extraction method. Food Chem. 2014;146:597–602. doi: 10.1016/j.foodchem.2013.09.006. [DOI] [PubMed] [Google Scholar]
- 25.European Commission Commission Regulation No. 1881/2006 of 19 December 2006 setting maximum levels of certain contaminants in food stuffs. Off. J. Eur. Union. 2006 [Google Scholar]
- 26.European Commission Commission Regulation No. 836/2011 of 19 August 2011 amending Regulation (EC) No 333/2007 laying down the methods of sampling and analysis for the official control of the levels lead, cadnium, mercury, inorganic tin, 3-MCPD and benzo(a)pyrene in foodstuffs. Off. J. Eur. Union. 2011:9–16. [Google Scholar]
- 27.FAO (Food and Agriculture Organization), (2020). The state of food security and nutrition in the world 2020: transforming food systems for affordable healthy diets. Food & Agriculture Org.
- 28.Forsberg N.D., Stone D., Harding A., Harper B., Harris S., Matzke M.M., Cardenas A., Waters K.M., Anderson K.A. Effect of Native American fish smoking methods on dietary exposure to polycyclic aromatic hydrocarbons and possible risks to human health. J. Agric. Food Chem. 2012;60(27):6899–6906. doi: 10.1021/jf300978m. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.FSSAI, I. (2011). Food Safety and Standards (Contaminants, Toxins and residues) Regulations, 2011. Ministry of Health and Family Welfare, India, (August, 1 2011), 2.
- 30.Gao, Z., Chen, Z., & Hui, S.-P. (2021). Effect of charcoal grilling on polycyclic aromatic hydrocarbons (PAHs): Content, composition, and health risk in edible fish in Japan. 10.2116/analsci.21P197. [DOI] [PubMed]
- 31.Ge M., Wang X., Yang G., Wang Z., Li Z., Zhang X., Xu Q. Persistent organic pollutants (POPs) in deep-sea sediments of the tropical western Pacific Ocean. Chemosphere. 2021;277 doi: 10.1016/j.chemosphere.2021.130267. [DOI] [PubMed] [Google Scholar]
- 32.Gorji M.E., Ahmadkhaniha R., Moazzen M., Yunesian M., Azari A., Rastkari N. Polycyclic aromatic hydrocarbons in Iranian Kebabs. Food Control. 2016;60:57–63. doi: 10.1016/j.foodcont.2015.07.022. [DOI] [Google Scholar]
- 33.Hori T., Nakagawa R., Tobiishi K., Iida T., Tsutsumi T., Sasaki K., Toyoda M. Effects of cooking on concentrations of polychlorinated dibenzo-p-dioxins and related compounds in fish and meat. J. Agric. Food Chem. 2005;53(22):8820–8828. doi: 10.1021/jf050978l. [DOI] [PubMed] [Google Scholar]
- 34.ICAR & Worldfish Fish consumption in India: patterns and trends. Indian Counc. Agric. Res. World Fish. 2023 [Google Scholar]
- 35.Iwegbue C.M.A., Odogbor D., Egobueze F.E., Emoyan O.O., Tesi G.O., Odali W., Nwajei G.E., Martincigh B.S. Polycyclic aromatic hydrocarbons in smoked ethmalosa fimbriata and gymnarchus niloticus from selected fish markets in the Niger Delta, Nigeria. Taylor Fr. 2020;40(5):1367–1380. doi: 10.1080/10406638.2018.1550794. [DOI] [Google Scholar]
- 36.Iwegbue C.M.A., Osijaye K.O., Igbuku U.A., Egobueze F.E., Tesi G.O., Bassey F.I., Martincigh B.S. Effect of the number of frying cycles on the composition, concentrations and risk of polycyclic aromatic hydrocarbons (PAHs) in vegetable oils and fried fish. J. Food Compos. Anal. 2020;94 doi: 10.1016/J.JFCA.2020.103633. [DOI] [Google Scholar]
- 37.Iwegbue C.M., Tesi G.O., Overah L.C., Bassey F.I., Nwadukwe F.O., Martincigh B.S. Concentrations and profiles of polycyclic aromatic hydrocarbons in some popular fish species in Nigeria. J. Food Prot. 2015;78(3):554–560. doi: 10.4315/0362-028X.JFP-14-432. [DOI] [PubMed] [Google Scholar]
- 38.Jahurul M.H.A., Jinap S., Zaidul I.S.M., Sahena F., Farhadian A., Hajeb P. Determination of fluoranthene, benzo[b]fluoranthene and benzo[a]pyrene in meat and fish products and their intake by Malaysian. Food Biosci. 2013;1:73–80. doi: 10.1016/j.fbio.2013.03.006. [DOI] [Google Scholar]
- 39.JECFA, (2016). Evaluation of Certain Food Additives and Contaminants: Eightieth Report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organization. [PubMed]
- 40.Jin W., Otake M., Eguchi A., Sakurai K., Nakaoka H., Watanabe M., Todaka E., Mori C. Dietary habits and cooking methods could reduce avoidable exposure to PCbs in maternal and cord sera. Sci. Rep. 2017;7(1):1–10. doi: 10.1038/s41598-017-17656-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Jinadasa B.K.K.K., Monteau F., Fowler S.W. Review of polycyclic aromatic hydrocarbons (PAHs) in fish and fisheries products; a Sri Lankan perspective. Environ. Sci. Pollut. Res. 2020;27(17):20663–20674. doi: 10.1007/s11356-020-08305-2. [DOI] [PubMed] [Google Scholar]
- 42.Kadac-Czapska K., Knez E., Grembecka M. Food and human safety: the impact of microplastics. Crit. Rev. Food Sci. Nutr. 2024;64(11):3502–3521. doi: 10.1080/10408398.2022.2132212. [DOI] [PubMed] [Google Scholar]
- 43.Kafouris D., Koukkidou A., Christou E., Hadjigeorgiou M., Yiannopoulos S. Determination of polycyclic aromatic hydrocarbons in traditionally smoked meat products and charcoal grilled meat in Cyprus. Meat Sci. 2020;164 doi: 10.1016/J.MEATSCI.2020.108088. [DOI] [PubMed] [Google Scholar]
- 44.Kalteh S., Ahmadi E., Ghaffari H., Yousefzadeh S., Abtahi M., Dobaradaran S., Saeedi R. Occurrence of polycyclic aromatic hydrocarbons in meat and meat products: Systematic review, meta-analysis and probabilistic human health risk. Int. J. Environ. Anal. Chem. 2024;104(15):3533–3547. doi: 10.1080/03067319.2022.2087517. [DOI] [Google Scholar]
- 45.Kim H.-J., Cho J., Kim D., Park T.S., Jin S.K., Hur S.J., Lee S.K., Jang A. Effects of Gochujang (Korean Red Pepper Paste) marinade on polycyclic aromatic hydrocarbon formation in charcoal-grilled pork belly. Food Sci. Anim. Resour. 2021;41(3):481–496. doi: 10.5851/kosfa.2021.e12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Kim M.-J., Hwang J.-H., Shin H.-S. Evaluation of polycyclic aromatic hydrocarbon contents and risk assessment for fish and meat products in Korea. Food Sci. Biotechnol. 2014;23(3):991–998. doi: 10.1007/s10068-014-0134-0. [DOI] [Google Scholar]
- 47.Kumar R., Krishnan M., Kumar P., Narayan G.B. Estimation of demand for fish In Delhi And NCR, India. Socioecon. Chall. 2021;5:2021. 〈https://doi.org/10.21272/Section5(4).46-54.2021〉 [Google Scholar]
- 48.Lauby-Secretan B., Loomis D., Grosse Y., El Ghissassi F., Bouvard V., Benbrahim-Tallaa L., Guha N., Baan R., Mattock H., Straif K. Carcinogenicity of polychlorinated biphenyls and polybrominated biphenyls. Lancet Oncol. 2013;14(4):287–288. doi: 10.1016/S1470-2045(13)70104-9. [DOI] [PubMed] [Google Scholar]
- 49.Lee C.-C., Chen C.S., Wang Z.-X., Tien C.-J. Polycyclic aromatic hydrocarbons in 30 river ecosystems, Taiwan: Sources, and ecological and human health risks. Sci. Total Environ. 2021;795 doi: 10.1016/j.scitotenv.2021.148867. [DOI] [PubMed] [Google Scholar]
- 50.Li A., Tang Q., Kearney K.E., Nagy K.L., Zhang J., Buchanan S., Turyk M.E. Persistent and toxic chemical pollutants in fish consumed by Asians in Chicago, United States. Sci. Total Environ. 2022;811 doi: 10.1016/J.SCITOTENV.2021.152214. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Li G., Wu S., Wang L., Akoh C.C. Concentration, dietary exposure and health risk estimation of polycyclic aromatic hydrocarbons (PAHs) in youtiao, a Chinese traditional fried food. Food Control. 2016;59:328–336. doi: 10.1016/j.foodcont.2015.06.003. [DOI] [Google Scholar]
- 52.Liu Y.P., Wang Y.H., Ye C., Xie B., Yang H. Sedimentary record of polycyclic aromatic hydrocarbons from the Shuanglong catchment, Southwest China. J. Chem. 2017;2017(1):4976574. [Google Scholar]
- 53.Manda P., Dano S., Ehile S.-J., Koffi M., Amani N., Assi Y.A. Evaluation of polycyclic aromatic hydrocarbons (PAHs) content in foods sold in Abobo market, Abidjan, Côte d’Ivoire. J. Toxicol. Environ. Health Sci. 2012;4(6):99–105. doi: 10.5897/JTEHS11.085. [DOI] [Google Scholar]
- 54.MASTAN O.A., COROIAN A., LONGODOR A.L., MARIȘ Ș., BECZE A., TORODOC A., Damian A. Content of polycyclic aromatic hydrocarbons in fish after heat treatment. Sci. Pap. Ser. D. Anim. Sci. 2023;66(2) [Google Scholar]
- 55.Masuda M., Wang Q., Tokumura M., Miyake Y., Amagai T. Simultaneous determination of polycyclic aromatic hydrocarbons and their chlorinated derivatives in grilled foods. Ecotoxicol. Environ. Saf. 2019;178:188–194. doi: 10.1016/j.ecoenv.2019.04.046. [DOI] [PubMed] [Google Scholar]
- 56.Monferran M.V., Garnero P.L., Wunderlin D.A., Bistoni M. de los A. Potential human health risks from metals and As via odontesthes bonariensis consumption and ecological risk assessments in a eutrophic lake. Ecotoxicol. Environ. Saf. 2016;129:302–310. doi: 10.1016/j.ecoenv.2016.03.030. [DOI] [PubMed] [Google Scholar]
- 57.Moon H., Kim D.H., Oh J.E. Dietary exposure to PCBs by seafood cooking method: A Korean study. Chemosphere. 2019;215:775–782. doi: 10.1016/J.CHEMOSPHERE.2018.10.044. [DOI] [PubMed] [Google Scholar]
- 58.Moya J., Garrahan K.G., Poston T.M., Durell G.S. Effects of cooking on levels of PCBs in the fillets of winter flounder. Bull. Environ. Contam. Toxicol. 1998;60(6):845–851. doi: 10.1007/S001289900704. [DOI] [PubMed] [Google Scholar]
- 59.NIN. (2024). Dietary guidelines for Indians. National Institute of Nutrition, India.
- 60.Nisbet I.C.T., LaGoy P.K. Toxic equivalency factors (TEFs) for polycyclic aromatic hydrocarbons (PAHs) Regul. Toxicol. Pharmacol. 1992;16(3):290–300. doi: 10.1016/0273-2300(92)90009-X. [DOI] [PubMed] [Google Scholar]
- 61.Omar W., Mahmoud H. Risk assessment of polychlorinated biphenyls (PCBs) and trace metals in River Nile up- and downstream of a densely populated area. Environ. Geochem. Health. 2017;39 doi: 10.1007/s10653-016-9814-4. [DOI] [PubMed] [Google Scholar]
- 62.Onopiuk A., Kołodziejczak K., Szpicer A., Wojtasik-Kalinowska I., Wierzbicka A., Półtorak A. Analysis of factors that influence the PAH profile and amount in meat products subjected to thermal processing. Trends Food Sci. Technol. 2021;115:366–379. doi: 10.1016/j.tifs.2021.06.043. [DOI] [Google Scholar]
- 63.Oz E. The impact of fat content and charcoal types on quality and the development of carcinogenic polycyclic aromatic hydrocarbons and heterocyclic aromatic amines formation of barbecued fish. Int. J. Food Sci. Technol. 2021;56(2):954–964. [Google Scholar]
- 64.Paiano V., Generoso C., Mandich A., Traversi I., Palmiotto M., Bagnati R., Fattore E. Persistent organic pollutants in sea bass (Dicentrarchus labrax L.) in two fish farms in the Mediterranean Sea. Chemosphere. 2013;93(2):338–343. doi: 10.1016/j.chemosphere.2013.04.086. [DOI] [PubMed] [Google Scholar]
- 65.Peivasteh-Roudsari L., Rahmani A., Shariatifar N., Tajdar-Oranj B., Mazaheri M., Sadighara P., Khaneghah A.M. Occurrence of histamine in canned fish samples (Tuna, Sardine, Kilka, and Mackerel) from Markets in Tehran. J. Food Prot. 2020;83(1):136–141. doi: 10.4315/0362-028X.JFP-19-288. [DOI] [PubMed] [Google Scholar]
- 66.Perelló, G., Martí-Cid, R., Castell, V., Llobet, J.M., & Domingo, J.L. (2009). Concentrations of polybrominated diphenyl ethers, hexachlorobenzene and polycyclic aromatic hydrocarbons in various foodstuffs before and after cooking. Elsevier. Retrieved August 30, 2022, from https://www.sciencedirect.com/science/article/pii/S0278691508007266. [DOI] [PubMed]
- 67.Perelló G., Martí-Cid R., Castell V., Llobet J.M., Domingo J.L. Influence of various cooking processes on the concentrations of PCDD/PCDFs, PCBs and PCDEs in foods. Food Control. 2010;21(2):178–185. doi: 10.1016/J.FOODCONT.2009.05.003. [DOI] [Google Scholar]
- 68.Rasmussen R.R., Søndergaard A.B., Bøknæs N., Cederberg T.L., Sloth J.J., Granby K. Effects of industrial processing on essential elements and regulated and emerging contaminant levels in seafood. Food Chem. Toxicol. 2017;104:85–94. doi: 10.1016/j.fct.2017.02.008. [DOI] [PubMed] [Google Scholar]
- 69.Rawn D.F., Breakell K., Verigin V., Tittlemier S.A., Del Gobbo L., Diamond M., Vanderlinden L., Sit D. Impacts of cooking technique on polychlorinated biphenyl and polychlorinated dioxins/furan concentrations in fish and fish products with intake estimates. J. Agric. Food Chem. 2013;61(4):989–997. doi: 10.1021/jf304010n. [DOI] [PubMed] [Google Scholar]
- 70.Reizer E., Viskolcz B., Fiser B. Formation and growth mechanisms of polycyclic aromatic hydrocarbons: A mini-review. Chemosphere. 2022;291 doi: 10.1016/j.chemosphere.2021.132793. [DOI] [PubMed] [Google Scholar]
- 71.Renieri E.A., Goumenou M., Kardonsky D.A., Veselov V.V., Alegakis A., Buha A., Tzatzarakis M.N., Nosyrev A.E., Rakitskii V.N., Kentouri M., Tsatsakis A. Indicator PCBs in farmed and wild fish in Greece—Risk assessment for the Greek population. Food Chem. Toxicol. 2019;127:260–269. doi: 10.1016/J.FCT.2019.03.027. [DOI] [PubMed] [Google Scholar]
- 72.Rey-Salgueiro L., García-Falcón M.S., Martínez-Carballo E., Simal-Gándara J. Effects of toasting procedures on the levels of polycyclic aromatic hydrocarbons in toasted bread. Food Chem. 2008;108(2):607–615. doi: 10.1016/J.FOODCHEM.2007.11.026. [DOI] [PubMed] [Google Scholar]
- 73.Sahin S., Ulusoy H.I., Alemdar S., Erdogan S., Agaoglu S. The presence of polycyclic aromatic hydrocarbons (PAHs) in grilled beef, chicken and fish by considering dietary exposure and risk assessment. Food Sci. Anim. Resour. 2020;40(5):675. doi: 10.5851/kosfa.2020.e43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74.Sampaio G.R., Guizellini G.M., da Silva S.A., de Almeida A.P., Pinaffi-Langley A.C.C., Rogero M.M., de Camargo A.C., Torres E.A.F.S. Polycyclic aromatic hydrocarbons in foods: biological effects, legislation, occurrence, analytical methods, and strategies to reduce their formation. Int. J. Mol. Sci. 2021;22(11):6010. doi: 10.3390/ijms22116010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75.Sharifiarab G., Ahmadi M., Shariatifar N., Ariaii P. Investigating the effect of type of fish and different cooking methods on the residual amount of polycyclic aromatic hydrocarbons (PAHs) in some Iranian fish: a health risk assessment. Food Chem.: X. 2023;19 doi: 10.1016/j.fochx.2023.100789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76.Sherer, R.A., & Price, P.S. (1993). The effect of cooking processes on PCB levels in edible fish tissue. Quality Assurance (San Diego, Calif.), 2(4), 396–407. [PubMed]
- 77.Siddique R., Zahoor A.F., Ahmad H., Zahid F.M., Karrar E. Impact of different cooking methods on polycyclic aromatic hydrocarbons in rabbit meat. Food Sci. Nutr. 2021;9(6):3219–3227. doi: 10.1002/fsn3.2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Singh L., Agarwal T. Polycyclic aromatic hydrocarbons in diet: concern for public health. Trends Food Sci. Technol. 2018;79:160–170. [Google Scholar]
- 79.Singh L., Agarwal T., Simal-Gandara J. Summarizing minimization of polycyclic aromatic hydrocarbons in thermally processed foods by different strategies. Food Control. 2023;146 doi: 10.1016/j.foodcont.2022.109514. [DOI] [Google Scholar]
- 80.Singh L., Varshney J., Chemistry T.A.-F. Elsevier; 2016. Polycyclic aromatic hydrocarbons’ formation and occurrence in processed food.〈https://www.sciencedirect.com/science/article/pii/S0308814615303526〉 Retrieved July 7, 2022, from. [DOI] [PubMed] [Google Scholar]
- 81.Sun K., Song Y., He F., Jing M., Tang J., Liu R. A review of human and animals exposure to polycyclic aromatic hydrocarbons: health risk and adverse effects, photo-induced toxicity and regulating effect of microplastics. Sci. Total Environ. 2021;773 doi: 10.1016/J.SCITOTENV.2021.145403. [DOI] [PubMed] [Google Scholar]
- 82.Trotter W.J., Corneliussen P.E., Laski R.R., Vannelli J.J. Levels of polychlorinated biphenyls and pesticides in bluefish before and after cooking. J. Assoc. Off. Anal. Chem. 1989;72(3):501–503. [PubMed] [Google Scholar]
- 83.USEPA. (1997). Exposure factors handbook. United States Environmental Protection Agency Philadelphia, PA.
- 84.USEPA, U. (2000). Risk-based concentration table. United States Environmental Protection Agency Philadelphia, PA.
- 85.Viegas O., Novo P., Pinto E., Pinho O., Ferreira I.M.P.L.V.O. Effect of charcoal types and grilling conditions on formation of heterocyclic aromatic amines (HAs) and polycyclic aromatic hydrocarbons (PAHs) in grilled muscle foods. Food Chem. Toxicol. 2012;50(6):2128–2134. doi: 10.1016/J.FCT.2012.03.051. [DOI] [PubMed] [Google Scholar]
- 86.Visciano P. Environmental contaminants in fish products: food safety issues and remediation strategies. Foods. 2024;13(21):3511. doi: 10.3390/foods13213511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 87.Wang Y., Jiao Y., Kong Q., Zheng F., Shao L., Zhang T., Jiang D., Gao X. Occurrence of polycyclic aromatic hydrocarbons in fried and grilled fish from Shandong China and health risk assessment. Environ. Sci. Pollut. Res. 2021;28(25):32802–32809. doi: 10.1007/S11356-021-13045-Y. 2021 28:25. [DOI] [PubMed] [Google Scholar]
- 88.Wang Z., Ng K., Warner R.D., Stockmann R., Fang Z. Reduction strategies for polycyclic aromatic hydrocarbons in processed foods. Compr. Rev. Food Sci. Food Saf. 2022;21(2):1598–1626. doi: 10.1111/1541-4337.12905. [DOI] [PubMed] [Google Scholar]
- 89.Wenaty A., Mabiki F., Chove B., Dalsgaard A., Mdegela R. Occurrence, quantities and probable human health risks of indicatory polychlorinated biphenyls in processed Lates niloticus (L.) products from Lake Victoria in Tanzania. Afr. J. Environ. Sci. Technol. 2019;13(11):417–424. doi: 10.5897/AJEST2019.2728. [DOI] [Google Scholar]
- 90.Willett W., Rockström J., Loken B., Springmann M., Lang T., Vermeulen S., Murray C.J. Food in the Anthropocene: the EAT–Lancet Commission on healthy diets from sustainable food systems. lancet. 2019;393(10170):447–492. doi: 10.1016/S0140. [DOI] [PubMed] [Google Scholar]
- 91.Wirnkor V.A., Ejike Ejiako J., Ngozi V.E., Godson Ndubuisi I., Ebere Enyoh C. Potential health risk index of polyaromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) in fish species from Oguta Lake, Nigeria. Int. J. Environ. Anal. Chem. 2021:1–15. doi: 10.1080/03067319.2021.1946687. [DOI] [Google Scholar]
- 92.Wongmaneepratip W., Vangnai K. Effects of oil types and pH on carcinogenic polycyclic aromatic hydrocarbons (PAHs) in grilled chicken. Food Control. 2017;79:119–125. doi: 10.1016/J.FOODCONT.2017.03.029. [DOI] [Google Scholar]
- 93.Xie Y., Geng Y., Liu X., Chen F., Hu X., Ji J., Ma L. Insights into potential mitigation strategies for polycyclic aromatic hydrocarbons in foods. Food Rev. Int. 2024;40(6):1805–1823. doi: 10.1080/87559129.2023.2238053. [DOI] [Google Scholar]
- 94.Xu X., Liu X., Wang S., Zou Y., Zhang J., Liang L., Wen C., Li Y., Xu X., He X., Liu G., Xu X. Relationship between PAH4 formation and thermal reaction products in model lipids and possible pathways of PAHs formation. J. Hazard. Mater. 2024;465 doi: 10.1016/j.jhazmat.2023.133374. [DOI] [PubMed] [Google Scholar]
- 95.Zabik M.E., Booren A.M., Daubenmire S., Pascall M.A., Zabik M.J., Welch R., Humphrey H. Pesticides and total polychlorinated biphenyls residues in raw and cooked walleye and white bass harvested from the Great Lakes. Bull. Environ. Contam. Toxicol. 1995;54(3) doi: 10.1007/BF00195111. 〈https://www.osti.gov/biblio/45296〉 [DOI] [PubMed] [Google Scholar]
- 96.Zabik M.E., Zabik M.J. Polychlorinated biphenyls, polybrominated biphenyls, and dioxin reduction during processing/cooking food. Adv. Exp. Med. Biol. 1999;459:213–231. doi: 10.1007/978-1-4615-4853-9_14/COVER. [DOI] [PubMed] [Google Scholar]
- 97.Zahir A., Ge Z., Khan I.A. Public health risks associated with food process contaminants – a review. J. Food Prot. 2025;88(2) doi: 10.1016/j.jfp.2024.100426. [DOI] [PubMed] [Google Scholar]
- 98.Zelinkova Z., Wenzl T. The occurrence of 16 EPA PAHs in food – a review. Polycycl. Aromat. Compd. 2015;35(2–4):248–284. doi: 10.1080/10406638.2014.918550. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 99.Zhang Y., Chen X., Zhang Y. Analytical chemistry, formation, mitigation, and risk assessment of polycyclic aromatic hydrocarbons: from food processing to in vivo metabolic transformation. Compr. Rev. Food Sci. Food Saf. 2021;20(2):1422–1456. doi: 10.1111/1541-4337.12705. [DOI] [PubMed] [Google Scholar]
- 100.Zhu Y., Li X., Huang J., Zhao C., Qi J., Jin Q., Wang X. Correlations between polycyclic aromatic hydrocarbons and polar components in edible oils during deep frying of peanuts. Food Control. 2018;87:109–116. doi: 10.1016/J.FOODCONT.2017.12.011. [DOI] [Google Scholar]
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