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. 2022 Dec 11;8(12):e12168. doi: 10.1016/j.heliyon.2022.e12168

Evaluation of polycyclic aromatic hydrocarbons (PAHs) in processed cereals: A meta-analysis study, systematic review, and health risk assessment

Mahtab Einolghozati a, Elaheh Talebi-Ghane b, Sahar Amirsadeghi c, Fereshteh mehri c,∗
PMCID: PMC9758409  PMID: 36536913

Abstract

Background

The present study investigated the contamination of processed cereals such as bread, spaghetti, flour, and bran, with polycyclic aromatic hydrocarbons (PAHs).

Scope and approach

The databases such as PubMed, Scopus, and Science Direct were searched from 14/December/1972 to 25/May/2021.

Key findings

We identified 639 articles and selected 18. The highest PAH concentrations found in bread, spaghetti, flour, and bran were related to anthracene, chrysene, fluorene, and naphthalene, respectively. On the other hand, the lowest PAH concentrations found in bread, spaghetti, flour, and bran were related to benzo[k]fluoranthene, benzo[a]pyrene, dibenz[a,h]anthracene, anthracene and dibenz[a,h]anthracene, respectively. Moreover, carcinogenetic and mutagenic risk assessment of the PAHs revealed a country-to-country variation. As a result, evaluation and control of PAHs in cereals should be done.

Keywords: Polycyclic aromatic hydrocarbons (PAHs), Processed cereals, Systematic review, Meta-analysis

Polycyclic aromatic hydrocarbons (PAHs); Processed cereals; Systematic review; Meta-analysis

1. Introduction

Polycyclic aromatic hydrocarbons (PAHs) are a group of hydrophobic and lipophilic compounds containing two or more molten aromatic rings that have excellent durability and environmental transport characteristics. (Keyte et al., 2013; Purcaro et al., 2013; Yebra-Pimentel et al., 2015; Zelinkova and Wenzl, 2015). There are two groups of PAHs based on the number of aromatic rings, light (2–3 rings) and heavy (4–6 rings). Heavy PAHs such as benzo[g,h,i]perylene, benzo[a]-pyrene, and indeno[1,2,3-c,d]pyrene are more toxic and stable than the lighter ones due to their higher octanol-water partition coefficients (KOW) (Bandowe and Meusel, 2017). PAHs transfer and partition differently between environments depending on their respective characteristics. In addition to acute and chronic health risks such as metabolic disorders, PAH may cause cancer in a variety of tissues, including the prostate, gonads, and breasts (Khanverdiluo et al., 2021). During incomplete combustion of coal, oil, gas, wood, waste, and other organic materials, such as tobacco and food, PAHs are released. 16 PAHs have been classified by the US Environmental Protection Agency (EPA) as “priority pollutants”. Food products may become contaminated as a result of PAH contamination in air, water, and soil (Falcó et al., 2003; Martorell et al., 2010; Kacmaz, 2019, Ihedioha et al., 2021). Further, PAHs could be originated from environmental contaminants such as forest fires, volcanic eruptions, industrial food processing, packaging materials, and some cooking methods (Veiga et al., 2014). For example, in the baking process of processed cereals, the temperature is the most important parameter to prevent PAH contamination. Processed cereals such as bread may also get contaminated by raw bakery sources, such as wheat, flour, water, yeast, and salt (Kamalabadi et al., 2020). PAHs are primarily absorbed from cereals which are one of the main food sources for humans (Udowelle et al., 2017). Food and Agriculture Organization (FAO) states that global cereal consumption is about 147.1 kg per person per year, of which Europe, Africa, and America consume 132.0, 151.0, and 118.0 kg per person, respectively (Rascón et al., 2018). In all parts of the world, cereal crops such as wheat, rice, and maize and cereal-based foods such as bread, pasta, and bakery products are primarily consumed. Cereals provide a good source of energy due to their vitamins, proteins, lipids, and minerals (Rozentale et al., 2017; Kamalabadi et al., 2020; Moradi et al., 2020). In some countries such as the Netherlands, Italy, Britain, New Zealand, and Spain, cereals are the main source of diet (Ding et al., 2012). Studies have previously reported the presence of PAHs and other pollutants in some cereal products (Mehri et al., 2020a; Einolghozati et al., 2021; Khazaei et al., 2021). According to Li et al., wheat-based fried foods have PAH levels between 9.90 and 90.0 μg kg−1 (Li et al., 2016). Rozentale et al. found PAH levels in bread and cereals between 0.22 and 1.62 μg kg−1 (Rozentale et al., 2017). In the current study, we used a meta-analysis and systematic review to analyze the PAH concentrations in processed cereals, including bread, spaghetti, flour, and bran worldwide. Further, we studied the effects of PAH on human health. Our findings may provide useful guidance for monitoring PAH levels in cereals and identifying potential contamination gaps.

2. Materials and methods

2.1. Literature search

The current study evaluated the residual concentrations of the PAHs in processed cereals in several parts of the world based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines as shown in Figure 1 (Liberati et al., 2009). A comprehensive search was conducted for this purpose between 14/December/1972 and 25/May/2021 using the International databases, such as Scopus, PubMed, and Web of science. The following keywords were searched in the title/abstract/keywords “polycyclic aromatic hydrocarbons” OR “PAHs” AND “Food” OR “Processed cereals” OR “Bread” OR “Spaghetti” OR “Flour” OR “Bran” OR “Cereal products” OR contaminants, residual, AND concentration. Additional articles were obtained from reference lists.

Figure 1.

Figure 1

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Selection process evidence searches and inclusion.

2.2. Inclusion and exclusion criteria

The identification of the articles was based on the selection criteria. Inclusion criteria included (a) articles published in the English language; (b) original studies; (c) cross-sectional studies; (d) studies that have reported the mean standard deviation of PAHs in processed cereals. On the other hand, exclusion criteria included (a) books; (b) workshops; (c) clinical trials and review articles (Salahinejad and Aflaki, 2010; Piskin et al., 2013; Özden and Özden, 2018).

2.3. Data extraction

In this systematic review, according to inclusion and exclusion criteria all articles were independently evaluated by two researchers (FM, and ME) who screened parameters such as titles, abstract and full text and abstracted the data in prepared form including author’s name, publication year, country, type of coffee, sample size, mean and standard deviations. These researchers examined the quality of the articles based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines as shown in Figure 1. The difference between manuscripts among the investigators was agreed by re-examining the articles and was subsequently approved by a third author. All toxic metal measurement units including μg/L, ppb, mg/L and ng/g were changed to μg/kg.

2.4. Meta-analysis and statistical analysis

The concentrations of PAHs in processed cereals including bread, spaghetti, flour, and bran were evaluated using the mean and standard error (SE). The SE of PAH levels was calculated using the following Eq. (1) (Ghane et al., 2021):

SE = SD/√n (1)

Here, SD represents standard deviation and N represents the sample size. The study was divided into subgroups based on type of PAH and country of origin. The random effect model was performed to calculate pooled concentration of PAHs in processed cereals. Subgroup analysis was independently conducted based on country and processed cereals. A chi-square test was conducted to detect heterogeneity. To assess the risk of bias (quality assessment) of studies Newcastle-Ottawa Scale (NOS) was utilized (Mehri et al., 2020b). The NOS has three sections including comparability (two items), selection (four items), and exposure or outcomes (three items) and ranges from 0 to 9. Final score >7 points and <7 points were respectively regarded as high quality and low quality. A test of heterogeneity was conducted using I2 and Q tests. Cochran Q test (Q statistic, p < 0.10) indicated statistical significance. I2 statistic (I2 > 50%) revealed a large degree of heterogeneity. Moreover, meta-regression was used to investigate whether the year of study could be a source of heterogeneity. Stata software version 14 (Stata Corp, USA) program was used to examine the records. P value of 0.05 was defined as the level of significance.

2.5. Risk assessment

Based on the BaP equivalent dose of mutagenic or carcinogenic PAHs (BaPEQ), the mutagenic and carcinogenic risks of 7 PAH compounds in processed cereals were calculated (Asamoah, 2017). BaPEQ value is dependent on toxicity equivalent quotient (TEQ BaP) () or MEQBaP calculated by the sum of mutagenic equivalent factor (MEF) or toxicity equivalent factor (TEF) multiplied by each PAH concentration. TEQBaP or MEQBaP and also BaPEQ were calculated using the following Eqs. (2) and (3):

TEQBaP = ∑ (TEFi × Ci) (2)
MEQBaP = ∑ (MEF i × Ci) (3)

where Ci is the individual PAH concentration with its corresponding TEFi or MEFi value, Values of TEFi for BaA, BaP, BbFlu, BkFlu, Chr, DahA, and IndP were 0.1, 1, 0.1, 0.01, 0.001, 1, and 0.1, respectively (USEPA, 1993). Values of MEFi for BaA, BaP, BbFlu, BkFlu, Chr, DahA and IndP were 0.082, 1, 0.25, 0.11, 0.017, 0.290 and 0.310 respectively (Durant et al., 1996). The BaP equivalent dose was calculated based on the following Eq. (4):

BaPEQ= (TEQ or MEQ) × IR × EF× ED/ BW × AT (4)

Based on Eq. (4), IR is the ingestion rate of cereal (mg day−1) which was shown in Table 1, EF represents the exposure frequency (350 days/year), ED is the exposure duration (adults = 30 years), BW is body weight (adults = 70 kg), according to the bodyweight studies by EPA (Phillips et al., 2015), and ATn (EF×ED) is the average time exposure (adults = 10,950 days) (Heshmati et al., 2020; Mehri et al., 2020; Ghane et al., 2021). Global ingestion of processed cereals was calculated as per capita cereals consumption in each country. The mutagenic or cancer risk was calculated using the following Eq. (5):

The risk of cancer or mutation = SFBaP×BaP equivalent dose of a mixture of PAHs (5)

where SFBaP is the oral carcinogenic slope factor for benzo[a]pyrene (7.30 mg/kg per day). As per USEPA guidelines, cancer risks (CR) greater than 10−4 indicates risk; CR between 10−6 to 10−4 is acceptable; and CR less than 10−6 indicates safe (Heshmati et al., 2020).

Table 1.

Meta-analysis of concentration of PAH (μg.kg) in processed cereals based on the type of cereal.

Metal Meat N of studies ES (95% CI) Heterogeneity
Weight (%) Statistics df P-value I2 (%)
Acenaphthene Bread 13 0.234 (0.121, 0.347) 80.58 83.30 12 <0.001 85.6
Spaghetti 6 0.253 (-0.048, 0.553) 15.21 8.21 5 0.145 39.1
Flour 2 0.300 (-0.116, 0.716) 4.11 0.00 1 1 0.0
Bran 1 0.800 (-2.336, 3.936) 0.10 - - - -
Cereals 0 - - - - - -
Total 22 0.236 (0.137, 0.336) 100.0 96.81 21 <0.001 78.3
Acenaphthylene Bread 11 0.158 (0.083, 0.233) 46.73 19.05 10 0.040 47.5
Spaghetti 11 0.313 (0.156, 0.471) 38.23 63.02 10 <0.001 84.1
Flour 0 - - - - - -
Bran 0 - - - - - -
Cereals 2 0.045 (0.019, 0.071) 15.04 0.29 1 0.589 0.0
Total 24 0.221 (0.121, 0.322) 100.0 348.04 23 <0.001 93.4
Anthracene Bread 13 0.394 (0.193, 0.595) 39.70 52.52 12 <0.001 77.2
Spaghetti 11 0.286 (-0.065, 0.637) 20.74 45.22 10 <0.001 76.5
Flour 2 0.062 (-0.112, 0.236) 11.42 1.40 1 0.237 28.4
Bran 3 0.010 (-0.024, 0.044) 18.62 0.25 2 0.883 0.0
Cereals 1 0.040 (0.008, 0.072) 9.52 - - - -
Total 30 0.170 (0.094, 0.246) 100.0 126.27 29 <0.001 77.0
Benzo[a]pyrene Bread 17 0.079 (0.047, 0.110) 57.59 45.72 16 <0.001 65.0
Spaghetti 15 0.130 (0.064, 0.196) 13.48 17.81 14 0.216 21.4
Flour 3 0.044 (-0.036, 0.124) 4.45 1.33 2 0.514 0.0
Bran 2 0.214 (-0.568, 0.995) 0.08 0.21 1 0.644 0.0
Cereals 6 0.017 (0.006, 0.028) 24.39 3.20 5 0.669 0.0
Total 43 0.071 (0.050, 0.093) 100.0 93.25 42 <0.001 55.0
Benzo[b]flouranthene Bread 10 0.077 (0.039, 0.115) 40.88 28.38 9 0.001 68.3
Spaghetti 15 0.222 (0.064, 0.381) 23.62 87.02 14 <0.001 83.9
Flour 2 0.021 (-0.034, 0.076) 6.03 0.17 1 0.676 0.0
Bran 2 0.012 (-0.059, 0.083) 5.57 0.21 1 0.645 0.0
Cereals 6 0.018 (0.007, 0.029) 23.90 4.04 5 0.544 0.0
Total 35 0.101 (0.061, 0.142) 100.0 292.82 34 <0.001 88.4
Benzo[k]fluoranthene Bread 4 0.045 (-0.001, 0.090) 5.43 0.24 3 0.971 0.0
Spaghetti 14 0.143 (0.069, 0.216) 2.09 7.15 13 0.895 0.0
Flour 5 0.020 (-0.027, 0.066) 5.22 0.36 4 0.986 0.0
Bran 3 0.012 (-0.050, 0.074) 2.95 0.24 2 0.888 0.0
Cereals 4 0.016 (0.004, 0.028) 84.32 1.90 3 0.593 0.0
Total 30 0.020 (0.010, 0.031) 100.0 22.22 29 0.811 0.0
Benzo(e)pyrene Bread 3 0.057 (-0.006, 0.120) 65.77 0.83 2 0.660 0.0
Spaghetti 0 - - - - - -
Flour 3 0.133 (-0.045, 0.311) 8.23 0.37 2 0.831 0.0
Bran 2 0.225 (-0.595, 1.046) 0.39 0.21 1 0.647 0.0
Cereals 2 0.049 (-0.052, 0.150) 25.62 0.34 1 0.558 0.0
Total 10 0.071 (0.027, 0.116) 100.0 2.60 9 0.978 0.0
Benzo(g,h,i)perylene Bread 8 0.078 (0.055, 0.101) 62.95 5.07 7 0.651 0.0
Spaghetti - - - - - - -
Flour 2 0.072 (-0.104, 0.247) 3.05 0.11 1 0.746 0.0
Bran 1 0.270 (-0.788, 1.328) 0.09 - - - -
Cereals 4 0.016 (0.004, 0.028) 33.90 2.42 3 0.490 0.0
Total 15 0.061 (0.028, 0.093) 100.0 30.69 14 0.006 54.4
Benzo[a]anthracene Bread 11 0.075 (0.035, 0.115) 42.35 33.47 10 <0.001 70.1
Spaghetti 14 0.182 (0.089, 0.274) 8.02 18.20 13 0.150 28.6
Flour 4 0.025 (-0.025, 0.075) 7.87 0.59 3 0.898 0.0
Bran 4 0.010 (-0.013, 0.033) 17.88 0.48 3 0.922 0.0
Cereals 6 0.034 (0.004, 0.065) 23.89 7.01 5 0.220 28.7
Total 39 0.055 (0.0346, 0.075) 100.0 81.14 38 <0.001 53.2
Chrysene Bread 11 0.105 (0.054, 0.157) 40.05 28.74 10 0.001 65.2
Spaghetti 10 0.629 (0.322, 0.937) 30.51 377.15 9 <0.001 97.6
Flour 3 0.040 (-0.049, 0.128) 9.58 0.29 2 0.866 0.0
Bran 1 0.390 (-1.139, 1.919) 0.18 - - - -
Cereals 6 0.031 (-0.000, 0.062) 19.68 6.11 5 0.296 18.2
Total 31 0.157 (0.091, 0.223) 100.0 524.45 30 <0.001 94.3
Dibenz[a,h]anthracene Bread 9 0.060 (0.025, 0.095) 38.53 44.87 8 <0.001 82.2
Spaghetti - - - - - - -
Flour 2 0.005 (-0.008, 0.019) 16.05 0.16 1 0.692 0.0
Bran 3 0.028 (-0.047, 0.103) 2.57 0.09 2 0.954 0.0
Cereals 4 0.010 (0.002, 0.018) 42.85 2.71 3 0.439 0.0
Total 18 0.019 (0.006, 0.031) 100.0 48.61 17 <0.001 65.0
Fluoranthene Bread 14 0.284 (0.171, 0.397) 38.49 2.17 13 <0.001 72.5
Spaghetti 12 0.150 (0.074, 0.225) 25.21 96.55 11 0.717 0.0
Flour 8 0.019 (-0.053, 0.090) 19.59 120.17 7 0.921 0.0
Bran 4 0.040 (-0.067, 0.146) 7.43 75.04 3 0.926 0.0
Cereals 4 0.042 (0.010, 0.074) 9.29 127.39 3 0.441 0.0
Total 42 0.153 (0.100, 0.205) 100.0 96.55 41 <0.001 55.5
Fluorene Bread 12 0.202 (0.138, 0.265) 72.42 26.36 11 0.006 58.3
Spaghetti 9 0.270 (-0.049, 0.589) 15.26 14.71 8 0.065 45.6
Flour 2 0.670 (-0.265, 1.605) 0.39 0.03 1 0.865 0.0
Bran 1 2.950 (-8.614, 14.514) 0.0 - - - -
Cereals 1 0.040 (0.008, 0.072) 11.92 - - - -
Total 25 0.180 (0.121, 0.240) 100.0 70.46 24 <0.001 65.9
Indeno (l,2,3-c,d) pyrene Bread 6 0.129 (0.092, 0.166) 52.63 4.15 5 0.528 0.0
Spaghetti - - - - - - -
Flour 2 0.080 (-0.126, 0.287) 4.55 0.17 1 0.684 0.0
Bran 1 0.540 (-1.577, 2.657) 0.06 - - - -
Cereals 4 0.016 (0.005, 0.028) 42.77 1.65 3 0.647 0.0
Total 13 0.088 (0.038, 0.138) 100.0 38.34 12 <0.001 68.7
Naphthalene Bread 13 0.208 (0.010, 0.405) 60.61 83.54 12 <0.001 85.6
Spaghetti 14 0.158 (-0.039, 0.354) 29.50 19.99 13 0.095 35.0
Flour - - - - - - -
Bran - - - - - - -
Cereals 1 0.205 (0.041, 0.369) 9.89 - - - -
Total 28 0.184 (0.060, 0.308) 100.0 116.42 27 <0.001 76.8
Phenanthrene Bread 14 0.365 (0.228, 0.502) 52.73 77.0 13 <0.001 83.1
Spaghetti 11 0.323 (-0.082, 0.729) 22.40 48.46 10 <0.001 79.4
Flour 6 0.109 (-0.099, 0.317) 11.96 1.92 5 0.860 0.0
Bran 3 0.071 (-0.287, 0.429) 4.91 0.26 2 0.878 0.0
Cereals 1 0.040 (0.008, 0.072) 80.56 - - - -
Total 35 0.262 (0.167, 0.357) 100.0 168.67 34 <0.001 79.8
Pyrene Bread 13 0.299 (0.159, 0.439) 24.90 41.32 12 <0.001 71.0
Spaghetti 12 0.189 (0.017, 0.361) 34.41 84.73 11 <0.001 87.0
Flour 8 0.024 (-0.030, 0.079) 19.56 2.83 7 0.900 0.0
Bran 4 0.030 (-0.072, 0.132) 13.74 0.36 3 0.948 0.0
Cereals 4 0.041 (0.009, 0.073) 7.39 2.92 3 0.403 0.0
Total 41 0.167 (0.092, 0.241) 100.0 233.75 40 <0.001 82.9
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3. Results and discussion

3.1. Processing the systematic review

The search process used in this study was summarized in Figure 1 based on the PRISMA flow chart. 639 articles were retrieved from international databases, including Scopus (310), PubMed (80), and Web of Science (279) between 14/December/1972 and 25/May/2021. 296 articles were excluded at the start of the study due to repetition. Only 343 articles were deemed relevant based on their titles. As a result, 174 articles were excluded from the analysis due to their irrelevant titles. 169 articles were investigated based on the abstracts, while 143 articles were excluded. 26 articles were reviewed of study due to lack of access to the full text or PDF of the articles to find the necessary information from the text of the article, and 8 articles were excluded due to insufficient full texts. The full texts of 18 articles were reviewed.

3.2. Characteristics of reviewed studies

Table s1 shows The main characteristics of collected studies worldwide (Tuominen et al., 1988; Kayali-Sayadi et al., 2000; Falco et al., 2003; Ciecierska and Obiedziński, 2013, Kumosani et al., 2013; Iwegbue, 2016, Rozentale et al., 2017; Udowelle et al., 2017; Peiravian et al., 2021). Study zones were ranked as follows: Europe (38.46%) > Africa (35.34%) > America (19.96 %) > Asia (6.24 %).

3.3. The concentration of various PAHs in processed cereals

Bread, pasta, and other bakery products are good sources of macronutrients (carbohydrates, proteins, and oils) and micronutrients (essential minerals and vitamins). Therefore, determining PAH levels in these products is important to protect people against toxic and carcinogenic effects. Cochran’s Q test and I2 statistics revealed significant heterogeneity among the PAH-related studies (Q = 3289.30, df = 480, p < 0.001, and I2 = 85.40%). Based on PAH types and countries, we performed subgroup analyses to reduce heterogeneity (Tables 2 and 3). The results showed that the maximum PAH concentrations in bread, spaghetti, flour, bran, and cereals products were 0.39, 0.62, 0.67, 2.95, and 0.20 μg kg−1, respectively, as indicated in Table 2. These concentrations were related to anthracene, chrysene, fluorene, fluorine, and naphthalene, respectively. In contrast, the lowest levels of PAHs found in bread, spaghetti, flour, bran, and cereals were 0.04, 0.13, 0.005, 0.01, and 0.01 μg kg−1 respectively which were associated with benzo[k]fluoranthene, benzo[a]pyrene, dibenz[a,h]anthracene, anthracene and dibenz[a,h]anthracene, respectively. The results showed that the concentration of PAHs types in processed cereals varied significantly (p < 0.05). These results were consistent with previous studies. For example, the mean concentrations of naphthalene, fluorine, and phenanthrene as in wheat flour samples in Russia, reported by Amelin et al., were 0.009, 0.001, and 0.009 μg kg−1, respectively (Amelin et al., 2011). Further, as determined by Ciecierska, M. et al., the mean concentrations of phenanthrene, anthracene, fluoranthene, pyrene, benzo[a]anthracene, 5-methylchrysene, benzo[b]fluoranthene, benzo[k]fluoranthene and dibenzo[a,h]anthracene in wheat bran samples in Poland were 0.79, 0.07, 0.17, 0.28, 0.05, 0.08, 0.11, 0.10, and 0.22 μg kg−1, while in Rye bran samples in Poland, the mean concentrations of the aforementioned chemicals were 0.76, 0.08, 0.59, 0.24, 0.05, 0.43, 0.30, and 0.20 μg kg−1, respectively (Ciecierska and Obiedziński, 2013). According to Ihedioha et al., the mean concentrations of fluoranthene, pyrene, benzo[a]anthracene, chrysene, benzo[b]fluoranthene, benzo[k] fluoranthene, and benzo[a]pyrene in Nigerian spaghetti were 0.51, 0.22, 0.60, 0.21, 0.10, 0.51, and 0.70 μg kg−1 respectively (Ihedioha et al., 2021). Jahed Khaniki et al. found PAHs, LPAHs, and HPAHs in Barbari bread to be 2.64, 2.35, and 1.56 μg kg−1, Lavash bread to be 2.51, 2.33, and 0.64 μg kg−1, and Sangak bread to be 2.51, 2.33, and 0.64 μg/kg, respectively (Jahed Khaniki et al., 2021). Kacmaz, S. et al. determined the mean concentrations of benz[a]anthracene, chrysene, benzo[b]fluoranthene and benzo[a]pyrene in breakfast cereals samples from Turkey to be 0.09, 0.11, 0.08, and 0.22 μg kg−1, respectively (Kacmaz, 2016). This study and recent studies found that the different PAH concentrations in processed cereals such as bread, spaghetti, flour, bran, and cereals) may result from the temperature during the processing of the cereal and incomplete combustion of organic matter such as wood and fossil fuels. Furthermore, the physicochemical properties of PAHs in food preparation, different processing methods including drying, smoking, grilling, frying, roasting, and baking, as well as the raw materials used for food preparation can determine the amount of PAHs in cereal food (Authority, 2008; Singh and Agarwal, 2018; Mottier et al., 2000). Processed cereals can contain different concentrations of PAHs depending on their physicochemical properties, such as solubility in water and fats, volatility, chemical reactivity, biotic and abiotic degradability, and hydrophobicity. Chawda et al. noted that direct coal burning for an extended period may be responsible for high concentrations of five and six-ring PAHs in bread. During coal heating, PAHs with more than five rings and high molecular weight tend to stay in the solid phase (bread) and pose a severe health risk to consumers (Chawda et al., 2020). Ciecierska et al. reported that PAH levels in baked bread were 2–6 times higher than in flour used for bread production depending on the temperature and the method of cooking The PAH level in the wheat bran and rye used for baking bread in the bakery ranged from 1.07–3.65 μg kg−1 as compared to bread baked at a different temperature (1.59–13.6 l μg kg1). According to the previous studies, in addition to the raw material, such as flour, the baking process and temperature play a significant role in the level of PAHs in processed cereals (Ciecierska and Obiedziński, 2013). The amount of PAHs in processed cereals also depends on the type of baking thermal treatment (direct or indirect), the temperature of baking, the thickness of bread, and the time of baking (Eslamizad et al., 2016; Kamalabadi et al., 2020; Jahed Khaniki et al., 2021). In addition to the contamination of bakery raw materials, such as water and flour, cooking and baking can contaminate the processed cereals (Moradi et al., 2020). Apart from the type of energy used in heating (e.g., electricity, wood, flame, or solar), and the distance at which the food is heated, the design of the food processor may also form PAH in food (Moradi et al., 2020). Despite toasting the bread at higher temperatures in an electric oven, Al-Rashdan et al. (2010) found that the levels of PAHs such as H-PAH and L-PAH were not significantly increased (Al-Rashdan et al., 2010). Udowelle et al. (2017) found that the total mean PAH levels of bread samples baked in wooden ovens ranged from 0.64 to 7.57 μg kg−1, whereas the total mean PAH levels in bread samples baked in electric ovens ranged from 0.49 to 2.88 μg kg−1 (Udowelle et al., 2017).

Table 2.

Meta-analysis of concentration of PAH (μg.kg) in processed cereals based on the WHO.

Metal Meat N of studies ES (95% CI) Heterogeneity
Weight (%) Statistics df P-value I2 (%)
Acenaphthene EURO1 4 0.341 (-0.050, 0.731) 0.18 0.33 3 0.955 0.0
SEARO2 2 0.080 (-0.191, 0.351) 0.37 0.0 1 1.0 0.0
EMRO3 8 0.237 (0.186, 0.288) 10.44 19.0 7 0.008 63.2
AFRO4 8 0.022 (0.005, 0.040) 89.02 14.10 7 0.049 50.4
Acenaphthylene EURO 2 0.045 (0.019, 0.071) 49.81 0.29 1 0.589 0.0
SEARO 2 0.010 (-3.947, 3.967) 0.0 0.0 1 1.0 0.0
EMRO 8 0.111 (0.077, 0.145) 28.52 18.53 7 0.010 62.2
AFRO 12 0.432 (0.393, 0.471) 21.66 63.02 11 <0.001 82.5
Anthracene EURO 6 0.027 (0.004, 0.049) 87.14 3.23 5 0.664 0.0
SEARO 2 0.010 (-0.121, 0.141) 2.59 0.0 1 0.998 0.0
EMRO 10 0.332 (0.240, 0.424) 5.26 33.54 9 <0.001 73.2
AFRO 12 0.124 (0.030, 0.219) 5.01 46.73 11 <0.001 76.5
Benzo[a]pyrene EURO 16 0.022 (0.012, 0.032) 73.37 8.95 15 0.880 0.0
SEARO 2 0.057 (-1.593, 1.708) 0.0 0.0 1 0.993 0.0
EMRO 9 0.057 (0.040, 0.075) 24.04 39.07 8 <0.001 79.5
AFRO 16 0.123 (0.069, 0.176) 2.58 22.45 15 0.097 33.2
Benzo[b]flouranthene EURO 10 0.021 (0.012, 0.029) 92.86 9.19 14 0.819 0.0
SEARO 15 0.023 (-1.429, 1.476) 0.0 0.0 1 0.976 0.0
EMRO 2 0.147 (0.103, 0.192) 3.68 0.25 2 0.882 0.0
AFRO 2 0.334 (0.288, 0.380) 3.45 87.02 14 <0.001 83.9
Benzo[k]fluoranthene EURO 4 0.017 (0.007, 0.028) 97.48 3.64 13 0.994 0.0
SEARO 2 0.078 (-0.083, 0.239) 0.44 0.01 1 0.927 0.0
AFRO 3 0.143 (0.069, 0.216) 2.09 7.15 13 0.895 0.0
Benzo(e)pyrene EURO 3 0.062 (0.011, 0.113) 100.0 2.60 9 0.978 0.0
Benzo(g,h,i)perylene EURO 9 0.017 (0.006, 0.029) 81.02 4.76 8 0.783 0.0
SEARO 2 0.032 (-0.585, 0.469) 0.03 0.0 1 0.950 0.0
EMRO 3 0.080 (0.056, 0.104) 18.95 0.0 2 1.0 0.0
AFRO 1 3.710 (0.458, 9.962) 0.0 - - - -
Benzo[a]anthracene EURO 19 0.020 (0.013, 0.028) 92.40 14.22 18 0.715 0.0
SEARO 2 0.070 (-0.784, 0.924) 0.01 0.0 1 0.998 0.0
EMRO 3 0.088 (0.058, 0.118) 6.28 8.70 2 0.013 77.0
AFRO 15 0.162 (0.097, 0.227) 1.32 22.86 14 0.063 38.7
Chrysene EURO 15 0.023 (0.013, 0.033) 87.24 14.58 14 0.407 4.0
SEARO 2 0.070 (-8.603, 8.743) 0.0 0.0 1 0.997 0.0
EMRO 3 0.109 (0.073, 0.146) 6.59 7.88 2 0.019 74.6
AFRO 11 0.229 (0.192, 0.267) 6.17 380.87 10 <0.001 97.4
Dibenz[a,h]anthracene EURO 12 0.007 (0.002, 0.011) 99.06 5.39 11 0.911 0.0
SEARO 2 0.041 (-0.210, 0.293) 0.03 0.0 1 0.978 0.0
EMRO 3 0.150 (0.105, 0.195) 0.91 0.0 2 1.0 0.0
AFRO 1 3.050 (0.377, 5.723) 0.0 0.0 - - -
Fluoranthene EURO 14 0.041 (0.013, 0.068) 66.51 8.74 18 0.965 0.0
SEARO 2 2.474 (-1.722, 6.670) 0.0 0.32 1 0.571 0.0
EMRO 8 0.179 (0.132, 0.225) 23.36 43.68 7 <0.001 84.0
AFRO 4 0.160 (0.089, 0.231) 10.14 92.15 12 0.738 0.0
Fluorene EURO 4 0.041 (0.009, 0.073) 44.87 2.01 3 0.570 0.0
SEARO 2 0.080 (-0.454, 0.614) 0.16 0.0 1 0.998 0.0
EMRO 8 0.167 (0.132, 0.202) 38.39 24.94 7 0.001 71.9
AFRO 11 0.115 (0.062, 0.167) 16.59 15.62 10 0.111 36.0
Indeno (l,2,3-c,d) pyrene EURO 9 0.018 (0.006, 0.029) 91.87 4.53 8 0.807 0.0
EMRO 3 0.130 (0.091, 0.169) 8.12 0.0 2 1.0 0.0
AFRO 1 1.140 (0.141, 2.139) 0.01 0.0 - - -
Naphthalene EURO 2 0.207 (0.043, 0.371) 0.0 0.89 1 0.346 0.0
SEARO 2 0.001 (0.000, 0.002) 99.97 0.0 1 0.997 0.0
EMRO 9 0.186 (0.109, 0.263) 0.01 59.34 8 <0.001 86.5
AFRO 15 0.114 (0.030, 0.198) 0.01 20.97 14 0.102 33.2
Phenanthrene EURO 11 0.042 (0.011, 0.074) 55.24 3.57 10 0.965 83.1
SEARO 2 0.041 (-8.615, 8.698) 0.0 0.0 1 0.999 79.4
EMRO 10 0.195 (0.159, 0.232) 41.13 71.73 9 0.0 0.0
AFRO 12 0.189 (0.066, 0.312) 3.63 53.02 11 0.0 0.0
Pyrene EURO 18 0.038 (0.012, 0.065) 52.72 8.62 17 0.952 71.0
SEARO 2 0.055 (-7.535, 7.645) 0.0 0.0 1 0.996 87.0
EMRO 8 0.120 (0.083, 0.157) 26.61 35.63 7 <0.001 0.0
AFRO 13 0.293 (0.251, 0.335) 20.67 89.31 12 <0.001 0.0
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1- European Region; 2- South East Asia Region; 3- Eastern Mediterranean Region; 4- Western Pacific Region; 5- African Region.

Table 3.

Carcinogenic risk assessment based on BaP equivalency for processed cereals.

Country IR (kg) BaA BaP BbFlu BkFlu Chr DahA IndP Total
Finland 18.74 5.31E-04 5.31E-04 - - - - - 1.06E-03
India 27.24 7.67E-06 5.11E-05 3.58E-06 6.64E-07 6.64E-08 4.60E-05 - 1.09E-04
Iran 40.82 2.46E-05 2.99E-04 2.29E-05 - 2.71E-07 2.30E-04 1.99E-05 5.96E-04
Latvia 14.29 3.87E-06 2.02E-05 4.09E-06 - 6.79E-08 - - 2.82E-05
Nigeria 14.76 5.65E-05 4.11E-04 2.14E-05 1.62E-06 7.30E-07 1.69E-03 6.32E-05 2.24E-03
Poland 22.62 1.13E-06 - 8.49E-07 1.53E-07 2.55E-08 2.12E-05 - 2.34E-05
Saudi Arabia 10.28 - 7.72E-06 - - - - - 7.72E-06
Spain 24.44 9.25E-06 4.04E-05 5.77E-06 3.62E-07 1.37E-07 5.17E-05 2.05E-06 1.10E-04
Turkey 31.62 4.62E-06 7.06E-05 3.50E-06 - 5.25E-08 - - 7.87E-05
UK 19.51 1.00E-05 5.76E-05 3.61E-06 5.48E-07 1.14E-07 6.84E-06 1.15E-05 9.03E-05
Total 6.49E-04 1.49E-03 6.57E-05 3.35E-06 1.46E-06 2.05E-03 9.67E-05 4.35E-03
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Chr = chrysen, BaA = benzo[a]anthracene, BaP = benzo[a]pyrene, BkF = benzo[k]fluoranthene, BbF = benzo[b]fluoranthene BghiP = benzo[g,h,i]perylene, DahA = dibenz[a,h]anthracene, IndP = indeno[1,2,3,c,d]pyrene.

3.4. Level of PAHs in processed cereals according to the classification of the World Health Organization (WHO)

The processed cereals such as bread, spaghetti, flour, and bran contained different levels of PAHs depending on the country studied. The highest concentrations of acenaphthene (0.34 μg kg−1) and naphthalene (0.20 μg kg−1) were observed in European Region (EURO). Acenaphthylene (0.43 μg kg−1), benzo[a]pyrene (0.12 μg kg−1), benzo[k]fluoranthene (0.14 μg kg−1), benzo(g,h,i)perylene (3.71 μg kg−1), benzo[a]anthracene (0.16 μg kg−1), chrysene (0.22 μg kg−1), dibenz[a,h]anthracene (3.05 μg kg−1), fluoranthene (2.47 μg kg−1), and pyrene among (0.29 μg kg−1) concentrations were observed in African Region (AFRO). Anthracene (0.33 μg kg−1), benzo[b]fluoranthene (0.33 μg kg−1), indeno (l, 2, 3-c, d) pyrene (1.14 μg kg−1) and phenanthren (0.19 μg kg−1) was observed in Eastern Mediterranean Region (EMRO). Fluorene (0.16 μg kg−1) was found in South East Asia Region (SEARO). Based on these findings, the lowest concentrations of benzo[a] pyrene (0.02 μg/kg), benzo[b]fluoranthene (0. 02 μg/kg), benzo[k]fluoranthene (0.01 μg kg−1), benzo(g, h, i)perylene (0.01 μg kg−1), benzo[a]anthracene (0.02 μg kg−1), chrysene (0.02 μg kg−1), dibenz[a,h]anthracene (0.07 μg kg−1), fluoranthene (0.04 μg kg−1), Fluorene (0.04 μg kg−1), indeno (l, 2, 3-c,d) pyrene (0.01 μg/kg), phenanthren (0.04 μg kg−1), and pyrene among (0.03 μg kg−1) in processed cereal belonged to EURO. However, the lowest concentrations of acenaphthene (0.02 μg kg−1) were related to AFRO, and the lowest concentrations of acenaphthylene (0.01 μg kg−1), anthracene (0.01 μg kg−1), and naphthalene (0.001 μg kg−1) were related to SEARO. The results of the present meta-analysis revealed a significant difference (P < 0.05) in the PAH concentrations in different regions of the world. Further, the level of PAHs in processed cereals samples was assessed in different countries. In India, Chawda et al. investigated the content of PAH in breads. The amounts of naphthalene, anthracene, acenaphthene, and acenaphthylene were 5.08, 9.135, 0.31, and 4.95 μg kg−1, respectively (Chawda et al., 2020). The amount of fluoranthene, pyrene, benz(a)anthracene, chrysene, and benzo(e) pyrene in white flour samples from the United Kingdom was found to be 0.24, 0.46, 0.12, 0.12, and 0.17 μg kg−1, respectively (Dennis et al., 1991). Similarly, Ihedioha et al. concluded that the mean concentrations of fluorene, phenanthrene, anthracene, fluoranthene, and pyrene in the Turkish spaghetti samples were found to be 3.01, 0.71, 0.71, 0.42, and 0.20 μg kg−1 respectively, whereas the mean concentrations of the aforementioned chemicals in Nigerian spaghetti samples were found to be 2.00, 1.00, 3.01, 0.41, and 0.61 μg kg−1 respectively (Ihedioha et al., 2021). Kacmaz et al. observed that the mean concentration of benz[a]anthracene, chrysene, benzo[b]fluoranthene, and benzo[a]pyrene in Turkish bread samples were 0.03, 0.05, 0.05, and 0.17 μg kg−1 respectively (Kacmaz, 2016). PAH contamination in processed cereals in different countries is likely related to the pollution of air, soil, and water. Further, the type of industries and active mines, urban and rural environmental pollution, and food processing and cooking methods can cause PAH contamination (Ciemniak and Witczak, 2010; Shi et al., 2019). Further, geographical location and local climatic conditions exert influence on the content of PAH in food products in various countries. PAHs can be released by natural combustion processes, such as forest fires and volcanic eruptions, or by human source emissions such as vehicles, household heating such as coal and wood, and industrial processes such as asphalt and carbon black (Baek et al., 1991). In Tarragona, Vyskocil et al. indicated that the PAH concentration in the chemical area, residential zone, and petrochemical zone, was 476.2, 206.9, and 119.7 μg kg−1, respectively (Vyskocil et al., 2000). PAHs may be present in drinking water, due to the atmospheric fallout, urban run-off, municipal effluents, industrial effluents, and oil spillage or leakage (Chen et al., 2005). In line with these studies, King et al. observed a high level of atmospheric PAHs in the urban environment, possibly due to increased vehicular traffic and small dispersion of atmospheric pollutants (King et al., 2004). Yoon et al. found that levels of 2-naphthol derived from naphthalene were higher in the industrial regions of Korea than in the two metropolitan regions (Yoon et al., 2012). Similarly, Pagels et al.,reported that exposure to PAHs in homes in Italy was due to the burning of candles (Pagels et al., 2009). Nethery et al. also reported that exposure to the lower molecular weight PAHs in foods was affected by indoor sources such as candles and incense (Nethery et al., 2012). PAH accumulation in the soil could also influence the production of PAH food products, which can further cause the contamination of vegetables and food chains, resulting in direct or indirect human exposure. According to Hoseini et al. deep-frying produced more PAHs than other cooking methods, including roasting, grilling, and boiling. Therefore, cooking is a major source of PAHs in both indoor and outdoor air in cities around the world (Rose et al., 2015; Rocha et al., 2020). It can be mentioned that the limitations in the evidence and the processes of our study were include the lack of division standards, sample size; concentration PAH is processed cereals in some studies that resulted to exclude these studies of our study.

3.5. Health risk assessment

Foods contaminated with toxic substances, such as PAHs, can pose a health risk to humans. Various reports suggested that eating foods containing PAHs and inhaling PAHs account for 88 and 12% of the exposure to PAHs, respectively (Alomirah et al., 2011). PAHs have been listed as a priority pollutant by the International Agency for Research on Cancer (IARC) owing to their carcinogenic and mutagenic properties (Qamar et al., 2017). Numerous studies have demonstrated an association between exposure to PAHs and cancers of the lungs, respiratory system, and stomach (Ledesma et al., 2014). Tables 3 and 4 provide information on the carcinogenic or mutagenic risks of PAHs due to the consumption of processed cereals based on aP equivalent (μg/kg) in different countries. Finland ranked highest among countries according to carcinogenetic risk, followed by Nigeria > India > Spain > Iran > Poland > Latvia > UK > Saudi Arabia > Turkey. Further, the following order was determined by mutagenic risk: Nigeria > UK > Finland > Iran > Poland > Latvia > Turkey >> India > Spain > Saudi Arabia. There have been many studies regarding the carcinogenicity and metastasis risk of different products, which are in line with ours. The findings by Alomirah et al. (2011) were consistent with ours. There were high levels of genotoxic PAHs in the vegetables and smoked foods consumed by Kuwaiti children, teenagers, and adults which put them at the risk of cancer (Alomirah et al., 2011). PAH concentrations in processed cereals could be mainly responsible for differences in carcinogenicity and mutagenicity across different countries considering that the risk of cancer and non-cancer risks associated with PAHs in processed cereals were less than 10−6, and also due to the presence of PAHs in processed cereals, regulatory agencies should regularly evaluate and monitor these products to reduce contaminants.

Table 4.

Mutagenic risk assessment based on BaP equivalency for processed cereals.

Country BaA BaP BbFlu BkFlu Chr DahA IndP Total
Finland 1.63E-04 1.99E-04 - - - - - 3.62E-04
India 6.29E-06 5.11E-05 8.94E-06 7.31E-06 1.13E-06 1.33E-05 - 8.81E-05
Iran 2.01E-05 2.99E-04 5.71E-05 - 4.60E-06 6.66E-05 6.17E-05 5.09E-04
Latvia 3.17E-06 2.02E-05 1.02E-05 - 1.15E-06 - - 3.47E-05
Nigeria 4.64E-05 4.11E-04 5.36E-05 1.78E-05 1.24E-05 4.90E-04 1.96E-04 1.23E-03
Poland 9.28E-07 - 2.12E-06 1.68E-06 4.33E-07 6.16E-06 - 1.13E-05
Saudi Arabia - 7.72E-06 - - - - - 7.72E-06
Spain 7.59E-06 4.04E-05 1.44E-05 3.99E-06 2.33E-06 1.50E-05 6.36E-06 9.00E-05
Turkey 3.79E-06 7.06E-05 8.74E-06 - 8.92E-07 - - 8.40E-05
UK 8.21E-06 5.76E-05 9.03E-06 6.02E-06 1.93E-06 1.98E-06 3.57E-05 1.21E-04
Total 2.59E-04 1.16E-03 1.64E-04 3.68E-05 2.49E-05 5.93E-04 3.00E-04 2.53E-03
Open in a new tab

hr = chrysen, BaA = benzo[a]anthracene, BaP = benzo[a]pyrene, BkF = benzo[k]fluoranthene, BbF = benzo[b]fluoranthene BghiP = benzo[g,h,i]perylene, DahA = dibenz[a,h]anthracene, IndP = indeno[1,2,3,c,d]pyrene.

4. Conclusion

Herein, we assessed the PAH content of various processed cereals based on PAH subgroups and countries around the world. The carcinogenicity and the mutagenicity of PAHs were also evaluated based on cereal consumption and PAH concentrations in various countries. Based on the inclusion and exclusion criteria, 18 studies showed that PAH concentrations differed significantly in different countries, in line with other studies. Nigeria ranked highest in carcinogenic risk, followed by Finland, Iran, Spain, India, the UK, Turkey, Latvia, Poland, and Saudi Arabia. Physicochemical characteristics of PAHs, the temperature in which the cereal is processed, incomplete combustion of organic matter, and the physico-chemical of PAHs are also important influences on how much PAH is present in processed cereals. It was determined that PAHs may pose different carcinogenic and mutagenic risks in different countries. Thus, regulatory agencies need to monitor cereal products regularly to reduce contaminants in these high-consumption foods.

Declarations

Author contribution statement

Mahtab Einolghozati, Sahar Amirsadeghi, Fereshteh Mehri: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data; Wrote the paper.

Elaheh Talebi-Ghane: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data.

Funding statement

This work was supported by Deputy of Research and Technology, Hamadan University of Medical Sciences.

Data availability statement

No data was used for the research described in the article.

Declaration of interest’s statement

The authors declare no conflict of interest.

Additional information

No additional information is available for this paper.

Appendix A. Supplementary data

The following is the supplementary data related to this article:

supplementary Table final_V2
mmc1.docx (182KB, docx)

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