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Measurement of polycyclic aromatic hydrocarbons (PAHs) in edible mushrooms (raw, grilled and fried) using MSPE-GC/MS method: a risk assessment study

Measurement of polycyclic aromatic hydrocarbons (PAHs) in edible mushrooms (raw, grilled and... The purpose of this study was to evaluate the concentration of PAHs and health risk in edible mushrooms using magnetic solid phase extraction (MSPE) and gas chromatography/mass spectrometry (GC/MS) method. Based on the results, the concentration of total PAHs was in the range from 0.82 to 6.25 µg/kg (with the means of 3.85 ± 0.24 µg/ kg). In this study, acenaphthylene (Ace) had the maximum mean level in mushroom samples (0.84 ± 0.19 μg/kg) and benzo(a)pyrene (BaP), acenaphthene (Ac), phenanthrene (Pa), dibenzo[a,h]anthracene (DahA), benzo(a)anthracene (BaA), fluoranthene (Fl), indeno[1,2,3-cd]pyrene (IP) and benzo[g,h,i]perylene (BgP) had minimum mean level (non- detected). The highest mean values of total PAHs (4.88 ± 0.30 μg/kg) was detected in grilled mushroom samples and lowest mean of total PAHs (2.77 ± 0.04 μg/kg) was detected in raw mushroom samples. The concentration of contamination in edible mushrooms was raw < fried > grilled, respectively. Furthermore, heat map visualization was applied to evaluate the relationship between the quantity and type of 16 PAHs in edible mushroom samples. Ulti- mately, the incremental lifetime cancer risk in edible mushrooms for adults and children was 6.85E-08 and 3.47E-07, –6 respectively, which was lower than the acceptable risk limit (10 ) and all of the edible mushrooms sold in Tehran were considered safe for consumers. Keywords: Polycyclic aromatic hydrocarbons, Edible mushrooms, MSPE, GC–MS, Health risk assessment Introduction (Agaricus bisporus and Pleurotus ostreatus are two edi- Considering the high content of protein and essential ble mushrooms that are cultivated in most parts of the elements of edible mushrooms (cultivated and wild), its world) and due to the approach of people to use more daily consumption in the world is increasing. Further- plant proteins, the process of mushroom production is more, wild and farmed mushrooms have been partially expected in the future will increase [21]. substituted for animal proteins in many countries, espe- Studies have shown that mushrooms are low in fat but cially in Europe and Asia, due to their nutrients, health high in protein, carbohydrates and fiber. They also con - benefits, and pleasant taste [11, 57]. The number of cul - tain a variety of trace elements and minerals such as cop- tivated mushroom species has reached about 30 species per and potassium and vitamins such as folate, riboflavin and niacin [10, 45, 59]. Consumption of edible mush- rooms and mushrooms products in the daily diet can *Correspondence: nshariati@tums.ac.ir; moazzen.mojtaba@gmail.com be beneficial for human health (this product has anti- Department of Environmental Health Engineering, School of Public tumor, antioxidant, anti-viral, reduction of diabetes, cho- Health, Tehran University of Medical Sciences, Tehran, Iran Full list of author information is available at the end of the article lesterol, asthma, allergies, stress and insomnia). Edible © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 2 of 11 mushrooms commonly contain 10% dry matter and 90% HF-LPME [hollow fiber liquid phase micro-extraction water. Protein is an important component of the dry mat- (LPME)] [2, 43, 51, 52]. Fatty components and material ter of the mushrooms [9, 49]. with alcoholic caustic solutions, are saponified, to avoid PAHs chemically include 2 or more rings of benzene difficulties from lipids [13, 52, 53]. Next to the saponifica - attached at the levels of angular, cluster or linear. PAHs tion phase, SPE or LLE can be used for extraction [23, 26, are environmental pollutants that are mainly caused 27, 32, 34, 35]. To identify PAHs in food products, little by incomplete combustion of organic matter (oil, coal, research has ever been done using GC/FID (flame ioniza - wood, gasoline, etc.). These compounds are mostly tion detector) or GC/MS, HPLC (high performance liq- spread through anthropological activities. However, uid chromatography) equipped with detection of UV/FL some PAHs in the environment are caused by natural (ultraviolet and fluorescence) and FLD [2, 24, 25, 36, 37, resources like fires, natural disasters, or oil and coal dis - 39, 40, 42]. posal and volcanic activity, so they are existing in food, For the first time in Iran, this research was conducted soil, water and air [19, 20, 55]. by an effective, simple and reliable technique for deter - PAHs can be transported and accumulated in plant tis- mine of 16 PAHs in raw, fried, grilled edible mushrooms. sues through soil, air and water. The surface of vegeta - For this purpose, the sample was prepared and clean- ble wax can also absorb PAHs from the air. The levels of up based on the use of MWCNT (multi-walled carbon PAHs determined in vegetables are usually in concentra- nanotubes) as MSPE adsorbent. The prepared sample tions of 0.01–0.5 µg/kg, however, reliant on the environ- was injected into GC–MS and the PAHs level were meas- ment, higher concentrations are observed and in special ured and in the second stage, the carcinogenic and non- cases, it may exceed 5 µg/kg. On the other hands, several carcinogenic health risk was assessed. factors are involved in the formation of PAHs during the preparation of food. Some of these factors include fuel Materials and methods (gas, wood, charcoal and electric power supplies), cook- Reagents ing method (roasting, frying and baking), temperature, PAHs mix standards containing sixteen mentioned PAHs cooking time, food fat, oil drips on the flame, and prox - were obtained from Supelco Company (Bellefonte, PA, imity to or direct contact between the food and flame USA). In dichloromethane, the standard solutions were [19, 20]. ready, with all of 16 PAHs (0.1 mg/mL). After that, these Receipt rate PAHs in various parts of the world stock standard solutions with dichloromethane-methanol depends on their diet. According to classification of the (50:50, v/v) were diluted every week to make a solution WHO (World Health Organization), humans are exposed of working mixed (1  mg/mL for each PAH) that it was to PAHs through respiratory, gastrointestinal, and dermal applied to determine extraction function with variant modes of absorption. The absorption of contaminants situations. For internal standard (I.S.) biphenyl, was used from the gastrointestinal tract increases when it is solu- (0.05  µg/mL in methanol). Working and stock solutions ble in a high-fat varied diet. Experiments revealed that were preserved at four centigrade degree. MWCNT were in animals, 30–50% of PAHs are absorbed through the bought from Hanwha nanotech Company (MWCNT gastrointestinal tract, and it is mainly metabolized in the CM-95, Korea). Similar to the past research, MWCNT- liver [1, 6, 15]. MNP (as adsorbent) was ready [41]. Finally, all extra sol- The USEPA (United State Environmental Protection vents and chemicals were of grade of analytical-reagent. Agency) has mentioned sixteen PAH analytes including; chrysene (Ch), IP, fluorene (F), benzo(b)fluoranthene Preparation and sampling of mushrooms (BbF), naphthalene (NA), Ace, BaP, Ac, BgP, anthracene One hundred and twenty samples of packaged mush- (A), benzo(k)fluoranthene (BkF), Pa, pyrene (P), Fl, BaA rooms and bulk (3 branded packaging, and 1 bulk brand) and DahA. In terms of food safety, BaP can be deliber- were purchased in December 2020 from the main centers ated as a marker for carcinogenicity in foodstuff [8, 12, of supply of fruits and vegetables. The fresh mushroom 23]. samples with deionized water were washed and then There are several techniques to extract PAHs from dried with flow of air and cut into pieces in the shade, food samples [e.g., liquid liquid extraction (LLE), Soxhlet then some of them were fried and grilled. The samples apparatus, solid-phase extraction (SPE) and pressurized grilled on coal at 150 °C for 5 min and fried with a fryer at liquid extraction (PLE)]. The most ordinarily used plans a temperature of 120 °C for 5 min. After preparing sam- to extract PAHs compounds from an intricate solution ples, homogenized, in nylon vacuum-packed and kept at matrix include silica cartridges, straight immersion solid- − 18 °C in the place of dark until analysis (for no longer phase micro-extraction (SPME), LLE after saponification than 4  weeks). The samples were evaluated in duplicate with caustic soda, columns with gel beads and two phase and the mean values were applied for quantification. Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 3 of 11 Sample preparation at 230° (on the Celsius scale). At 70 eV, the energy of elec- Five grams of each frozen and crushed samples, weighed tronic beam of the MS was regulated. The qualification and transferred to 50 mL conical tube. Then, added 1 mL was done by comparing the achieved mass spectra and of the internal standard to the samples. Afterward, the times of retention to reference spectra. By injection cali- sample was homogeneous, and after adding 7.5  mL of bration standards in same GC/MS conditions, the times 1  M potassium hydroxide and 7.5  mL of 30%v/v metha- of retention were obtained. With using SIM mode, the nol–acetonitrile, homogenization was performed on PAH analytes were quantified. a shaker with 300 rounds for 5  min. The samples were placed in ultrasonic baths of German model Alma, at a temperature of 40–45 °C for 15–30 min at a frequency of Health risk assessment 130 Hz. After removing the conical tubes from the ultra- In this research, daily dietary (DD) PAHs contact levels sonic bath and their temperature reaches the ambient (µg.kg-1 body weight) and BaP daily intake equivalents temperature, for separation of the fat phase, the samples [∑(BaPeqi)] (µg/day) through consuming mushroom for half an hour were centrifuged at 4500 rpm. The super - was conducted based on Eq. 1 and 2: natant was then slowly moved to a 100  mL Erlenmeyer C × IR flask. The pH was measured by a pH meter. To adjust the DD = (1) BW pH to 6.5–7, because the initial pH of the samples was 13, a few drops of concentrated hydrochloric acid (about 6 drops) were added to the samples to reduce pH 9–10, ( C × TEF ) × IR i i i=1 DI = (2) BaPeq then with hydrochloric acid (1 M), slowly adjusted to pH BW 6.5–7. where IR is the weight of mushroom consumed After primary clean up, for adsorption of analytes, −1 (3.56 g  day ) [22]; C is the level of the PAHs congener 10 mg of magnetic nanocarbon adsorbent and 500 mg of i in mushroom,, the toxicity equivalency factor (TEF) NaCl were added to the samples and then homogenized was adopted to calculate BaP equivalent concentration with a shaker for 10  min. The samples were then trans - (Table  1), BW, the average Iranian weight of body (for ferred to the incubator at 40–45 °C for 12–24 h. The last adults 70 and children 15 kg). step involves separating the analytes from the absorbent, Besides, the ILCR (incremental lifetime cancer risk) which, after the relative drying of the samples, add 5 mL of mushroom due to PAHs dietary exposure was evalu of dichloromethane as solvent to the specimens. It was ated according to Eq. (2).[5, 56]: then homogenized with a shaker at 300 rpm for 10 min. Then, by a magnet (external), the non-impure fluid was ILCR = DI × EF × E × CSF/AT BaPeq D (3) slowly moved to the vials. The samples are then sealed, where DI , EF, AT, and CSF denote the daily intake covered with aluminum, and stored at − 18 °C until they BaPeq of BaP equivalents, exposure duration (year), lifespan are sent to the laboratory and injected into the GC–MC for carcinogens (25,550  days)[54] and the frequency of device to prevent light from entering. exposure (365  days/year) and slope factor of oral cancer for BaP which is 7.3  (mg/kg-day)(USEPA. Risk assess- ment guidance for Superfund: volume III part A and risk Analytical conditions and instrumental assessment. Washington), respectively. The examination was done on a device of Agilent GC 6890 with a detector of MS 5973 quadrupole (Technolo- gies of Agilent, Palo Alto, CA, USA). It was regulated with a column of capillary of DB-5  ms (30  m, 0.25  mm Table 1 PAHs and their toxic equivalent factors ( TEFs) i.d., 0.25  μm thickness of film). For inlet, the mode was splitless. The temperatures were regulated as follows: the PAHs TEF PAHs TEF primary temperature of oven 70° (on the Celsius scale), Benzo(a)pyrene (BaP) 1 Anthracene (A) 0.01 the temperature of injector 290° (on the Celsius scale); Dibenz(a,h)anthracene (DahA) 1 Naphthalene (NA) 0.001 retained for 1  min, at a rate of 10° (on the Celsius scale) Benzo(k)fluoranthene (BkF) 0.1 Acenaphthylene (Ac) 0.001 /min raised temperature to 295° (on the Celsius scale), Indeno(l,2,3-cd)pyrene (IP) 0.1 Acenaphthene (Ace) 0.001 retained for 7  minutes. The temperature of transfer line Benz(a)anthracene (BaA) 0.1 Phenanthrene (Pa) 0.001 was retained at 300° (on the Celsius scale). For carrier gas, Benzo(b)fluoranthene (BbF) 0.1 Fluorine (F) 0.001 helium (He) with constant flow was used (1  mL/min). Chrysene (Ch) 0.01 Pyrene (P) 0.001 The temperature of quadrupole was retained at 150° (on Benzo(g,h,i)perylene (BgP) 0.01 Fluoranthene (Fl) 0.001 the Celsius scale) and temperatures of source were kept Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 4 of 11 Table 2 Comparison of current research with other studies with different adsorbents and in different foods Sample Adsorbent Analysis method Instrumental LOD Linear range Recovery % Reference analysis Beef, lamb, MWCNT-Fe O Magnetic-SPE GC–MS 0.075–0.200 (µg/ 0.1–250 (µg/kg) 81.3–96.7 [41] 3 4 chicken meats kg) Tea and coffee MWCNT-Fe O Magnetic-SPE GC–MS 0.040–0.084 (µg/ 0.050–10.000 (µg/ 91.1–102.3 [52] 3 4 kg) kg) Milk and milk MWCNT-Fe O Magnetic-SPE GC–MS 0.040–0.075 (µg/ 0.050–1.000 (µg/ 86.1–100.3 [53] 3 4 powder kg) kg) Water sample MWCNT μ-SPE GC–MS 0.0042–0.0465 0.1–50.0 (ng/mL) 72.3–99.2 [16] (ng/mL) GC–FID 0.03–1.0 (ng/mL) 0.1–200 (ng/mL) 88–105 [31] Water sample MWCNT HS-μ-SPE c d Environmental IL-MIL-100(Fe) VA-d-μ-SPE GC–FID 0.002–0.005 (ng/ 0.02–200 (ng/mL) 97.0–103.5 [46] water, vegetable, mL) and fruit juice samples Environmental MWCNT SPE GC–MS 0.002–0.0085 (ng/ 0.02–5.00 (ng/mL) 76.0–125.5 [30] water samples mL) Environmental CTAB/TiO μ-SPE HPLC–UV 0.026–0.82 (ng/ 0.2–100.0 (ng/mL) 75.0–114 [17] water samples mL) Water samples Nylon 6 com- μ-SPE UPLC-DAD 0.050–0.580 (ng/ – 80–111 [50] posite mL) Environmental ZIF-8 μ-SPE GC–MS 0.002–0.012 (ng/ 0.1–50 (ng/mL) 96.9–106.5 [14] water samples mL) Water samples MCFG μ-SPE GC–MS 0.2–1.8 (ng/mL) 0.01–100 (ng/mL) 67.5–106.9 [44] Real water and PFu/Fe O μ-SPE GC–FID 0.005–0.02 (ng/ 0.02–200 (ng/mL) 93.2–99.2 [4] 3 4 urine samples mL) Mushroom MWCNT-Fe O Magnetic-SPE GC–MS 0.020–0.080 (µg/ 0.1–250 (µg/kg) 91.2–101.7 Current study 3 4 samples kg) μ-SPE solid-phase micro-extraction Headspace solid phase microextraction Liquid-modified metal–organic frameworks Vortex-assisted dispersive solid-phase microextraction Cetyltrimethylammonium bromide modified ordered TiO Zeolite imidazolate framework 8 Magnetic chitosan functionalized graphene oxide Magnetite nanoparticles modified with polyfuran Statistical analyses Results and discussion The results were analyzed using SPSS version 25 soft - Performance assessment of the analytical method ware. At first, descriptive indexes of variables such as In the 1st step, the analytical technique involved liquid variance, deviation of variance, mean, maximum and extraction of PAHs and in the 2nd phase, SPE technique minimum were obtained. To compare other PAHs values using a composite of MNP-sized. The extracted polycy - (means), analysis of variance (one-way) was applied. A clic aromatic hydrocarbons were then evaluated using a heat map clustering was performed to establish a more technique of GC–MS (sensitive instrument). The mass precise distinction among the PAHs congener in mush- spectrum (full scan), toward the recognition goal, the rooms [26–28]. Multivariate analysis of statistical was ratios of four characteristic ions and the ± 0.5 percent used to assess the correlation among NA, Ace, F, A, B(k) relative retention time (RRT) tolerance criteria compared F, Ch, B(b)F and P concentration. Analysis of heat map to the standard was applied. For purpose of quantifica - (variable scaling mode: z-score; method of clustering: tion, the most intense ion was applied of each compound. average linkage; distance measurement method: Pearson The compounds were quantified by SIM mode (selected was performed to evaluate the correlation between sam- ion monitoring). The dwell time (for each ion) was reg - ples online at http:// www. heatm apper. ca/. ulated at 100  min. To reduce the time of examination, the conditions of GC were selected while allowing all Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 5 of 11 Table 3 Statistics analysis of PAHs levels in mushroom samples were supplied and the calibration curves were made (µg/kg) (0.050–5.000 µg/kg) with a coefficient of correlation was 0.979–0.994. Based on the guideline of International Min. Max. Mean SD Council for Harmonization (ICH), the limit of quantifi - NA 0.1 1.03 0.67 0.15 cation (LOQ) for each compound, was determined [41]. Ace 0.24 1.38 0.84 0.19 The conclusion of validation tests designated that limit Ac nd nd nd nd of detection (LODs) and LOQs for the PAHs analytes F 0.09 0.43 0.28 0.07 altered 0.020–0.080 and 0.063–0.242 µg/kg, respectively. Pa nd nd nd nd According to the precision of interday via analysis QC A 0.14 0.61 0.37 0.1 (quality control) samples, ready on three repeated days Fl nd nd nd nd at four levels, the accuracy of the method was assessed. P 0.06 0.63 0.44 0.12 Other hands, for all of the PAH compounds, the preci- BaA nd nd nd nd sion of interday values were fewer than 8.9%. For repeat- Ch 0.09 0.81 0.34 0.09 ability, the estimated values were between 4.1 and 10.6 BbF nd 0.57 0.39 0.08 percent and the recoveries estimated between 91.2 and BkF 0.1 0.79 0.52 0.1 101.7 percent. By all these results to measurement the BaP nd nd nd – PAHs in kinds of edible mushroom samples, the reliabil- IP nd nd nd – ity and feasibility of the established technique were con- DahA nd nd nd – firmed. By examining 120 edible mushroom samples, the BgP nd nd nd – selectivity of the technique was confirmed. At the end, Total 0.82 6.25 3.85 0.24 no interfering peak was seen, in the area of the analytes PAH4 0.19 1.38 0.73 0.05 and internal standard. A comparison of the present study with other studies with adsorbents and in different foods can be seen in Table 2. The findings show acceptable lev - compounds (PAHs) to elute in acquisition collections els for different adsorbents in different foods. include a proper number of ions for checking. For each compound were controlled two qualifier ions and one quantitation [41]. For analysis, the conditions of optimum Table 4 Concentration of PAEs in raw samples and different process of mushroom samples (µg/kg) Process Raw Fried Grilled P-Value n Mean Std. deviation n Mean Std. deviation n Mean Std. deviation NA 20 0.45 0.01 20 0.66 0.01 20 0.89 0.02 0 Ace 20 0.69 0.02 20 0.85 0.02 20 0.98 0.03 0 Ac 20 nd – 20 nd – 20 nd – – F 20 0.21 0.01 20 0.28 0.01 20 0.35 0.02 0 Pa 20 nd – 20 nd – 20 nd – – A 20 0.23 0.01 20 0.38 0.01 20 0.49 0.03 0 Fl 20 nd – 20 nd nd 20 nd – – P 20 0.31 0.01 20 0.47 0.012 20 0.54 0.01 0 BaA 20 nd nd 20 nd – 20 nd – – Ch 20 0.18 0.01 20 0.34 0.01 20 0.52 0.02 0 B(b)F 20 0.33 0.01 20 0.36 0.02 20 0.49 0.01 0 B(k)F 20 0.38 0.02 20 0.52 0.03 20 0.65 0.03 0 BaP 20 nd – 20 nd – 20 nd – – IP 20 nd – 20 nd – 20 nd – – DhA 20 nd – 20 nd – 20 nd – – BgP 20 nd – 20 nd – 20 nd – – Total 20 2.77 0.04 20 3.88 0.12 20 4.88 0.3 0 PAH4 20 0.5 0.01 20 0.88 0.03 20 0.98 0.05 0 Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 6 of 11 Table 5 Uncertainly analysis for the daily intake (µg/kg bw/day) BaP concentration was below the standard levels (ND or of PAHs in mushroom non-detected) in all samples. In this research, Ace had the maximum mean level in edible mushroom samples Compound Percentiles name (0.84 ± 0.19 μg/kg) and Ac, Pa, Fl, BaA, BaP, IP, DhA and 5% 50% 75% 95% BgP had minimum mean level (ND). Among the groups recommended in EC Regulation Number 835/2011 Adults NA 2.55E-5 3.35E-5 3.74E-5 4.48E-5 (2011), for PAH4 maximum value of 1  μg/kg was regu- Ace 3.22E-5 4.28E-5 4.74E-5 5.72E-5 lated in processed cereal-based foods and 50  μg/kg in F 1.05E-5 1.40E-5 1.56E-5 1.89E-5 dried herbs. The mean levels of PAH4 detected in the A 1.39E-5 1.83E-5 2.08E-5 2.44E-5 current research were below the standard limits since the B(k)F 1.68E-5 2.23E-5 2.47E-5 2.90E-5 detected values were 0.73 ± 0.05 μg/kg in edible mush- P 1.28E-5 1.73E-5 1.96E-5 2.25E-5 room samples. B(b)F 1.50E-5 2.01E-5 2.26E-5 2.65E-5 Igbiri et  al. [18] by measuring PAHs in mushroom Ch 1.99E-5 2.64E-5 2.94E-5 3.41E-5 showed that the ƩPAHs varied from ND to 8320 µg/kg, Children NA 1.18E-4 1.58E-4 1.76E-4 2.06E-4 and BaP ranged ND-2460 µg/kg, which in some samples Ace 1.48E-4 1.97E-4 2.22E-4 2.62E-4 were lower and in others samples higher than the our F 5.11E-5 6.63E-5 7.41E-5 8.67E-5 study. Abou-Arab et al. [1] by measuring PAHs in fruits A 6.44E-5 8.63E-5 9.70E-5 1.12E-4 and vegetables showed that the maximum concentra- B(k)F 7.80E-5 1.04E-4 1.16E-4 1.36E-4 tion of ƩPAHs was 8.977  µg/kg in Spinach samples, P 6.12E-5 8.01E-5 8.96E-5 1.07E-4 6.196  µg/kg in potato samples, 2.867  µg/kg in apple B(b)F 7.03E-5 9.21E-5 1.04E-4 1.21E-4 samples and 2.334 µg/kg in guava samples, which were Ch 9.43E-5 1.22E-4 1.37E-4 1.65E-4 higher than the our study (except apple and guava). Ashraf et al. by measuring PAHs in fruits and vegetables showed that anthracene level was higher in all vegeta- bles, among all PAH congeners. The highest concentra - tion of BaP was in potatoes (2.90 ± 1.10 μg/kg) and in 0.12 turnip (2.10 ± 1.09  μg/kg), respectively. The levels of ƩPAH of the root vegetables like carrot and potato were 0.1 presented higher values (11  μg/kg), however levels of ƩPAH in turnip showed a lower ratio (9.26  μg/kg). In 0.08 tuberous vegetable cores, the cores were less contami- nated than the peels. For leafy vegetables, highest con- 0.06 centration of PAHs were presented in cabbage (8.34 μg/ kg), which were higher than our results [6]. Camargo 0.04 et  al. [8] by measuring PAHs in fruits and vegetables showed that the mean concentrations of ΣPAHs were 0.02 3.77 in grape, 3.87 in pear, 4.05 in apple, 8.86 in cab- bage, 9.50 in tomato and 13.53 μg/kg in lettuce, and Ch was not detected in any sample and total PAHs were more than our study (except in apple) and Ch was less NA Ace F A BkF P BbF Ch than our study. Bishnoi et al. [7] by examining PAHs in Fig. 1 Comparison of the most and least contribution to daily dietary intake of the PAH congeners in mushrooms fruits and vegetables showed that the ƩPAHs concen- tration in different fruit and vegetable samples ranged from 25.5 to 51.7 and 59.6 to 194.3  µg/kg, respec- tively that were higher than our study. Lee et  al. [28] Evaluation of PAHs levels in mushroom samples by measuring PAHs in fruits and vegetables showed In Table  3, the mean values of PAHs compounds in that the mean level of BaP in fruits was not detected mushroom samples are existing. The recorded means of and in vegetables was 0.05  µg/kg that was more than total PAHs in edible mushroom was 3.85 ± 0.24  μg/kg our study. Zhu et al. [62] by measuring PAHs in vegeta- (Table  3). The European Commission (EC) established bles showed that the estimated levels of total 15 PAHs maximum level of BaP in various foods (for dried herbs were 79 µg/kg in cabbage shoots and 83 µg/kg in carrot 10  µg/kg). According to existing regulations, concentra- roots that were higher than our results. Lei et al. [29] by tion of BaP in fruit and vegetable shouldn’t be more than measuring PAHs in vegetables showed that the ƩPAHs 1  µg/kg [47]. The present outcomes exhibited that the daily intake of benzo(a)pyrene equivalents Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 7 of 11 Fig. 2 Estimation of the ILCR of PAHs in mushroom by Monte Carlo simulation concentrations in these vegetables were from 3.91 to samples had minimum mean values of them (2.77 ± 0.04 96.98  µg/kg that were higher than our results. Waqas and 0.5 ± 0.01  μg/kg, respectively). BaP in all samples et  al. [61] by measuring PAHs in fruits and vegetables was not detected. The amount of contaminant in the reported that the level of total PAHs in vegetables were mushroom was raw < fried < grilled, which may be due from 51.6 to 402 μg/kg on dry weight bases, which were to the use of coal or the use of direct heat in grilled pro- higher than this research. Wan et al. [60] by measuring cess. Other studies were shown analogous results [3, 15, PAHs in vegetables reported that the PAHs levels in the 41]. vegetable samples were ranged from 26.35 to 3748  μg/ kg with the mean of 656.3 μg/kg that were higher than Human Risk assessment and exposure to toxic elements our results. In a research published by Paris et  al. [48] The daily dietary intake of the PAHs congener through reported that in several studies, the level of some PAHs edible mushrooms consumption for children and adults in various vegetables and fruits can exceed 0.5  μg/kg in Iran are listed in Table  5. For adults, the rank order and even reach 5 μg/kg. of PAHs congener based on DD (P95) was Ace (5.72E- The existence of PAHs in food products relies on the 05) > NA (4.48E-05) > Ch (3.41E-05) > B(k)F (2.90E-05) time of growing, the type of plants and plants growth > B(b)F [2.65E-05 > A (2.44E-05) > P (2.25E-05)]. > F environment (e.g., water, air and soil) as well as the prox- (1.89E-05). The rank order of PAHs congener based on imity of farms of plants to high-traffic highways and DD (P95) for children was Ace (2.62E-04) > NA (2.06E- industrial centers. 04) > Ch (1.65E-04) > B(k)F (1.36E-04) > B(b)F (1.21E- The results of this study show a lower level of pollution 04) > A (1.12E-04) > P (1.07E-04). > F (8.67E-05). compared to other studies, which could be due to reasons Furthermore, the higher and lower contribution to over- such as distance from contaminated areas, use of water, all, DD in mushrooms was related to BkF and F, respec- soil and compost free of pollution, careful and continu- tively (Fig. 1). ous monitoring of agricultural products especially edible Further, the outcomes of the Monte Carlo simulation mushrooms. revealed that the mean of ILCR for adults and children based on P95 was 6.85E-08 and 3.47E-07. In Fig.  2, the Comparison of the PAHs concentration between raw carcinogenic risk for PAHs congener was clearly lower –6 samples and various process (fried and grilled) than the acceptable risk level (10 ) by USEPA. In a In Table  4, the means of the level of PAHs among raw research conducted in Nigeria, the ILCR ranged from –8 –6 mushroom samples and process mushroom samples 1.56 × 10 to 1.73 × 10 with the uppermost calculated (grilled and fried) were demonstrated. The uppermost risk found for edible mushrooms [18]. mean values of total sixteen PAHs and PAH4 were The contamination profiles, human exposure risks of detected in grilled mushroom samples 4.88 ± 0.30 and PAHs and corresponding knowledge obtained are cru- 0.98 ± 0.05  μg/kg, respectively, and raw mushroom cial for contamination mitigation strategies and human Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 8 of 11 Fig. 3 Heat map of PAHs in mushroom health risk development on the PAHs study. The biologi - compounds change with food consumption, water, sedi- cal monitoring of human exposure about the dangers and ment, soil, sites and seasons, air–soil exchange and asso- potential side effects of PAHs depend on various param - ciated carcinogenic risks of PAH compounds [33, 38]. eters, including the route and concentration of exposure, Physical, chemical, and biological methods are the most as well as the toxicity of the PAHs. It is important to preferable and cost-effective remediation methods for demonstrate linkages between outcomes of risk patterns contamination degradation or transformation until safe and similar risk behavior of PAHs and may thus give the levels in food, air, water, and soil [35–37, 39]. best possible risk assessment in realistic, intermediate and complex contaminant distribution. The two main Multivariate analysis of PAH congeners parameters which contribute to general PAHs persis- Heat map was used to understanding the relationships tence in the environment depends on molecule stability among the PAHs congener in different raw, fried and and hydrophobicity. However, the percentages of PAH grilled samples. A basic heat map, in addition to grouping Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 9 of 11 3. Alomirah H, Al-Zenki S, Al-Hooti S, Zaghloul S, Sawaya W, Ahmed N, columns and rows of comparable variables, gives a very Kannan K (2011) Concentrations and dietary exposure to polycyclic general impression of the largest and smallest variables in aromatic hydrocarbons (PAHs) from grilled and smoked foods. Food the generating matrix. Furthermore, heat maps revealed Control 22:2028–2035. https:// doi. org/ 10. 1016/j. foodc ont. 2011. 05. 024 4. Amiri A, Baghayeri M, Kashmari M (2016) Magnetic nanoparticles modi- that the different samples (raw, fried and grilled is con - fied with polyfuran for the extraction of polycyclic aromatic hydrocar - sidered as independent factors in the PAHs congener bons prior to their determination by gas chromatography. Microchim clustering. The heat map clustered samples of edible Acta 183:149–156. https:// doi. org/ 10. 1007/ s00604- 015- 1622-5 5. Antoine JM, Fung LAH, Grant CN (2017) Assessment of the potential mushrooms into 2 major clusters and three sub clus- health risks associated with the aluminium, arsenic, cadmium and lead ters (Fig. 3). The first cluster such as A, Ace, B(k)F, Ch, F content in selected fruits and vegetables grown in Jamaica. Toxicol and P contains two sub-groups, The second cluster only Rep 4:181–187. https:// doi. org/ 10. 1016/j. toxrep. 2017. 03. 006 6. Ashraf MW, Salam A (2012) Polycyclic aromatic hydrocarbons (PAHs) in includes B(b)F. ClustVis was used to visualizing cluster- vegetables and fruits produced in Saudi Arabia. B Environ Contam Tox ing of similarity and variability data. The NA, Ace, Ch, F 88:543–547 and P concentrations were the closer, indicating that the 7. Bishnoi NR, Mehta U, Pandit G (2006) Quantification of polycyclic aro - matic hydrocarbons in fruits and vegetables using high performance concentration changes of these PAHs congener had simi- liquid chromatography. IJCT. https:// doi. org/ 10. 3923/ jest. 2011. 611. 620 lar trend in different samples (raw, fried and grilled). 8. Camargo MCR, Toledo MCLF (2003) Polycyclic aromatic hydrocarbons in Brazilian vegetables and fruits. Food Control 14:49–53. https:// doi. Acknowledgements org/ 10. 1016/ S0956- 7135(02) 00052-X This research was conducted with the support of Tehran University of Medical 9. Chen S, Yuan B, Xu J, Chen G, Hu Q, Zhao L (2018) Simultaneous sepa- Sciences, Tehran, Iran. ration and determination of six arsenic species in Shiitake (Lentinus edodes) mushrooms: method development and applications. Food Authors’ contributions Chem 262:134–141. https:// doi. org/ 10. 1016/j. foodc hem. 2018. 04. 036 NS: supervision, methodology, writing—reviewing and editing. GJK: data 10. Cheung P (2010) The nutritional and health benefits of mushrooms. curation, conceptualization, writing—reviewing and editing. MA: visualization, Nutr Bull 35:292–299. https:// doi. org/ 10. 1111/j. 1467- 3010. 2010. 01859.x investigation, software, methodology, validation. MM: methodology, software, 11. Chhetri K, Senapoty D, Sharma D (2018) Management of contaminant validation, MM: methodology, visualization, investigation, PS: validation, mycoflora of oyster mushroom (var-Pleurotus florida) with botanicals writing—reviewing and editing. All authors read and approved the final and GRAS chemicals. Int J Curr Microbiol App Sci 7:1972–1978 manuscript. 12. Di Bella C, Traina A, Giosuè C, Carpintieri D, Dico GML, Bellante A, Del Core M, Falco F, Gherardi S, Uccello MM (2020) Heavy metals and Availability of data and materials PAHs in meat, milk, and seafood from Augusta area (Southern Italy): The data set used will be available upon reasonable request from the cor- contamination levels, dietary intake, and human exposure assessment. responding author. Front. https:// doi. org/ 10. 3389/ fpubh. 2020. 00273 13. Dobaradaran S, Akhbarizadeh R, Mohammadi MJ, Izadi A, Keshtkar M, Tangestani M, Moazzen M, Shariatifar N, Mahmoodi M (2020) Deter- Declarations mination of phthalates in bottled milk by a modified nano adsorbent: presence, effects of fat and storage time, and implications for human Ethics approval and consent to participate health. Microchem J 159:105516. https:// doi. org/ 10. 1016/j. microc. 2020. This research does not include any human or animal experiments and is approved by Tehran University of Medical Sciences. The authors were fully 14. Ge D, Lee HK (2011) Water stability of zeolite imidazolate framework involved in this study. 8 and application to porous membrane-protected micro-solid-phase extraction of polycyclic aromatic hydrocarbons from environmental Consent for publication water samples. J Chromatogr A 1218:8490–8495. https:// doi. org/ 10. The authors agree with the publication. 1016/j. chroma. 2011. 09. 077 15. Gorji MEH, Ahmadkhaniha R, Moazzen M, Yunesian M, Azari A, Rastkari N Competing interests (2016) Polycyclic aromatic hydrocarbons in Iranian kebabs. Food Control Authors have no competing interests. 60:57–63. https:// doi. org/ 10. 1016/j. foodc ont. 2015. 07. 022 16. 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Tani A, Kiyota M, Aiga I (1995) Study of trace contaminant accumulated Publisher’s Note in closed system—measurement of trace contaminant generated in the Springer Nature remains neutral with regard to jurisdictional claims in pub- closed chamber in which lettuce and shiitake mushroom are cultivated. J lished maps and institutional affiliations. Environ Biol 33:151–154 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Applied Biological Chemistry Springer Journals

Measurement of polycyclic aromatic hydrocarbons (PAHs) in edible mushrooms (raw, grilled and fried) using MSPE-GC/MS method: a risk assessment study

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2468-0834
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Abstract

The purpose of this study was to evaluate the concentration of PAHs and health risk in edible mushrooms using magnetic solid phase extraction (MSPE) and gas chromatography/mass spectrometry (GC/MS) method. Based on the results, the concentration of total PAHs was in the range from 0.82 to 6.25 µg/kg (with the means of 3.85 ± 0.24 µg/ kg). In this study, acenaphthylene (Ace) had the maximum mean level in mushroom samples (0.84 ± 0.19 μg/kg) and benzo(a)pyrene (BaP), acenaphthene (Ac), phenanthrene (Pa), dibenzo[a,h]anthracene (DahA), benzo(a)anthracene (BaA), fluoranthene (Fl), indeno[1,2,3-cd]pyrene (IP) and benzo[g,h,i]perylene (BgP) had minimum mean level (non- detected). The highest mean values of total PAHs (4.88 ± 0.30 μg/kg) was detected in grilled mushroom samples and lowest mean of total PAHs (2.77 ± 0.04 μg/kg) was detected in raw mushroom samples. The concentration of contamination in edible mushrooms was raw < fried > grilled, respectively. Furthermore, heat map visualization was applied to evaluate the relationship between the quantity and type of 16 PAHs in edible mushroom samples. Ulti- mately, the incremental lifetime cancer risk in edible mushrooms for adults and children was 6.85E-08 and 3.47E-07, –6 respectively, which was lower than the acceptable risk limit (10 ) and all of the edible mushrooms sold in Tehran were considered safe for consumers. Keywords: Polycyclic aromatic hydrocarbons, Edible mushrooms, MSPE, GC–MS, Health risk assessment Introduction (Agaricus bisporus and Pleurotus ostreatus are two edi- Considering the high content of protein and essential ble mushrooms that are cultivated in most parts of the elements of edible mushrooms (cultivated and wild), its world) and due to the approach of people to use more daily consumption in the world is increasing. Further- plant proteins, the process of mushroom production is more, wild and farmed mushrooms have been partially expected in the future will increase [21]. substituted for animal proteins in many countries, espe- Studies have shown that mushrooms are low in fat but cially in Europe and Asia, due to their nutrients, health high in protein, carbohydrates and fiber. They also con - benefits, and pleasant taste [11, 57]. The number of cul - tain a variety of trace elements and minerals such as cop- tivated mushroom species has reached about 30 species per and potassium and vitamins such as folate, riboflavin and niacin [10, 45, 59]. Consumption of edible mush- rooms and mushrooms products in the daily diet can *Correspondence: nshariati@tums.ac.ir; moazzen.mojtaba@gmail.com be beneficial for human health (this product has anti- Department of Environmental Health Engineering, School of Public tumor, antioxidant, anti-viral, reduction of diabetes, cho- Health, Tehran University of Medical Sciences, Tehran, Iran Full list of author information is available at the end of the article lesterol, asthma, allergies, stress and insomnia). Edible © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 2 of 11 mushrooms commonly contain 10% dry matter and 90% HF-LPME [hollow fiber liquid phase micro-extraction water. Protein is an important component of the dry mat- (LPME)] [2, 43, 51, 52]. Fatty components and material ter of the mushrooms [9, 49]. with alcoholic caustic solutions, are saponified, to avoid PAHs chemically include 2 or more rings of benzene difficulties from lipids [13, 52, 53]. Next to the saponifica - attached at the levels of angular, cluster or linear. PAHs tion phase, SPE or LLE can be used for extraction [23, 26, are environmental pollutants that are mainly caused 27, 32, 34, 35]. To identify PAHs in food products, little by incomplete combustion of organic matter (oil, coal, research has ever been done using GC/FID (flame ioniza - wood, gasoline, etc.). These compounds are mostly tion detector) or GC/MS, HPLC (high performance liq- spread through anthropological activities. However, uid chromatography) equipped with detection of UV/FL some PAHs in the environment are caused by natural (ultraviolet and fluorescence) and FLD [2, 24, 25, 36, 37, resources like fires, natural disasters, or oil and coal dis - 39, 40, 42]. posal and volcanic activity, so they are existing in food, For the first time in Iran, this research was conducted soil, water and air [19, 20, 55]. by an effective, simple and reliable technique for deter - PAHs can be transported and accumulated in plant tis- mine of 16 PAHs in raw, fried, grilled edible mushrooms. sues through soil, air and water. The surface of vegeta - For this purpose, the sample was prepared and clean- ble wax can also absorb PAHs from the air. The levels of up based on the use of MWCNT (multi-walled carbon PAHs determined in vegetables are usually in concentra- nanotubes) as MSPE adsorbent. The prepared sample tions of 0.01–0.5 µg/kg, however, reliant on the environ- was injected into GC–MS and the PAHs level were meas- ment, higher concentrations are observed and in special ured and in the second stage, the carcinogenic and non- cases, it may exceed 5 µg/kg. On the other hands, several carcinogenic health risk was assessed. factors are involved in the formation of PAHs during the preparation of food. Some of these factors include fuel Materials and methods (gas, wood, charcoal and electric power supplies), cook- Reagents ing method (roasting, frying and baking), temperature, PAHs mix standards containing sixteen mentioned PAHs cooking time, food fat, oil drips on the flame, and prox - were obtained from Supelco Company (Bellefonte, PA, imity to or direct contact between the food and flame USA). In dichloromethane, the standard solutions were [19, 20]. ready, with all of 16 PAHs (0.1 mg/mL). After that, these Receipt rate PAHs in various parts of the world stock standard solutions with dichloromethane-methanol depends on their diet. According to classification of the (50:50, v/v) were diluted every week to make a solution WHO (World Health Organization), humans are exposed of working mixed (1  mg/mL for each PAH) that it was to PAHs through respiratory, gastrointestinal, and dermal applied to determine extraction function with variant modes of absorption. The absorption of contaminants situations. For internal standard (I.S.) biphenyl, was used from the gastrointestinal tract increases when it is solu- (0.05  µg/mL in methanol). Working and stock solutions ble in a high-fat varied diet. Experiments revealed that were preserved at four centigrade degree. MWCNT were in animals, 30–50% of PAHs are absorbed through the bought from Hanwha nanotech Company (MWCNT gastrointestinal tract, and it is mainly metabolized in the CM-95, Korea). Similar to the past research, MWCNT- liver [1, 6, 15]. MNP (as adsorbent) was ready [41]. Finally, all extra sol- The USEPA (United State Environmental Protection vents and chemicals were of grade of analytical-reagent. Agency) has mentioned sixteen PAH analytes including; chrysene (Ch), IP, fluorene (F), benzo(b)fluoranthene Preparation and sampling of mushrooms (BbF), naphthalene (NA), Ace, BaP, Ac, BgP, anthracene One hundred and twenty samples of packaged mush- (A), benzo(k)fluoranthene (BkF), Pa, pyrene (P), Fl, BaA rooms and bulk (3 branded packaging, and 1 bulk brand) and DahA. In terms of food safety, BaP can be deliber- were purchased in December 2020 from the main centers ated as a marker for carcinogenicity in foodstuff [8, 12, of supply of fruits and vegetables. The fresh mushroom 23]. samples with deionized water were washed and then There are several techniques to extract PAHs from dried with flow of air and cut into pieces in the shade, food samples [e.g., liquid liquid extraction (LLE), Soxhlet then some of them were fried and grilled. The samples apparatus, solid-phase extraction (SPE) and pressurized grilled on coal at 150 °C for 5 min and fried with a fryer at liquid extraction (PLE)]. The most ordinarily used plans a temperature of 120 °C for 5 min. After preparing sam- to extract PAHs compounds from an intricate solution ples, homogenized, in nylon vacuum-packed and kept at matrix include silica cartridges, straight immersion solid- − 18 °C in the place of dark until analysis (for no longer phase micro-extraction (SPME), LLE after saponification than 4  weeks). The samples were evaluated in duplicate with caustic soda, columns with gel beads and two phase and the mean values were applied for quantification. Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 3 of 11 Sample preparation at 230° (on the Celsius scale). At 70 eV, the energy of elec- Five grams of each frozen and crushed samples, weighed tronic beam of the MS was regulated. The qualification and transferred to 50 mL conical tube. Then, added 1 mL was done by comparing the achieved mass spectra and of the internal standard to the samples. Afterward, the times of retention to reference spectra. By injection cali- sample was homogeneous, and after adding 7.5  mL of bration standards in same GC/MS conditions, the times 1  M potassium hydroxide and 7.5  mL of 30%v/v metha- of retention were obtained. With using SIM mode, the nol–acetonitrile, homogenization was performed on PAH analytes were quantified. a shaker with 300 rounds for 5  min. The samples were placed in ultrasonic baths of German model Alma, at a temperature of 40–45 °C for 15–30 min at a frequency of Health risk assessment 130 Hz. After removing the conical tubes from the ultra- In this research, daily dietary (DD) PAHs contact levels sonic bath and their temperature reaches the ambient (µg.kg-1 body weight) and BaP daily intake equivalents temperature, for separation of the fat phase, the samples [∑(BaPeqi)] (µg/day) through consuming mushroom for half an hour were centrifuged at 4500 rpm. The super - was conducted based on Eq. 1 and 2: natant was then slowly moved to a 100  mL Erlenmeyer C × IR flask. The pH was measured by a pH meter. To adjust the DD = (1) BW pH to 6.5–7, because the initial pH of the samples was 13, a few drops of concentrated hydrochloric acid (about 6 drops) were added to the samples to reduce pH 9–10, ( C × TEF ) × IR i i i=1 DI = (2) BaPeq then with hydrochloric acid (1 M), slowly adjusted to pH BW 6.5–7. where IR is the weight of mushroom consumed After primary clean up, for adsorption of analytes, −1 (3.56 g  day ) [22]; C is the level of the PAHs congener 10 mg of magnetic nanocarbon adsorbent and 500 mg of i in mushroom,, the toxicity equivalency factor (TEF) NaCl were added to the samples and then homogenized was adopted to calculate BaP equivalent concentration with a shaker for 10  min. The samples were then trans - (Table  1), BW, the average Iranian weight of body (for ferred to the incubator at 40–45 °C for 12–24 h. The last adults 70 and children 15 kg). step involves separating the analytes from the absorbent, Besides, the ILCR (incremental lifetime cancer risk) which, after the relative drying of the samples, add 5 mL of mushroom due to PAHs dietary exposure was evalu of dichloromethane as solvent to the specimens. It was ated according to Eq. (2).[5, 56]: then homogenized with a shaker at 300 rpm for 10 min. Then, by a magnet (external), the non-impure fluid was ILCR = DI × EF × E × CSF/AT BaPeq D (3) slowly moved to the vials. The samples are then sealed, where DI , EF, AT, and CSF denote the daily intake covered with aluminum, and stored at − 18 °C until they BaPeq of BaP equivalents, exposure duration (year), lifespan are sent to the laboratory and injected into the GC–MC for carcinogens (25,550  days)[54] and the frequency of device to prevent light from entering. exposure (365  days/year) and slope factor of oral cancer for BaP which is 7.3  (mg/kg-day)(USEPA. Risk assess- ment guidance for Superfund: volume III part A and risk Analytical conditions and instrumental assessment. Washington), respectively. The examination was done on a device of Agilent GC 6890 with a detector of MS 5973 quadrupole (Technolo- gies of Agilent, Palo Alto, CA, USA). It was regulated with a column of capillary of DB-5  ms (30  m, 0.25  mm Table 1 PAHs and their toxic equivalent factors ( TEFs) i.d., 0.25  μm thickness of film). For inlet, the mode was splitless. The temperatures were regulated as follows: the PAHs TEF PAHs TEF primary temperature of oven 70° (on the Celsius scale), Benzo(a)pyrene (BaP) 1 Anthracene (A) 0.01 the temperature of injector 290° (on the Celsius scale); Dibenz(a,h)anthracene (DahA) 1 Naphthalene (NA) 0.001 retained for 1  min, at a rate of 10° (on the Celsius scale) Benzo(k)fluoranthene (BkF) 0.1 Acenaphthylene (Ac) 0.001 /min raised temperature to 295° (on the Celsius scale), Indeno(l,2,3-cd)pyrene (IP) 0.1 Acenaphthene (Ace) 0.001 retained for 7  minutes. The temperature of transfer line Benz(a)anthracene (BaA) 0.1 Phenanthrene (Pa) 0.001 was retained at 300° (on the Celsius scale). For carrier gas, Benzo(b)fluoranthene (BbF) 0.1 Fluorine (F) 0.001 helium (He) with constant flow was used (1  mL/min). Chrysene (Ch) 0.01 Pyrene (P) 0.001 The temperature of quadrupole was retained at 150° (on Benzo(g,h,i)perylene (BgP) 0.01 Fluoranthene (Fl) 0.001 the Celsius scale) and temperatures of source were kept Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 4 of 11 Table 2 Comparison of current research with other studies with different adsorbents and in different foods Sample Adsorbent Analysis method Instrumental LOD Linear range Recovery % Reference analysis Beef, lamb, MWCNT-Fe O Magnetic-SPE GC–MS 0.075–0.200 (µg/ 0.1–250 (µg/kg) 81.3–96.7 [41] 3 4 chicken meats kg) Tea and coffee MWCNT-Fe O Magnetic-SPE GC–MS 0.040–0.084 (µg/ 0.050–10.000 (µg/ 91.1–102.3 [52] 3 4 kg) kg) Milk and milk MWCNT-Fe O Magnetic-SPE GC–MS 0.040–0.075 (µg/ 0.050–1.000 (µg/ 86.1–100.3 [53] 3 4 powder kg) kg) Water sample MWCNT μ-SPE GC–MS 0.0042–0.0465 0.1–50.0 (ng/mL) 72.3–99.2 [16] (ng/mL) GC–FID 0.03–1.0 (ng/mL) 0.1–200 (ng/mL) 88–105 [31] Water sample MWCNT HS-μ-SPE c d Environmental IL-MIL-100(Fe) VA-d-μ-SPE GC–FID 0.002–0.005 (ng/ 0.02–200 (ng/mL) 97.0–103.5 [46] water, vegetable, mL) and fruit juice samples Environmental MWCNT SPE GC–MS 0.002–0.0085 (ng/ 0.02–5.00 (ng/mL) 76.0–125.5 [30] water samples mL) Environmental CTAB/TiO μ-SPE HPLC–UV 0.026–0.82 (ng/ 0.2–100.0 (ng/mL) 75.0–114 [17] water samples mL) Water samples Nylon 6 com- μ-SPE UPLC-DAD 0.050–0.580 (ng/ – 80–111 [50] posite mL) Environmental ZIF-8 μ-SPE GC–MS 0.002–0.012 (ng/ 0.1–50 (ng/mL) 96.9–106.5 [14] water samples mL) Water samples MCFG μ-SPE GC–MS 0.2–1.8 (ng/mL) 0.01–100 (ng/mL) 67.5–106.9 [44] Real water and PFu/Fe O μ-SPE GC–FID 0.005–0.02 (ng/ 0.02–200 (ng/mL) 93.2–99.2 [4] 3 4 urine samples mL) Mushroom MWCNT-Fe O Magnetic-SPE GC–MS 0.020–0.080 (µg/ 0.1–250 (µg/kg) 91.2–101.7 Current study 3 4 samples kg) μ-SPE solid-phase micro-extraction Headspace solid phase microextraction Liquid-modified metal–organic frameworks Vortex-assisted dispersive solid-phase microextraction Cetyltrimethylammonium bromide modified ordered TiO Zeolite imidazolate framework 8 Magnetic chitosan functionalized graphene oxide Magnetite nanoparticles modified with polyfuran Statistical analyses Results and discussion The results were analyzed using SPSS version 25 soft - Performance assessment of the analytical method ware. At first, descriptive indexes of variables such as In the 1st step, the analytical technique involved liquid variance, deviation of variance, mean, maximum and extraction of PAHs and in the 2nd phase, SPE technique minimum were obtained. To compare other PAHs values using a composite of MNP-sized. The extracted polycy - (means), analysis of variance (one-way) was applied. A clic aromatic hydrocarbons were then evaluated using a heat map clustering was performed to establish a more technique of GC–MS (sensitive instrument). The mass precise distinction among the PAHs congener in mush- spectrum (full scan), toward the recognition goal, the rooms [26–28]. Multivariate analysis of statistical was ratios of four characteristic ions and the ± 0.5 percent used to assess the correlation among NA, Ace, F, A, B(k) relative retention time (RRT) tolerance criteria compared F, Ch, B(b)F and P concentration. Analysis of heat map to the standard was applied. For purpose of quantifica - (variable scaling mode: z-score; method of clustering: tion, the most intense ion was applied of each compound. average linkage; distance measurement method: Pearson The compounds were quantified by SIM mode (selected was performed to evaluate the correlation between sam- ion monitoring). The dwell time (for each ion) was reg - ples online at http:// www. heatm apper. ca/. ulated at 100  min. To reduce the time of examination, the conditions of GC were selected while allowing all Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 5 of 11 Table 3 Statistics analysis of PAHs levels in mushroom samples were supplied and the calibration curves were made (µg/kg) (0.050–5.000 µg/kg) with a coefficient of correlation was 0.979–0.994. Based on the guideline of International Min. Max. Mean SD Council for Harmonization (ICH), the limit of quantifi - NA 0.1 1.03 0.67 0.15 cation (LOQ) for each compound, was determined [41]. Ace 0.24 1.38 0.84 0.19 The conclusion of validation tests designated that limit Ac nd nd nd nd of detection (LODs) and LOQs for the PAHs analytes F 0.09 0.43 0.28 0.07 altered 0.020–0.080 and 0.063–0.242 µg/kg, respectively. Pa nd nd nd nd According to the precision of interday via analysis QC A 0.14 0.61 0.37 0.1 (quality control) samples, ready on three repeated days Fl nd nd nd nd at four levels, the accuracy of the method was assessed. P 0.06 0.63 0.44 0.12 Other hands, for all of the PAH compounds, the preci- BaA nd nd nd nd sion of interday values were fewer than 8.9%. For repeat- Ch 0.09 0.81 0.34 0.09 ability, the estimated values were between 4.1 and 10.6 BbF nd 0.57 0.39 0.08 percent and the recoveries estimated between 91.2 and BkF 0.1 0.79 0.52 0.1 101.7 percent. By all these results to measurement the BaP nd nd nd – PAHs in kinds of edible mushroom samples, the reliabil- IP nd nd nd – ity and feasibility of the established technique were con- DahA nd nd nd – firmed. By examining 120 edible mushroom samples, the BgP nd nd nd – selectivity of the technique was confirmed. At the end, Total 0.82 6.25 3.85 0.24 no interfering peak was seen, in the area of the analytes PAH4 0.19 1.38 0.73 0.05 and internal standard. A comparison of the present study with other studies with adsorbents and in different foods can be seen in Table 2. The findings show acceptable lev - compounds (PAHs) to elute in acquisition collections els for different adsorbents in different foods. include a proper number of ions for checking. For each compound were controlled two qualifier ions and one quantitation [41]. For analysis, the conditions of optimum Table 4 Concentration of PAEs in raw samples and different process of mushroom samples (µg/kg) Process Raw Fried Grilled P-Value n Mean Std. deviation n Mean Std. deviation n Mean Std. deviation NA 20 0.45 0.01 20 0.66 0.01 20 0.89 0.02 0 Ace 20 0.69 0.02 20 0.85 0.02 20 0.98 0.03 0 Ac 20 nd – 20 nd – 20 nd – – F 20 0.21 0.01 20 0.28 0.01 20 0.35 0.02 0 Pa 20 nd – 20 nd – 20 nd – – A 20 0.23 0.01 20 0.38 0.01 20 0.49 0.03 0 Fl 20 nd – 20 nd nd 20 nd – – P 20 0.31 0.01 20 0.47 0.012 20 0.54 0.01 0 BaA 20 nd nd 20 nd – 20 nd – – Ch 20 0.18 0.01 20 0.34 0.01 20 0.52 0.02 0 B(b)F 20 0.33 0.01 20 0.36 0.02 20 0.49 0.01 0 B(k)F 20 0.38 0.02 20 0.52 0.03 20 0.65 0.03 0 BaP 20 nd – 20 nd – 20 nd – – IP 20 nd – 20 nd – 20 nd – – DhA 20 nd – 20 nd – 20 nd – – BgP 20 nd – 20 nd – 20 nd – – Total 20 2.77 0.04 20 3.88 0.12 20 4.88 0.3 0 PAH4 20 0.5 0.01 20 0.88 0.03 20 0.98 0.05 0 Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 6 of 11 Table 5 Uncertainly analysis for the daily intake (µg/kg bw/day) BaP concentration was below the standard levels (ND or of PAHs in mushroom non-detected) in all samples. In this research, Ace had the maximum mean level in edible mushroom samples Compound Percentiles name (0.84 ± 0.19 μg/kg) and Ac, Pa, Fl, BaA, BaP, IP, DhA and 5% 50% 75% 95% BgP had minimum mean level (ND). Among the groups recommended in EC Regulation Number 835/2011 Adults NA 2.55E-5 3.35E-5 3.74E-5 4.48E-5 (2011), for PAH4 maximum value of 1  μg/kg was regu- Ace 3.22E-5 4.28E-5 4.74E-5 5.72E-5 lated in processed cereal-based foods and 50  μg/kg in F 1.05E-5 1.40E-5 1.56E-5 1.89E-5 dried herbs. The mean levels of PAH4 detected in the A 1.39E-5 1.83E-5 2.08E-5 2.44E-5 current research were below the standard limits since the B(k)F 1.68E-5 2.23E-5 2.47E-5 2.90E-5 detected values were 0.73 ± 0.05 μg/kg in edible mush- P 1.28E-5 1.73E-5 1.96E-5 2.25E-5 room samples. B(b)F 1.50E-5 2.01E-5 2.26E-5 2.65E-5 Igbiri et  al. [18] by measuring PAHs in mushroom Ch 1.99E-5 2.64E-5 2.94E-5 3.41E-5 showed that the ƩPAHs varied from ND to 8320 µg/kg, Children NA 1.18E-4 1.58E-4 1.76E-4 2.06E-4 and BaP ranged ND-2460 µg/kg, which in some samples Ace 1.48E-4 1.97E-4 2.22E-4 2.62E-4 were lower and in others samples higher than the our F 5.11E-5 6.63E-5 7.41E-5 8.67E-5 study. Abou-Arab et al. [1] by measuring PAHs in fruits A 6.44E-5 8.63E-5 9.70E-5 1.12E-4 and vegetables showed that the maximum concentra- B(k)F 7.80E-5 1.04E-4 1.16E-4 1.36E-4 tion of ƩPAHs was 8.977  µg/kg in Spinach samples, P 6.12E-5 8.01E-5 8.96E-5 1.07E-4 6.196  µg/kg in potato samples, 2.867  µg/kg in apple B(b)F 7.03E-5 9.21E-5 1.04E-4 1.21E-4 samples and 2.334 µg/kg in guava samples, which were Ch 9.43E-5 1.22E-4 1.37E-4 1.65E-4 higher than the our study (except apple and guava). Ashraf et al. by measuring PAHs in fruits and vegetables showed that anthracene level was higher in all vegeta- bles, among all PAH congeners. The highest concentra - tion of BaP was in potatoes (2.90 ± 1.10 μg/kg) and in 0.12 turnip (2.10 ± 1.09  μg/kg), respectively. The levels of ƩPAH of the root vegetables like carrot and potato were 0.1 presented higher values (11  μg/kg), however levels of ƩPAH in turnip showed a lower ratio (9.26  μg/kg). In 0.08 tuberous vegetable cores, the cores were less contami- nated than the peels. For leafy vegetables, highest con- 0.06 centration of PAHs were presented in cabbage (8.34 μg/ kg), which were higher than our results [6]. Camargo 0.04 et  al. [8] by measuring PAHs in fruits and vegetables showed that the mean concentrations of ΣPAHs were 0.02 3.77 in grape, 3.87 in pear, 4.05 in apple, 8.86 in cab- bage, 9.50 in tomato and 13.53 μg/kg in lettuce, and Ch was not detected in any sample and total PAHs were more than our study (except in apple) and Ch was less NA Ace F A BkF P BbF Ch than our study. Bishnoi et al. [7] by examining PAHs in Fig. 1 Comparison of the most and least contribution to daily dietary intake of the PAH congeners in mushrooms fruits and vegetables showed that the ƩPAHs concen- tration in different fruit and vegetable samples ranged from 25.5 to 51.7 and 59.6 to 194.3  µg/kg, respec- tively that were higher than our study. Lee et  al. [28] Evaluation of PAHs levels in mushroom samples by measuring PAHs in fruits and vegetables showed In Table  3, the mean values of PAHs compounds in that the mean level of BaP in fruits was not detected mushroom samples are existing. The recorded means of and in vegetables was 0.05  µg/kg that was more than total PAHs in edible mushroom was 3.85 ± 0.24  μg/kg our study. Zhu et al. [62] by measuring PAHs in vegeta- (Table  3). The European Commission (EC) established bles showed that the estimated levels of total 15 PAHs maximum level of BaP in various foods (for dried herbs were 79 µg/kg in cabbage shoots and 83 µg/kg in carrot 10  µg/kg). According to existing regulations, concentra- roots that were higher than our results. Lei et al. [29] by tion of BaP in fruit and vegetable shouldn’t be more than measuring PAHs in vegetables showed that the ƩPAHs 1  µg/kg [47]. The present outcomes exhibited that the daily intake of benzo(a)pyrene equivalents Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 7 of 11 Fig. 2 Estimation of the ILCR of PAHs in mushroom by Monte Carlo simulation concentrations in these vegetables were from 3.91 to samples had minimum mean values of them (2.77 ± 0.04 96.98  µg/kg that were higher than our results. Waqas and 0.5 ± 0.01  μg/kg, respectively). BaP in all samples et  al. [61] by measuring PAHs in fruits and vegetables was not detected. The amount of contaminant in the reported that the level of total PAHs in vegetables were mushroom was raw < fried < grilled, which may be due from 51.6 to 402 μg/kg on dry weight bases, which were to the use of coal or the use of direct heat in grilled pro- higher than this research. Wan et al. [60] by measuring cess. Other studies were shown analogous results [3, 15, PAHs in vegetables reported that the PAHs levels in the 41]. vegetable samples were ranged from 26.35 to 3748  μg/ kg with the mean of 656.3 μg/kg that were higher than Human Risk assessment and exposure to toxic elements our results. In a research published by Paris et  al. [48] The daily dietary intake of the PAHs congener through reported that in several studies, the level of some PAHs edible mushrooms consumption for children and adults in various vegetables and fruits can exceed 0.5  μg/kg in Iran are listed in Table  5. For adults, the rank order and even reach 5 μg/kg. of PAHs congener based on DD (P95) was Ace (5.72E- The existence of PAHs in food products relies on the 05) > NA (4.48E-05) > Ch (3.41E-05) > B(k)F (2.90E-05) time of growing, the type of plants and plants growth > B(b)F [2.65E-05 > A (2.44E-05) > P (2.25E-05)]. > F environment (e.g., water, air and soil) as well as the prox- (1.89E-05). The rank order of PAHs congener based on imity of farms of plants to high-traffic highways and DD (P95) for children was Ace (2.62E-04) > NA (2.06E- industrial centers. 04) > Ch (1.65E-04) > B(k)F (1.36E-04) > B(b)F (1.21E- The results of this study show a lower level of pollution 04) > A (1.12E-04) > P (1.07E-04). > F (8.67E-05). compared to other studies, which could be due to reasons Furthermore, the higher and lower contribution to over- such as distance from contaminated areas, use of water, all, DD in mushrooms was related to BkF and F, respec- soil and compost free of pollution, careful and continu- tively (Fig. 1). ous monitoring of agricultural products especially edible Further, the outcomes of the Monte Carlo simulation mushrooms. revealed that the mean of ILCR for adults and children based on P95 was 6.85E-08 and 3.47E-07. In Fig.  2, the Comparison of the PAHs concentration between raw carcinogenic risk for PAHs congener was clearly lower –6 samples and various process (fried and grilled) than the acceptable risk level (10 ) by USEPA. In a In Table  4, the means of the level of PAHs among raw research conducted in Nigeria, the ILCR ranged from –8 –6 mushroom samples and process mushroom samples 1.56 × 10 to 1.73 × 10 with the uppermost calculated (grilled and fried) were demonstrated. The uppermost risk found for edible mushrooms [18]. mean values of total sixteen PAHs and PAH4 were The contamination profiles, human exposure risks of detected in grilled mushroom samples 4.88 ± 0.30 and PAHs and corresponding knowledge obtained are cru- 0.98 ± 0.05  μg/kg, respectively, and raw mushroom cial for contamination mitigation strategies and human Shariatifar et al. Appl Biol Chem (2021) 64:61 Page 8 of 11 Fig. 3 Heat map of PAHs in mushroom health risk development on the PAHs study. The biologi - compounds change with food consumption, water, sedi- cal monitoring of human exposure about the dangers and ment, soil, sites and seasons, air–soil exchange and asso- potential side effects of PAHs depend on various param - ciated carcinogenic risks of PAH compounds [33, 38]. eters, including the route and concentration of exposure, Physical, chemical, and biological methods are the most as well as the toxicity of the PAHs. It is important to preferable and cost-effective remediation methods for demonstrate linkages between outcomes of risk patterns contamination degradation or transformation until safe and similar risk behavior of PAHs and may thus give the levels in food, air, water, and soil [35–37, 39]. best possible risk assessment in realistic, intermediate and complex contaminant distribution. The two main Multivariate analysis of PAH congeners parameters which contribute to general PAHs persis- Heat map was used to understanding the relationships tence in the environment depends on molecule stability among the PAHs congener in different raw, fried and and hydrophobicity. However, the percentages of PAH grilled samples. A basic heat map, in addition to grouping Shar iatifar et al. Appl Biol Chem (2021) 64:61 Page 9 of 11 3. Alomirah H, Al-Zenki S, Al-Hooti S, Zaghloul S, Sawaya W, Ahmed N, columns and rows of comparable variables, gives a very Kannan K (2011) Concentrations and dietary exposure to polycyclic general impression of the largest and smallest variables in aromatic hydrocarbons (PAHs) from grilled and smoked foods. Food the generating matrix. Furthermore, heat maps revealed Control 22:2028–2035. https:// doi. org/ 10. 1016/j. foodc ont. 2011. 05. 024 4. Amiri A, Baghayeri M, Kashmari M (2016) Magnetic nanoparticles modi- that the different samples (raw, fried and grilled is con - fied with polyfuran for the extraction of polycyclic aromatic hydrocar - sidered as independent factors in the PAHs congener bons prior to their determination by gas chromatography. Microchim clustering. The heat map clustered samples of edible Acta 183:149–156. https:// doi. org/ 10. 1007/ s00604- 015- 1622-5 5. Antoine JM, Fung LAH, Grant CN (2017) Assessment of the potential mushrooms into 2 major clusters and three sub clus- health risks associated with the aluminium, arsenic, cadmium and lead ters (Fig. 3). The first cluster such as A, Ace, B(k)F, Ch, F content in selected fruits and vegetables grown in Jamaica. Toxicol and P contains two sub-groups, The second cluster only Rep 4:181–187. https:// doi. org/ 10. 1016/j. toxrep. 2017. 03. 006 6. Ashraf MW, Salam A (2012) Polycyclic aromatic hydrocarbons (PAHs) in includes B(b)F. ClustVis was used to visualizing cluster- vegetables and fruits produced in Saudi Arabia. B Environ Contam Tox ing of similarity and variability data. The NA, Ace, Ch, F 88:543–547 and P concentrations were the closer, indicating that the 7. Bishnoi NR, Mehta U, Pandit G (2006) Quantification of polycyclic aro - matic hydrocarbons in fruits and vegetables using high performance concentration changes of these PAHs congener had simi- liquid chromatography. IJCT. https:// doi. org/ 10. 3923/ jest. 2011. 611. 620 lar trend in different samples (raw, fried and grilled). 8. Camargo MCR, Toledo MCLF (2003) Polycyclic aromatic hydrocarbons in Brazilian vegetables and fruits. Food Control 14:49–53. https:// doi. Acknowledgements org/ 10. 1016/ S0956- 7135(02) 00052-X This research was conducted with the support of Tehran University of Medical 9. Chen S, Yuan B, Xu J, Chen G, Hu Q, Zhao L (2018) Simultaneous sepa- Sciences, Tehran, Iran. ration and determination of six arsenic species in Shiitake (Lentinus edodes) mushrooms: method development and applications. Food Authors’ contributions Chem 262:134–141. https:// doi. org/ 10. 1016/j. foodc hem. 2018. 04. 036 NS: supervision, methodology, writing—reviewing and editing. GJK: data 10. Cheung P (2010) The nutritional and health benefits of mushrooms. curation, conceptualization, writing—reviewing and editing. MA: visualization, Nutr Bull 35:292–299. https:// doi. org/ 10. 1111/j. 1467- 3010. 2010. 01859.x investigation, software, methodology, validation. MM: methodology, software, 11. Chhetri K, Senapoty D, Sharma D (2018) Management of contaminant validation, MM: methodology, visualization, investigation, PS: validation, mycoflora of oyster mushroom (var-Pleurotus florida) with botanicals writing—reviewing and editing. All authors read and approved the final and GRAS chemicals. Int J Curr Microbiol App Sci 7:1972–1978 manuscript. 12. Di Bella C, Traina A, Giosuè C, Carpintieri D, Dico GML, Bellante A, Del Core M, Falco F, Gherardi S, Uccello MM (2020) Heavy metals and Availability of data and materials PAHs in meat, milk, and seafood from Augusta area (Southern Italy): The data set used will be available upon reasonable request from the cor- contamination levels, dietary intake, and human exposure assessment. responding author. Front. https:// doi. org/ 10. 3389/ fpubh. 2020. 00273 13. Dobaradaran S, Akhbarizadeh R, Mohammadi MJ, Izadi A, Keshtkar M, Tangestani M, Moazzen M, Shariatifar N, Mahmoodi M (2020) Deter- Declarations mination of phthalates in bottled milk by a modified nano adsorbent: presence, effects of fat and storage time, and implications for human Ethics approval and consent to participate health. Microchem J 159:105516. https:// doi. org/ 10. 1016/j. microc. 2020. This research does not include any human or animal experiments and is approved by Tehran University of Medical Sciences. The authors were fully 14. Ge D, Lee HK (2011) Water stability of zeolite imidazolate framework involved in this study. 8 and application to porous membrane-protected micro-solid-phase extraction of polycyclic aromatic hydrocarbons from environmental Consent for publication water samples. J Chromatogr A 1218:8490–8495. https:// doi. org/ 10. The authors agree with the publication. 1016/j. chroma. 2011. 09. 077 15. Gorji MEH, Ahmadkhaniha R, Moazzen M, Yunesian M, Azari A, Rastkari N Competing interests (2016) Polycyclic aromatic hydrocarbons in Iranian kebabs. Food Control Authors have no competing interests. 60:57–63. https:// doi. org/ 10. 1016/j. foodc ont. 2015. 07. 022 16. Guo L, Lee HK (2011) Development of multiwalled carbon nanotubes Author details based micro-solid-phase extraction for the determination of trace levels Department of Environmental Health Engineering, School of Public Health, of sixteen polycyclic aromatic hydrocarbons in environmental water sam- Tehran University of Medical Sciences, Tehran, Iran. Food Safety Research ples. J Chromatogr A 1218:9321–9327. https:// doi. org/ 10. 1016/j. chroma. Center (Salt), Semnan University of Medical Sciences, Semnan, Iran. 2011. 10. 066 17. Huang Y, Zhou Q, Xie G (2011) Development of micro-solid phase extrac- Received: 17 July 2021 Accepted: 17 August 2021 tion with titanate nanotube array modified by cetyltrimethylammonium bromide for sensitive determination of polycyclic aromatic hydrocarbons from environmental water samples. J Hazard Mater 193:82–89. https:// doi. org/ 10. 1016/j. jhazm at. 2011. 07. 025 18. 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Tani A, Kiyota M, Aiga I (1995) Study of trace contaminant accumulated Publisher’s Note in closed system—measurement of trace contaminant generated in the Springer Nature remains neutral with regard to jurisdictional claims in pub- closed chamber in which lettuce and shiitake mushroom are cultivated. J lished maps and institutional affiliations. Environ Biol 33:151–154

Journal

Applied Biological ChemistrySpringer Journals

Published: Dec 1, 2021

Keywords: Polycyclic aromatic hydrocarbons; Edible mushrooms; MSPE; GC–MS; Health risk assessment

References