Levels and health risk assessment of polycyclic aromatic hydrocarbons in protein foods from Lagos and Abeokuta, Southwestern Nigeria

Journal of Food Composition and Analysis 79 (2019) 28–38

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Original research article

Levels and health risk assessment of polycyclic aromatic hydrocarbons in protein foods from Lagos and Abeokuta, Southwestern Nigeria

T

⁎

A.M. Taiwo , E.C. Ihedioha, S.C. Nwosu, O.A. Oyelakin, P.C. Efubesi, J.S. Shitta, T.O. Osinubi Department of Environmental Management and Toxicology, Federal University of Agriculture, PMB 2240, Abeokuta, Ogun States, Nigeria

A R T I C LE I N FO

A B S T R A C T

Keywords: Non-carcinogenic Cancer risk The Olyclic Polycyclic Aromatic Hydrocarbons Protein Foods Food composition Food analysis

The present study assessed levels and health risk of polycyclic aromatic hydrocarbons (PAHs) in protein foods collected from selected locations in Lagos and Abeokuta, Southwestern Nigeria. Forty eight protein food samples (meat, cowskin, fish and crayfish) were collected between July and September 2018 and subjected to chemical analysis of polycyclic aromatic hydrocarbons (PAHs) using standard method. Data collected were subjected to simple descriptive statistics of mean and standard deviation using SPSS for Windows (22.0). The health risk assessment was evaluated for average daily dose (ADD), hazard quotient (HQ), hazard index (HI) and cancer risk (CR) using the United States Environmental Protection Agency model. Results revealed higher concentrations of ∑PAHs in protein food samples from Abeokuta than those from Lagos (except smoked cowskin). Indeno[1,2,3cd]pyrene (96.817 ± 65.922 mg kg−1) was the highest PAH congener measured in protein foodstuffs (raw fish samples from Abeokuta). The ∑CR values of PAHs in Abeokuta fish (smoked) and crayfish (raw and smoked) samples were higher than the priority risk level of 1.0 × 10-4 indicating possible risk of developing cancer through consumption of protein foodstuffs.

1. Introduction The presence of polycyclic aromatic hydrocarbons (PAHs) in foodstuffs has attracted much attention by researchers all over the world due to adverse health problems. PAHs are large groups of organic chemicals containing two or more fused aromatic rings of carbon and hydrogen atoms. Notable sources of PAHs in the environment are incomplete combustion of fossil fuels (coal, oil and gas), wood fuels, oil spills, garbage and other organic substances (ATSDR, 1995; Gu et al., 2013). Other sources of PAHs are tobacco smoke, machineries, asphalt, coal tar, creosote-treated wood products and volcanic eruption (Masih et al.,2008; Kozak et al., 2017). The study of Zhang et al. (2018) has adopted principal component analysis to identify sources of particulate PAHs in China. The identified sources were cooking, biomass combustion, coal combustion (from coking, power plant and domestic sources), waste incineration and diesel/gasoline engines. PAHs are hydrophobic and chemically stable (Zhang and Tao, 2009; Xu et al., 2006; Ogbuagu and Ayoade, 2012). They can be found in soil, water and food (Falco et al.,2003). As the numbers of PAH rings grow larger; there is a corresponding increase in lipid solubility, carcinogenicity and mutagenicity (Tian and Zheng, 2004). Foods can be contaminated with PAHs present in air, soil and water, or from food processing (drying or smoking) and cooking (grilling, roasting or frying). ⁎

Foodstuffs may contribute to more than 90% of total exposure to PAHs for non-smokers (Omodara et al., 2014). The presence of PAHs in roasted foods has been directly linked with distance from heat source, fat contents, duration of exposure, temperature and fuel types (SCF, 2002; Ogbuagu and Ayoade, 2012). A linear relationship has been established between PAH concentration and combustion temperature range between 400 °C and 1000 °C (Mihalca et al., 2011). The major concern of PAHs may be linked to cancer development. The Joint FAO/WHO Expert Committee on Food Additives (JECFA) reported that benzo[a]pyrene (BaP) could be used as a tracer for genotoxic and carcinogenic PAH in foods (JECFA, 2005). Workers exposed to PAHs experienced different cancer types such as skin, bladder, lung and gastrointestinal (IDPH (llinois Department of Public Health), 2019). Cancer ranks the second most common cause of deaths in both developed developing countries (Lyon et al., 2014; Bray et al., 2018). There were 6.7 million global cancer deaths in 2002; out of which only less than 5% were reported in sub-Saharan Africa. By the year 2020, this figure is expected to rise to 10.3 million with a 50–75% increase in cancer mortality in sub-Saharan Africa (Ferlay, 2004; Ferlay et al., 2015). The non-carcinogenic health effects of PAHs are reported in animal studies to include adverse reproductive, dermal and developmental effects (IDPH (llinois Department of Public Health), 2019). Health problems of BaP include neurobehavioral effects, decreased

Corresponding author. E-mail address: [email protected] (A.M. Taiwo).

https://doi.org/10.1016/j.jfca.2019.03.001 Received 5 December 2018; Received in revised form 20 February 2019; Accepted 5 March 2019 Available online 06 March 2019 0889-1575/ © 2019 Elsevier Inc. All rights reserved.

Journal of Food Composition and Analysis 79 (2019) 28–38

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sites of food samples in Lagos and Abeokuta, southwestern Nigeria. During collection, samples were covered with aluminium foil (to avoid contamination) and placed inside a cooler packed with ice block. Samples were transported to the CTX-ION Analytics Ltd. Laboratory, Ikeja, Lagos, Nigeria for PAH analysis.

fertility and adverse birth outcomes such as reduced birth and postnatal body weight, and head circumference (TOXNET, 2017). Many studies had reported PAHs in different protein foodstuffs from Nigeria (Igwe et al., 2012; Amos-Tautua et al., 2013; Agbozu, 2014; Benson et al., 2017; Tongo et al., 2017; Akpoghelie, 2018; Nnaji and Ekwe, 2018). However, few studies were carried out on human health risk assessment of PAHs (Benson et al., 2017; Tongo et al., 2017). To our knowledge, no study has reported detailed levels and health risk assessment of PAHs in four different protein foods (meat, cowskin, fish and crayfish) from Nigeria. The objective of this study is to assess the levels and health risk of PAHs in raw and smoked protein foodstuffs from selected locations in Lagos and Abeokuta, southwestern Nigeria.

2.2. PAHs analysis Extraction of PAHs followed the procedures described in Wang et al. (1999). This involves maceration of 15 g of tissue sample (meat, cowskin, fish and crayfish) with Teflon pestle homogenizer alongside 10 g of anhydrous sodium sulphate until completely dried and homogenized. A 50 mL of 1 + 1 Hexane: Dichloromethane (GC grade, Merck KGaA, Darmstadt, Germany) was introduced for extraction. A 10 g quantity of the homogenized sample was placed in a Teflon extraction bottle. The covered Teflon bottle with the content was then vortexed in an ultrasonic bath at 70 °C for 1 h. Organic layer was carefully decanted into a round bottom flask and further dried with sodium sulphate. Clean-up procedure was carried out using the Florisil procedure, which entails introduction of 4 mL hexane to a 1000 mg Florisil cartridge (EPA, 2014). The cartridge was allowed to soak for 5 min. A 1 mL of the sample was added and pulled through the Florisil SPE cartridge at a drop-wise rate, until the hexane level reaches the top of the frit. The flow was stopped. The cartridge was filled with 90:10 hexane/acetone

2. Materials and methods 2.1. Sample collection A total of 48 protein food samples were purchased from different locations in Lagos and Abeokuta, southwestern Nigeria between July and September 2018. The protein food samples were meat (raw and smoked beef, 12 samples), cowskin (raw and smoked, 12 samples), fish (raw and smoked catfish, 12 samples) and crayfish (raw and smoked, 12 samples). The protein foodstuffs (0.25 kg) were collected in triplicates across the sampling sites (Taiwo et al., 2018). Fig. 1 shows the sampling

Fig. 1. The sampling locations of the protein foods in southwestern Nigeria. 29

Journal of Food Composition and Analysis 79 (2019) 28–38

A.M. Taiwo, et al.

solutions, while the drop-wise flow was restarted. The effluent from the cartridge was collected into a 10 mL volumetric flask until 10 mL has been collected. The sample extract was then concentrated to 2 mL using a rotary evaporator (Buchi R215, Sigma-Aldrich Chemie GmbH, Darmstadt, Germany). Determination of PAHs in the sample was carried out using gas chromatography mass spectrophotometer (GC–MS, Agilent 7820, CA, United States) by operating a mass selective detector (MSD) in selective ion monitoring (SIM) and scan mode to ensure low level detection of the target constituents (Agilent Technologies Inc., 2012). A gas chromatograph coupled to 5975C inert mass spectrometer with electronimpact source (Agilent Technologies Inc, 2012) was used. The Agilent 5975C inert MSD uses Triple-Axis Detector (TAD) to offer high performance, capabilities and flexibility. The stationary phase of separation of the compounds was HP-5 capillary column coated with 5% Phenyl Methyl Siloxane (30 m length x0.32 mm diameter x 0.25 μm film thickness). The carrier gas was helium used at constant flow of 1.48 mL/min at an initial nominal pressure of 77.05 torr and average velocity of 44.22 cm/s. A 1.0 μL of the sample was injected into splitless mode at an injection temperature of 300 °C. The purge flow to spilt vent was 15.0 mL/min at 0.75 min with a total flow of 16.67 mL/min; gas saver mode was switched off. Oven was initially programmed at 40 °C (1 min) and then ramped at 12 °C/min to 300 °C (10 min). Run time was 32.67 min with a 3 min. solvent delay (Agilent Technologies Inc., 2012). The mass spectrometer was operated in electron-impact ionization mode at 70 eV with ion source temperature of 230 °C, quadrupole temperature of 150 °C and transfer line temperature of 300 °C (Agilent Technologies Inc., 2012). The identification of PAHs was based on comparison of the retention times of the peaks with those obtained from standard mixture of PAHs and from spiked samples determined under the same conditions (Olabemiwo, 2013). Quantification involved external calibration curves prepared from the standard solution of each of the PAHs. The PAHs standard, 1000 mg/L (Catalog Number: H-QME-01) containing 23 environmental PAHs components was purchased from AccuStandard (New Haven, CT). Prior to calibration, the mass spectrophotometer was auto-tuned to perfluorotributylamine (PFTBA) using already established criteria to check the abundance of m/z 69, 219, 502 and other instrument optimal and sensitivity conditions (Agilent Technologies Inc., 2012). Analytical procedures observed during the laboratory analysis include running the blank samples to cancel the matrix effects of extracting reagents and to calculate the limit of detection of instruments as 3 x standard deviation (Taiwo et al., 2018). All solvents used for extraction were of GC grade (Merck KGaA, Darmstadt, Germany). The analytical method was validated by spiking some of the food samples according to the standard procedure (Zazzi et al., 2005). The percent recovery of the spike was determined by splitting the samples into two portions (spiked and unspiked) and a known amount of a standard solution of analyte was added to one portion. The spiking procedure follows mixing 1 mL of 500 mg L−1 PAH standard thoroughly with 10 g of homogenised tissue samples alongside 10 g of anhydrous sodium sulphate. The spiked samples were mixed at least 1 h before Hexane/ Dichloromethane extraction procedures described above. The percent recovery was calculated as:

2.3. Data analysis PAH data were subjected to simple descriptive statistics (mean and standard deviation), and multivariate analysis of principal component analysis (PCA) using SPSS for Windows package (version 22.0). 2.4. Health risk assessment The health risk assessment of PAHs was calculated for average daily dose (ADD), hazard quotient (HQ), hazard index (HI), cancer risk (CR) using the formulae highlighted by USEPA (2001, 2002, 2007).

ADD =

C x IR x EF x ED BW x AT

(2) −1

-1

Where, ADD = Average daily dose (mg kg day ) C = Concentration of PAHs in protein foods (mg kg−1), IR = Ingestion rate of protein foods (24.7 g day−1) (FAO, 2008), ED = Exposure duration (years) = 30 years for carcinogenic effects for adults, EF = Exposure frequency (day/year) = 350 days year−1 (Li et al., 2009), AT = Averaging time or life expectancy = 54.5 years (WHO, 2015; Taiwo et al., 2018), AT = ED for non-carcinogenic effects, while AT = 54.5 × 365 days for carcinogenic effects in adult (Taiwo et al., 2018), BW = Body weight (kg); 60 kg for an adult (Taiwo et al., 2018). n

HI =

∑ HQ i=1…n

(3)

i=1

HQ =

ADD RfD

(4) −1

-1

Where, ADD = Average daily dose (mg kg day ), RfD = Reference dose (mg kg−1 day-1) (USEPA, 2001), N = numbers of elements observed. HQ > 1 denotes non-carcinogenic adverse health effects, HQ < 1 denotes no adverse effects, Cancer Risk = ADD × SF (5) Where, ADD = Average daily dose (mg kg−1 day-1), SF = Slope factor Benzo[a]pyrene [BaP]-equivalent concentration was carried out for BaP-TEQ (carcinogenic equivalents, mg kg−1) using the equation outlined by Jung et al. (2010). The concentration of each PAH compound was multiplied with its carcinogenic equivalent factor (TEF) for cancer potency relative to BaP. (BaP-TEQ)Σ8PAH = [Benz[a]anthracene] × 0.1 + [Chrysene] × 0.01 + [Benzo[b]fluoranthene] × 0.1 + [Benzo[k]fluoranthene] × 0.1 + [Benzo[a]pyrene] × 1 + [Indeno[1,2,3-cd]pyrene] × 0.1 + [Dibenz [a,h]anthracene] × 5 + [Benzo[ghi]perylene] × 0.01. (6) 3. Results and discussion 3.1. Distribution of PAH congeners in protein foodstuffs Table 2 shows the levels of PAH congeners in meat and cowskin samples. PAHs were generally measured at higher concentrations in smoked meat than raw samples. The major PAH congener measured in raw meat samples from Lagos was 3-Methylcholanthrene (0.246 ± 0.052 mg kg−1), while Indeno[1,2,3-cd]pyrene was found at the highest concentration (4.552 ± 7.733 mg kg−1) in raw meat samples from Abeokuta. The smoked meat sample from Lagos was contaminated with 13 PAH congeners, of which 3-Methylcholanthrene contributed more than 20% of the total PAHs. The smoked meat samples from Abeokuta also

% Recovery Spiked Sample Concentration− Unspiked Sample Concentration = Known Concentration of a Standard Solution of Analyte (1) The data of % recovery are presented in Table 1. The % recovery results varied from 91 ± 3% for Anthracene and Benzo[b]fluoranthene to 114 ± 2% for Acenaphthene.

30

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Table 1 % Recovery of PAH components. Components

Naphthalene Acenaphthylene Acenaphthene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[c]phenanthrene Benz[a]anthracene Chrysene Benzo[e]pyrene Benzo[k]fluoranthene Benzo[b]fluoranthene 3-Methylcholanthrene Indeno[1,2,3-cd]pyrene Dibenz[a,h]anthracene Benzo[ghi]perylene Dibenzo[a,h]pyrene Dibenzo(a,i)pyrene Dibenzo(a,l)pyrene Benzo[a]pyrene

Spike Concentration (mg L−1)

Spiked Sample (mg L−1)

Un-spiked Sample (mg L−1) Mean

SD

Mean

SD

3.46 0.16 0.16 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.44 0.00 0.00 0.00 0.00 0.00 0.08

1.75 0.23 0.22 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.62 0.00 0.00 0.00 0.00 0.00 0.00

529.27 507.02 570.12 480.25 466.45 453.27 474.59 485.29 481.79 476.85 477.03 537.86 484.46 456.07 480.82 512.72 488.65 482.89 525.61 470.86 509.82 513.93

36.67 6.56 10.23 50.16 47.33 13.39 66.64 24.08 25.96 25.12 13.46 45.17 67.21 22.48 16.51 32.18 41.67 42.50 25.78 34.50 9.55 5.50

500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500 500

% Spike Recovery

Mean

SD

105% 101% 114% 96% 93% 91% 95% 97% 96% 95% 95% 108% 97% 91% 96% 102% 98% 97% 105% 94% 102% 103%

7% 1% 2% 10% 9% 3% 13% 5% 5% 5% 3% 9% 13% 4% 3% 6% 8% 8% 5% 7% 2% 1%

The major constituent of PAH in raw fish samples from Lagos was 3Methylcholanthrene (0.187 ± 0.1337 mg kg−1), which constitutes 45% of ∑PAHs. Indeno[1,2,3-cd]pyrene (9.374 ± 7.545 mg kg−1) was the most abundant PAH measured in Abeokuta raw fish samples, forming 90% of ∑PAHs. Similar PAH concentration trends were observed in smoked fish samples from both sampling locations. However, in smoked fish samples from Lagos, 3-Methylcholanthrene and Indeno [1,2,3-cd]pyrene forms 28% and 97% of ∑PAHs, respectively. Similarly, Indeno[1,2,3-cd]pyrene was the major fraction of PAHs measured in Abeokuta crayfish constituting 92 and 97% of ∑PAHs, respectively for raw and smoked samples, respectively. The past study by Ongwech et al. (2013) on smoked Lates niloticus from three markets in Gulu district of northern Uganda revealed Indeno[1,2,3-cd]pyrene as the highest measured PAH. The congener formed 45–56% of the total PAHs in fish samples. In raw and smoked crayfish samples from Lagos, 3Methylcholanthrene (0.196 ± 0.091 mg kg−1) and Benzo[a]pyrene (0.093 ± 0.001 mg kg−1) were the dominating PAHs. These two components represent 46 and 22% of ∑PAHs, respectively. Eighteen PAH congeners were measured in smoked crayfish samples from Abeokuta. Most of the PAH components were higher in smoked (fish and crayfish) than their respective raw samples except 3Methylcholanthrene (from Lagos fish samples) and Naphthalene (from Abeokuta crayfish samples). The high concentration of Indeno[1,2,3cd]pyrene measured in the present study is a concern to public health. Fish and crayfish samples were generally dominated by high molecular weight PAHs, which are very deleterious to human health (JECFA, 2005). Many past studies from Nigeria have measured different PAH congeners at high concentrations in smoked fish samples (Silva et al., 2011; Amos-Tautua et al., 2013; Tongo et al., 2017). Acenaphthene and fluorene were the main congeners of PAHs determined in some locally consumed fish samples from Ijora, Lagos (Silva et al., 2011). A high level of Phenanthrene up to 9.98 mg kg−1 was determined in smoked fish from Amassoma, Niger Delta (Amos-Tautua et al., 2013). Tongo et al. (2017) revealed the highest concentrations of BaP in smoked Clarias gariepinus and Ethmalosa fimbriata, and Naphthalene in smoked Tilapia Zilli and Scomber scombus collected in markets from southern Nigeria. Benson et al. (2017) reported Indeno[1,2,3-cd]pyrene,

showed more PAH components than the raw meat. Indeno[1,2,3-cd] pyrene contributed more than 70% of the total PAHs in smoked meat from Abeokuta. The patterns of PAH distribution in raw and smoked cowskin samples are similar. 3-Methylcholanthrene and naphthalene were the main components of PAHs determined in smoked cowskin samples from Lagos and Abeokuta. These two PAH congeners represent around 39 and 84% of ∑PAHs, respectively. The previous study of Akpoghelie (2018) measured Phenanthrene and Benz[a]anthracene as the highest PAH concentration in smoked meat samples collected from Warri, Delta State, Nigeria. In smoked beef samples analysed by AmosTautua et al. (2013), the major constituents of PAHs were Benzo[a] anthracene (7.23 mg kg−1), 1, 2 Benzanthracene (4.6 mg kg−1) and Chrysene (2.95 mg kg−1). These three PAH components constitute more than 98% of the total PAHs. The total amount of PAHs measured in meat and cowskin samples varied from 0.414 ± 0.085 mg kg−1 (raw meat from Lagos) to 6.701 ± 2.751 mg kg−1 (smoked meat from Abeokuta). These values were lower than the ∑PAH value of 14.83 mg kg-1 reported in smoked meat by Amos-Tautua et al. (2013). The ∑PAHs in smoked cowskin from Lagos and Abeokuta were 9 and 3 times higher than their respective raw samples; for meat sample, ∑PAH was 2 times higher in Lagos smoked samples than the raw samples. The meat and cowskin samples measured appreciably similar concentrations of Benzo[a]pyrene (BaP) (0.019 ± 0.002 – 0.092 ± 0.001 mg kg−1). The BaP contents of meat and cowskin (raw and smoked) samples were higher than the European Food Safety Authority (EFSA) permissible limit of 0.002 mg kg−1 (EFSA (European Food Safety Authority), 2008). The sums of PAH concentrations obtained in meat and cowskin samples were also found above the EFSA permissible standard of 0.01 mg kg-1 (EFSA (European Food Safety Authority), 2008). The smoked meat samples were generally dominated by high molecular weight PAHs, while the smoked cowskin samples were dominated by low molecular weight PAHs. High molecular weight PAHs are usually more carcinogenic, mutagenic and teratogenic (Agbozu, 2014). The distribution of PAH composition in fish and crayfish samples are presented in Table 3. At least 14 and 12 PAH congeners were measured in smoked fish and crayfish samples from Lagos, respectively. 31

32

SD-standard deviation.

Naphthalene Acenaphthylene Acenaphthene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[c]phenanthrene Benz[a]anthracene Chrysene Benzo[e]pyrene Benzo[k]fluoranthene Benzo[b]fluoranthene 3-Methylcholanthrene Indeno[1,2,3-cd]pyrene Dibenz[a,h]anthracene Benzo[ghi]perylene Dibenzo[a,h]pyrene Dibenzo[a,i]pyrene Benzo[a]pyrene PAH4 ∑PAHs

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.019 < 0.001 < 0.001 0.057 < 0.001 < 0.001 0.246 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.091 0.091 0.413

0.0001 0.0001 0.0852

0.052

0.0001

0.033

0.512 0.046 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 4.552 < 0.001 < 0.001 < 0.001 < 0.001 0.015 0.015 5.125 0.001 0.001 8.006

7.733

0.232 0.040

0.011 0.018 0.020 < 0.001 0.013 0.008 0.018 < 0.001 0.042 0.018 0.021 0.058 < 0.001 < 0.001 0.097 < 0.001 < 0.001 0.017 < 0.001 < 0.001 0.091 0.13 0.432

Mean

0.0001 0.0661 0.2881

0.014

0.089

0.036 0.031 0.035 0.001

0.001 0.001 0.030

0.018 0.015 0.017

SD

Mean

Mean

SD

Lagos (N = 3)

Abeokuta (N = 3)

Lagos (N = 3)

SD

Smoked Meat (mg kg−1 wet weight)

Raw Meat

Table 2 : The distribution of PAH constituents in meat and cowskin samples from Lagos and Abeokuta.

0.598 0.044 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.197 0.057 0.141 < 0.001 5.554 0.086 < 0.001 < 0.001 < 0.001 0.023 0.164 6.7

Mean

0.002 0.054 2.753

2.417 0.069

0.143 0.015 0.052

0.017 0.038

SD

Abeokuta (N = 3)

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.021 < 0.001 < 0.001 0.019 < 0.001 < 0.001 0.094 < 0.001 < 0.001 < 0.001 0.074 < 0.001 0.091 0.091 0.299

Mean

0.0001 0.0001 0.1881

0.063

0.057

0.033

0.035

SD

Lagos (N = 3)

Raw cowskin

0.479 0.031 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.017 0.017 0.527

Mean

0.006 0.006 0.158

0.099 0.053

SD

Abeokuta (N = 3)

< 0.001 < 0.001 < 0.001 < 0.001 0.005 0.003 0.018 < 0.001 0.037 < 0.001 < 0.001 0.038 < 0.001 < 0.001 0.224 < 0.001 < 0.001 < 0.001 0.111 0.050 0.092 0.092 0.578

Mean

0.002 0.001 0.001 0.001 0.25

0.138

0.033

0.032

0.007 0.005 0.031

SD

Lagos (N = 3)

Smoked cowskin

1.135 0.081 0.064 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.03 < 0.001 < 0.001 < 0.001 0.028 0.001 < 0.001 < 0.001 < 0.001 0.019 0.019 1.358

Mean

0.309

0.002

0.047 0.001

0.051

0.183 0.024 0.001

SD

Abeokuta (N = 3)

A.M. Taiwo, et al.

Journal of Food Composition and Analysis 79 (2019) 28–38

33

SD-standard deviation.

Naphthalene Acenaphthylene Acenaphthene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[c]phenanthrene Benz[a]anthracene Chrysene Benzo[e]pyrene Benzo[k]fluoranthene Benzo[b]fluoranthene 3-Methylcholanthrene Indeno[1,2,3-cd]pyrene Dibenz[a,h]anthracene Benzo[ghi]perylene Dibenzo[a,h]pyrene Dibenzo[a,i]pyrene Benzo[a]pyrene PAH4 ∑PAHs

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.019 < 0.001 < 0.001 0.039 < 0.001 < 0.001 0.123 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.091 0.091 0.627

0.001 0.001 0.513

0.060

0.033

0.033

0.504 0.082 0.042 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.215 0.075 0.101 < 0.001 9.374 0.028 < 0.001 < 0.001 < 0.001 0.035 0.136 10.457 0.013 0.062 7.843

7.545 0.031

0.112 0.020 0.049

0.012 0.025 0.036

0.005 0.021 0.030 < 0.001 0.015 0.008 0.056 < 0.001 0.055 0.054 0.062 0.057 < 0.001 < 0.001 0.187 < 0.001 < 0.001 0.008 < 0.001 0.020 0.094 0.21 1.047

Mean

0.033 0.001 0.005 0.684

0.013

0.133

0.001 0.002 0.002 0.001

0.002 0.001 0.001

0.007 0.018 0.001

SD

Mean

Mean

SD

Lagos (N = 3)

Abeokuta (N = 3)

Lagos (N = 3)

SD

Smoked fish (mg kg−1 wet weight)

Raw fish

Table 3 The distribution of PAH constituents in fish and crayfish samples from Lagos and Abeokuta.

1.320 0.083 0.075 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.031 0.070 0.015 < 0.001 50.491 0.003 < 0.001 < 0.001 < 0.001 0.022 0.037 52.111

Mean

0.005 0.031 86.535

86.059 0.003

0.053 0.120 0.026

0.230 0.020 0.019

SD

Abeokuta (N = 3)

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.021 < 0.001 < 0.001 0.019 < 0.001 < 0.001 0.196 < 0.001 < 0.001 0.008 0.037 0.053 0.093 0.093 0.428

Mean

0.014 0.063 0.004 0.001 0.001 0.241

0.091

0.033

0.036

SD

Lagos (N = 3)

Raw crayfish

1.069 0.057 0.022 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.068 0.034 0.023 < 0.001 15.921 0.055 < 0.001 < 0.001 < 0.001 0.027 0.05 17.275

Mean

0.021 0.041 14.436

13.647 0.052

0.059 0.029 0.020

0.522 0.049 0.038

SD

Abeokuta (N = 3)

< 0.001 0.023 0.021 < 0.001 0.014 0.008 0.054 < 0.001 0.019 < 0.001 < 0.001 0.039 < 0.001 < 0.001 0.113 < 0.001 < 0.001 0.016 0.074 0.017 0.091 0.091 0.791

Mean

0.014 0.063 0.029 0.001 0.001 0.566

0.012

0.033

0.031

0.020 0.017 < 0.001 0.002 0.001 0.001

SD

Lagos (N = 3)

Smoked crayfish

1.027 0.229 0.277 0.275 0.037 0.023 0.010 0.024 0.073 0.024 0.018 0.255 0.201 0.483 0.111 96.817 0.209 < 0.001 < 0.001 < 0.001 0.047 0.572 100.142

Mean

0.036 0.516 67.861

0.311 0.144 0.137 0.172 0.036 0.019 0.017 0.04 0.126 0.041 0.03 0.006 0.173 0.409 0.119 65.922 0.121

SD

Abeokuta (N = 3)

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were identified with a total of 78% dataset explained. Component 1 has high loadings for Acenaphthylene, Acenaphthene, Fluorene, Phenanthrene, Anthracene, Benzo[e]pyrene, Benzo[k]fluoranthene, Benzo[b] fluoranthene, Dibenz[a,h]anthracene and Indeno[1,2,3-cd]pyrene. This factor explained 38% of the total variance, and could be designated mixed industrial and traffic source. Emissions of low molecular weight PAHs such as Phenanthrene, Anthracene and Fluorene have been attributed to cokemaking and unburned petroleum from vehicles (Xiao et al., 2014). Benzo[k]fluoranthene and Benzo[b]fluoranthene are components of fossil fuel combustion (Kavouras et al., 2011). Indeno [1,2,3-cd]pyrene has also been adopted a fingerprint for gasoline engine emission (Li et al., 2011). Jang et al. (2013) reported Benzo[e] pyrene, Benzo[k]fluoranthene and Indeno[1,2,3-cd]pyrene as tracers for traffic emissions. Similarly, Ke et al. (2017) assigned Acenaphthylene, Phenanthrene, Anthracene, Benzo[k]fluoranthene, Dibenz[a,h] anthracene and Indeno[1,2,3-cd]pyrene determined in soil samples from Guangzhou, China to traffic emission. The emission source of component 1 can further be established using the Phenanthracene to Anthracene (Ph/An) ratio, which has been adopted to distinguish pyrogenic (biomass combustion) and petrogenic (petroleum) PAHs (Wang et al., 2009). The Ph/An ratio value less than 10 signifies pyrogenic source, while the Ph/An ratio greater than 10 indicates petrogenic emission source. The Ph/An values calculated for Lagos smoked fish, crayfish, cowskin and meat were 1.9 and 1.8, 1.7 and 1.6, respectively; while the Ph/An value for Abeokuta smoked crayfish was 2.6. These Ph/An ratios less than 10 indicate that Phenanthracene and Anthracene might originate from pyrogenic source, probably from fossil fuel combustion. Exposure of protein foods to road dust and vehicular emissions might be responsible for contamination by PAHs (Zhang et al., 2018). Component 2 has a significant affinity for Fluoranthene, Benzo[c] phenanthrene, Benz[a]anthracene and Chrysene. This component was dominated mainly by 4-ring PAHs, which has been attributed to domestic cooking practices including cooking, smoking, grilling and frying (Zhu and Wang, 2003). Wang et al. (2009) adopted Benzo [a]Anthracene to Chrysene (BaA/Ch) ratio to infer the source emission of PAHs. The BaA/Ch data for smoked fish and meat from Lagos was 0.9, while Abeokuta smoked crayfish has a BaA/Ch ratio of 1.3. This indicates mixed sources of Benzo[a]Anthracene and Chrysene in the

Phenanthrene and Pyrene as the major PAH components in the analysed imported sardine fish samples. Akpoghelie (2018) measured high concentrations of Phenanthrene and Benz[a]anthracene in smoked fish samples from Warri, Delta. However, the levels of Indeno[1,2,3-cd] pyrene in the present study are far higher than the values previously reported in food samples from Nigeria. 3.2. PAH contamination levels in protein foodstuffs The ∑PAHs of protein foods were generally higher in Abeokuta than Lagos samples. The ∑PAHs of Abeokuta raw fish samples was 38 times higher than Lagos raw fish samples. For smoked fish samples, the sum of PAHs was 78 times higher in Abeokuta than Lagos samples. The discrepancies between the concentrations of PAHs in food samples from Abeokuta and Lagos can be attributed to factors including levels of exposure to atmospheric contaminants at the point of sales, different processing methods and probably, the lipid contents (Akpan et al., 1994; Silva et al., 2011; Igwe et al., 2012). The PAH contents determined in this present study were higher than the reported values in protein foodstuffs from other parts of the world e.g. Kuwait (Alomirah et al., 2011), Latvia (Miculis et al., 2011), Korea (Kim et al., 2014), China (Duan et al., 2016) and Malaysia (Nasher et al., 2016). The sums of PAH4 (Benz[a]anthracene, Benzo[b]fluoranthene, Benzo[a]pyrene and Chrysene) in smoked fish samples from Lagos (0.210 mg kg−1) and Abeokuta (0.037 mg kg−1) were higher than the European Commission (EC) Regulation maximum level of 0.03 mg kg-1 for smoked fish (EC, 2006; Miculis et al., 2011). The sum of PAH4 in raw fish samples was also higher than this permissible limit. The major health concerns of PAH4 are mutagenic and carcinogenic toxicities (Miculis et al., 2011). 3.3. Source identification of PAHs in food samples The rotated varimax principal component analysis (PCA) of PAH data measured in protein food samples are presented in Table 4. The PCA was carried out to identify the possible contaminated sources of PAHs in food samples. The results of Kaiser-Meyer-Olkin (KMO) measure of sampling adequacy and Bartlett's test of sphericity are 0.733 and 1662.036, respectively. In the rotated varimax PCA, four components Table 4 Rotated varimax principal component analysis of PAH data. Component

Naphthalene Acenaphthylene Acenaphthene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo[c]phenanthrene Benz[a]anthracene Chrysene Benzo[e]pyrene Benzo[k]fluoranthene Benzo[b]fluoranthene 3-Methylcholanthrene Indeno[1,2,3-cd]pyrene Dibenz[a,h]anthracene Benzo[ghi]perylene Dibenzo[a,h]pyrene Dibenzo(a,i)pyrene Benzo[a]pyrene

1

2

3

4

Communalities

.374 .718 .916 .845 .695 .825 .034 .440 .241 .142 .060 .649 .668 .950 .019 .716 .928 .013 −.048 −.120 −.113 32 Industrial & Unburned fuel

−.266 .110 .074 .191 .561 .459 .670 .329 .575 .903 .922 −.013 .093 .006 .281 .029 −.057 .481 −.130 −.018 .433 18 Cooking Practices

−.630 −.290 −.129 .045 .185 .168 .328 .072 .367 −.032 −.051 −.176 −.137 −.051 .799 −.108 −.124 .249 .765 .738 .755 16 Wood/Coal Combustion

.380 .523 .128 .425 .324 .089 −.108 .765 .567 .285 .147 .045 .637 .082 .120 .496 .020 −.417 −.086 .027 −.033 12 Diesel Combustion

.752 .886 .878 .933 .937 .927 .569 .892 .845 .918 .878 .455 .880 .912 .732 .771 .880 .467 .612 .560 .772 (78%)

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Fig. 2. Hazard index values of PAHs in food samples.

food samples, which might emanate from either pyrogenic (smoked fish and meat samples from Lagos) or petrogenic (smoked crayfish samples from Abeokuta). The ratio of Fluoranthene (Fla) to Pyrene (Pyr) has also been used to derive the sources of PAHs in the environment (Benlahcen et al., 1997; Collins et al., 1998). The Fla/Pyr value greater than 1.0 indicates pyrogenic source, while the Fla/Pyr ratio less than 1.0 represents petrogenic source. Even though, Pyrene was weakly correlated (r = 0.329) in component 2, but Fluoranthene was strongly significant. The Fla/Pyr value for smoked crayfish from Abeokuta was 0.4 indicating a pyrogenic source. Ke et al. (2017) linked high molecular weight of PAHs (4–6 rings) to pyrogenic origin. Component 3 is characterized by high significant loadings for 3Methylcholanthrene, Dibenzo[a,h]pyrene, Dibenzo(a,i)pyrene, and Benzo[a]pyrene. This factor is anti-correlated with Naphthalene. Most of the congeners occurring in this factor are high molecular weight PAHs. Dibenzopyrenes are usually associated with coal combustion (Masala et al., 2012). This component may therefore be attributed to wood/coal combustion. Jang et al. (2013) also connected emissions of Benzo[a]pyrene to wood combustion. Component 4 has a strong affinity for Pyrene and Benzo[k]fluoranthene; with 5% of the total variance explained. This component may be related to diesel fuel combustion. Benzo[k]fluoranthene has been reportedly associated with combustion of fossil fuel (Kavouras et al., 2001), while Pyrene was associated to diesel emission (Jang et al., 2013).

average daily dose (ADD) values of PAHs in food samples. The ADD was calculated based on the assumption that an adult weighing 60 kg consumes 24.7 g of any of the protein foods for 350 days per year (Taiwo et al., 2018). Results show that the highest dosed PAH through meat consumption was Dibenz[a,h]anthracene (0.0024 ± 0.0011 mg kg−1 day−1) from Abeokuta smoked meat samples, while Phenanthrene (0.00091 ± 0.0015 mg kg−1 day−1) was the highest PAH taken daily in smoked cowskin samples from Lagos. The most dosed PAH in fish and crayfish samples was Dibenz[a,h]anthracene from Abeokuta smoked fish (0.022 ± 0.038 mg kg−1 day−1) and crayfish (0.042 ± 0.029 mg kg−1 day−1). The daily intake values of Benzo[a]pyrene (BaP) in meat and cowskin samples ranged from 6.6 ± 0.6 × 10−6 mg kg-1 day-1 (Abeokuta smoked fish) to 40 ± 0.41 × 10−6 mg kg-1 day-1 (Lagos smoked cowskin). In fish samples, the ADD levels of BaP varied from 15 ± 5.6 × 10−6 mg kg-1 day-1 (Abeokuta raw fish samples) to 41 ± 0.6 × 10−6 mg kg-1 day-1 (Lagos smoked fish and raw crayfish). The ADD values of BaP in fish and crayfish samples (Lagos and Abeokuta) were generally higher than the JECFA estimated high- level average daily intake concentration of 10 × 10−6 mg BaP kg-1 day-1 in consumer foods (JECFA, 2005). This may pose significant health threats to consumers due to mutagenic and carcinogenic characteristics of BaP (Delgado-Saborit et al., 2011). Table S3 shows the data of hazard quotients (HQs), while Fig. 2 highlights the hazard index values (HI) of PAHs through consumption of protein food samples. HQ and HI values were generally less than 1.0, which suggest non-carcinogenic adverse effects. However, the toxic nature of BaP, Indeno[1,2,3-cd]pyrene, Fluorene, Fluoranthene has placed their HQs at 0.1 (Bulder et al., 2006). The HQ of BaP was higher than 0.1, therefore depicting possible non-carcinogenic health

3.4. Health risk assessment Tables S1 and S2 (in the supplementary information) present the 35

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Fig. 3. Sum of cancer risk values of PAHs in food samples.

crayfish > smoked crayfish > smoked cowskin > raw meat > raw fish > raw cowskin > smoked meat. Previous studies have reported PAH cancer risk values higher than both the acceptable and priority limits in protein food samples from Nigeria (Tongo et al., 2017), China (Xia et al., 2010; Nie et al., 2014; Qu et al., 2015; Duan et al., 2016), Malaysia (Nasher et al., 2016).

problems. Non-carcinogenic adverse effects of BaP include neurobehavioral effects, decreased fertility and adverse birth outcomes (e.g. reduced birth and postnatal body weight, and head circumference) (TOXNET, 2017). This study reveals BaP and Naphthalene as main contributors to non-carcinogenic hazard index in protein foodstuffs from Abeokuta, while BaP was the major fraction of HI in food samples from Lagos. The cancer risk data of individual PAHs in protein food samples are presented in Table S4. BaP shows the highest CR level varying from 3.44 × 10−5 (Abeokuta raw cowskin) to 2.19 × 10-2 (Abeokuta smoked crayfish). The high CR level of BaP in Abeokuta smoked crayfish suggests that at least 2 persons out of 100 may develop cancer during their life time through consumption of smoked crayfish. This cancer risk value is undoubtedly very high and alarming. The CR of metals measured in protein foods from Abeokuta and Lagos has shown high value of 2.0 × 10-3 (Taiwo et al., 2018). Most of the carcinogenic PAHs analysed in protein revealed CR levels were higher than the USEPA acceptable limit of 1.0 × 10-6 except Benzo[k]fluoranthene in smoked cowskin (Lagos and Abeokuta), smoked meat (Lagos), smoked fish (Lagos and Abeokuta) raw fish (Lagos) and crayfish (Lagos). The sums of cancer risk (∑CR) data are presented in Fig. 3. Many protein foodstuffs have the ∑CR values higher than the priority limit of 1.0 × 10−4. This depicts that more than 1 person out of 10,000 people have the tendency of developing cancer in their lifetime. However, the ∑CR values of PAHs determined in Abeokuta smoked cowskin samples were higher than the acceptable risk level of 1.0 × 10-6 indicating risk of cancer development for 1 in 1,000,000 population. The ∑CR values of PAHs in Lagos foodstuffs were generally higher than those of Abeokuta. The sum of CR follows the decreasing pattern of smoked fish > raw

4. Conclusion This study has assessed the levels and health risk of PAHs in meat, cowskin, fish and crayfish samples. The highest measured PAH in protein foodstuffs was Indeno[1,2,3-cd]pyrene. PAH levels were generally higher in smoked than raw protein food samples. The order of ∑PAH abundance in foodstuffs follows the trend of crayfish > fish > meat > cowskin. The smoked meat samples were generally dominated by high molecular weight PAHs, while the smoked cowskin samples were dominated by low molecular weight PAHs. Both smoked and raw fish and crayfish samples were dominated by high molecular weight PAHs. The rotated varimax principal component analysis of PAH data in protein food samples was able to identify four major contaminated sources of PAHs. The sources revealed were industrial and unburned fuel, cooking practice, wood/coal combustion and diesel combustion. The non-carcinogenic health risk assessment of hazard quotient (HQ) and hazard index (HI) of PAHs in food samples were generally less than 1.0 indicating non-carcinogenic adverse effects. However, the HQ of BaP exceeds the toxic level of 0.1. BaP and Naphthalene were major contributors to adverse effects in food samples. The cancer risk (CR) values of PAHs in Abeokuta fish (smoked) and crayfish (raw and smoked) samples were higher than the priority risk level of 1.0 × 10−4 36

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indicating risk of cancer development. The sum of CR follows the following distribution pattern: smoked fish > raw crayfish > smoked crayfish > smoked cowskin > raw meat > raw fish > raw cowskin > smoked meat. This study has established that BaP is the most toxic PAH measured in protein foodstuffs.

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