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DOI:http://dx.doi.org/10.7314/APJCP.2016.17.1.15 Polycyclic Aromatic and Bioaccessibility in Meat: a Tool for Assessing Human Cancer Risk

REVIEW

Polycyclic Aromatic Hydrocarbons (PAHs) and their Bioaccessibility in Meat: a Tool for Assessing Human Cancer Risk

Elliyana Nadia Hamidi1, Parvaneh Hajeb2, Jinap Selamat1, Ahmad Faizal Abdull Razis1,3*

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are primarily formed as a result of thermal treatment of food, especially barbecuing or grilling. Contamination by PAHs is due to generation by direct of food and deposition from smoke produced through incomplete combustion of thermal agents. PAHs are ubiquitous compounds, well-known to be carcinogenic, which can reach the food in different ways. As an important human exposure pathway of contaminants, dietary intake of PAHs is of increasing concern for assessing cancer risk in the human body. In addition, the risks associated with consumption of barbecued meat may increase if consumers use cooking practices that enhance the concentrations of contaminants and their bioaccessibility. Since total PAHs always overestimate the actual amount that is available for absorption by the body, bioaccessibility of PAHs is to be preferred. Bioaccessibility of PAHs in food is the fraction of PAHs mobilized from food matrices during gastrointestinal digestion. An in vitro human digestion model was chosen for assessing the bioaccessibility of PAHs in food as it offers a simple, rapid, low cost alternative to human and animal studies; providing insights which may not be achievable in in vivo studies. Thus, this review aimed not only to provide an overview of general aspects of PAHs such as the formation, carcinogenicity, sources, occurrence, and factors affecting PAH concentrations, but also to enhance understanding of bioaccessibility assessment using an in vitro digestion model.

Keywords: Polycyclic aromatic hydrocarbons - barbecued meat - bioaccessibility - in vitro human digestion model

Asian Pac J Cancer Prev, 17 (1), 15-23

Introduction Rashdan et al., 2010; Plaza-Bolańos et al. 2010; Viegas et al., 2012; Abou-Arab et al, 2014). Meanwhile, light Concern over polycyclic aromatic hydrocarbons PAHs are more volatile, soluble and less lipophilic (PAHs) in foodstuffs was started during the 1960s and compared to heavy PAHs (Farhadian et al., 2010). PAHs 1970s, where two classes of food producing containing between two and seven rings are tumours have been focused i.e. polycyclic aromatic the most PAHs that can be found in the environment. hydrocarbons (PAHs) and N-nitroso compounds It might be thought that the wide presence of PAHs in (Jägerstad and Skog, 2005). PAHs are referring to a the atmosphere is due to the lipophilic characteristics series of organic compound containing two or more fused allowing their adsorption onto atmospheric particles and aromatic rings (Danyi et al., 2009; El-Badry, 2010). PAHs direct deposition in sediments, and (Danyi et constitute a large class of organic compounds (about al., 2009). 10,000 substances) characterized by a structure made Importantly, the 16 Environmental Protection up of and (Danyi et al., 2009; Agency (EPA) PAHs have been the main focus of the Ishizaki et al., 2010; Plaza-Bolańos et al. 2010). PAHs are research community and extensively been monitored as non-polar compounds with the characteristic of lipophilic, ‘priority pollutants’ to be controlled in the United States semi-volatile and persistence properties (Plaza-Bolańos et Environmental Protection Agency ( Plaza-Bolańos et al., 2010; Palm et al., 2011). al., 2010; Viegas et al., 2012). In 2005, 15 compounds PAHs comprise of light PAHs (those containing up have also been included in the monitoring studies in the to four fused benzene rings) and heavy PAHs (those European Union (EU) (Plaza-Bolańos et al., 2010). Among containing more than four benzene rings). Heavy PAHs these compounds, eight high molecular weight from the are known to be more stable and toxic than light PAHs (Al- US-EPA list i.e. Benzo(a), Chrysene, Benzo(b)

1Food Safety Research Centre, Faculty of Food Science and Technology, 2Laboratory of UPM-MAKNA Cancer Research, Institute of Bioscience, Universiti Putra Malaysia, Selangor, Malaysia *For correspondence: [email protected] Asian Pacific Journal of Cancer Prevention, Vol 17, 2016 15 DOI:http://dx.doi.org/10.7314/APJCP.2016.17.1.15 Elliyana Nadia Hamidi et al Polycyclic Aromatic Hydrocarbons and Bioaccessibility in Meat: a Tool for Assessing Human Cancer Risk fluoranthene, Benzo(k)fluoranthene, Benzo(a), categories based on their molecular weight but having the grilling in charcoal to flame formation, thus respiratory system, larynx, skin and kidney, and primarily Indeno(1,2,3-cd)pyrene, Benzo(ghi)pyrene, Dibenzo(ah) similar environmental fates i.e. low, medium and high increasing the release of smoke that carries PAHs and the in the lungs site (Jarvis et al., 2014). In that case, several anthracene were selected to be the most suitable indicators molecular weights. These groups of categories are temperature near the surface during the flashing (Viegas factors have been linked to the exposure of PAHs and of the occurrence and potential carcinogenic of the entire classified according to the number of condensed aromatic et al., 2012). cancer such as smoking, cooking, dietary intake as well class of PAHs (Viegas et al., 2012). Table 1 shows the rings, their molecular weights and the examples of each as wood burning. Tobacco smoking is known to be the molecular weights and formula structures of the 16 EPA category are shown in Table 2. Human Exposure to PAHs larger contributor to lung cancer incidence in humans, priority PAHs and European Union PAHs of concern in which account approximately 90% of all lung incidences food. Formation of PAHs PAHs can reach to the human body by different and 1.2 million deaths per year worldwide (IARC, 2004; PAHs also can be divided into three groups of modes of exposure. The routes of exposure to PAHs can Jarvis et al., 2014). Polycyclic aromatic hydrocarbons are produced during be through inhalation, skin contact as well as through In addition, smoking has also been identified as a cause Table 1. Molecular Weights and Formula Structures of variation of combustion and pyrolysis processes from consumption of contaminated food. The ways that human of cancer in a number of other human organ sites. The the 16 EPA Priority PAHs and European Union PAHs anthropogenic and natural sources including carbon- can be exposed to PAHs are presented in Table 3. interaction between tobacco smoking, B(a)P and DNA of Concern in Food (Adapted from Purcaro et al., 2013) containing materials such as oil, wood, garbage or coal Among these routes, consumption of contaminated damage have been reviewed recently as B(a)P was one (Danyi et al., 2009; Silva et al., 2011; Jahurul et al., 2013; food has been identified as a principal route of human of the first carcinogenic compounds detected in tobacco Omwukeme et al., 2015). Environmental contamination exposure to PAHs as it contributes about 88 to 98% of smoke (Jarvis et al., 2014). Besides, from the case study and food processing i.e. smoking, heating (grilling and/or such contamination (Plaza-Bolanos et al., 2010; Silva et by Jagerstad and Skog (2005), the exposure of PAHs from roasting), drying which allow the direct contact between al., 2011; Omwukeme et al., 2015). Based on Al-Rashdan tobacco smoking and the workplace indicated the target food and combustion products also can be the significant et al. (2010), exposure of PAHs to human does not present organs include lung, breast and gastrointestinal tracts. In source for the presence of PAHs in foodstuff (Plaza- individually, but in complex mixtures of PAHs. In fact, addition, consumption of grilled/barbecued red meat was Bolanos et al., 2010; Viegas et al., 2012). PAHs usually present in a mixture of two or more of associated with pancreatic and stomach cancer (Anderson Generally, at least three possible mechanisms exist these compounds, for instance soot, coal tar and diesel et al., 2002). in the formation of PAHs in grilled/smoked foods even fuel (Knightes and Peters, 2006; Marti-Cid et al., 2008). On the other hand, the primary route of non-smokers though the exact mechanism is not precisely known PAHs may present a health risk to human as PAHs to be exposed to PAHs is mostly through dietary (Alomirah et al., 2011). The possible mechanisms are: become activated in liver, intestine and other extra exposure to complex PAH mixtures which can also give First mechanism: The pyrolysis of hepatic tissues to reactive metabolites that interfere with significant risk for human cancer development such as such as , and at temperature target organ function, leading to fatal and cause colorectal, pancreatic and prostate cancer. Apart of food above 200ºC where the favourable condition of PAHs (Marques et al., 2011). The factors which contribute to formation is at the temperature ranging from 500-900ºC. absorption of dietary PAHs can be the size of PAHs, The highest concentration of PAHs is shown to arise from lipophilicity of PAHs compound and the content of pyrolysis of fat. food (Marques et al., 2011). After being absorbed, PAHs Second mechanism: The yield of dripping in are distributed by blood to several tissues, especially direct contact over the flame at intense heat. This condition those with a high fat content, and some are metabolized is suitable in the formation of volatile PAHs, which then to DNA-active mutagen or genotoxic carcinogenic deposited on the meat surface as the smoke rises. compounds (diol epoxides) (Marques et al., 2011). It has Third mechanism: The incomplete combustion of been reported that absorption of 14C-BaP in Wistar rats charcoal which can generate PAHs that in turn is adhered was increased with the diet containing high lipid contents to the surface of the food. and was restrained when feeding high-fibre foods (Purcaro PAHs were produced in the processed and cooked food et al., 2013). as a consequence of organic matter combustion during Many case-control studies have been extensively cooking and smoking process and also direct deposition described on exposure of human workers to PAHs through Figure 1. Estimated Contributions (%) of Nine PAHs of PAHs from produced smoke through incomplete their occupation as well as through dietary exposure (fluoranthene, pyrene, benzo (a) anthracene, chrysene, combustion of different thermal agents (Farhadian et (Anderson et al., 2002; Jagerstad and Skog, 2005; Jarvis benzo(b)fluoranthene, benzo (j) fluoranthene/ benzo(k) al., 2011; 2012). Incomplete combustion is, by itself, et al., 2014). From the case control studies, occupational fluoranthene, benzo(e)pyrene, benzo(a)pyrene and responsible for the formation of PAHs contaminating exposure associated with human cancers were observed indeno(1,2,3-cd)pyrene) in Various Food Groups of grilled food. The heat on the surface of the muscle food at various sites including bladder, esophagus/stomach, Swedish diet (Adapted from Jägersted et al., 2005) generates these contaminants by direct pyrolysis of food nutrients. Additionally, the natural meat and fish juices Table 3. Routes of Human Exposure to PAHs which are released during the grilling and fall from the Route of exposure Occurrences References muscle food into the charcoal can suffer pyrolysis and lead Inhalation Inhalation of tobacco smoke, wood smoke and ambient air Abou-Arab et al. (2014) to formation of PAHs, which being dragged by the smoke Inhalation of engine exhaust Jarvis et al. (2014) and deposited on the surface of the food. Fat dripping from People working in industries such as mining, Silva et al. (2011) oil refining and working Public Health England (2008) Table 2. Categories of PAHs Based on their Molecular Weight (Adapted from Palm et al., 2011) Falco et al. (2003) Skin contact Breathing in or touching PAHs for a long time were Jarvis et al. (2014) Low molecular Medium molecular weight High molecular suggested to cause lung or skin cancer Silva et al. (2011) Categories weight (LMW) (MMW) weight (HMW) Public Health England (2008) Aromatic rings two- and three rings four- rings five- to seven- rings Falco et al. (2003) Molecular weight 152 g/mol – 178 g/mol 202 g/mol 228 g/mol – 278 g/mol Consumption of Eating food containing PAHs Abou-Arab et al. (2014) Example i) phenanthrene 100.0i) fluoranthene i) benzo(a)pyrene contaminated food Fruits and vegetables grown in contaminated Jarvis et al. (2014) Processed food (charbroiling and grilling at high temperatures) Silva et al. (2011) ii) pyrene 6.3 ii) dibenzo(a,h)anthracene 12.8 10.1 20.3 Public Health England (2008) iii) indeno(1,2,3-cd)pyrene 10.3 25.0 30.0 16 Asian Pacific Journal of Cancer Prevention, Vol 17, 201675.0 Asian Pacific Journal of Cancer Prevention, Vol 17, 2016 17 46.8 75.0 56.3 51.1 51.7 50.0 54.2 31.3 30.0

25.0 38.0 31.3 31.3 30.0 33.1 23.7 25.0 27.6

0 0 None Remission Radiotherapy Chemotherapy Persistence or recurrence or Persistence Concurrent chemoradiation Concurrent Newly diagnosed with treatment withtreatment diagnosed Newly Newly diagnosed without treatment withouttreatment diagnosed Newly DOI:http://dx.doi.org/10.7314/APJCP.2016.17.1.15 Elliyana Nadia Hamidi et al Polycyclic Aromatic Hydrocarbons and Bioaccessibility in Meat: a Tool for Assessing Human Cancer Risk Table 4. IARC Classification of PAHs according to Possibility to be Carcinogenic to Human (Adapted from Joint FAO/WHO Expert Committee on Food Additives PAHs in Processed and Cooked Food IARC, 2010) (JECFA) has stated the amount of BaP in foods should not exceed 10 ppb (Chung et al., 2011). As far as toxic PAHs is concerned, several studies have Group 1 Group 2A Group 2B Group 3 PAHs are regarded as potential genotoxic and been carried out evaluating PAHs in processed and cooked (carcinogenic to human) (probably carcinogenic to human) (possibly carcinogenic to human) (unclassified as carcinogenic to human) carcinogenic to humans. After metabolic activation food, especially in grilled and smoked foods (Reinik et Benzo(a)pyrene Benzo(a)anthracene Benzo(a)anthracene Fluoranthene in mammalian cells to diol-epoxides, PAHs will bind al., 2007; Akpambanga et al., 2009; Perello et al., 2009; Dibenzo(a,h)anthracene Benzo(k)fluoranthene covalently to cellular macromolecules, including DNA, Farhadian et al., 2010; 2011). Recently, Omwukeme et al. Dibenzo(a,l)pyrene Benzo(b)fluoranthene thereby causing errors in DNA replication and mutations (2015) reported that PAHs concentration was detected as Benzo(j)fluoranthene high as 200 µg/kg of individual PAH in smoked fish and Dibenzo(a,h)pyrene that initiate the carcinogenic process (Reinik et al., 2007; Dibenzo(a,i)pyrene Farhadian et al., 2010; 2012). Exposure to high levels meat. Jahurul et al. (2013) has also measured the sum of 5-methylchrysene 100.0 of dietary and environmental PAHs has been associated three PAHs (fluoranthene, benzo(b)fluoranthene, benzo(a) Indeno(1,2,3-cd)pyrene 6.3 with numbers of incidences for instance12.8 esophageal and pyrene) and reported that the level of PAHs in beef satay 10.1 20.3 colorectal cancers development as well as endocrine 10.3(66.28 ng/g), chicken satay (42.31 ng/g), charcoal grilled 75.0 disruption-related25.0 infertility30.0 (Ramesh et al., 2004). fish (40.69 ng/g), mutton satay (30.76 ng/g) and chicken Table 5. Sources of PAHs Contamination in Food Products The PAHs content in smoked meat and fish has been barbecued (17.86 ng/g). 46.8 extensively reported as an increased risk of stomach75.0 cancer In other study by Farhadian et al. (2010), PAHs appear Sources Occurrences References 56.3 51.1 observed in certain population who consumed the food at in grilled meat or fish at variable rates of 0 to 130 ng/g with 1. Soils, air and water: PAHs can accumulate on the waxy surface of many vegetables and fruits Jahurul et al. (2013) 51.7 50.0 54.2 the concentration of benzo(a)pyrene (BaP) were in the because of particulate deposition on vegetables and fruits resulting from air high frequency31.3 (Viegas et al.,30.0 2012). pollution. Moreover, a number of epidemiological studies also range of 0.2 to 50 ng/g. Some of the highest concentration soil (by deposition) Seafood and fish can be exposed to PAHs that present in water and sedi- Chung et al. (2011) evaluated the relationship between preference for well- of PAHs was also found in the food cooked over open ments. (e.g: bivalve mollusks species contaminated with a wide range of 25.0 done cooked meat with risk of cancer (Marchand et al., flames such as barbecued meat with total PAHs detected PAHs due to the oil spills present in the sea. 38.0 2002; Jinap et al., 2013). Several cases have been shown to to be up to 164 ppb and B(a)P at concentration as high as 31.3 31.3 30.0 33.1 air (by transfer) Farhadian et al. (2011) 23.7give positive correlations between well-done cooked25.0 meat 27.630 ppb (Farhadian et al., 2010). In Estonia, high BaP levels water (by deposition and transfer) Plaza-Bolańos et al. (2010) intake with cancer incidences especially for colorectal and were found in homemade ham, smoked meat, smoked 0 0 2. Mode of cooking: Smoking, heating (grilling, roasting and drying) permit the direct contact Chung et al. (2011) breast cancer (Sinha et al., 2000; 2001; Afzaninawati et chicken and smoked sausages with concentration of 30.6, between food and combustion products (i.e. important sources of PAHs al., 2013; Jinap et al., 2013). 31.2, 15.0 and 20.0 µg/kg, respectively (Reinik et al., contamination for seeds, edible oils, meat and dairy products). None None 2007). In grilled chicken breast on charcoal, fluoranthene

smoke curing Plaza-Bolańos et al. (2010) Sources Remission Remission of PAHs as Food Contaminant and benzo(a)pyrene were found at concentration of 0.57

broiling Radiotherapy Radiotherapy ng/g and 0.15 ng/g, respectively (Janoszka et al., 2004). Chemotherapy Chemotherapy roasting PAHs can contaminate foodstuffs by several ways, , phenanthrene, fluoranthene and pyrene either via direct or indirect contact with smoke (Al- were reported to be the predominant PAHs in food by grilling over open fires or charcoal Rashdan et al., 2010). Direct contact with smoke occurs Farhadian et al. (2011); while dibenzo(ah)anthracene,

3. Food additives: Smoke flavouring products (SFP), which are utilized to improve..organo- Chung et al. (2011) recurrence or Persistence recurrence or Persistence

when involving no obstacles between the foodstuffs and benzo(b)fluoranthenechemoradiation Concurrent chemoradiation Concurrent and benzo(k)fluoranthene were leptic characteristics produced from smoke condensates, which can be a significant source of PAHs in food. smoke; while, indirect contact with smoke is a placing of found to be low in concentration in food screened by

Newly diagnosed with treatment withtreatment diagnosed Newly withtreatment diagnosed Newly Martorell et al. (2010). Recently, the levels of PAHs were smoking flavour agents Recycled polyethylene film in oil..packaging..could contaminate vegetable Plaza-Bolańos et al. (2010) an obstacle, i.e. a stainless plate above the smoke oils with PAHs by rediffusion. withouttreatment diagnosed Newly withouttreatment diagnosed Newly generator (Gomes et al., 2009). Direct exposure of meat determined in a few Malaysian foods. Table 6 shows the lubricants products to smoke contributed to higher levels of PAHs level of PAHs in different Malaysian grilled meat dishes compared to indirect methods due to partially elimination among three different cooking methods i.e. charcoal of PAHs by condensation in tars (Šimko, 2002). grilling, gas grilling and oven grilling. propellents Interestingly, PAHs can be detected in wide range of In reference to Table 6, beef satay grilled by charcoal glazing agents food products such as dairy products, vegetables, fruits, grilling showed the highest level of PAHs in the range of protective coatings oils, coffee, tea, cereals and smoked meat (Chung et al., 81.0 to 132 ng/g. In turn, the lowest level of PAHs was 4. Traffic 2011; Jahurul et al., 2013). Figure 1 shows the estimated found in grilled chicken by oven grilling (3.51-7.14 ng/g). Exposure to PAHs and nitro-PAHs (derivatives of PAHs) when roads are Plaza-Bolańos et al. (2010) contribution (%) of commonly nine PAHs reported in The levels of PAHs in meat products can be minimized nearby to crops or livestock. food within various food groups in Swedish diet including through alternative cooking methods for instance broiling, grilled food, smoked meat, smoked fish, coffee/tea, baking, stewing as well as cooking at lower temperature /oils, fruit, other vegetables, root vegetables, leafy and shorter time (Anderson et al., 2002). As charcoal consumption, cooking also has been linked to human conclusion and categorized the into few groups; vegetables and cereals. Contamination of these food grilling can be applied to foods both as direct or indirect cancer development as reported in China. High levels Group 1 (carcinogenic to human), Group 2A (probably products arises generally emanate from various sources. way, no carcinogenic PAHs will be detected in the grilled exposure of unvented smoke from indoor cooking was carcinogenic to human), Group 2B (possibly carcinogenic Foods can be contaminated by environmental PAHs that products if dripping of melted fat onto the heat source resulted in unusually high levels of lung cancer mortality to human) and Group 3 (unclassified as carcinogenic to are present in the soil (by deposition); air (by transfer); is prevented. Therefore, avoiding direct contact of meat rates among women (Alomirah et al., 2011; Jahurul et al., human). The examples of PAHs included in these groups water (by deposition and transfer); mode of cooking i.e. with the cooking flame or grilling at low temperature can 2013; Jarvis et al., 2014). can be seen as tabulated in Table 4. smoke curing, broiling, roasting, grilling over open fires reduce the formation of PAHs during charcoal grilling According to the group listed above, benzo(a)pyrene or charcoal; through adding food additives to foods i.e. (Farhadian et al., 2012). (BaP) has been a subject of concern where in 1987, IARC Carcinogenicity of PAHs smoking flavour agents, lubricants, solvents, propellants, Furthermore, meat and other meat products, especially has classified BaP as the most probable human carcinogen. glazing agents, protective coatings as well as by traffic when they are in well-done cooked situation, may induce The presence of PAHs in food is of considerable Thus, the determination of BaP has been widely used (Plaza-Bolańos et al. 2010; Chung et al. 2011; Farhadian the production of chemical carcinogens exposure, like interest since some of them has the ability to cause cancer. as an indicator for the carcinogenic of PAHs present in et al. 2011; Jahurul et al. 2013). Table 5 summarizes the PAHs and other pyrolysis products which vary accordingly Concerning PAHs, these cooked food toxicants have environmental since the profile of the measured PAHs sources of PAHs contamination in food products. to cooking processes, duration of cooking and type of been evaluated by the International Agency for Research in various foodstuffs do not seems to differ very much meat (Farhadian et al., 2012). Similar findings were also on Cancer (IARC, 2010), which has come out with the (Plaza-Bolańos et al., 2010; Purcaro et al., 2013). The reported by Jahurul et al. (2013), showing that the highest 18 Asian Pacific Journal of Cancer Prevention, Vol 17, 2016 Asian Pacific Journal of Cancer Prevention, Vol 17, 2016 19 DOI:http://dx.doi.org/10.7314/APJCP.2016.17.1.15 Elliyana Nadia Hamidi et al Polycyclic Aromatic Hydrocarbons and Bioaccessibility in Meat: a Tool for Assessing Human Cancer Risk Table 6. The Level of PAHs in Different Grilled Meat the formation of PAHs quantitatively (Palm et al., 2011). reference to Purcaro et al. (2013), the longer the distance, studies reported that the bioaccessibility of PAHs in small Dishes among three Different Cooking Methods Based on Purcaro et al. (2013), fat is the major precursor the lower the amount of PAHs in food. Charcoal grilling, intestine ranging from 9.2% to 60.5% was significantly (Adapted from Farhadian et al., 2010) of PAHs formation where the amount of fat content in as the high temperature process, can be applied to foods higher than in stomach which ranging from 3.9% to 54.9%. the processed food affects the level of PAHs. Grilling as an indirect or direct way. No carcinogenic PAHs will An interest in the structural design of food-based Samples Cooking method Sum of three meat with appreciable fat content would contribute to be detected in the grilled products if fat dripping onto delivery systems in encapsulating, protecting and releasing PAHs (ng/g)* high presence of PAHs (Alomirah et al., 2011) while; in the heat source is prevented. Therefore, avoiding direct bioactive components which believed to give advantage Beef satay Charcoal grilled 81.0-132 contrast, food with low fat content contains insignificant contact of meat with the cooking flame or grilling at to human health is increasing in these past few years. The Ayam bakar Charcoal grilled 28.9-51.1 amount of PAHs (Marques et al., 2011). intense temperature can reduce the occurrence of PAHs functions of designing these delivery systems were to Chicken satay Charcoal grilled 14.3-37.6 during charcoal grilling (Farhadian et al., 2012). release the bioactive components at a specific location in Ikan bakar Charcoal grilled 9.36-15.0 Beef kebab Gas grilled 9.36-15.0 iii) Cooking method (frying, grilling, roasting, boiling the human gastrointestinal tract (GIT), and its release is Chicken kebab Gas grilled 8.23-20.4 and smoking) Bioaccessibility of Food Contaminant triggered by external stimuli such as pH, ionic strength and Grilled chicken Gas grilled 4.63-12.4 Among the method of cooking, heating i.e. grilling and activity as well as to control the rate of bioactive Tandoori (chicken) Oven grilled 4.65-9.66 smoking of food directly in contact with combustion gases The term ‘bioaccessibility’ is one of the critical release in the form of burst release or prolonged release Oven grilled chicken Oven grilled 3.51-7.14 is an important source of the contamination (Purcaro et al., issues in order to accurately assess the exposure risk (Hur et al., 2011). In vivo feeding methods which usually * [fluoranthene, benzo(b)fluoranthene, benzo(a)pyrene] 2013). According to Marques et al. (2011), the presence of contaminants from food which become available for tested on animals or humans, provide the most accurate of PAHs in the cooked meat is greatly depending on the intestinal absorption after digestion (Wang et al., 2011; results; however, they are costly and time consuming. level of benzof(a)pyrene was found in very well-done cooking method, being lower in oven baking and higher Hu et al., 2013). Non-digested contaminants are not Hence, much effort has been devoted to the development grilled/barbecued beef satay, charcoal grilled fish and very in wood fire grilled products. Furthermore, Perellό et al. accessibly been absorbed in the human gastrointestinal of the in vitro method. In general, well-designed in vitro well-done chicken satay. (2009) has also revealed the levels of 16 PAHs in various tract. This unreleased contaminant which is bound to the digestion models provide an alternative to animal and Significance numbers of PAHs normally occur at the foodstuffs that formed by cooking. Their finding stated food matrices will be excreted together with the faeces human models as well as serving a rapid, accurate and surface of the product; however, diffusion into the inner that a considerable amount of PAHs has been detected in (Yu et al., 2011). Therefore, the concept of contaminant lesser time for screening foods or delivery system with parts can take place during storage (Gomes et al., 2009; roasted samples. bioaccessibility has been applied by some researchers as different composition and structures (Coles et al., 2005; Marques et al., 2011). Almost 99% of all PAHs were the intestinal absorption rate is important to evaluate the Hur et al., 2011). detected in the outer layer of dry sausage as reported from iv) Cooking temperature human daily intake of contaminants (Yu et al., 2012). the previous studies on the migration of PAHs compound Severe temperature of cooking method such as grilling Bioaccessibility can also be defined as the fraction In vitro digestion model for bioaccessibility into smoked meat products (Jira et al, 2006; Roseiro et to formation of PAHs (Viegas et al., 2012). As the of contaminant that mobilized from its matrix which In vitro digestion model has been proposed as a tool to al., 2008; Gomes et al., 2009; Marques et al., 2011). The temperature rises, more PAHs are present (Farhadian is normally obtained via simulation of the human calculate the bioaccessibility of food-borne toxicants (Yu maximum concentration of PAHs in smoked products et al., 2010). All compounds containing carbon and gastrointestinal digestion process (Yu et al., 2011; et al., 2010). The bioaccessible amount of a contaminant is attained immediately after the smoking was hydrogen can be optimal precursor of PAHs at high 2012). In fact, nutrition in foods is available for human represent the maximal amount available in human completed, decreasing afterwards due to , temperature (500-700ºC) (Purcaro et al., 2013). In fact, absorption only after digestion (Intawongse and Dean, gastrointestinal tract, and become available for absorption. triggered by light and interaction with other compounds PAHs were involved in pyrolysis and pyrosynthesis, 2006). Bioaccessibility is easier to be carried out via This amount has been considered as the actual absorbed (Marques et al., 2011; Palm et al., 2011). However, PAHs where PAHs compound are partially cracked into smaller, in vitro experiments and it was commonly used as a amount of toxicants in human exposure assessment, concentration from the inner parts of the food product is unstable (pyrolysis), these fragments, mostly substitute of bioavailability when estimating human which was normally determined through multiplying usually stable due to the protection from light and radicals, recombine to yield larger, relatively stable PAHs exposure to food-borne contaminants (Yu et al., 2010). total amount of a contaminant by the bioaccessibility (Yu (Šimko, 2002; Marques et al., 2011). (pyrosynthesis)(Purcaro et al., 2013). PAHs can also Indeed, bioaccessibility assessment is thus very desirable. et al., 2011). In vitro digestion model has been widely formed at lower temperatures (100-150ºC) but they require Likewise, studies related to bioaccessibility were also been used in the purpose of studying the structural changes, Factors Affecting PAHs Concentration in a period on the geological time-scale and huge amount of evaluated on heavy and soil (Tang et al., 2006; Yu digestibility, and release of food components under Grilled Meat alkylated PAHs were originated, as in the case of natural et al., 2010; Maulvault et al., 2011). A study by Maulvault simulated gastrointestinal conditions (Hur et al., 2011; formation (Purcaro et al., 2013). et al. (2011) on the bioaccessibility of (Hg) in Omar et al., 2013). This model purports to simulate the Concentration of PAHs in grilled meat depends on raw and cooked black scabbard fish, as well as cadmium digestion process in the gastrointestinal tract by applying several factors. The most important factors contribute to v) Cooking duration/level of doneness (Cd) and arsenic (As) in edible steamed and boiled crab physiological based conditions including gastric pH, the concentration of PAHs are types of meat, fat content of Cooking duration was also contributed to the increase tissues concluded that the Cd and As revealed high intestinal pH, food constituents, residence time and the food, cooking methods, cooking temperature, cooking of PAHs level since the longer the cooking time, the higher bioaccessibility rates in raw and cooked black scabbard particle size (Intawongse and Dean, 2006; Omar et al., duration/level of doneness, type of fuel used/type of heat the amount of PAHs (Purcaro et al., 2013). For example, fish with up to 100%, whereas lower bioaccessibility of 2013). sources and proximity/direct contact with heat source. The level of heterocyclic compound which also has the Hg was observed with up to 40%. The most predominant food samples tested using in influence of these factors has been subjected to several same metabolizing pathways as PAHs, was also increased Moreover, in a study on the bioaccessibility of diphenyl vitro digestion model were plants (45%), meats (18%), studies as following: with increasing of cooking duration or level of doneness (PBDEs) by Yu et al. (2010) in 13 types of foods fish (9%), dairy (9%) and emulsion-based foods (9%) (Hur (Jinap et al., 2013). including fish, meat, rice, flour and vegetables using in et al., 2011; Omar et al., 2013). According to the surveys i) Type of meat vitro digestion model, the bioaccessibility were ranged conducted in all the in vitro digestion models, the digestion Type of meat such as chicken and beef meat can be vi) Type of fuel used or type of heat sources (electrical, from 2.6% to 41.3%. Besides, an assessment of PAHs temperature was set 37ºC despite the variations types different in terms of fat content, marbling as well as gas, wood and charcoal) bioaccessibility in soils from Beijing was also been and concentrations of employed. Enzymes and myoglobin content which may influence the level of PAHs Type of fuel used was also influenced the level of done by Tang et al. (2006) using an in vitro test. Their other biological molecules commonly used in the model released (Kulp et al., 2003). Some studies have reported PAHs formed such as electric, gas, wood and charcoal. that the concentration of PAHs is higher in grilled meat According to Purcaro et al. (2013), carbon burning Table 7. Enzymes Utilized in in vitro Digestion Model (Adapted from Hur et al., 2011) as compared to grilled chicken samples (Alomirah et al., produced a low level of PAHs than wood. Furthermore, Enzyme Locations Functions 2011). Alomirah et al. (2011) has also revealed that grilling of meat in charcoal oven released substantial quantities of a. Amylase mouth; stomach convert starches to oligosaccharides and monosaccharides (glucose). PAHs than meat that roasted in an electric oven. b. Protease stomach (pepsin) breaking down / into smaller peptides and amino . ii) Fat content of the food small intestine (trypsin and chymotrypsin) Fat content of food can contribute to the generation of c. Lipase stomach (gastric lipase) convert triacylglycerols and diacylglycerols to monoacylglycerols and free PAHs through either thermal degradation or polymerization vii) Proximity and direct contact with heat source pancreas (pancreatic lipase) fatty acids. as well as through different thermal processes which affect Proximity is the distance from the heat source. In 20 Asian Pacific Journal of Cancer Prevention, Vol 17, 2016 Asian Pacific Journal of Cancer Prevention, Vol 17, 2016 21 DOI:http://dx.doi.org/10.7314/APJCP.2016.17.1.15 Elliyana Nadia Hamidi et al Polycyclic Aromatic Hydrocarbons and Bioaccessibility in Meat: a Tool for Assessing Human Cancer Risk were digestive enzymes (pancreatin, pepsin, trypsin, and dietary exposure to polycyclic aromatic hydrocarbons coupled with high-performance liquid chromatography- Purcaro G, Moret S, Conte LS (2013). Overview on polycyclic chymotrypsin, peptidase, α-amylase, and lipase), bile salts (PAHs) from grilled and smoked foods. Food Control, 22, fluorescence detection.J Chromatogr A, 1217, 5555-63. aromatic hydrocarbons: Occurrence, legislation and and mucin (Hur et al., 2011). However, the main enzymes 2028-35. Jägerstad M, Skog K (2005). Genotoxicity of heat-processed innovative determination in foods. Talanta, 105, 292-305. 574 utilized in in vitro digestion models were amylase (for Al-Rashdan A, Helaleh MIH, Nisar A, et al (2010). Determination foods. Mutat Res, , 156-72. Ramesh A, Walker SA, Hood DB, et al (2004). Bioavailability of the levels of polycyclic aromatic hydrocarbons toasted Jahurul MHA, Jinap S, Zaidul ISM, et al (2013). Determination and risk assessment of orally ingested polycyclic aromatic starch digestion), protease (for protein digestion) and bread using spectrometry. Int J of fluoranthene, benzo(b)fluoranthene and benzo(a)pyrene in hydrocarbons. Int J Toxicol, 23, 301-33. lipase (for lipid digestion) (Hur et al., 2011). The location of Anal Chem, doi:10.1155/2010/821216. meat and fish product and their intake by Malaysian. Food Reinik M, Tamme T, Roasto M, et al (2007). Polycyclic aromatic and function of these enzymes is shown in Table 7. Anderson KE, Sinha R, Kulldorff M, et al (2002). Meat intake Bioscience, 1, 73-80. hydrocarbons (PAHs) in meat products and estimated PAH An in vitro digestion model should fulfil the following and cooking techniques: associations with pancreatic cancer. Janoszka B, Warzecha L, Blaszczyk U, et al (2004). Organic intake by children and the general population in Estonia. criteria: i) the model has to represent physiology of Mutat Res, 506-507, 225-31. compound formed in thermally treated high-protein Food Addit Contam, 24, 429-37. human, ii) the last compartment in the model must be Chung SY, Yetella RR, Kim JS, et al (2011). Effects of food part i: polycyclic aromatic hydrocarbons. Acta Roseiro LC, Gomes A, Santos C (2008). Polycyclic aromatic small intestine, as the absorption of compounds takes place grilling and roasting on the levels of polycyclic aromatic Chromatographica, 14, 115-28. hydrocarbons profile in a Portugese traditional meat product. mainly in the small intestine and, iii) the model also has to hydrocarbons in beef and pork. Food Chem, 129, 1420-26. Jarvis IWH, Dreiji K, Mattson A, et al (2014). Interactions IAFP’s Fourth European Symposium on Food Safety. be applicable, robust and reproducible (Versantvoort et al., Coles LT, Moughan PJ, Darragh, AJ (2005). In vitro digestion between polycyclic aromatic hydrocarbons in complex Advancements in Food Safety, 19-21 November, Lisbon, and methods, including gas production mixtures and implications for cancer risk assessment. Portugal. 47. 2004; Omar et al., 2013). Moreover, this model offer the techniques, as applied to nutritive evaluation of foods in Toxicol, 321, 27-39. Silva BO, Adetunde OT, Oluseyi TO, et al (2011). Effects of the advantages of being simple, easy and fast, straightforward the hindgut of humans and other simple-stomached animals. Jinap S, Mohd-Mokhtar MS, Farhadian A, et al (2013). Effects of methods of smoking on the levels of PAH in some locally model, cost effective, provide accurate results within a Anim Feed Sci Tech, 123-124, 421-44. varying degrees of doneness on the formation of heterocyclic consumed fishes in Nigeria.African Journal of Food Science, short time, reduces the need to experimental animals, Danyi S, Brose F, Brasseur C, et al (2009). Analysis of EU priority aromatic amines in chicken and beef satay. Meat Sci, 94, 5, 284-391. can investigate a large number of different samples and polycyclic aromatic hydrocarbons in food supplements using 202-7. Šimko P (2002). Determination of polycyclic aromatic matrices as well as allowing replication and can provide high performance liquid chromatography coupled to an Jira W (2004). A GC/MS method for the determination of hydrocarbons in smoked meat products and smoke insights that are not achievable in animal studies. These , diode array or fluorescence detector. Analytica carcinogenic polycyclic aromatic hydrocarbons (PAHs) in flavouring food additives.J Chromatogr B, 770, 3-18. characteristics make it very useful tool for the human Chimica Acta, 633, 293-9. smoked meat products and liquid smokes. Eur Food Res Sinha R, Chow WH, Kulldorff M, et al (1999). Well-done grilled 218 health risk assessment (Oomen et al., 2003; Omar et al., El-Badry, N (2010). Effect of household cooking methods and Technol, , 208-12. red meat increases the risk of colorectal adenomas. Cancer some food additives on polycyclic aromatic hydrocarbons Knightes CD, Peters CA (2006). Multisubstrate biodegradation Res, 59, 4320-24. 2013). (PAHs) formation in chicken meat. World Applied Sciences kinetics for binary and complex mixtures of polycyclic Sinha R, Rothman N, Salmon CP, et al (1998). 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