Current innovative approaches in reducing polycyclic aromatic hydrocarbons (PAHs) in processed meat and meat products
Chemical and Biological Technologies in Agriculture volume 10, Article number: 109 (2023)
The presence of polycyclic aromatic hydrocarbons (PAHs) in processed meat and meat products is a global concern as they are known to be carcinogenic, mutagenic, teratogenic, and genotoxic to living beings. PAHs are generated in processed meat through different thermo-processing techniques, such as smoking, grilling, barbecuing, roasting, and frying, which involve abnormal high-temperature treatments and extruded fuels. These carbonaceous compounds with two or more cyclic benzene rings are highly stable and toxic, and their generation is enhanced by faulty thermal processing techniques, contaminated raw materials, and environmental pollution. Based on their degree of toxicity, Benzo[a]pyrene (B[a]P) is recognized as the most probable human carcinogen among different fractions of PAHs by the European Commission Regulation (EC-No.1881/2006). Furthermore, the association between dietary PAHs exposures and their role as carcinogen in human beings has been reported clinically. Therefore, it is necessary to focus on prevention and control of PAHs formation in processed meat products through various strategies to avert public health concerns and safety issues. Accordingly, several approaches have been used to reduce the risk of PAHs formation by employing safe processing systems, harmless cooking methods, marination by natural plant components, use of biological methods etc. to eliminate or reduce the harmful effects of PAHs in the food system. This review provides a comprehensive insight into the occurrence and formation of PAHs in meat and meat products and their toxicological effects on human beings. Furthermore, the different cost-effective and environment friendly methods that have been employed as “green strategies” to mitigate PAHs in meat and meat products at both household and commercial levels are discussed.
Meat is one of the most significant foods in our daily diet for its valuable constituents and essential nutrients . To improve the quality, safety, sensory attributes and shelf-life of meat and meat products, various processing and preservation methods are employed . However, the traditional and modern thermal processing of meats such as smoking, grilling, baking, barbecuing, roasting, frying etc. produce genotoxic compounds due to incomplete combustion of organic matter under insufficient oxygen . Alongside these meat processing techniques, process time, temperature, distance between the food and heat source, food components, water activity, fuel, smoke used etc. are responsible for the formation of polycyclic aromatic hydrocarbons (PAHs) . The formation of PAHs into food surface may be associated with different possible mechanisms, such as the pyrolysis of organic components (protein, fat or carbohydrate) of foods at high temperature (more than 150 °C), dripping of fat onto heat sources leading to incomplete combustion, incomplete burning of coal, fossil fuel, wood or other fuels under reduced oxygen levels, chemical modification of oil used as cooking medium etc., [4,5,6]. Akbari-Adergani et al.  and Yousefi et al.  have reported about generation of PAHs by identifying several aromatic compounds in edible cooking oils. After absorption into cell membrane and metabolism into human body, these metabolites bind with DNA and proteins by intervention of different pathways leading to formation of DNA, RNA and glutathione adducts resulting in structural disruption, DNA mutations, alteration in gene expression and carcinogenesis [6, 9].
Apart from thermal processing, PAHs can also be generated by either organic environmental pollutions, or migratory properties of packaging materials. As far as non-smokers are concerned, carcinogenesis or mutagenesis is directly related to their unhealthy dietary habits contaminated with PAHs . According to the current epidemiological surveys, prevalence of cancer among human beings is extensively attributed to dietary exposures of PAHs . Overall, the most human exposures to PAHs occur by inhalation, ingestion or direct contact of these toxic substances through contaminated foods [4, 11].
Out of almost 200 organic compounds of PAHs identified in environment as particulate matter, almost sixteen PAHs are found in meat products with high carcinogenic, mutagenic and teratogenic properties, especially in human beings . The International Agency for Research on Cancer (IARC) has classified processed and red meat as group 1 carcinogen to humans due to the presence of N-nitroso compounds, heterocyclic aromatic amines, and PAHs. The International Agency for Research on Cancer  has categorized the toxicant PAHs into the following few groups; Group 1 (carcinogenic to human), Group 2A (probably carcinogenic to human), Group 2B (possibly carcinogenic to human) and Group 3 (unclassified as carcinogenic to human) (Table 1). Based on the risk of carcinogenicity, different regulatory agencies have classified the PAHs. The European Commission has separated 4 major PAHs that exhibit carcinogenic activity, i.e., benz [a]anthracene (BaA), chrysene (Chr), benzo[b]fluoranthene (BbF), and benzo[a]pyrene (BaP) . The European Food Safety Authority has also divided these toxicant PAHs into PAH2 (BaP and Chr), PAH4 (BaA, BaP, BbF, and Chr), and PAH8 (BaA, BaP, Chr, BkF, BbF, IcdP, DahA, and BghiP) . Amongst these, the Joint FAO/WHO Expert Committee has widely announced BaP as the most probable human carcinogen or an indicator of carcinogenesis, as the occurrence of PAHs and their associations with increased risk of colo-rectal cancer is primarily attributed to benzopyrene . Epidemiological surveys have also found a positive correlation between higher intake of thermo-processed red meat with high fat content and colo-rectal cancers in humans. Therefore, identifying the meat-based products with high risk for PAHs contamination and detection of their carcinogenic concentrations is required from public health safety point of view.
Currently, various processing/cooking methods in combination with innovative strategies are employed by different workers as some of the PAHs reduction strategies in meat and meat products. These includes optimization of the processing conditions, including time, temperature during smoking and grilling, and selection of wood/charcoal type. Inclusion of natural plant extracts during marination of meat, use of probiotics and lactic acid bacteria, natural cellulosic adsorbents and casings as packaging for smoked sausages etc. are also being explored as bioremediation measures for PAHs [16,17,18,19]. This review summarizes various points, providing a comprehensive insight to the occurrence and formation of PAHs in meat and meat products, and their adverse effects on human health. Furthermore, various cost effective, and environment friendly approaches to mitigate PAHs in meat and meat products are also discussed in this paper.
Mechanism of PAHs formation in processed meat
Meat is no doubt a highly recommended nutritious food and performs a significant role in human health system . However, the presence of PAHs in meat may be either by different food processing mechanisms, including curing, heating, drying, smoking, grilling, barbecuing etc., or environmental pollutants contaminating air, soil and water [3, 21]. Although the exact reason is not known, three possible mechanisms for formation of PAHs in processed meat have been conferred here [4, 22]. The formation of PAHs into meat goes through a series of radical reactions, including incomplete combustion of organic components (pyrolysis) present in meat, such as fat, protein, and carbohydrate at 200 °C and above. Dripping of fat onto flame during grilling or smoking and leaching of natural-nutrient rich juices from meat into the fuel may hasten the mechanism of pyrolysis generating volatile PAHs which are towed by smoke and get accumulated on the surface of meat [23, 24]. Another very important and common reason of PAHs formation and deposition on meat surface may be the incomplete and unstable combustion of fuels, such as charcoal, hardwood, or straw under insufficient oxygen [4, 25], and use of oils as cooking medium .
In fact, pyrolysis and pyrosynthesis are two typical processes, where chemical modifications of carbonaceous organic compounds are common to produce PAHs during thermal processing, though the responsible mechanism is still under investigation . A favorable atmosphere for pyrolysis which is stimulated by raised temperature leads to fragmentation of large organic compounds into small molecules such as propane and ethylene along with intermediate free radicals with high reactivity. Propargyl recombination, hydrogen abstraction and acetylene addition (HACA) mechanism, Diels–Alder mechanism, and phenyl-addition–cyclization (PAC) are different elusive mechanisms involved for cyclization, benzene ring formation and ultimately ring–ring condensation producing high molecular weight polyamides [22, 24]. In addition, it has been reported that Maillard reaction between proline and reduced sugar under very high temperature and short time (600–840 °C for 1 s) may promote PAHs formation by pyrolysis of proline . However, the levels of PAHs formation in thermally processed meat is influenced by the meat type and fat content, processing/cooking method employed, temperature, distance, duration and type of fuels, food additives used etc., which have been discussed extensively later.
PAHs: the structure, metabolism, toxicity and health effects
PAHs are a group of chemicals with two or more conjugated benzene or cyclopentadiene rings composed of 5–6 carbon and hydrogen atoms , produced either by incomplete burning (pyrolysis) of carbon-containing materials, or organic materials, such as greasy meat. Based upon the number of benzene rings and molecular weights, PAHs show their toxicities towards human beings, animals and even bacteria . Light PAHs (naphthalene, phenanthrene, fluorene, acenaphthene etc.) consist of two to three aromatic rings, and are less toxic, more unstable and volatilize immediately. On the other hand, heavy PAHs, such as pyrene, benzo[a]anthracene, chrysene, benzo[a]pyrene, having four and more rings, are more stable and toxic . In general, PAHs are highly soluble in non-polar solvents and edible oils but have low solubility in water. Furthermore, they are lipophilic in nature with high melting, boiling point, vapour pressure, octanol–water partition coefficient indicating high bioaccumulation into living beings with less biodegradability [27, 29,30,31].
Living organisms get exposures of PAHs either by direct contact with skin or through different routes, such as inhalation, and ingestion of food, including meat and meat products. After being absorbed, these compounds are circulated to different systems and organs of body and bio-accumulated in liver, intestine, skeletal muscle system, adipose tissue, extra hepatic tissues etc. by blood capillaries and lymphatic vessels and exhibit their toxic metabolisms disturbing regular cellular functions [3, 32]. Their metabolism and biotransformation are complex processes forming different intermediates ended up with diol-epoxides and radical cations assisted by cytochrome P450 peroxidase and aldo–keto reductase enzymes. Figure 1 depicts the formation, exposure and metabolism of PAHs in human health chain.
The metabolites bind covalently to cellular macromolecules, such as proteins, DNA and RNA forming adducts . If not phagocytosed by macrophages and excreted in feces and urine, they cause biochemical disruption and cellular damage, alter gene expression inducing carcinogenic, unpreventable mutagenic, immunosuppressive, and teratogenic damage [3, 6, 29].
Based upon the route of exposure, concentration and time, PAHs can show acute or chronic symptoms, including eye irritation, nausea, vomiting, diarrhea, skin allergies, liver and kidney damage etc. [24, 34]. Long-term exposures to unvented smokes, generated during traditional indoor smoking, might be the cause of high mortality rate in lung cancer among women [3, 35]. Besides, indoor cooking, grilling, barbecuing etc. are the significant risk factors for incidences of cancer in nasopharyngeal, blood, prostate, skin, breast etc. among exposed people [3, 22, 27]. The consumption of grilled meat has been reported to increase the risk of renal cell carcinoma . Reports available suggest that, consuming smoked meat and fish more frequently, containing PAHs enhance the risk of stomach cancer in human beings . PAHs, particularly increased B[a]P concentration in processed and ready-to-eat (RTE) meat samples, are capable of causing genetic changes by significantly modifying the expression of KRAS, a key gene related to colo-rectal cancers . BaP is also reported to cause disrupted human endocrine system-related infertility [29, 38]. Furthermore, the risk of cancer due to consumption of foods of animal origin is reported to be 2.63/107 and 9.3/107 BaP equivalents for children/adolescents and adults, respectively . Upon long-term exposure, the organs rich in adipose tissue might develop tumors due to accumulation and bioavailability of PAHs, that are lipophilic in nature .
Research on toxic effects of PAHs conducted at cellular levels in different animal models and case–control studies in human have highlighted its veracity [38, 40]. Deformation of mouse micronucleus red blood cells, lethargy and anxiety of fish larvae are few examples of toxicity of PAHs on cell level [24, 40]. The teratogenic effects of PAHs and their covalently attached metabolites with DNA may create congenital disabilities, such as low birth weight, premature delivery, heart malformations and low intelligence quotient of offspring. In animal models and case control studies on human beings, the harmful effects of B(a)P and B(a)A, two leading PAHs, responsible for causing irreversible DNA damage, lung, breast and stomach tumors, esophageal, skin, colorectal and gastric cancer, papillomas, hepatomas with reported malignancy have been extensively reported [24, 35, 40].
PAHs in meat products and human health risk assessment
Over the last few years, the threat of cancer has increased ubiquitously among human beings because of modern lifestyle and daily dietary intake of PAHs . Several studies have now acknowledged the positive correlation between PAHs contaminated meat intake and prevalence of cancer throughout the globe. Thus, PAHs toxicity is slowly becoming the silent epidemic. To protect the health of consumers from negative effects of PAHs intake from diet, the maximum admissible limits for PAHs compounds, especially BaP and ∑PAH4, have been set by various agencies and regulatory bodies for various raw and treated meat products which are presented in Table 2. As the consumption of PAHs contaminated meat products above permissible levels can be potentially harmful to human health, the ALARA (as low as reasonably achievable) principle is in force in the EU. However, epidemiological studies conducted in different parts of the globe on formation of PAHs in meat and meat products depict a different picture. In most of the cases, PAHs levels often surpass the established limits deemed acceptable by current legislations. Several reports are available in this regard investigating the presence of PAHs in different food matrices .
In a study conducted in Taiwan, Kao et al.  reported total PAHs formation in charcoal grilling of poultry (6.3–238.8 ng/g) and red meat (0.1–547.5 ng/g) and the highest amount of BaP (4.0 ppb) in chicken drumstick grilled at 74 °C for 20 min. It was postulated that concentration of PAHs formation depends on duration and temperature of grilling, unsaturation of fatty acids in meat, lipid oxidation and degradation products, such as cyclohexane and hydroperoxides. Estimating BaP and PAH4 concentrations in grilled and fried pork in Shandong of China, Jiang et al.  stated that some samples crossed the maximum permissible limits of 2 and 12 μg/kg set for BaP and PAH4 by European Union (Commission Regulation (EC) No 1881/2006 amended by Commission Regulation (EU) No 835/2011). In Finland and Sweden, same reflections were seen for traditionally smoked meat and fish products with high BaP and PAH4 contents, especially in pork products with 5.6–13.2 µg kg−1 of BaP contents, though Commission Regulation (EU) No. 1327/2014 set maximum limits in finished products should not be beyond 5.0 µg kg−1 and 30.0 µg kg−1 for BaP and PAH4, respectively. Likewise, Hokkanen et al.  made several experiments on different modified smoking processes to check the levels of PAHs formed and noticed that traditional direct smoking method could be a significant risk factor for cancerous toxicity with exceptionally high PAH4 formation, which is non-compliant with legislations. Wretling et al.  also reported similar findings in Sweden with increased BaP (6.6–36.9 µg kg−1) in traditionally “sauna” smoked meat products.  investigated the effect of traditional smoking methods on the formation of BaP and PAH4 in smoked dry sausage Hercegovaˇckakobasica in Herzegovina, a part of Bosnia. The PAH4 concentrations in this pork-based sausage stuffed into natural casings was 24.46 µg/kg, which was almost double of legislative prescribed values (12 µg/kg).
Bogdanović et al.  made a survey in Croatian population on acute and chronic exposures of BaP and PAH4 through contaminated meat products and found that dry sirloin (39.0 ng/day), Kulen (32.4 ng/day) and dry homemade sausage (20.72 ng/day) were the largest contributors for daily BaP intake. In another study, potential human health risk assessment was carried out in local markets of Iran by investigating the content of PAHs in raw and cooked meat products . The scientific survey report claimed that in sausages and burgers, anthracene (14.12 μg/kg) and acenaphthylene (13.4 μg/kg) were present in higher amount than the normal European Standard (2 μg/kg), and fried meat products showed very high level of PAHs (23.31 μg/kg).
Puljić et al.  conducted research on drycured smoked pork meat products “Hercegovaˇckapeˇcenica” for different smoking procedures of traditional and industrial methods to elucidate the threatful intervention of PAHs. The researchers concluded that PAH4 was in much more than critical limit when conventional smoking method was carried out. Furthermore, as far as PAH16 is concerned, surface layer of meat was more exposed to the risk than inner part. Supportive statements regarding these research findings were justified with probable cause of less contamination with PAHs in inner core of meat products may be due to protection from light and oxygen. However, in case of longer storage, diffusion occurs into inner part also, otherwise surface layer detection of PAHs are reported as major findings [3, 32].
From different epidemiological studies, it is evident that several factors are cognate with formation of different concentrations of PAHs in meat products. Some militating factors will be emphasized here in this review. PAHs formation depends upon the amount of fat present in meat or the type of oil present as cooking medium during different thermal degradation processes. For example, in barbecued-grilled meat the concentration of PAHs and BaP are highly correlated with presence of higher amount of unsaturated fatty acids, responsible for more benzene rings agglomeration . In addition, new challenges such as oxidation of fatty acids present in oil may create new derivatives from photo-induced PAHs that may enhance their toxicities [4, 49]. In Malaysian charcoal-grilled satay from beef and chicken, significant differences were noticed for BaP concentration (7.4 mg/kg and 2.0 mg/kg) by Mohammadi and Valizadeh-kakhki . Similar kind of result was reported by Kao et al.  for highest BaP concentrations in lamb steak (5.8 mg/kg) followed by chicken drumstick (4.0 mg/kg). Over and above that, this principle may vary based upon related and intermediate factors, when are interlaced with each other. Chicken and beef grilled products may show higher PAHs concentrations when they are either grilled with skin or possibly a large surface to volume ratio is plotted in barbequed minced beef burger or chicken breast etc. [51, 52].
Although thermal processes/different cooking methods such as smoking, frying, grilling, baking, boiling barbecuing, roasting etc. are employed to enhance the sensory attributes of meat products, these processes are accompanied with high temperatures, pyrolysis, fat dripping and intense smoke generation which can increase the levels of PAHs in meat . In fact, the use of distinct types of fuels, i.e., gas, electric, wood, charcoal etc. have persuasive contributions for formation of different levels of PAHs in meat, as partial combustion of fuels under insufficient oxygen, result in formation, deposition, and penetration of volatile particles upon the smoked products [3, 13]. From different comparative studies on heating methods and PAHs generation, it has been found that electric and gas grilling, broiling, indirect smoking produces comparatively less concentrations of PAHs and BaP in different species of meat [22, 52]. Smoking, grilling or roasting with different wood (log fire, pinecones, ear leaf locust tree, acacia, hickory sawdust, aspen, spruce etc.) sources have significant influence on generating higher concentration of PAHs compared to charcoal grilling [52, 53]. Kim et al.  got positive alternatives of using wood smoking by “flameless and smokeless charcoal”, coconut shells, broadleaf trees, oak etc. that decreased the PAHs noticeably in beef, chicken and salmon. Viegas et al.  made aware of harmful aspect of reusing same charcoal of gas for barbecuing continuously without cleaning that may produce higher molecular weight PAHs (BaP from 3.1 to 8.7 mg/kg) with more potential detrimental effects.
Liquid smoking is always beneficial and getting advantages over conventional direct smoking method, as liquid fumigants are prepared through a series of fractionation, filtration and purification that can reduce the PAHs contamination in food [24, 29]. Zachara et al.  reported the lowest PAHs concentration in pork ham in case of liquid smokes (0.75–2.97 μg/kg) compared to industrial (1.27–7.76 μg/kg) and traditional (8.90–24.57 μg/kg) smoking methods. In case of traditional fermented smoked sausage preparations, it is advisable to use cellulose casings instead of natural casings, as generated BaP and PAHs cannot penetrate the hydrophilic cellulose casings easily due to their low porosity, smooth geomorphology and negligible relation with carbon particles . Another well-connected information was stated by different research findings with a conclusion that distance between heat source and food components affect inversely PAHs levels [52, 57].
The extent of ventilation and smoke density have a significant impact on the levels of PAHs formation into smoked chamber. In fact, improper inflow of air into the smoke chamber rises the temperature, thereby increasing the smoke density [29, 58]. Epidemiological surveys suggest that extended period of cooking (well done) or degree of doneness and distance from the heat source have a negative influence on PAHs formation, including BaP in meat [13, 52]. Purcaro et al.  also revealed that higher cooking temperature (500–700 °C) always favor for higher level of PAHs formation in meat, though in lower temperature range (100–150 °C) also PAHs can be formed in longer geological timescale when carbon and hydrogen containing components are present as the precursor of PAHs. Therefore, it is always advised to reduce the cooking temperature with concomitant cooking time and increase the distance between meat and fuel sources, or opt for indirect heating process to avoid the charring or overcooking .
Apart from smoking as a method, different researchers have also worked on other cooking methods to find their effect on PAHs formation in meat products. Mirzazadeh et al.  investigated the effects of microwave, pan-frying, and grilling in smoked beef sausages and found the microwave cooking procedure as a healthier method compared to others with decreased levels of PAHs formation. Olatunji et al.  reported grilling and boiling processes better, as these methods reduced the concentrations of PAH4 in smoked chicken (10.52 μg/kg by 51% and 64.35%, respectively). Comparing the electric and charcoal grilling processes, Hamzawy et al.  concluded that electric grills are better and should be frequently used to reduce the B(a)P contamination in grilled chicken. Employing different cooking methods, Onwukeme et al.  found boiling as the safest cooking process followed by barbecued and roasted methods, whereas the concentrations of PAHs was the highest in fried chicken product. Comparing the roasting and frying cooking processes, Arfaeinia et al.  opined that, frying chicken is better option with 45.29% and 30.72% lower 16PAHs and B(a)P, respectively, than roasting process. The authors also suggested gas roasting for achieving reduction in PAHs concentration (1.15 fold) compared to charcoal roasting. In a study conducted by Büyükkurt et al. , pan frying was also adjudged as a safer cooking method for beef meat than barbecuing with regard to the formation of PAHs and its human exposure through diet, as pan fried beef meat had lower levels of BaP (1.39 versus 1.62 μg/kg) and PAH4 (5.58 versus 5.73 μg/kg) compared to barbecued ones. Ohmic heating and infrared heating are new cooking techniques that can be employed to reduce PAHs formation in meat products or keep within the safe limits . For example, cooking beef-based meat ball employing these techniques produced 4.44 μg/kg of 16 PAHs, which were within the safe limits defined by EU, i.e., 5 μg/kg .
The type of oil is also important, as findings suggest that use of rapeseed, soybean, sesame, and sunflower oil reduce PAHs and BaP formations [68, 69]. To reduce PAHs formation during frying of meat, fresh and unused oils may be used . Furthermore, shallow-pan frying or hot air-frying technique is recommended, as it is comparatively safer than deep-frying [71, 72]. However, given a choice, cooking techniques such as steaming, boiling, and bracing are better because of a lesser carcinogenic risk than frying .
Mitigation strategies for PAHs
So far, discussion on different processing techniques of traditional meat products and formation of life-threatening carcinogenic compounds and their toxicities has been made in this article. As the consumption of PAHs contaminated meat and meat products is becoming a subject of wide scientific concern because of public health issues, there is a need to shed light on best possible ways of PAHs reduction strategies, The strategies for reduction and control measures of PAHs formation have been divided into two segments, i.e., (i) treatment of raw materials before thermal processing, including selection of lean masses, use of suitable fuels, filters, marinades and probiotics, heating methods etc. and (ii) treatment after thermal processing, including warm water rinsing and suitable packaging. Recent innovative strategies that are being employed by various researchers to reduce PAHs formation in meat and meat products, are also enlisted in Table 3.
Utilization of suitable resources of fuels and alternative cooking methods
Raw materials such as meat, fuels and cooking oils have the possibility of pre-contamination by PAHs prior to processing. Furthermore, most PAHs in processed meat products are generated during traditional and faulty cooking processes. Therefore, preventive measures would be beneficial to minimize the density of PAHs formation during cooking. In this regard, use of hard wood containing less lignin instead of soft wood is recommended, as the later burn out quickly at high temperature resulting more PAHs formation in traditional smoking method [24, 29]. In favor of this statement, it has been found that log fire, pine cones, mesquite wood produced high BaP and 4PAHs content in different traditional meat products during smoking . Even coconut shells are used as “flameless and smokeless’’ charcoal reducing the pyrolysis process . Essumang et al.  noticed that use of bagasse instead of woods as a source of smoke generator could effectively reduce the content of PAH4 in smoked fish.Hitzel et al.  made an investigation with different wood chips (spruce, oak, alder, poplar, beech, hickory) and found that poplar and hickory reduced PAHs contamination in frankfurters and mini-salamis made up of pork and beef by 35–55%, whereas alder and beech produced highest concentration of PAHs. Malarut and Vangnai  reported in their study that BaP and PAH4 concentrations were found in the range of 0.4–0.5 µg/kg and 1.1–1.5 µg/kg, respectively, in smoked sausages, when beech, neem (Azadirachta indica), copper pod (Cassia siamea), ear leaf acacia (Acacia auriculiformis) and eucalyptus camaldulensis (Eucalyptus camaldulensis) wood were used. The noticeable fact is that both the concentrations of toxins were below the legislative limits by EU, i.e., 2 µg/kg and 12 µg/kg for BaP and sum of PAH4, respectively. Using different charcoal types, Kim et al.  demonstrated that white charcoal was little producer of PAH4 when compared with black and extruded charcoal in different meat grilling processes. Therefore, traditional smoked meat producers can be advised to use hard wood (maple, oak, hickory etc. or bagasse) or white charcoal as preventive measures. Pre-heating and charring the wood or charcoal to generate the smoke at high temperature range and extinguishing the flame before grilling or barbecuing the meat may be suitable physical or chemical approaches to alter the chemical profile of generated smoke specially PAHs. Furthermore, reheating of pre-burn charcoal to generate the flame, exposure to high-level temperature for longer time, fat dripping, maintaining improper distance (< 25 cm) from heat sources should be prohibited to lessen PAHs concentration in meat products. These general instructions need to be internalized by small stakeholders. For example, Chaemsai et al.  pre-heated (650 °C) mangrove charcoal for 5 min, 20 min and 5 h before their use to grill meat and opined that charcoal should glow fully before starting grilling. From the above discussion, it is clear that several factors are intermixed for fat/wood pyrolysis and pyro-synthesis process; therefore, each possible and responsible factor needs to be remedied.
Most of the commercial setups use gas/electric ovens for roasting or barbecuing and indirect smoking methods using different filters (zeolite, granular activated carbon, and gravel filters) to reduce PAHs content in meat products. In a study, Sampaio et al.  could be able to show that zeolite and carbon filters reduced the BaP content and PAH4 by 90% and 85%, respectively. Thriving result was observed when chicken samples were grilled wrapping in banana leaf (34.7 μg/kg) and aluminum foil (45.4 μg/kg) to check the 3PAHs [4, 76] and these type of innovative approaches are always appreciable to terminate the current issue, especially for traditional food makers or roadside vendors. Eldaly et al.  also utilized this wrapping principle of meat grilling using some barriers between product and flame and a significant reduction of BaP content was observed in mutton and beef. Casings (natural/artificial) play an important role in preventing the contamination of PAHs, specially while preparing sausages, by creating a barrier layer, where surface deposition of smoke particles gradually form clogging pores . In comparison with natural casings, cellulose or collagen casings are more effective to act as good blockade of PAHs penetration. It is because of the fact that natural casings have high porosity and uneven morphology that elevates the chances of PAHs contamination into food, whereas synthetic casings with smooth and compact surface get the deposition of PAHs in very little amount and their penetration ability is also less [29, 56, 78]. During smoking or barbecuing of meat, indirect heating or use of electric or gas oven instead of charcoal, grilling of leaner portion of meat, maintaining proper distance from heat source etc. should be followed by producers for lesser contamination of toxic carcinogens into food. Besides, additional precautions need to be taken by producers to decontaminate the raw materials with toxic environmental pollutants as the possible risk factors of PAHs contamination into food. Therefore, extensive investigation is required for thorough monitoring of the raw materials during transportation, processing, storage, and possibility of environmental exposures (e.g., air, soil, and surface water quality) from safety point of view. Furthermore, successful industrial PAHs reduction strategies need to be adapted by traditional smoked meat manufacturers, irrespective of the consumer preferences and sensory attributes.
Use of marinades to decrease PAHs
Marination is a universal practice used specially for improving the texture and quality attributes (tenderness, juiciness, flavour) of thermo-processed meat products. Selection of appropriate marinade ingredients can reduce the level of PAHs in the end product by influencing the physico-chemical properties of the processed meat. The reason being, pretreatment of meat with a mixture of spices, fruits or vegetables or their extracts containing inimitable active principles, such as citric acid, ascorbic acid, antioxidants, phenolic components etc. before thermal processing can inhibit the formation of carcinogenic components or may accelerate the process by the faulty practices .
Research findings of several workers are available in this aspect. For example, addition of onion (30 g/100 g of meat) or garlic (15 g/100 g of meat) during meat processing resulted in a 60% and 54% decrease in 6PAHs levels . Pretreatment with tomato juice, garlic paste, onion, salt and spices (cumin, coriander, and black pepper) reduced down the PAHs level significantly in chicken after thermal processing compared to using of garlic alone and that may be due to antioxidative properties of spice mixtures . Sinaga et al.  marinated duck meat before charcoal grilling for 60 min with juice of pepper (Zanthoxylum acanthopodium) and observed a 2.6 times reduction of BaP in treatment (295 µg/kg) compared to control group (787 µg/kg).In a recent study, Onopiuk et al.  incorporated different plant extracts individually or as mixture (bay leaf, black pepper, turmeric, jalapeno pepper and tamarind paste) of marinates for pre-treatment of pork neck before grilling. The authors reported that although plant extracts significantly reduced the concentration of PAHs formation in pork products, phenolic components, especially of jalapeno pepper reduced almost 95% of 12PAHs (4.76 ± 0.08 µg/kg). The authors concluded that biologically active substance capsaicin present in jalapeno acted as scavenger of produced free radicals, which prevented the cyclisation and oxidation reactions thereby enhancing the safety and shelf life of grilled meat products. Similarly, effect of different beers (Pilsner beer, non-alcoholic Pilsner beer, and dark beer) for marinating pork before heat processing showed noticeable changes to diminish BaP concentration up to 1 μg/kg .
Vinegar, which is a fermented product, possesses active components such as phenolic compounds and is often used to improve the microbiological quality, safety, and shelf-life of food products . In a study conducted by Cordeiro et al. , vinegars with different levels of antioxidative performances showed significant differences in inhibiting the PAHs concentration in smoked meat products. It was reported that use of acidic substances in marinate could reduce remarkable levels of PAHs during thermal processing of meat, in lieu of alkaline ingredients or oil in marination that enhance the level of heavy PAHs formation in meat. In this regard, lemon juice or tamarind juice showed fruitful results to inhibit PAHs formation in grilled meat products other than their role in improving textural and physico-chemical properties of meat [6, 76, 85]. Eldaly et al.  studied the effect of yoghurt in combination with different spice mixtures on marination of beef for preparation of kabab and kofta. Marinating beef before grilling reduced PAHs levels to 57.93 µg/kg in grilled kebabs and 30.2 µg/kg in grilled kofta compared to 119.8 µg/kg of PAHs in kabab and 59.2 µg/kg of PAHs in kofta of untreated samples. Marinating with vinegars brought positive result reducing 4PAH content of charcoal grilled pork loin . The highest PAHs reduction was with Elderberry vinegar (82%) followed by white wine vinegar (79%), red wine and cider vinegars (66%), and fruit vinegar with raspberry juice (55%). Natural resources of food with effective phenolic components and their free radical scavenging capacity may act as potential inhibitors for carcinogen formation in smoked meat products. Still then, more advanced research is needed in this field to unwind the exact mysterious mechanisms of application of acidic marinades and their restricting actions on PAHs formation upon severe heat treatment. Likewise, marinades containing different antioxidants (epigallocatechin gallate, gallocatechin, catechin, epicatechingallate, catechingallate, eriodictyol, naringenin, quinic acid) extracted from green tea made notable droppings in PAHs concentrations during grilling or roasting of chicken wings or pork meat [86,87,88] possibly due to presence of polyphenols as active key components. Darwish et al.  studied the antioxidative effects of micronutrients rosmaric and ascorbic acids against heat-treated meat and concluded that such molecules protected human colon (CaCo-2) cells from BaP induced mutagenicity and oxidative stress. From the above findings, it can be deduced that marination with different phytochemicals containing polyphenols and flavonoids, spice mixes, curd etc. together with associated precautions might be used successfully to reduce PAHs content in thermally processed meat products.
Packaging systems, adsorbents and ultraviolet (UV) applications
The purpose of packaging is to safeguard quality, reduce losses, and extend shelf-life, till the processed food products reaches to the end user. With technological advancements, packaging materials now offer new prospects in eliminating hazardous compounds, such as PAHs content from various foods, including smoked meat products. Kuzmicz and Ciemniak  reported that different kinds of packaging materials, including high density polyethylene (HDPE), low density polyethylene (LDPE), polypropylene, oxo-degradable, and polyethylene terephthalate etc. have good PAHs adsorbent properties, to where the PAHs can migrate from food. In separate studies, BaP reduction has been reported by application of LDPE packaging system for smoked sausages and roasted meat products, respectively, by different researchers [91, 92]. Likewise, Chen and Chen  have reported that packaging of roasted duck meat into LDPE at 25 °C reduced almost 73% of BaP level after 24 h of storage. Besides, application of UV (2–3 h) to LDPE film also reduced BaP content specifically up to 13.5–29.2%.
In recent years, a great attention is being paid on the development of novel aerogels as an ideal alternative to various adsorbents because of their desirable quality properties, such as low density, high porosity, and large surface area . Conducting a study, Kim et al.  used natural, renewable and environment friendly cellulosic aerogels (NaOH/urea, LiBr, and LiOH/urea) as adsorbent layer to remove PAHs from smoked meat and meat products. Based upon surface structure and pore size distribution of the cellulosic aerogels, the LiBr-functionalized absorbent exhibited the highest adsorptive efficiency for total PAHs. Even chlorinated polyethylene (CPE), which is microplastics polymer obtained through structural or surface modification of conventional polyethylene, is reported to adsorb many organic compounds, including PAHs and benzene derivatives faster, present in freshwater . The efficacy or adsorption behavior of CPE may be tested in different food matrices, including PAHs contaminated meat and products. In a recent study, gamma irradiation of smoked guinea fowl (Numida meleagris) meat at a dose of 5 kilo grey (kGy) was reported to have the potential to reduce the concentrations of PAHs and their carcinogenic derivatives compared to non-irradiated meat . Therefore, it can be assumed that progressive advanced research on smart or active packaging system and application of ultraviolet rays may be the great reduction tools of PAHs for ensuring safety of meat products.
Washing of smoked meat products
Washing of smoked meat products refers to the removal of skin or outer layer of the product, rinsing with lukewarm water, cleaning under running tap water etc. [96, 97]. Few reports are available indicating that washing as a procedure is effective in reducing the PAHs content in smoked meat products. Mahugija and Njale  observed the effect of washing of smoked products with purified lukewarm water (60 °C, 2–3 min) to decrease the total PAHs content significantly. Though this technique is quite helpful to mitigate the problem, sometimes may not pass the organoleptic tests. Furthermore, washed products showed lesser shelf-life suggesting future studies to focus on storage and preservation of the washed smoked products. In another study, pork loins rinsed immediately after smoking error had reduced PAHs content (BaP = 3.43 ± 0.21 µg/kg; PAH4 = 25.33 ± 1.88 µg/kg) in the surface part of samples, compared to PAHs content (BaP = 7.33 ± 0.77 µg/kg; PAH4 = 61.14 ± 1.72 µg/kg) in smoked but unrinsed surface samples . The PAHs (BaP and PAH4) values obtained after rinsing smoked dry-cured pork loin be considered safe, as are within the permissible values (BaP < 5 µg/kg; PAH4 < 30 µg/kg) of the EU Regulation for traditional meat and meat products.
Application of probiotics and LAB
Biological methods are now becoming promising alternatives over physical and chemical decontamination methods to eliminate carcinogenic and mutagenic compounds from foods. It is because of their GRAS (Generally Recognized as Safe) status, inexpensive nature, and nature-friendly properties. The reason being many microorganisms (bacteria, algae, and fungi) have the ability to utilize PAHs as carbon source, required for their growth and development. In recent years, a novel environment friendly mitigation strategy to reduce the PAHs contamination in food has drawn the attention by biological degradation procedure with lactic acid bacteria (LAB) and probiotics [99, 100]. Various literatures have also mentioned the mechanisms involved to deactivate the toxicity of food-borne carcinogens, especially PAHs and acrylamides. The steps involved in PAHs breakdown include activation of antioxidative enzymes, such as oxidase, manganese peroxidases, lipases etc., conversion of organic and stable carcinogens into less toxic degradable hydrophilic metabolites, and above all, the binding of heat generated carcinogen to the cell wall and peptidoglycans of these bacteria may detoxify them biologically [99, 101, 102].
An elaborative description about the probable decontamination mechanisms of lactic acid bacteria against food carcinogens, specially BaP has been described by Shoukat . The physical binding of DBP (Di-n-butyl phthalate) of organic toxins with C–O, OH and/or NH functionals groups of peptidoglycan layer of cell wall of probiotics and lactic acid bacteria by formation of hydrogen bonds has been illustrated by FTIR (Fourier transform infrared spectroscopy) and MD (molecular dynamics) techniques in laboratory [17, 103]. However, the binding efficiency of individual organism varies based upon their different specificities, such as pH, incubation temperature and time, stability with acid and heat treatment, nutritional availability, concentration of bacterial cells etc. For instance, heat treated dead LAB showed similar kind of BaP binding ability of live viable pellets in a study conducted by Zhao et al. . Likewise, the binding rate of the viable cell of Lactobacillus pentosus CICC 23163 and Lactobacillus plantarum CICC 22135 with toxins were 64.36% and 66.73%, respectively, and showed no significant differences compared to the binding ability (67.83% and 62.18%) of heat-treated (121 ℃ for 15 min) pellets from the same strain .
As mentioned earlier, biological detoxifications of PAHs are a promising alternative to chemical methods and challenging task with highest efficacy in near future. Lactobacillus delbrueckii subsp. lactisATCC 4797, Lactobacillus plantarum ATCC 8014, Lactobacillus casei ATCC11578, Lactobacillus sakei 23 K, and Lactobacillus plantarum WCFS1, Bifidobacterium adoleascentis ATCC 15703, B. infantis, B. bifidum, B. adolescentis, B. longum, B. lactis, and B. breve, Streptococcus thermophilus are different probiotics and LABs detoxified different PAHs from food system, specially the smoked meat products successfully either in-vivo or in-vitro [17, 102]. It was reported that acidic pH, higher incubation time and temperature and concentrations are linearly correlated with PAHs binding ability of probiotics and LAB . Yousefi et al.  made an experiment with artificiallycontaminated PAH4 (BaA, BaP, BbF and Chr) phosphate buffer saline to check the detoxification efficiency of Lactobacillus brevis TD4 and observed that maximum binding rate was obtained at initial concentration of 10 ppm, pH 5, bacterial population of 109 CFU/mL and 24 h of incubation time.
In yet another study, fermented potato juices containing metabolites (bacteriocin, pediocin etc.) of different strains of lactic acid bacteria (Pediococcus acidilactici KTU05-7, Pediococcus pentosaceus KTU05-9 and Lactobacillus sakei KTU05-6) isolated from spontaneous rye sour dough were applied over the surface of pork sausages at 18 °C and for 60 min before or after smoking . It was interesting to note that not only BaP and chrysene, the toxic carcinogens from surface of sausages, but also different biogenic amines (cadaverine, spermidine and putrescine) from either surface or core of the sausages were reduced simultaneously. Lactic acid bacteria and their fermented metabolites are also reported to significantly inhibit the growth of different pathogenic and food spoilage organisms, including Pseudomonas aeruginosa and Escherichia coli, enhancing the shelf stability of products. Different experiments in gastrointestinal digestion cell lines and animal model have also proved the role of LAB for removing the BaP and other dietary toxins .
Although the role of probiotics detoxifying diet contaminated with BaP or other PAHs is known, introduction of genetically modified organisms (GMO) for better binding ability with toxins may lead to a new possible hope for dietary PAHs induced cancer. Furthermore, synthesis of biosurfactants by suitable and safe microorganisms also could be helpful in bioremediation of toxins , as the microbial biosurfactants have the ability to break down and disperse the toxins and PAHs. In this regard, the probiotic bacteria bind to PAHs on the meat surface. The bound PAHs along with the probiotics can be eliminated from meat surface using further processing methods, such as slicing, washing, marination etc. As limited studies have been conducted on role of the potentials of probiotics to remove PAHs as compared to other bioremediation strategies, further research is needed.
In this review, we conducted a critical discussion about the formation, occurrence, mechanisms of toxicity and different reduction strategies of PAHs in heat processed meat products. It is worth to mention that the fatal effects of PAHs such as toxicity, carcinogenicity, teratogenicity, and mutagenicity on living organisms have been recognized and reported by several epidemiological studies and government organizations. Furthermore, the association between dietary PAHs exposures and their role as carcinogens in human beings has been established. Therefore, it is necessary to focus on prevention and control of PAHs formation in processed meat products through various strategies to avert public health concerns and safety issues. However, the task is truly challenging because of the diversity of regional and type of foods, consumer preferences and end-point cooking temperatures  and meat processing/preparation systems practiced throughout the globe . To reduce the PAHs content, efforts should be made in terms of the optimization of the cooking and processing conditions during thermal processing of meat products. This is possible through innovative approaches such as right combination of heating treatments, cooking conditions, and technical processes (wood types, time–temperature combination, smoking filters and adsorbents, plant-derived antioxidants and phenolic components as marinades, bio-elimination processes by applying LAB and probiotics) to remove the already existing PAHs from meat products. While doing so, it should be kept in mind that strategies adopted to reduce PAHs during grilling or smoking process should not drastically alter/affect sensory characteristics of meat products. Above all, food safety policies and regulations must be revised, reinforced and monitored by legislative authorities from time to time. This is required to ensure that the meat products contain PAHs within permissible limits and are safe for human consumption.
Availability of data and materials
Nadeem HR, Akhtar S, Ismail T, Sestili P, Lorenzo JM, Ranjha MMAN, et al. Heterocyclic aromatic amines in meat: formation, isolation, risk assessment, and inhibitory effect of plant extracts. Foods. 2021;10(7):1466.
Biswas O, Kandasamy P, Nanda PK, Biswas S, Lorenzo JM, Das A, et al. Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products. Food Mater Res. 2023. https://doi.org/10.4813/FMR-2023-0005.
Hamidi EN, Hajeb P, Selamat J, Razis AFA. Polycyclic aromatic hydrocarbons (PAHs) and their bioaccessibility in meat: a tool for assessing human cancer risk. Asian Pacific J Cancer Prev. 2016;17(1):15–23.
Singh L, Agarwal T, Simal-Gandara J. PAHs, diet and cancer prevention: cooking process driven-strategies. Trends Food Sci Technol. 2020;99:487–506.
Babu AG, Reja SI, Akhtar N, Sultana M, Deore PS, Ali FI. Bioremediation of polycyclic aromatic hydrocarbons (PAHs): current practices and outlook. Microb Metab Xenobiotic Compd. 2019. https://doi.org/10.1007/978-981-13-7462-3_9.
Sampaio GR, Guizellini GM, da Silva SA, de Almeida AP, Pinaffi-Langley ACC, Rogero MM, et al. Polycyclic aromatic hydrocarbons in foods: biological effects, legislation, occurrence, analytical methods, and strategies to reduce their formation. Int J Mol Sci. 2021. https://doi.org/10.3390/ijms22116010.
Akbari-Adergani B, Mahmood-babooi K, Salehi A, Khaniki GJ, Shariatifar N, Sadighara P, et al. GC–MS determination of the content of polycyclic aromatic hydrocarbons in bread and potato Tahdig prepared with the common edible oil. Environ Monit Assess. 2021. https://doi.org/10.1007/s10661-021-09347-w.
Yousefi M, Shemshadi G, Khorshidian N, Ghasemzadeh-Mohammadi V, Fakhri Y, Hosseini H, et al. Polycyclic aromatic hydrocarbons (PAHs) content of edible vegetable oils in Iran: a risk assessment study. Food Chem Toxicol. 2018;118:480–9.
Katona BW, Lynch JP. Mechanisms of Gastrointestinal Malignancies. In: Physiology of the Gastrointestinal Tract: Sixth Edition. 2018. p. 1615–42.
Hokkanen M, Luhtasela U, Kostamo P, Ritvanen T, Peltonen K, Jestoi M. Critical effects of smoking parameters on the levels of polycyclic aromatic hydrocarbons in traditionally smoked fish and meat products in Finland. J Chem. 2018. https://doi.org/10.1155/2018/2160958.
Adeyeye SAO, Ashaolu TJ. Polycyclic aromatic hydrocarbons formation and mitigation in meat and meat products. Polycycl Aromat Compd. 2020. https://doi.org/10.1080/10406638.2020.1866039.
IARC. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans Some Non-Heterocyclic Polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum. 2010.
Duedahl-Olesen L, Ionas AC. Formation and mitigation of PAHs in barbecued meat–a review. Crit Rev Food Sci Nutr. 2022;62(13):3553–68.
EFSA. Polycyclic aromatic hydrocarbons in food scientific opinion of the panel on contaminants in the food chain. Eur Food Safety Auth. 2008. https://doi.org/10.2903/j.efsa.2008.724.
Fraqueza MJ, Laranjo M, Alves S, Fernandes MH, Agulheiro-Santos AC, Fernandes MJ, et al. Dry-cured meat products according to the smoking regime: process optimization to control polycyclic aromatic hydrocarbons. 2020. Foods. https://doi.org/10.3390/foods9010091.
Ledesma E, Rendueles M, Díaz M. Characterization of natural and synthetic casings and mechanism of BaP penetration in smoked meat products. Food Control. 2015;51:195–205.
Shoukat S. Potential anti-carcinogenic effect of probiotic and lactic acid bacteria in detoxification of benzo[a]pyrene: a review. Trends Food Sci Technol. 2020;99:450–9.
Kim HJ, Cho J, Jang A. Effect of charcoal type on the formation of polycyclic aromatic hydrocarbons in grilled meats. Food Chem. 2021. https://doi.org/10.1016/j.foodchem.2020.128453.
Xu M, Wu M, Zhang Y, Zhang H, Liu W, Chen G, et al. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by bacterial mixture. Int J Environ Sci Technol. 2022;19(5):3833–44.
Adeyeye SAO, Bolaji OT, Abegunde TA, Adesina TO. Processing and utilization of snail meat in alleviating protein malnutrition in Africa: a review. Nutr Food Sci. 2020;50(6):1085–97.
Viegas O, Novo P, Pinto E, Pinho O, Ferreira IMPLVO. Effect of charcoal types and grilling conditions on formation of heterocyclic aromatic amines (HAs) and polycyclic aromatic hydrocarbons (PAHs) in grilled muscle foods. Food Chem Toxicol. 2012;50(6):2128–34.
Alomirah H, Al-Zenki S, Al-Hooti S, Zaghloul S, Sawaya W, Ahmed N, et al. Concentrations and dietary exposure to polycyclic aromatic hydrocarbons (PAHs) from grilled and smoked foods. Food Control. 2011;22(12):2028–35.
Lawal AT. Polycyclic aromatic hydrocarbons. A review. Cogent Environ Sci. 2017. https://doi.org/10.1080/23311843.2017.1339841.
Zhu Z, Xu Y, Huang T, Yu Y, Bassey AP, Huang M. The contamination, formation, determination and control of polycyclic aromatic hydrocarbons in meat products. Food Control. 2022. https://doi.org/10.1016/j.foodcont.2022.109194.
Lee JG, Kim SY, Moon JS, Kim SH, Kang DH, Yoon HJ. Effects of grilling procedures on levels of polycyclic aromatic hydrocarbons in grilled meats. Food Chem. 2016;199:632–8.
Britt PF, Buchanan AC, Owens CV, Skeen JT. Does glucose enhance the formation of nitrogen containing polycyclic aromatic compounds and polycyclic aromatic hydrocarbons in the pyrolysis of proline? Fuel. 2004;83(11–12):1417–32.
Zhang J, Zhang X, Hu T, Xu X, Zhao D, Wang X, et al. Polycyclic aromatic hydrocarbons (Pahs) and antibiotics in oil-contaminated aquaculture areas: bioaccumulation, influencing factors, and human health risks. SSRN Electron J. 2022. https://doi.org/10.2139/ssrn.4071623.
Sharma P. Microbial communication during bioremediation of polyaromatic hydrocarbons. Syst Microbiol Biomanuf. 2022;2(3):430–44.
Onopiuk A, Kołodziejczak K, Szpicer A, Wojtasik-Kalinowska I, Wierzbicka A, Półtorak A. Analysis of factors that influence the PAH profile and amount in meat products subjected to thermal processing. Trends Food Sci Technol. 2021;115:366–79.
Yebra-Pimentel I, Fernández-González R, Martínez-Carballo E, Simal-Gándara J. A critical review about the health risk assessment of pahs and their metabolites in foods. Crit Rev Food Sci Nutr. 2015;55(10):1383–405.
Pirsaheb M, Irandost M, Asadi F, Fakhri Y, Asadi A. Evaluation of polycyclic aromatic hydrocarbons (PAHs) in fish: a review and meta-analysis. Toxin Rev. 2020;39(3):205–13.
Marques A, Lourenço HM, Nunes ML, Roseiro C, Santos C, Barranco A, et al. New tools to assess toxicity, bioaccessibility and uptake of chemical contaminants in meat and seafood. Food Res Int. 2011;44(2):510–22.
Xue W, Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol Appl Pharmacol. 2005;206(1):73–93.
Lee JG, Suh JH, Yoon HJ. Occurrence and risk characterization of polycyclic aromatic hydrocarbons of edible oils by the margin of exposure (MOE) approach. Appl Biol Chem. 2019. https://doi.org/10.1186/s13765-019-0454-0.
Jarvis IWH, Dreij K, Mattsson Å, Jernström B, Stenius U. Interactions between polycyclic aromatic hydrocarbons in complex mixtures and implications for cancer risk assessment. Toxicology. 2014;321(1):27–39.
Daniel CR, Schwartz KL, Colt JS, Dong LM, Ruterbusch JJ, Purdue MP, et al. Meat-cooking mutagens and risk of renal cell carcinoma. Br J Cancer. 2011;105(7):1096–104.
Cheng T, Chaousis S, Gamage SMK, Lam AKY, Gopalan V. Polycyclic aromatic hydrocarbons detected in processed meats cause genetic changes in colorectal cancers. Int J Mol Sci. 2021. https://doi.org/10.3390/ijms222010959.
Wang F, Zhang H, Geng N, Ren X, Zhang B, Gong Y, et al. A metabolomics strategy to assess the combined toxicity of polycyclic aromatic hydrocarbons (PAHs) and short-chain chlorinated paraffins (SCCPs). Environ Pollut. 2018;234:572–80.
Abdel-Shafy HI, Mansour MSM. A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet. 2016;25(1):107–23.
Tiwari M, Sahu SK, Pandit GG. Distribution of PAHs in different compartment of creek ecosystem: ecotoxicological concern and human health risk. Environ Toxicol Pharmacol. 2017;50:58–66.
Iko Afé OH, Douny C, Kpoclou YE, Igout A, Mahillon J, Anihouvi V, et al. Insight about methods used for polycyclic aromatic hydrocarbons reduction in smoked or grilled fishery and meat products for future re-engineering: a systematic review. Food Chem Toxicol. 2020. https://doi.org/10.1016/j.fct.2020.111372.
Kao TH, Chen S, Huang CW, Chen CJ, Chen BH. Occurrence and exposure to polycyclic aromatic hydrocarbons in kindling-free-charcoal grilled meat products in Taiwan. Food Chem Toxicol. 2014;71:149–58.
Jiang Y, Zhang Z, Zhang X. Co-biodegradation of pyrene and other PAHs by the bacterium Acinetobacter johnsonii. Ecotoxicol Environ Saf. 2018;163:465–70.
Wretling S, Eriksson A, Eskhult GA, Larsson B. Polycyclic aromatic hydrocarbons (PAHs) in Swedish smoked meat and fish. J Food Compos Anal. 2010;23(3):264–72.
Mastanjević K, Kartalović B, Puljić L, Kovačević D, Habschied K. Influence of different smoking procedures on polycyclic aromatic hydrocarbons formation in traditional dry sausage Hercegovačka kobasica. Processes. 2020. https://doi.org/10.3390/pr8080918.
Bogdanović T, Pleadin J, Petričević S, Listeš E, Sokolić D, Marković K, et al. The occurrence of polycyclic aromatic hydrocarbons in fish and meat products of Croatia and dietary exposure. J Food Compos Anal. 2019;75:49–60.
Samiee S, Fakhri Y, Sadighara P, Arabameri M, Rezaei M, Nabizadeh R, et al. The concentration of polycyclic aromatic hydrocarbons (PAHs) in the processed meat samples collected from Iran’s market: a probabilistic health risk assessment study. Environ Sci Pollut Res. 2020;27(17):21126–39.
Puljić L, Mastanjević K, Kartalović B, Kovačević D, Vranešević J, Mastanjević K. The influence of different smoking procedures on the content of 16 PAHs in traditional dry cured smoked meat “Hercegovačka pečenica.” 2019. Foods. https://doi.org/10.3390/foods8120690.
Mocek K, Ciemniak A. Influence of physical factors on polycyclic aromatic hydrocarbons (PAHs) content in vegetable oils. J Environ Sci Heal - Part B Pestic Food Contam Agric Wastes. 2016;51(2):96–102.
Mohammadi M, Valizadeh-kakhki F. Polycyclic aromatic hydrocarbons determination in grilled beef and chicken. Polycycl Aromat Compd. 2018;38(5):434–44.
El Husseini M, Mourad R, Abdul Rahim H, Al Omar F, Jaber F. Assessment of polycyclic aromatic hydrocarbons (PAH4) in the traditional lebanese grilled meat products and investigation of broasted frying cooking method and meat size on the PAH4 formation. Polycycl Aromat Compd. 2021;41(1):124–42.
Rose M, Holland J, Dowding A, Petch SRG, White S, Fernandes A, et al. Investigation into the formation of PAHs in foods prepared in the home to determine the effects of frying, grilling, barbecuing, toasting and roasting. Food Chem Toxicol. 2015;78:1–9.
Malarut Anan J, Vangnai K. Influence of wood types on quality and carcinogenic polycyclic aromatic hydrocarbons (PAHs) of smoked sausages. Food Control. 2018;85:98–106.
Kim HJ, Cho J, Kim D, Park TS, Jin SK, Hur SJ, et al. Effects of gochujang (Korean Red Pepper Paste) marinade on polycyclic aromatic hydrocarbon formation in charcoal-grilled pork belly. Food Sci Anim Resour. 2021;41(3):481–96.
Zachara A, Gałkowska D, Juszczak L. Contamination of smoked meat and fish products from Polish market with polycyclic aromatic hydrocarbons. Food Control. 2017;80:45–51.
Ledesma E, Rendueles M, Díaz M. Spanish smoked meat products: Benzo(a)pyrene (BaP) contamination and moisture. J Food Compos Anal. 2015;37:87–94.
Purcaro G, Moret S, Conte LS. Overview on polycyclic aromatic hydrocarbons: occurrence, legislation and innovative determination in foods. Talanta. 2013;105:292–305.
Zastrow L, Schwind KH, Schwägele F, Speer K. Influence of smoking and barbecuing on the contents of anthraquinone (ATQ) and polycyclic aromatic hydrocarbons (PAHs) in frankfurter-type sausages. J Agric Food Chem. 2019;67(50):13998–4004.
Anjum Z, Shehzad F, Rahat A, Shah HU, Khan S. Effect of marination and grilling techniques in lowering the level of polyaromatic hydrocarbons and heavy metal in barbecued meat. Sarhad J Agric. 2019;35(2):639–46.
Mirzazadeh M, Sadeghi E, Beigmohammadi F. Comparison of the effects of microwave cooking by two conventional cooking methods on the concentrations of polycyclic aromatic hydrocarbons and volatile N-nitrosamines in beef cocktail smokies (smoked sausages). J Food Process Preserv. 2021. https://doi.org/10.1111/jfpp.15560.
Olatunji OS, Fatoki OS, Opeolu BO, Ximba BJ. Determination of polycyclic aromatic hydrocarbons [PAHs] in processed meat products using gas chromatography—flame ionization detector. Food Chem. 2014;156:296–300.
Hamzawy AH, Khorshid M, Elmarsafy AM, Souaya ER. Estimated daily intake and health risk of polycyclic aromatic hydrocarbon by consumption of grilled meat and chicken in Egypt. Int J Curr Microbiol Appl Sci. 2016;5(2):435–48.
Onwukeme VI, Okafor RN. Impact of cooking methods on the levels of polycyclic aromatic hydrocarbons (PAHs) in chicken meat. IOSR J Environ Sci Ver I. 2015;9(4):2319–99.
Arfaeinia H, Cheshmazar E, Karimyan K, Darvishmotevalli M, Hashemi SE. Data on concentrations of polycyclic aromatic hydrocarbons (PAHs) in roasted and fried chicken—a case study: bushehr. Iran Data Br. 2018;21:1842–7.
Büyükkurt ÖK, Aykın Dinçer E, Burak Çam İ, Candal C, Erbaş M. The influence of cooking methods and some marinades on polycyclic aromatic hydrocarbon formation in beef meat. Polycycl Aromat Compd. 2020;40(2):195–205.
Uzun Özcan A, Maskan M, Bedir M, Bozkurt H. Effect of ohmic cooking followed by an infrared cooking method on lipid oxidation and formation of polycylic aromatic hydrocarbons (PAH) of beef muscle. Grasas Aceites. 2018. https://doi.org/10.3989/gya.0101181.
Sengun IY, Yildiz Turp G, Icier F, Kendirci P, Kor G. Effects of ohmic heating for pre-cooking of meatballs on some quality and safety attributes. Lwt. 2014;55(1):232–9.
Hao X, Li J, Yao Z. Changes in PAHs levels in edible oils during deep-frying process. Food Control. 2016;66:233–40.
Siddique R, Zahoor AF, Ahmad H, Zahid FM, Karrar E. Impact of different cooking methods on polycyclic aromatic hydrocarbons in rabbit meat. Food Sci Nutr. 2021;9(6):3219–27.
Iwegbue CMA, Osijaye KO, Igbuku UA, Egobueze FE, Tesi GO, Bassey FI, et al. Effect of the number of frying cycles on the composition, concentrations and risk of polycyclic aromatic hydrocarbons (PAHs) in vegetable oils and fried fish. J Food Compos Anal. 2020. https://doi.org/10.1016/j.jfca.2020.103633.
Lee JS, Han JW, Jung M, Lee KW, Chung MS. Effects of thawing and frying methods on the formation of acrylamide and polycyclic aromatic hydrocarbons in chicken meat. 2020. Foods. https://doi.org/10.3390/foods9050573.
Jiao Y, Liu Y, Quek SY. Systematic evaluation of nutritional and safety characteristics of Hengshan goat leg meat affected by multiple thermal processing methods. J Food Sci. 2020;85(4):1344–52.
Essumang DK, Dodoo DK, Adjei JK. Effect of smoke generation sources and smoke curing duration on the levels of polycyclic aromatic hydrocarbon (PAH) in different suites of fish. Food Chem Toxicol. 2013;58:86–94.
Hitzel A, Pöhlmann M, Schwägele F, Speer K, Jira W. Polycyclic aromatic hydrocarbons (PAH) and phenolic substances in meat products smoked with different types of wood and smoking spices. Food Chem. 2013;139(1–4):955–62.
Chaemsai S, Kunanopparat T, Srichumpuang J, Nopharatana M, Tangduangdee C, Siriwattanayotin S. Reduction of the polycyclic aromatic hydrocarbon (PAH) content of charcoal smoke during grilling by charcoal preparation using high carbonisation and a preheating step. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2016;33(3):385–90.
Farhadian A, Jinap S, Faridah A, Zaidul ISM. Effects of marinating on the formation of polycyclic aromatic hydrocarbons (benzo[a]pyrene, benzo[b]fluoranthene and fluoranthene) in grilled beef meat. Food Control. 2012;28(2):420–5.
Eldaly E, Hussein M, El-Gaml A, El-hefny D, Mishref M. Polycyclic aromatic hydrocarbons (PAHs) in charcoal grilled meat (Kebab) and kofta and the effect of marinating on their existence. Zagazig Vet J. 2016;44(1):40–7.
Gomes A, Santos C, Almeida J, Elias M, Roseiro LC. Effect of fat content, casing type and smoking procedures on PAHs contents of portuguese traditional dry fermented sausages. Food Chem Toxicol. 2013;58:369–74.
Janoszka B. HPLC-fluorescence analysis of polycyclic aromatic hydrocarbons (PAHs) in pork meat and its gravy fried without additives and in the presence of onion and garlic. Food Chem. 2011;126(3):1344–53.
Badry N. Effect of household cooking methods and some food additives on polycyclic aromatic hydrocarbons (PAHs) formation in chicken meat. World Appl Sci J. 2010;9(9):963–74.
Sinaga K, Legowo AM, Supriatna E, Pramono YB. Reduction of benzo (A) pyrene in charcoal grilled duck meat by marinating with andaliman (Zanthoxylum Acanthopodium, DC) fruit juice. J Indones Trop Anim Agric. 2016;41(4):204–8.
Viegas O, Yebra-Pimentel I, Martínez-Carballo E, Simal-Gandara J, Ferreira IMPLVO. Effect of beer marinades on formation of polycyclic aromatic hydrocarbons in charcoal-grilled pork. J Agric Food Chem. 2014;62(12):2638–43.
Laranjo M, Potes ME, Elias M. Role of starter cultures on the safety of fermented meat products. Front Microbiol. 2019. https://doi.org/10.3389/fmicb.2019.00853.
Cordeiro T, Viegas O, Silva M, Martins ZE, Fernandes I, Ferreira IMLPVO, et al. Inhibitory effect of vinegars on the formation of polycyclic aromatic hydrocarbons in charcoal-grilled pork. Meat Sci. 2020. https://doi.org/10.1016/j.meatsci.2020.108083.
Wongmaneepratip W, Vangnai K. Effects of oil types and pH on carcinogenic polycyclic aromatic hydrocarbons (PAHs) in grilled chicken. Food Control. 2017;79:119–25.
Wang H, Pan L, Si L, Miao J. The role of Nrf2-Keap1 signaling pathway in the antioxidant defense response induced by PAHs in the calm Ruditapes philippinarum. Fish Shellfish Immunol. 2018;80:325–34.
Wang L, Lee WW, Cui YR, Ahn G, Jeon YJ. Protective effect of green tea catechin against urban fine dust particle-induced skin aging by regulation of NF-ΚB, AP-1, and MAPKs signaling pathways. Environ Pollut. 2019;252:1318–24.
Park KC, Pyo HS, Kim WS, Yoon KS. Effects of cooking methods and tea marinades on the formation of benzo[a]pyrene in grilled pork belly (Samgyeopsal). Meat Sci. 2017;129:1–8.
Darwish WS, Chiba H, El-Ghareeb WR, Elhelaly AE, Hui SP. Determination of polycyclic aromatic hydrocarbon content in heat-treated meat retailed in Egypt: health risk assessment, benzo[a]pyrene induced mutagenicity and oxidative stress in human colon (CaCo-2) cells and protection using rosmarinic and ascorbic ac. Food Chem. 2019;290:114–24.
Kuzmicz K, Ciemniak A. Assessing contamination of smoked sprats (Sprattus sprattus) with polycyclic aromatic hydrocarbons (pahs) and changes in its level during storage in various types of packaging. J Environ Sci Heal Part B Pestic Food Contam Agric Wastes. 2018;53(1):1–11.
Semanová J, Skláršová B, Šimon P, Šimko P. Elimination of polycyclic aromatic hydrocarbons from smoked sausages by migration into polyethylene packaging. Food Chem. 2016;201:1–6.
Chen J, Chen S. Removal of polycyclic aromatic hydrocarbons by low density polyethylene from liquid model and roasted meat. Food Chem. 2005;90(3):461–9.
Franco P, Cardea S, Tabernero A, De Marco I. Porous aerogels and adsorption of pollutants fromwater and air: a review. Molecules. 2021. https://doi.org/10.3390/molecules26154440.
Gui B, Xu X, Zhang S, Wang Y, Li C, Zhang D, et al. Prediction of organic compounds adsorbed by polyethylene and chlorinated polyethylene microplastics in freshwater using QSAR. Environ Res. 2021. https://doi.org/10.1016/j.envres.2021.111001.
Otoo EA, Ocloo FCK, Appiah V, Nuviadenu C, Asamoah A. Reduction of polycyclic aromatic hydrocarbons concentrations in smoked guinea fowl (Numida meleagris) meat using gamma irradiation. CYTA J Food. 2022;20(1):343–54.
Sava A, Uiuiu P, Lațiu C, Cocan D, Muntean GC, Papuc T, et al. PAHs, physicochemical and microbiological analyses of trout processed by traditional smoking, in different types of packaging. Fishes. 2023. https://doi.org/10.3390/fishes8080424.
Vranešević J, Kartalović B, Vidaković Knežević S, Škaljac S, Jokanović M. Reduction of polycyclic aromatic hydrocarbons to improve safety of traditional (Homemade) smoked dry-cured pork loin. Polycycl Aromat Compd. 2022. https://doi.org/10.1080/10406638.2022.2153883.
Mahugija JAM, Njale E. Effects of washing on the polycyclic aromatic hydrocarbons (PAHs) contents in smoked fish. Food Control. 2018;93:139–43.
Yousefi M, Khorshidian N, Hosseini H. In vitro PAH-binding ability of lactobacillus brevis TD4. Polycycl Aromat Compd. 2022;42(7):4343–58.
Yousefi M, Hosseini H, Khorshidian N, Rastegar H, Shamloo E, Abdolshahi A. Effect of time and incubation temperature on ability of probiotics for removal of polycyclic aromatic hydrocarbon in phosphate buffer saline. J Microbiol Biotechnol Food Sci. 2022;12(1):e1918.
Khorshidian N, Yousefi M, Shadnoush M, Siadat SD, Mohammadi M, Mortazavian AM. Using probiotics for mitigation of acrylamide in food products: a mini review. Curr Opin Food Sci. 2020;32:67–75.
Yousefi M, Khorshidian N, Mortazavian AM. Detoxification properties of microorganisms in foods. In: Ray RC, editor. Microbial biotechnology in food and health. Amsterdam: Elsevier; 2021.
Lili Z, Hongfei Z, Shoukat S, Xiaochen Z, Bolin Z. Screening lactic acid bacteria strains with ability to bind di-n-butyl phthalate via Turbiscan technique. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol. 2017;110(6):759–69.
Zhao H, Zhou F, Qi Y, Dziugan P, Bai F, Walczak P, et al. Screening of lactobacillus strains for their ability to bind Benzo(a)pyrene and the mechanism of the process. Food Chem Toxicol. 2013;59:67–71.
Bartkiene E, Bartkevics V, Mozuriene E, Krungleviciute V, Novoslavskij A, Santini A, et al. The impact of lactic acid bacteria with antimicrobial properties on biodegradation of polycyclic aromatic hydrocarbons and biogenic amines in cold smoked pork sausages. Food Control. 2017;71:285–92.
Slotkin TA, Skavicus S, Card J, Giulio RTD, Seidler FJ. In vitro models reveal differences in the developmental neurotoxicity of an environmental polycylic aromatic hydrocarbon mixture compared to benzo[a]pyrene: neuronotypic PC12 Cells and embryonic neural stem cells. Toxicology. 2017;377:49–56.
Singh L, Agarwal T. Polycyclic aromatic hydrocarbons in diet: concern for public health. Trends Food Sci Technol. 2018;79:160–70.
Zelinkova Z, Wenzl T. The occurrence of 16 EPA PAHs in food—a review. Polycycl Aromat Compd. 2015;35(2–4):248–84.
Commission E. Commission regulation (EU) 2020/1255 of 7 September 2020 amending regulation (EC) No 1881/2006 as regards maximum levels of polycyclic aromatic hydrocarbons (PAHs) in traditionally smoked meat and smoked meat products and traditionally smoked fish and smo. Off J Eur Union. 2018;2016(68):48–119.
Shen X, Huang X, Tang X, Zhan J, Liu S. The effects of different natural plant extracts on the formation of polycyclic aromatic hydrocarbons (PAHs) in roast duck. 2022. Foods. https://doi.org/10.3390/foods11142104.
Onopiuk A, Kołodziejczak K, Marcinkowska-Lesiak M, Wojtasik-Kalinowska I, Szpicer A, Stelmasiak A, et al. Influence of plant extract addition to marinades on polycyclic aromatic hydrocarbon formation in grilled pork meat. Molecules. 2022. https://doi.org/10.3390/molecules27010175.
Saputro E, Radiati LE, Warsito W, Rosyidi D. Mitigation of polycyclic aromatic hydrocarbons formation in goat satay by shallots juices marination. Trop Anim Sci J. 2022;45(2):227–38.
Kim DY, Han GT, Shin HS. Adsorption of polycyclic aromatic hydrocarbons (PAHs) by cellulosic aerogels during smoked pork sausage manufacture. Food Control. 2021. https://doi.org/10.1016/j.foodcont.2021.107878.
Da XuQ, Zhou ZQ, Jing Z, He Q, Sun Q, Zeng WC. Pine needle extract from Cedrus deodara: potential applications on hazardous chemicals and quality of smoked bacon and its mechanism. Food Control. 2021. https://doi.org/10.1016/j.foodcont.2021.108368.
Santisavekun NS. Factors affecting the formation of carcinogenic polycyclic aromatic hydrocarbons (PAHs) and qualities of grilled and deep fried pork. Bangkok: Kasetsart University; 2019.
Cho J, Barido FH, Kim HJ, Kwon JS, Kim HJ, Kim D, et al. Effect of extract of perilla leaves on the quality characteristics and polycyclic aromatic hydrocarbons of charcoal barbecued pork patty. Food Sci Anim Resour. 2023;43(1):139–56.
Wang C, Xie Y, Wang H, Bai Y, Dai C, Li C, et al. Phenolic compounds in beer inhibit formation of polycyclic aromatic hydrocarbons from charcoal-grilled chicken wings. Food Chem. 2019;294:578–86.
Coroian CO, Coroian A, Becze A, Longodor A, Mastan O, Radu-Rusu RM. Polycyclic aromatic hydrocarbons (PAHs) occurrence in traditionally smoked chicken, turkey and duck meat. Agriculture. 2022;13(1):57.
Racovita RC, Secuianu C, Ciuca MD, Israel-Roming F. Effects of smoking temperature, smoking time, and type of wood sawdust on polycyclic aromatic hydrocarbon accumulation levels in directly smoked pork sausages. J Agric Food Chem. 2020;68(35):9530–6.
Wongmaneepratip W, Jom KN, Vangnai K. Inhibitory effects of dietary antioxidants on the formation of carcinogenic polycyclic aromatic hydrocarbons in grilled pork. Asian-Australas J Anim Sci. 2019;32(8):1205–10.
Yu Y, Cheng Y, Wang C, Huang S, Lei Y, Huang M, et al. Inhibitory effect of coriander (Coriandrum sativum L.) extract marinades on the formation of polycyclic aromatic hydrocarbons in roasted duck wings. Food Sci Hum Wellness. 2023;12(4):1128–35.
Onopiuk A, Kołodziejczak K, Szpicer A, Marcinkowska-Lesiak M, Wojtasik-Kalinowska I, Stelmasiak A, et al. The effect of partial substitution of beef tallow on selected physicochemical properties, fatty acid profile and PAH content of grilled beef burgers. 2022. Foods. https://doi.org/10.3390/foods11131986.
Lai YW, Lee YT, Inbaraj BS, Chen BH. Formation and inhibition of heterocyclic amines and polycyclic aromatic hydrocarbons in ground pork during marinating. 2022. Foods. https://doi.org/10.3390/foods11193080.
He X, Li B, Yu X, Zhuang Y, Li C, Dong L, et al. Inhibiting effects of ginger and rosemary on the formation of heterocyclic amines, polycyclic aromatic hydrocarbons, and trans fatty acids in fried pork balls. 2022. Foods. https://doi.org/10.3390/foods11233767.
Hu Y, Tian H, Hu S, Dong L, Zhang J, Yu X, et al. The effect of in-package cold plasma on the formation of polycyclic aromatic hydrocarbons in charcoal-grilled beef steak with different oils or fats. Food Chem. 2022. https://doi.org/10.1016/j.foodchem.2021.131384.
Chiang CF, Hsu KC, Cho CY, Tsai TY, Hsu CH, Yang DJ. Comparison and establishment of appropriate methods to determine EU priority PAHs in charcoal-grilled chicken drumsticks with different treatments and their dietary risk assessments. Food Chem Toxicol. 2020. https://doi.org/10.1016/j.fct.2020.111400.
Nor Hasyimah AK, Jinap S, Sanny M, Ainaatul AI, Sukor R, Jambari NN, et al. Effects of honey-spices marination on polycyclic aromatic hydrocarbons and heterocyclic amines formation in gas-grilled beef satay. Polycycl Aromat Compd. 2022;42(4):1620–48.
Min Zhang X, Yang Xu C, Hui T, Zhou Cai K, Zhou H, Gui Chen C, et al. Vinegars inhibiting of the generation of BaP in barbecued pork sausages by decreasing the pH and free radical scavenging. Food Control. 2023. https://doi.org/10.1016/j.foodcont.2022.109404.
Lai YW, Lee YT, Cao H, Zhang HL, Chen BH. Extraction of heterocyclic amines and polycyclic aromatic hydrocarbons from pork jerky and the effect of flavoring on formation and inhibition. Food Chem. 2023. https://doi.org/10.1016/j.foodchem.2022.134291.
Esfahani Mehr A, Hosseini SE, Seyadain Ardebili SM. Effects of nutmeg and ginger essential oils and their nanoemulsions on the formation of heterocyclic aromatic amines and polycyclic aromatic hydrocarbons in beef patties during 90 days freezing storage. J Food Meas Charact. 2019;13(3):2041–50.
Hu G, Cai K, Li Y, Hui T, Wang Z, Chen C, et al. Significant inhibition of garlic essential oil on benzo[a]pyrene formation in charcoal-grilled pork sausages relates to sulfide compounds. Food Res Int. 2021. https://doi.org/10.1016/j.foodres.2021.110127.
Oz E. The presence of polycyclic aromatic hydrocarbons and heterocyclic aromatic amines in barbecued meatballs formulated with different animal fats. Food Chem. 2021. https://doi.org/10.1016/j.foodchem.2021.129378.
Zhu Li Y, Zhou Cai K, Feng Hu G, Nie W, Liu XY, Xing W, et al. Γ-Ray irradiation reduces the formation of polycyclic aromatic hydrocarbons during the baking of sausage. Radiat Phys Chem. 2021. https://doi.org/10.1016/j.radphyschem.2021.109406.
Nie W, Cai Zhou K, Li Zhu Y, Hu Feng G, Xing W, Wang Xi X, et al. Application of grape seed extract lead to a higher formation of polycyclic aromatic hydrocarbons in roasted pork sausage at the end of storage. J Food Process Preserv. 2020. https://doi.org/10.1111/jfpp.14532.
Tian H, Yu J, Li M, Li J, Lu Y, Yu X, et al. https://ssrn.com/abstract=4258347. 2020. Effect of Curcumin on the Formation of Polycyclic Aromatic Hydrocarbons (Pahs) in Grilled Chicken Wings a.
Yunita CN, Radiati LE, Rosyidi D. Effect of lemon marination on polycyclic aromatic hydrocarbons (PAH) and quality of chicken satay. J Penelit Pendidik IPA. 2023;9(6):4723–30.
Cao J, Yang L, Ye B, Chai Y, Liu L. Effect of apple polyphenol and three antioxidants on the formation of polycyclic aromatic hydrocarbon in barbecued pork. Polycycl Aromat Compd. 2022. https://doi.org/10.1080/10406638.2022.2110906.
Aoudeh E, Oz E, Oz F. Effect of beef patties fortification with black garlic on the polycyclic aromatic hydrocarbons (PAHs) content and toxic potency. Food Chem. 2023. https://doi.org/10.1016/j.foodchem.2023.136763.
Bulanda S, Janoszka B. Polycyclic aromatic hydrocarbons (PAHs) in roasted pork meat and the effect of dried fruits on PAH content. Int J Environ Res Public Health. 2023. https://doi.org/10.3390/ijerph20064922.
Gagaoua M, Terlouw C, Richardson I, Hocquette JF, Picard B. The associations between proteomic biomarkers and beef tenderness depend on the end-point cooking temperature, the country origin of the panelists and breed. Meat Sci. 2019;157:107871.
Gagaoua M, Boudechicha H-R. Ethnic meat products of the North African and Mediterranean countries: an overview. J Ethnic Foods. 2018;5(2):83–98.
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Das, A.K., Bhattacharya, D., Das, A. et al. Current innovative approaches in reducing polycyclic aromatic hydrocarbons (PAHs) in processed meat and meat products. Chem. Biol. Technol. Agric. 10, 109 (2023). https://doi.org/10.1186/s40538-023-00483-8