Chemical hazards in smoked meat and fish (2024)

Table of Contents
Associated Data Abstract 1. INTRODUCTION 2. METHODOLOGY 3. RESULTS 3.1. Smoking process 3.2. Nitrosamine, heterocyclic amines, and polycyclic aromatic hydrocarbons TABLE 1 TABLE 2 TABLE 3 TABLE 4 3.3. Other hazards in grilled or smoked fish and meat TABLE 5 TABLE 6 TABLE 7 TABLE 8 3.4. Risk assessment TABLE 9 TABLE 10 TABLE 11 4. CONCLUSION CONFLICT OF INTEREST ETHICAL APPROVAL ACKNOWLEDGMENTS Notes DATA AVAILABILITY STATEMENT REFERENCES References

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Chemical hazards in smoked meat and fish (1)

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Food Sci Nutr. 2021 Dec; 9(12): 6903–6922.

Published online 2021 Oct 18. doi:10.1002/fsn3.2633

PMCID: PMC8645718

PMID: 34925818

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Associated Data

Data Availability Statement

Abstract

This review aims to give an insight into the main hazards currently found in smoked meat and fish products. Literature research was carried out on international databases such as Access to Global Online Research in Agriculture (AGORA) database, Science direct, and Google scholar to collect and select 92 relevant publications included in this review. The smoking process was described and five hazards mostly found in smoked fish and meat were presented. The heat‐induced compounds such as polycyclic aromatic hydrocarbons, heterocyclic amines, and nitrosamines were found in smoked fish and meat. Other hazards such as biogenic amines and heavy metals were also present in smoked fish and meat. The levels of these hazards reported from the literature exceeded the maximal limits of European Union. A brief description of risk assessment methodology applicable to such toxic compounds and risk assessment examples was also presented in this review. As most of the hazards reported in this review are toxic and even carcinogenic to humans, actions should be addressed to reduce their presence in food to protect consumer health and to prevent public health issue.

Keywords: benzo(a)pyrene, food safety, heat‐induced compounds, nitrosamines, systematic review

‐Main hazards reported in smoked meat and fish are toxic and carcinogenic to humans

‐Levels of chemical hazards reported from literature exceeded the maximal limits of European Union

‐Consumption of smoked meat and fish presents risk for consumers ‘health

Chemical hazards in smoked meat and fish (3)

1. INTRODUCTION

Fish and meat preservation is a big challenge in different regions of the world. Among fish preservation methods, smoking is the mostly used method (Berkel etal.,2005; Nout etal.,2003; Toth & Potthast,1984). It extends shelf life and confers special taste and aroma to the end products (Igwegbe etal.,2015; Yusuf etal.,2015). Despite these advantages, the consumption of smoked fish or meat products presents health concern due to process contaminants. Several authors reported acrolein, acrylamide, furan, heterocyclic amines, monochloropropanediol (MCPD), nitrosamine, and polycyclic aromatic hydrocarbons (PAHs) as heat‐induced toxic compounds in foods and dealt with their risk assessment (Akpambang etal.,2009; Alomirah etal.,2011; Domingo & Nadal,2015; Larsen,2006; Mey etal.,2014; Skog, Johansson, & Jaègerstad, 1998; Stadler & Lineback,2009; Swann,1977; Yurchenko & Molder,2007). Among these various heat‐induced compounds, PAHs and heterocyclic amines are mainly associated with smoking or grilling process. Moreover, due to the amino acid composition of fish and meat, some toxic compounds like biogenic amines and even nitrosamines may be formed. Other environmental hazards like heavy metals can also be found in fish and meat. The consumption of food contaminated with these compounds could result in adverse effects on human health including cancer (EFSA (European Food Safety Authority), 2008; EFSA (European Food Safety Authority), 2011). This literature review aims to focus on chemical hazards (nitrosamines, heterocyclic amines, PAHs, heavy metals, and biogenic amines) commonly reported in smoked fish and meat.

2. METHODOLOGY

Publications included in this review were from international databases such as Access to Global Online Research in Agriculture (AGORA) database, Science direct, and google scholar. Original and review papers were collected on December 2019 and updated on July 2021 using key words such as “smoking,” “heterocyclic amines,” “PAHs,” “benzo(a)pyrene (BaP),” “heavy metals,” “nitrosamine,” “biogenic amines,” “histamine,” “risk assessment,” “fish,” and “meat.” Only 112 relevant papers in accordance with the topic of this review were included on the basis of their keywords. The software Endnote, version 13 was used to manage and rank the collected publications in different subgroups according to each topic.

3. RESULTS

3.1. Smoking process

Smoking is a food processing method used as a preservation method to extend shelf life of food by reducing moisture content and microorganism load (Köse,2010). Smoking is also used to improve sensorial characteristics including taste, aroma, and appearance of smoked fish and meat (Berkel etal.,2005; Codex Alimentarius,2009). Two types of smoking processes are commonly used. The “cold” smoking process in which the temperature of the product does not exceed 30°C and “hot” smoking process during which food such as fish is well cooked and temperature in the center of the product may reach up to 60–85°C (Berkel etal.,2005; Stołyhwo & Sikorski,2005). According to Berkel etal.(2005), there is a third smoking process called smoke‐drying which is hot smoking followed by a drying step carried out in the smoking equipment. Hot smoking and smoke‐drying are frequently used to preserve fish in African countries (Assogba etal.,2019). According to Codex Alimentarius (2013), the smoke‐drying process enables us to obtain dried products with a water activity lower or equal to 0.75, allowing keeping the end product at room temperature and to control bacterial and fungi alteration.

During smoking, fish or meat and their products are submitted directly or indirectly to smoke produced by partial burning of wood. Direct smoking is a process during which fish or meat is laid on mesh trays above the embers, whereas in indirect smoking, smoke is produced in a separate chamber and fish is smoked in another chamber (Codex Alimentarius,2009). Traditional fish smoking is carried out in kilns (barrel of locally made clay) using fuel such as wood, charcoal, wood sawdust, wood chips, bagasse, corn cobs, coconut husks, and shells (Assogba etal.,2019; Codex Alimentarius,2009; Kpoclou etal.,2014; Stołyhwo & Sikorski,2005). Smoke is composed of a mixture of about 380 compounds, mainly phenols, aldehydes, ketones, organic acids, alcohols, esters, hydrocarbons, and various heterocyclic compounds (Codex Alimentarius,2009; Toth & Potthast,1984). Some of them such as phenolic, carbonyls, furan derivatives, organic acids, and their esters affect the sensory quality, but could also improve the shelf life of the product by inhibiting the growth of spoilage bacteria (Ciecierska & Obiedzinski,2007; Gomez‐Guillén etal.,2009; Igwegbe etal.,2015; Stołyhwo & Sikorski,2005; Yusuf etal.,2015). However, carcinogenic compounds such as PAHs, nitrosamines, and heterocyclic amines may be formed during the smoking process either from pyrolysis of organic matter and transferred inside the food or directly produced inside the food as a result of reactions between food composition and heat (Skog etal.,1998; Stołyhwo & Sikorski,2005; Viegas etal.,2012; Yurchenko & Molder,2007). Figure1 shows different smoking methods of fish and meat reported from the literature.

Chemical hazards in smoked meat and fish (4)

(a) Flow chart of smoked fish production (Adeyemi etal.,2013; Adeyeye etal.,2015; Assogba etal.,2019; Dègnon etal.,2013; Goulas & Kontominas,2005; Ubwa etal.,2015) and (b) smoked meat production (Poligné etal.,2001; Roseiro etal.,2011)

3.2. Nitrosamine, heterocyclic amines, and polycyclic aromatic hydrocarbons

3.2.1. Nitrosamines

Nitrosamines (Figure2) or N‐nitroso compounds (N‐nitrosodiméthylamine (NDMA), N‐nitrosométhyléthylamine (NMEA), N‐nitrosodiethylnitrosoamine (NDEA), Nitrosodipropylamine (NDPA), N‐nitrosodibutylamine (NDBA), N‐nitrosomorpholine (NMOR), 1‐nitrosopiperidine (NPIP), 1‐nitrosopyrrolidine (NPYR), N‐nitrosodiéthanolamine (NDELA), 1‐methyl‐3‐nitro‐1‐nitrosoguanidine (MNNG), N‐nitroso‐N‐ethylbutylamine (NEBA), N'‐nitrosoanabasine (NAB), and 4‐(N‐nitrosomethylamino)‐1‐(3‐pyridyl)‐1‐butanone (NNK)) are a group of toxic compounds produced mainly in meat products during heat processing (Belitz etal.,2009; Domanska & Kowalski,2003; Reinik,2007).

Chemical hazards in smoked meat and fish (5)

Chemical structure of four examples of nitrosamines: N‐nitrosodiméthylamine (NDMA); N‐nitrosodiethylnitrosoamine (NDEA);1‐nitrosopiperidine (NPIP) and 1‐nitrosopyrrolidine (NPYR) (PubChem,2020).

N‐nitroso compounds can be subdivided into two groups (Herrmann etal.,2015): volatile nitrosamines (NDMA, NMOR, NMEA, NPYR, NDEA, and NPIP) and nonvolatile nitrosamines (N‐nitrososarcosine (NSAR), N‐nitrosoproline (NPRO), N‐nitrosomethylaniline (NMA), N‐nitroso‐thiazolidine‐4‐carboxylic (NTCA) acid, and N‐nitroso‐2‐methylathiazolidine‐4‐carboxylic acid (NMTCA)).

The human exposure to N‐nitroso compounds is from environment, tobacco smoke, and the diet which has been identified to be the main source (Jakszyn etal.,2005). N‐nitroso compounds formation requires substrates (primary amine, secondary amine, tertiary amine, amides, secondary amino acids, quaternary ammonium salts, etc.) and a nitrosating agent (nitrite, nitrates, and nitrogen oxides) through several reactions (Filho etal.,2003; INERIS (Institut National de l'Environnement Industriel et des RISques), 2014; Reinik,2007). Nitrogen oxides are formed either from the addition of nitrate and/or nitrite to foods or from the heating process of food such as smoking, during which nitrogen molecular can be oxidized or present in the smoke (INERIS (Institut National de l'Environnement Industriel et des RISques), 2014; Jakszyn etal.,2005). Al Bulushi etal.(2009) reported NPYR and NPIP in vitro formation at high temperature (160°C, 2h). Microorganisms (Aspergillus sp.; Pseudomonas sp.; P.stutzeri; E.coli) can be involved in N‐nitrosamine formation by reducing nitrates to nitrites, by degrading proteins to amines and amino acids, or by producing enzymes working at a suitable pH (2–4) for nitrosation (Al Bulushi etal.,2009; Ayanaba & Alexander,1973; Drabik‐Markiewicz etal.,2009; Jägerstad & Skog,2005; Jägerstad etal.,1998; Mills & Alexander,1976; Rostkowska etal.,1998; Yurchenko & Molder,2007). Nitrite and nitrate are frequently used in meat preservation and lead to nitrosamines formation due to reaction with amino compounds either in the stomach or within the food product (Filho etal.,2003; Pan etal.,2011; Sebranek & Bacus,2007; Swann,1977). It is the case of meat products such as sausages, ham, and salami where the addition of nitrite and nitrate was used to inhibit the formation of spoilage bacteria (Drabik‐Markiewicz etal.,2009; Filho etal.,2003; Hustad etal.,1973). The nitrosamines are found in smoked meat, grilled meat, canned meat, and pickled meat at different levels (Table1), but not in raw meat where there is not enough nitrite and amines for its production (Yurchenko & Molder,2007). Studies carried out on nitrosamine determination in fish products mostly focused on NDMA determination because of its precursor dimethylamine (DMA) which is widely formed in marine fish (Al Bulushi etal.,2009). NDMA is classified in Group 2A (probably carcinogenic to humans) by the International Agency for Research on Cancer (IARC (International Agency for Research on Cancer), 2010), whereas N‐nitrosonornicotine (NNN) and 4‐(N‐nitrosomethylamino)‐1‐(3‐pyridyl)‐1‐butanone (NNK) are classified in Group 1 (carcinogenic to humans). Belitz etal.(2009) reported NDMA in cured meat processed with pickling with levels ranging between 0.5 and 15μg/kg (Table1). Herrmann etal.(2014) also reported NDMA in smoked pork fillet (1.3µg/kg) and smoked ham (2.1µg/kg).

TABLE 1

Concentrations of volatile N‐nitrosamines in various smoked or grilled fish and meat as reported from the literature

ProcessingN‐nitrosamines (µg/kg)References
NDMANDEANPYRNPIPNDBANDPA
Smoked meat0.2–1.40.3–0.70.2–19.50.4–2.30.4–0.90.3Al‐Kaseem etal.(2014); Reinik (2007); Yurchenko and Molder (2007)
Cured meat (pickling salt)0.5–15nd3.2–4.2ndNdndBelitz etal.(2009)
Grilled meat0.2–3.20.3–0.60.8–14.61.0–2.80.2–0.4˂0.1–0.3Al‐Kaseem etal.(2014); Reinik (2007); Yurchenko and Molder (2007)
Smoked fish˂0.1–2.8˂0.1–0.50.4–25.4˂0.2–7.8˂0.2–6.0ndReinik (2007)
Smoked chicken1.2–2.1˂0.1–0.30.5–22.1˂0.1–5.30.1–6.3nd

Abbreviations: nd, not determined;NDBA, N‐nitrosodibuthylnitrosamine; NDEA, N‐nitrosodiethylnitrosamine; NDMA, N‐nitrosodimethylnitrosamine; NDPA, N‐nitrosodipropylamine; NPIP, N‐nitrosopiperidine; NPYR, N‐nitrosopyrrolidine.

Different analytical methods were used to analyze nitrosamines. The method of gas chromatography and mass spectrometry detection with ion monitoring using different columns has been used by several authors to identify and quantify nitrosamines (Filho etal.,2003; Herrmann etal.,2014; Swann etal.,1977; Yurchenko & Molder,2007). However, only Thermal Energy Analyzer (TEA) detection is recognized as specifically for nitrosamines but expensive (Filho etal.,2003). Filho etal.(2003) developed methods for nitrosamine compounds analysis (extraction, preconcentration, and analysis) which allowed their determination even at trace levels. The separation of nitrosamines was performed using micellar electrokinetic chromatography and confirmation was achieved using gas chromatography coupled with mass spectrometry detection (Filho etal.,2003; Herrmann etal.,2014).

3.2.2. Heterocyclic amines

Heterocyclic amines are toxic compounds produced in meat and fish during processing at temperature over 150°C (Haskaraca etal.,2014; Jägerstad & Skog,2005; Puangsombat etal.,2011; Sinha etal.,1998; Solyakov & Skog,2002). According to their chemical structures, two groups of heterocyclic amines can be distinguished: pyrolytic heterocyclic amines also known as amino‐carboline heterocyclic amines and thermic heterocyclic amines composed of imidazo‐quinolines (e.g., IQ ((2‐Amino‐3,4‐dimethylimidazo[4,5‐f]quinolone)), imidazoquinoxalines (e.g., MeIQx (MeIQx (2‐Amino‐3,8‐dimethylimidazo[4,5‐f]quinoxaline)), and imidazopyridines (e.g., PhIP (2‐Amino‐1‐methyl‐6‐phenylimidazo[4,5‐b]pyridine)) (Jägerstad & Skog,2005; Viegas, Novo, Pinto, etal.,2012). The imidazo‐quinolines, imidazoquinoxalines, and imidazopyridines are three groups of precursors present in raw meat and fish muscle and could be produced from creatine or creatinine, free amino acids, and sugars through the Maillard reaction (Jägerstad & Skog,2005; Viegas, Novo, Pinto, etal.,2012). The IARC (International Agency for Research on Cancer) classified MeIQx, MeIQ, and PhiP as possibly carcinogenic to humans (Group 2B). The 2‐amino‐3,8‐dimethylimidazo[4,5‐f]quinoxaline (8‐MeIQx) and 2‐amino‐1‐methyl‐6‐ phenylimidazo[4,5‐b]pyridine (PhIP) (Figure3) are the most abundant heterocyclic amines formed in grilled beef, bacon, fish, and poultry (Turesky,2007). Skog etal.(1998) reported the presence of heterocyclic amines in smoked fish and fried meat products. The authors showed that the use of wood charcoal induced high production of heterocyclic amines (1.6–4ng/g MeIQx; 1.5–7.8ng/g PhIP) contrary to coconut charcoal (0.7–1ng/g MeIQx; 0.9–3ng/g PhIP) (data not shown) in grilled salmon and beef samples (Viegas, Novo, Pinto, etal.,2012). Gibis (2016) reported high temperature (180°C and 220°C) and duration as key factors of heterocyclic amines production, mainly IQ, MeIQ, MeIQx, 4,8‐DiMeIQx, and PhIP. Table2 shows different concentrations of some heterocyclic amines reported from the literature. Very few studies reported the presence of IQ in grilled or smoked foods. Levels of 1.6–2ng/g were reported in grilled beef (Table2). However, MeIQx was reported in several foods such as processed bacon and pork (Sinha etal.,1998) with levels ranging from 0.4 to 5.4ng/g (Table2). High levels of PhIP (till 480ng/g) were reported from the literature (Table2). Even though no maximal limit of heterocyclic amines was reported in the literature, their presence in food is a health concern and adequate food preparation procedures should be implemented having the ALARA (ALARA=as low as reasonably achievable) principle in mind. Lu etal.(2018) reported that the use of different spices (Garlic, onion, red chili, paprika, black pepper, and ginger) before deep‐frying of beef and chicken had inhibitory effects (43%–87%) on the formation of heterocyclic amines (data not shown).

Chemical hazards in smoked meat and fish (6)

Chemical structure of three examples of heterocyclic amines: IQ ((2‐Amino‐3,4‐dimethylimidazo[4,5‐f]quinolone)); MeIQx (2‐amino‐3,8‐dimethylimidazo[4,5‐f]quinoxaline) and PhIP (2‐amino‐1‐methyl‐6‐phenylimidazo[4,5‐b]pyridine) (PubChem,2020)

TABLE 2

Concentration of main heterocyclic amines in cooked meat, as reported from the literature

ProductsCooking methods.Heterocyclic amines (µg/kg)References
MeIQxDiMeIQxPhIPIQMeIQ
BaconPan‐fried0.4–4.3nd0.7–4.8ndndSinha etal.(1998)
Oven‐broiled1.5–4nd1.4–30.3ndnd
microwaved0.4–1.5nd3.1ndnd
Grilled1.0–27nd−9.3nd−36ndnd

Knize etal.(1997);

Skog etal.(1998).

PorkPan‐fried0.4–5.4nd0.1–2.3ndndSinha etal.(1998)
Oven‐broiledndndndndnd
BeefGrilled0.5–60.1–1.20.6–270.2nd

Fay etal.,(1997);

Murray and Lynch (1993); Wakabayashi etal.(1993);

Barbecued4.42.7381.6ndSkog etal.(1998)
ChickenBarbecued0.3–90.1–3.127–480ndndKnize etal.(1996); Murray and Lynch (1993); Sinha etal.(1995)
Grilled0.6–2.30.5–3.121–315ndndKnize, Salmon, Hopmans, etal.(1997); Knize etal.(1997); Wakabayashi etal.(1993)

Abbreviations: nd, not determined; MeIQx=2‐amino‐3,8‐dimethylimidazo[4,5‐f] quinoxaline; DiMeIQx=2‐amino‐3,4,8‐trimethylimidazo[4,5‐f]quinoxaline; PhIP=2‐amino‐1‐methyl‐6‐phenylimidazo[4,5‐b]pyridine; IQ=2‐amino‐3‐methylimidazo[4,5‐f ]quinoline; MeIQ=2‐amino‐3,4‐dimethylimidazo[4,5‐f]quinoline.

Heterocyclic amine determination was performed according to methods including extraction, purification injection, and quantification using high‐performance liquid chromatography coupled with diode array and fluorescence detectors (HPLC‐DAD/FLD) (Melo etal.,2008). Heterocyclic amines can also be extracted by solid‐phase extraction and analyzed by reverse phase HPLC or LC/MS (Oz & Yuze,2016; Santos etal.,2004; Sinha etal.,1998; Viegas, Novo, Pinto, etal.,2012).

3.2.3. Polycyclic aromatic hydrocarbons

Polycyclic aromatic hydrocarbons are toxic compounds having a low solubility in water and constitute a large class of organic compounds, containing 2 or more fused aromatic rings composed of carbon and hydrogen atoms (EFSA (European Food Safety Authority), 2008; SCF (Scientific Committee on Food), 2002). They are produced from incomplete combustion of the organic matter when foods such as fish or meat are processed by smoking, grilling, or roasting (Battisti etal.,2015; EFSA (European Food Safety Authority), 2008; Ingenbleek etal.,2019; Yusuf etal.,2015). Several studies reported that fat dropping in the flame during grilling processing contributes to PAHs formation (Chen etal.,2013; Viegas, Novo, Pinto, etal.,2012). Additionally, studies showed that PAHs formation depends on the type of raw material, smoking methods, fuel and kiln type, smoke composition and degree of exposure to smoke, and combustion temperature (Chen etal.,2013; Codex Alimentarius,2009; Kpoclou etal.,2014; Stołyhwo & Sikorski,2005). Traditional smoking or grilling is responsible for the production of high amounts of PAH in meat and fish as reported by Forsberg etal.(2012); Onyango etal.(2012); Iko Afé etal.(2020); Ubwa etal.(2015).

Consumers are exposed to PAHs according to three possible ways: by inhalation, contact with the skin, and consumption of contaminated food (EFSA (European Food Safety Authority), 2008; Silva etal.,2011). Likewise, foods are contaminated with PAHs either by environment (exhaust fumes of the engines, bush fires, etc.) or by traditional food processing (drying, smoking, grilling, etc.) (ANSES (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail), 2011). The main route of human exposure to PAHs is diet (ANSES (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail), 2011; EFSA (European Food Safety Authority), 2008). PAHs are genotoxic, carcinogenic, and mutagen (EFSA (European Food Safety Authority), 2008; SCF (Scientific Committee on Food), 2002). Due to their genotoxicity, sixteen PAHs have been included in a priority list of the European Union (EU) (SCF (Scientific Committee on Food), 2002). Among these 16 priority EU PAHs, benzo[a]anthracene (BaA), chrysene (CHR), benzo[a]pyrene (BaP), and benzo[b]fluoranthene (BbF) are four PAHs (named PAH4) (Figure4) relevant in food due to their toxicity and occurrence (EFSA (European Food Safety Authority), 2008). PAHs are metabolized in the liver by cytochrome P450 (CYP1A1 in particular) into compounds named epoxides, which are able to bind to macromolecules such as proteins and nucleic acids (EFSA (European Food Safety Authority), 2008). After ingestion, before to reach the liver, PAHs come in contact with the intestinal microbiota, which can also have a metabolization role. Van de Wiele etal.(2005) evaluated the possible ways of biotransformation of PAHs in the human intestine using a simulator of the human intestinal microbial ecosystem (SHIME). These authors showed that PAHs are bioactivated in colon digestion into estrogenic metabolites, whereas the digestion of the stomach and small intestine does not generate any estrogenic metabolite. Moreover, the inactivation of the colon microbiote eliminated these estrogenic effects, which suggests that the estrogenic activity would be related to the bio‐activation of PAHs by the microbiote of the colon (Van de Wiele & Al,2005). In addition to be carcinogenic, PAHs can thus be qualified of endocrine disrupters.

Chemical hazards in smoked meat and fish (7)

Chemical structure of the PAH4 for which a maximum limit in food has been set in EU (PubChem,2020).

Among PAHs, BaP is the mostly used one for in vivo toxicological studies. After giving female mice BaP at doses >10mg/kg b.w. (body weight) per day, impaired fertility was observed in their offspring. The studies on carcinogenicity of PAHs showed that the type of cancer developed after PAHs exposure depends on the exposure way. Indeed, a dermic exposure would induce tumors on the skin, whereas an exposure by oral way would induce gastric tumors. After oral exposure of laboratory animals to BaP, gastrointestinal tract, liver, and lung tumors were reported (EFSA (European Food Safety Authority), 2008). After feeding female mice with diets containing BaP at a concentration of 0, 5, 25, or 100mg/kg of diet for 2years, papillomas and carcinomas were observed in the forestomach, oesophagus, and tongue (Culp etal.,1998). Several authors also associate colorectal cancer with meat consumption and some of them established colorectal cancer (Gunter etal.,2007; Ronco etal.,2011; Sinha etal.,2005). Sinha etal.(2005) reported an increased risk of colorectal adenomas resulting from high BaP intake from both meat consumption and other food sources.

Benzo(a)pyrene is classified as carcinogenic to humans (Group 1), and CHR, BaA, and BbF are classified as possibly carcinogenic to humans (Group 2B) (IARC (International Agency for Research on Cancer), 2010).

The European commission set maximum levels of 2 and 12μg/kg for benzo(a)pyrene (BaP) and the PAH4, respectively, in smoked meat and smoked fish products (EC (European Commission), 2006). Table3 shows some examples of PAH4 levels reported from the literature (between 2015 and 2020), far above the EU limit of 12µg/kg (25 times (Iko Afé etal.,2020) or 52 times (Rozentale etal.,2018) this limit).

TABLE 3

Examples of levels of PAH4 above the maximal EU limit of 12µg/kg in various smoked or grilled meat and fish

ProductsPAH4 (µg/kg)References
Smoked fish198Ingenbleek etal.(2019)
Smoked sprats25.6Gheorghe etal.(2019)
Grilled pork53.8–300.6Iko Afé etal.(2020)
Slavonska kobasica, smoked pork sausage12.8–42.6Mastanjević etal.(2020)
Smoked meat56.2–628Rozentale etal.(2018)
Smoked meat34.6Rozentale etal.(2015)
Barbecued pork25.2Duedahl‐Olesen etal.(2015)
Barbecued beef48

Note

PAH4: sum of benzo[a]pyrene, chrysene, benzo[b]fluoranthene, and benz[a]anthracene.

Determination of PAH in food can be performed after using an accelerated solvent extractor (ASE) for the extraction, and HPLC coupled with fluorescence and photo diode array detectors (FLD/PDA) or gas chromatography coupled with mass spectrometry (GC/MS) for quantification (Brasseur etal.,2007; Kendirci etal.,2014; Saito etal.,2014; Viegas etal.,2012).

During these past decades, several studies dealt with PAHs in processed food, especially in smoked meat and fish. Some of these studies reported in Tables3 and ​and44 were from different continents: Asia (15.8%), Africa (42.1%), and Europe (42.1%). In Africa, Nigeria is the country in which more studies were carried out on PAHs. The PAHs data reported in Table4 showed that most studies are recent (published between 2017 and 2021), showing that there is a new interest for scientists to update data on the presence of PAHs in smoked or grilled fish and meat. However, for countries such as Benin and Egypt, very few relevant data were available on PAHs contamination in fish and meat products before 2016 (Table4). Most of the reported concentrations were above the EU maximal limit for BaP, and the highest BaP level (288µg/kg) was about one hundred and forty‐four times above this limit, showing that consumers could be highly exposed to PAHs through the consumption of this kind of food.

TABLE 4

Examples of polycyclic aromatic hydrocarbon levels found in smoked or grilled fish and meat products in these past decades

CountryType of foodBenzo(a)pyrene (µg/kg)PAH4 (µg/kg)References
BeninSmoked Scomber Scombrus5.6±2.452.6±20.4Assogba etal.(2021)
Smoked Cypselurus cyanopterus23.0±19.390.1±93.3
Smoked‐dried Cypselurus cyanopterus30.9±16.2153.8±85.8 b
Grilled pork28.9±18.0161.8±87.2Iko Afé etal.(2020)
Smoked fish21.8±21.2119.3±107.5Iko Afé etal.(2021)
Smoked‐dried fish78.5±53.8484.2±305.6
CroatiaSmoked sprat2.2±0.512.5±1.9Racovita etal.(2021)
EgyptGrilled beef meat2.7±0.44.8±0.9Darwish al.(2019
Grilled beef (kebab)9.2‐Eldaly etal.(2016)
Grilled beef (kofta)26‐
EstoniaSmoked meat products3.926.3Rozentale etal.(2018)
FranceSmoked boucané (pork product)6.9±2.4‐Poligné etal.(2001)
GhanaSmoked Atlantic chub mackerel (Scomber colias)15.5±16.6121.6±98.9Asamoah etal.(2021)
Smoked barracuda (Sphyraena Sphyraena)1.3±2.168±32.6
Ivory CostSmoked Cyprinus carpio16.9‐Ake Assi (2012)
Smoked Esox lucius56.5‐
Smoked Pagellus erythrinus36.7‐
Smoked Sarda spp.55.4‐
Smoked Sarpa salpa18.0‐
KoreaCharcoal broiled pork2.6±0.3‐Kim etal.(2014)
KuwaitMeat tikka2.5‐Alomirah etal.(2011)
LatviaSmoked pork35.1‐Stumpe‐Viksna etal.(2008)
Smoked meat products8.153.8Rozentale etal.(2018)
LithuaniaSmoked meat products1.99.5Rozentale etal.(2018)
NigeriaSmoked Arius heude loti5.7‐Ubwa etal.(2015)
Smoked Mud minnow5.4‐
Smoked Scomber scombrus2.4‐Amos‐Tautua etal.(2013)
Smoked Clarias gariepinus204±20‐Tongo etal.,2017; Zachara etal.(2017)
Smoked Ethmalosa fimbriata288±230‐
Smoked Scomber scombrus7±13‐
Smoked Pseudotolithus elongates44‐Akpan etal.(1994)
Smoked Pomadasys perotati25‐
Smoked Heterotis niloticus19.4‐
Grilled suya*10.1‐Akpambang etal.(2009)
Grilled antelope*7.9‐
Smoked Clarias gariepinus*38.0‐
Smoked Selar crumenophthalmus*3.0‐
Smoked Scomber scombrus*6.6‐
Smoked Pseudotolithus senegalensis*21.5‐
PolandSmoked sprat110.3Zachara etal.(2017)
Smoked sausage324.3
Smoked pork hams1.815.5
PortugalChouriço grosso, dry‐cured fermented pork sausages*3.3‐Roseiro etal.(2011)
Grilled Salmon4.7±0.8‐Viegas, Novo, Pinto, etal.(2012)
Chicken8.7±0.3‐
SpainChorizo, Spanish smoked pork meat3.2‐Ledesma etal.(2015)
TurkeyGrilled anchovy fish (Engraulis encrasicolus)0.7±0.043.3±0.1Sahin etal.(2020)
Grilled chicken<LOD (0.05)2.1±0.1

Abbreviations: ‐, data not presented in the cited paper; PAH4, sum of benzo[a]pyrene, chrysene, benzo[b]fluoranthene and benz[a]anthracene.

*Data of this author were presented in dry weight.

3.3. Other hazards in grilled or smoked fish and meat

3.3.1. Heavy metals

Trace elements include environmental contaminants (heavy metals such as cadmium, mercury, and lead) which can have toxic effects on human health (Aina etal.,2012; Ismail etal.,2015) and oligo‐elements (copper, nickel, iron, cobalt, zinc, manganese, etc.) which play important physiological roles when they are at low concentrations. Heavy metals such as cadmium (Cd), mercury (Hg), and lead (Pb) are toxic even at low concentrations (Amos‐Tautua etal.,2013; Daniel etal.,2013; Ersoy etal.,2006; Şireli etal.,2006). Cadmium and arsenic are classified as carcinogenic for humans (Group 1) and lead is classified as possibly carcinogenic for humans (Group 2B) by the IARC (International Agency for Research on Cancer) (2010). Environmental pollution is the main way of food contamination with heavy metals (Costa etal.,2016; EFSA (European Food Safety Authority), 2010). In 2010, the European Food Safety Authority reported that human exposure to lead through diet results in its bioaccumulation responsible for adverse effects on the cardiovascular, renal, endocrine, gastrointestinal, immune, and reproductive systems. The Codex Alimentarius reported that lead was responsible for the low intellectual quotient based on lead exposure studies in children (Codex Alimentarius,2004). European Commission set a maximum limit of 0.1mg/kg for lead in meat (excluding offal) of bovine animals, sheep, pig, and poultry and 0.3mg/kg in muscle of fish (EC (European Commission), 2006). For cadmium, the maximal limit is 0.1mg/kg in muscle of mackerel (Scomber spp.), tuna (Thunnus spp., Katsuwonus pelamis, Euthynnus spp.), and bichique (Sicyopterus lagocephalus), whereas in meat products, the maximal limits range between 0.05 and 1mg/kg, depending on the species and the tissue of the animal.

Several authors reported the presence of trace elements in smoked fish (Anigboro etal.,2011; Ibanga etal.,2019; Inobeme etal.,2018). Şireli etal.(2006) reported the presence of lead (0.01–0.8mg/kg) in vacuum packaged smoked fish marketed on the Ankara market in Turkey (Table5). In that study, 37% of the smoked fish samples were not compliant to the Turkish acceptable limit of 0.2mg/kg. Likewise, Anigboro etal.(2011) reported high levels of lead (13–59mg/kg) in smoked fish samples (Table5) collected from different local markets in Nigeria. Arsenic was found in smoked Dicentrarchus labrax (0.4mg/kg), Scomber scombrus (0.4mg/kg), Clarias gariepinus (0.02mg/kg), and Ethmalosa fimbriata (0.02mg/kg) (Table5). For cadmium, examples of concentration reported from the literature are shown in Table5.

TABLE 5

Mean concentrations of heavy metals in smoked or grilled fish (a) and meat (b) products as reported from the literature

(a)
CountryFish speciesHeavy metals (mg/kg)References
PbCdHgNiAsCr
EgyptCtenopharyngodon idelland0.2nd7.7ndndAbbas etal.(2021)*
IranRutilus frissi0.0030.002ndndnd0.002Mehdipour etal.(2018)*
NigeriaScomber scombrusndndndnd0.400.1Aremu etal.(2014)
Clarias gariepinus0.22.50.0212.80.02ndIbanga etal.(2019)*
Ethmalosa fimbriata0.219.50.0212.40.02nd
Heteroclaria18.71nd123.3nd50.3Anigboro etal.(2011)
Ethmalosa fimbriata21.32.2nd120.7nd54.3
Tilapia guineensis43.7ndnd148.7nd71
PolandHerring0.040.004ndndndndRajkowska‐Myśliwiec etal.(2021)
Sprats0.020.02ndndndnd
SpainSardine0.040.0020.033.3ndPerello etal.(2008)
Hake0.02nd0.21.4nd
Tuna0.030.0020.41.6nd
TurkeyDicentrarchus labrax0.3ndnd0.20.40.05Ersoy etal.(2006)
Salmo salar0.20.02ndndndndŞireli etal.(2006)*
Oncorhynhus mykiss0.10.01ndndndnd
Mackerel0.050.01ndndndnd
Oncorhynhus mykiss0.40.02ndndndnd
(b)
CountryMeat productsHeavy metals (mg/kg)References
PbCdHgNiAsCr
Burkina‐FasoBraised chicken0.20.5ndndNdBazié etal.(2021)
Flamed chicken0.10.2ndndNd
GhanaBush meat3.60.1ndndndndKobia etal.(2016)
SpainVeal steak0.02ndndnd0.2ndPerello etal.(2008)
Loin porkndndndnd0.2nd
Chickenndndndnd0.1nd
Lambndndndnd0.2nd

Abbreviation: nd, not determined.

*Reported data were expressed in dry matter.

Perello etal.(2008) reported the increase of Pb, As, and Hg contents in fish and meat products processed with grilling, frying, boiling, and roasting, compared to the raw products collected from Spain markets (data not shown). Even though an increase of heavy metal levels was recorded after processing in different studies, this increase could be due to the absorption phenomenon or environmental contamination as the culinary practices were not carried out in controlled close space. It could also be a concentration of the contaminants due to water loss during smoking and drying.

Heavy metal concentrations can be measured by a graphite furnace atomic absorption spectrometer (GFAAS) or an atomic absorption spectrophotometer (Anigboro etal.,2011; Şireli etal.,2006). They could also be determined using atomic absorption spectrometry after microwave digestion and inductively coupled plasma mass spectrometry (ICP/MS) (Kabir etal.,2011; Uluozlu etal.,2009). The studies on the occurrence of heavy metals in smoked or grilled fish and meat reported in this section were mainly from Africa. Indeed, although some studies were from Turkey (Ersoy etal.,2006; Şireli etal.,2006), Spain (Perello etal.,2008) and Poland (Rajkowska‐Myśliwiec etal.,2021), the majority of them were from Nigeria (Amos‐Tautua etal.,2013; Anigboro etal.,2011; Aremu etal.,2014; Daniel etal.,2013; Ersoy etal.,2006; Ibanga etal.,2019) and other African countries such as Egypt (Abbas etal.,2021), Ghana (Kobia etal.,2016) and Burkina Faso (Bazié etal.,2021). Heavy metals contamination data (Table5) showed that before 2015 (2006–2014) many studies from different countries especially Turkey and Nigeria were carried out on the occurrence of these environmental contaminants in smoked or grilled fish and meat. From 2015 to 2021, additional studies from Nigeria were carried out again on these compounds showing the necessity to update contamination data in smoked or grilled fish and meat. However, for other countries such as Burkina‐Faso or Egypt, very few relevant data were available on heavy metals contamination in smoked or grilled fish and meat before 2015 (Table5).

3.3.2. Biogenic amines

Biogenic amines are found in protein‐rich foods such as fish and meat products (Chong etal.,2011; Latorre‐Moratalla etal.,2017; Sagratini etal.,2012). Despite the important role of some biogenic amines in human and animal physiology, the consumption of a high amount of these amines can result in food intoxication (EFSA (European Food Safety Authority), 2011; Lehane & Olley,2000). They are usually produced from decarboxylation of free amino acids by bacterial enzymes (Table6), before or after processing. They are also heat resistant, so not destroyed by the cooking practices. Among biogenic amines, histamine received particular attention due to its toxicity. Several authors reported histamine as responsible for foodborne intoxication in reference to scombroid fish poisoning (EFSA (European Food Safety Authority), 2011; Latorre‐Moratalla etal.,2017). Intoxication with histamine is associated with symptoms such as hypertension, headache, and allergy reactions including reddening on the face, neck and upper chest, vomiting, sweating, nausea, abdominal cramps, diarrhea, rash, dizziness, palpitations, spasm of bronchi, and flushing (Hassan, El‐ Shater, & Waly, 2017; Marissiaux etal.,2018; da Silva, Pinho, Ferreira, Plestilova, & Gibbs, 2002; Zaman etal.,2010). Several papers reported biogenic amines in smoked fish and grilled meat products (Douny etal.,2019; Köse etal.,2012; Ntzimani etal.,2008; Simunovic et al., 2019). The histamine concentrations reported by several authors in these kinds of food are summarized in Table7. The presence of histamine was reported in smoked salmon at levels ranging between 2.5 and 171mg/kg, in smoked Sardinella sp. (18mg/kg), and in hot smoked bonito (98.7±0.6mg/kg) (Table7). The presence of histamine was also reported in grilled pork (<11.2–81.5mg/kg) and in smoked turkey (32.9±1.4mg/kg) (Table7).

TABLE 6

Structure, precursors, and microorganisms producing decarboxylase of some biogenic amines

Amino acid precursorsBiogenic amineChemical structure and formulaMain microorganisms producing amino acid decarboxylase
HistidineHistamineChemical hazards in smoked meat and fish (8)C5H9N3

Hafnia alvei, Morganella morganii, Klebsiella pneumonia, Morganella psychrotolerans,

Photobacterium phosphoreum,

Photobacterium psychrotolerans

TryptophanTryptamineChemical hazards in smoked meat and fish (9)C10H12N2‐
TyrosineTyramineChemical hazards in smoked meat and fish (10)C8H11NO

Enterococcus (Ent. faecalis, Ent. faecium)

Lactobacillus (Lact. curvatus; Lact. brevis)

Leuconostoc spp, Carnobacterium spp

Staphylococcus spp

Phenylalanine2‐Phenylethylamine

Chemical hazards in smoked meat and fish (11)C8H11N

Enterococcus,

Lactobacillus curvatus,

Staphylococcus (S. carnosus)

HydroxytryptophanSerotoninend‐
LysineCadavérineChemical hazards in smoked meat and fish (12)NH2(CH2)5NH2

Enterobacteriaceae (Citrobacter, Klebsiella, Escherichia, Proteus, Salmonella et Shigella)

Pseudomonadaceae, Shewanellaceae

Ornithine; argininePutrescineChemical hazards in smoked meat and fish (13)NH2(CH2)4NH2

Enterobacteriaceae (Citrobacter, Klebsiella, Escherichia, Proteus, Salmonella et Shigella)

Pseudomonadaceae, Shewanellaceae

Ornithine; arginineSpermineChemical hazards in smoked meat and fish (14)C10H26N4‐
Ornithine; arginineSpermidineChemical hazards in smoked meat and fish (15)C7H19N3‐

Source: Santos (1996); Kim etal.(2002), Onal (2007); EFSA (2011); Tosukhowong etal.(2011); Ali etal.(2016).

TABLE 7

Histamine levels in smoked or grilled fish and meat products

ProductConcentration (mg/kg)Analytical methodReferences
Smoked salmon2.5–171Extraction with Trichloroacetic acid; LC‐MS/MSSimunovic et al. (2019)
Smoked Sardinella sp.18

Extraction trichloroacetic acid

ion‐exchange chromatography

Plahar etal.(1999)
Cold‐smoked salmon30.9±0.4

Extraction with perchloric acid

high‐performance liquid chromatography with a diode array detector

Köse etal.(2012)
Hot‐smoked Bonito (Tuna fish)98.7±0.6
Grilled tuna4,400Not mentionedMarissiaux etal.(2018)
Smoked fish from different species11–63Quantification colorimetrically at 495nm using a spectrophotometer.CSIR (2017)
Smoked turkey breast fillets stored at 4°C after 30days32.9±1.4

Extraction trichloroacetic acid

With liquid chromatography. Quantification was performed coupled with a UV detector

Ntzimani etal.(2008)
Grilled pork<11.2–81.5Extraction with perchloric acid and injection on UPLC coupled with a fluorescence detectorDouny etal.(2019)

European Commission set maximal limits for histamine (100–200mg/kg) in fish and fishery products from fish species associated with a high amount of histidine (EC (European Commission), 2005). No maximal limit of histamine is available for meat products. However, several authors reported the use of biogenic index (sum of putrescine, tyramine, cadaverine, and histamine levels) to assess the freshness and quality of pork (Cheng etal.,2016; Douny etal.,2019).

The highest histamine concentration in fish reported in this review was 44 times over the authorized European limit and resulted in histamine fish poisoning (HFP) (Marissiaux etal.,2018). Similar concentration (4,384.2mg/kg) was also reported in smoked‐dried fish from Benin (Table8). Regarding the geographical location, the selected paper reported in the Tables7 and ​and88 was from America (5%), Asia (20%), Africa (30%), and Europe (45%). Although several studies dealt with the production of biogenic amines in fish, very few studies were available about grilled and/or smoked fish and meat products. From 2015 to 2021, studies dealing with biogenic amines in grilled or smoked fish and meat mainly focused on their occurrence (Tables7 and ​and88).

TABLE 8

Mean (maximum) concentrations of histamine and tyramine in fish (a) and meat products (b) from different countries

(a)
CountryType of foodHistamine (mg/kg)Tyramine (mg/kg)References
AustriaSmoked tuna

  • ‐

    (63)

‐Rauscher‐Gabernig etal.(2009)
Smoked mackerel

  • ‐

    (219)

‐
Smoked salmon

  • ‐

    (165)

‐
BelgiumGrilled tuna fish

  • ‐

    (4,400)

‐Marissiaux etal.(2018)
BeninSmoked Cypselurus cyanopterus471.7 (1,139.4)810.9 (1766.5)Assogba etal.(2021)
Smoked‐dried Cypselurus cyanopterus754.3 (2,255.1)19.1 (20.6)
Smoked fish<10 (1,511.3)151.9 (700.9)Iko Afé etal.(2021)
Smoked‐dried fish1,340.2 (4,384.2)33.1 (45.8)
CambodiaSmoked fish16.6 (24.2)9.9 (38.4)Douny etal.(2021)
DenmarkCold‐smoked tuna4,548 (‐)150 (‐)Emborg and Dalgaard (2006)
(b)
CountryType of foodHistamine (mg/kg)Tyramine (mg/kg)References
BeninGrilled pork59.7 (86.4)2 (3.8)Douny etal.(2019)
EgyptBeef shawarma80.2 (30)‐Sallam etal.(2021)
Chicken shawarma103 (36)‐
SpainDry fermented sausages27 (475)139 (742)Latorre‐Moratalla etal.(2017)

Abbreviation: ‐, data not presented in the cited paper.

*Numbers in parentheses represent the maximum value.

3.4. Risk assessment

3.4.1. Risk assessment methodology applicable to toxic compounds

The risk assessment is part of the risk analysis concept, which, as reported by Larsen (2006), includes risk assessment, risk evaluation, and risk communication. These three elements are separate tasks, performed by different actors, but should be part of an interactive process (Larsen,2006; Stadler & Lineback,2009). Risk assessment is a scientific process used to quantify the risk linked to a hazard and requires expertise in toxicology and nutrition (for the intake assessment). It is used to determine whether a particular chemical poses a significant risk to human health (FASFC (Federal Agency for the Safety of the Food Chain), 2005; Larsen,2006; Reinik,2007; Stadler & Lineback,2009; Scholl etal.,2012). Risk assessment follows four steps (EFSA (European Food Safety Authority), 2008; FASFC (Federal Agency for the Safety of the Food Chain), 2005; FASFC (Federal Agency for the Safety of the Food Chain), 2006; Larsen,2006) which are as follows:

Hazard identification: It will indicate which dangers can be associated with the consumption of a specific foodstuff and what harmful effects they can cause for consumers.

Hazard characterization: This step aims to describe and evaluate the dose–response relationship, the mode of action, including dynamic and kinetic aspects, and how to establish an acceptable daily intake (ADI) or a tolerable daily intake (TDI) using a safety factor to consider for the intra‐ and inter‐species variation.

Exposure assessment: To assess the exposure, consumption data and contamination data are needed to calculate the estimated daily intake (EDI) by multiplying the concentration of hazard by the daily consumption of food contaminated with this hazard. EDI can be calculated for several categories of population (i.e., babies, children, teenager, and adults). EDI can be calculated either following a deterministic approach using median, mean, or maximum of consumption or contamination data, or following a probabilistic approach using distributions of consumption and contamination data.

Risk characterization: This step consists of comparing the calculated EDI with a toxicological reference dose (classical way) which can be a tolerable daily intake (TDI) or an acceptable daily intake (ADI). For carcinogenic compounds such as PAHs, the margin of exposure (MoE) suggested by EFSA (European Food Safety Authority) (2005) and Constable and Barlow (2009) is used. MOE is calculated as follows:

MOE=BMDL10(mgperkgbwperday)EDI(mgperkgbwperday),

where BMDL10 is the 95% lower confidence limit of the benchmark dose causing 10% extra risk of cancer in laboratory animals (in case of PAHs, of rat hepatocellular adenomas, and carcinoma), and EDI is the estimated daily intake. For carcinogenic compounds such as PAHs, the risk may be considered as negligible or very low only when MOE is above 10,000.

3.4.2. Examples reported from the literature of risk assessment for some chemical hazards (PAHs, heavy metals, and biogenic amines)

Examples of risk assessments related to PAH ingestion through consumption of grilled and/or smoked fish and meat (Table9) pointed out a health concern for consumers of several countries such as Cambodia (Douny etal.,2021), Benin (Iko Afé etal.,2020, 2021), Turkey (Sahin etal.,2020), Nigeria (Akpambang etal.,2009), and Latvia (Rozentale etal.,2018). Before 2015, the mean values of MoE associated with the consumption of smoked or grilled fish (Table9a) and meat products (Table9b) contaminated with PAHs including BaP and PAH4 were globally above 10,000, showing a very low concern for the consumers of these products. After 2015, the studies reported showed MoE globally below 10,000 for consumers of smoked or grilled fish and meat products from different countries such as Benin, Cambodia, Turkey, and Latvia (Table9). MOE below 10,000 indicates a high concern (risk of cancer) for consumers for carcinogenic compounds such as PAHs.

TABLE 9

Estimated daily intakes (EDI) and margin of exposure (MOE) for polycyclic aromatic hydrocarbons (PAH) through consumption of smoked or grilled fish (a) and meat (b) products, in different countries

(a)
CountryType of foodEstimated daily intake (ng/kg bw/day)Margin of exposureReferences
BeninSmoked fishBaP: 2.3‐809.9BaP: 30,978‐86Iko Afé etal.(2021)
PAH4: 12.0‐4,314.9PAH4: 28,241‐79
Smoked‐dried fishBaP: 2.5‐1,974.8BaP: 27,718‐35
PAH4: 17.4‐13,627.2PAH4: 19,510‐25
CambodiaSmoked fishBaP: 1,407BaP: 50Douny etal.(2021)
PAH4: 5,773PAH4: 59
ChinaGrilled fishBaP: 0.2BaP: 333,000Wang etal.(2021)
PAH4: 1.0PAH4: 336,000
CroatiaShellfish productsBaP: ‐BaP: 1,643,906Bogdanovic etal.(2019)
PAH4: ‐PAH4: 298,900
NigeriaSmoked fishBaP: 4‐52BaP: 17,722‐1,346Akpambang etal.(2009)
PAH4: ‐PAH4: ‐
TurkeyGrilled fishBaP: 0.2BaP: 389Sahin etal.(2020)
PAH4: 0.8PAH4: 425
(b)
CountryType of foodEstimated daily intake (ng/kg bw/day)Margin of exposureReferences
BeninGrilled porkBaP: 07‐235.7BaP: 96,871‐297Iko Afé etal.(2020)
PAH4: 4.1‐1,321.3PAH4: 83,925‐257
ChinaGrilled meatBaP: 0.5BaP: ‐Jiang etal.(2018)
PAH4: 4.0PAH4: ‐
CroatiaSmoked meat productsBaP: ‐BaP: 280,657Bogdanovic etal.(2019)
PAH4: ‐PAH4: 66,213
DenmarkHome grilled meat (beef, pork, and chicken)BaP: ‐BaP: ‐Duedahl‐Olesen etal.(2015)
PAH4: 10PAH4: 33,800
EgyptGrilled beef meatBaP: 290.5BaP: ‐Darwish al.(2019
PAH4: ‐PAH4: ‐
FranceFoodstuffs (28 different foods)BaP: 0.2BaP: ‐Veyrand etal.(2013)
PAH4: 1.5PAH4: 230,000
Korea

Smoked meat products

(bacon, chicken, duck, pork, salmon, tuna, and turkey).

BaP: 0.014BaP: 666,667Kim etal.(2014)
PAH4: 0.038PAH4: 265,957
KuwaitGrilled chickenBaP: 15.6BaP: ‐Alomirah etal.(2011)
PAH4: ‐PAH4: ‐
LatviaSmoked meat productsBaP: 5.4BaP: 12,952Rozentale etal.(2018)
PAH4: 35.9PAH4: 9,475
Smoked meat (pork, pork breast, chop, speck, ham, and chicken) and meat products (sausages, small sausages, semi‐dry sausages, and roulette)BaP: 2.3BaP: 30,606Rozentale etal.(2015)
PAH4: 13.7PAH4: 24,776
NigeriaGrilled meatBaP: 10.5‐14.0BaP: 5,015‐6,652Akpambang etal.(2009)
PAH4: ‐PAH4: ‐
TurkeyGrilled chickenBaP: ‐BaP: ‐Sahin etal.(2020)
PAH4: 1.8PAH4: 190

Abbreviations: ‐, data not presented in the cited paper; PAH4, sum of benzo[a]pyrene, chrysene, benzo[b]fluoranthene, and benz[a]anthracene; bw, body weight.

Regarding consumers exposure to heavy metals from consumption of smoked or grilled fish and meat products, very few data were available from the literature. Recently, two papers have been published on exposure of consumers from Burkina‐Faso (Bazié etal.,2021) and Poland (Rajkowska‐Myśliwiec etal.,2021).

The cancer risk index linked to lead exposure calculated for consumers of braised and flamed chicken processed in Burkina Faso ranged between 7×10−7 and 3×10−6 (Table10). None of the index risk values was above the threshold set by US‐EPA (IR>10−4). Similar to the cancer risk index, a noncancer risk index was calculated using the median consumption level of braised and flamed chicken. This Hazard Index (HI), which is the sum of individual metal hazard (Ag, Cd, Pb, Zn, Ni, Co, Fe, Mn, Cu, and Cr) quotients, ranged between 0.07 and 0.15. These values were below the reference value (HI=1) (Hough etal.,2004) showing also the absence of noncancer risk linked to heavy metals exposure for Burkina‐Faso consumers of braised and flamed chicken (Bazié etal.,2021). However, the HI (sum of hazard quotient of Zn, Fe, Mn, Cu, Al, Pb, and Cd) calculated for polish consumers was 1.4 (Table10), so above the reference value of 1. The HI obtained for polish consumers was similar to HI values reported for Ugandan consumers of heat‐processed meat which ranged from 1.2 to 1.9 for different types of meats (Table10).

TABLE 10

Cancer and noncancer risks related to heavy metals through consumption of smoked or grilled fish and meat products reported from the literature

CountryType of foodNoncancer risk: Hazard index (HI)Cancer index risk (IR)References
Burkina‐FasoFlamed chicken0.2Pb: 7×10−7 to 3×10−6Bazié etal.(2021)
Braised chicken0.1Pb: 7×10−7 to 3×10−6
PolandSmoked fish1.4‐Rajkowska‐Myśliwiec etal.(2021)
UgandaRoasted pork1.7Pb: 4.5×10–5Bamuwamye etal.(2015)
Cd: 1.0×10–3
As: 7.4×10–5
Roasted beef1.7Pb: 3.92×10–5
Cd: 6.30×10–4
As: 2.00×10–4
Roasted goat1.2Pb: 2.95×10–6
Cd: 2.60×10–3
As: 9.94×10–5
Roasted chicken1.9Pb: 2.50×10–5
Cd: 2.00×10–3
As: 3.00×10–4

Abbreviation: ‐, data not presented in the cited paper.

Among biogenic amines, histamine and tyramine are two dietary biogenic amines which are present in food are undesirable due to their adverse effects on consumer's health such as hypertension, headache, and allergic reactions (EFSA,2011; Marissiaux etal.,2018). To our best knowledge, there are few relevant studies showing the exposure to histamine or tyramine for consumers of smoked or grilled fish and meat products. Four studies dealing with histamine exposure were reported in Table11. These four studies were published during the period of 2017–2021. The mean histamine intake calculated from the consumption of smoked fish and smoked‐dried fish marketed in Benin was 146mg/meal and 116mg/meal, respectively, whereas the acute reference dose (ARfD) of histamine suggested by the European Food Safety Authority (EFSA) is 50mg histamine/meal (EFSA,2011). In Spain, Cambodia, and Egypt, the mean histamine exposure (Table11) was well below this ARfD. Based on the limited published data, no adverse health effects have been observed in healthy volunteers exposed to a level of 25–50mg of histamine per person per meal (EFSA,2011). The mean histamine exposure reported in Table11 revealed a health concern for Beninese consumers of smoked fish and smoked‐dried fish (Iko Afé etal.,2021). Although the mean histamine exposure reported for consumers of Cambodia, Spain, and Egypt showed an absence of intoxication risk, there is risk of histamine poisoning in case of extreme consumption of smoked or grilled fish and meat products during the same meal or for sensitive consumers.

TABLE 11

Histamine and tyramine exposure from consumption of fish and meat products

CountryType of foodHistamine exposure (mg/meal)Tyramine exposure (mg/meal)References
BeninSmoked fish145.6 (1,019.1)*‐Iko Afé etal.(2021)
Smoked‐dried fish115.9 (1,236.2)‐
CambodiaSmoked fish<50 (‐)‐Douny etal.(2021)
EgyptBeef shawarma16.0‐Sallam etal.(2021)
Chicken shawarma31‐
SpainDry fermented sausages1.4 (45.8)6.2 (92.5)Latorre‐Moratalla etal.(2017)

Abbreviation: ‐, data not presented in the cited paper.

*Numbers in parentheses represent the maximum value.

4. CONCLUSION

Smoked fish and meat products may be contaminated by various toxic compounds including carcinogenic compounds. Most of the chemical hazards reported in this review are processing contaminants. Some of them can be formed when high temperature is reached inside the product (heterocyclic amines and nitrosamines) and others during pyrolysis of the fuel during processing (PAHs). Biogenic amines are not related to the smoking process but can be present in raw or smoked fish due to decarboxylation of free amino acids occurring after microbial contamination. In case of heavy metals, they are environmental pollutants found in raw and processed food. In traditionally smoked fish or grilled meat, most of the chemical hazards mentioned in this review exceed the maximal limits established by EU. Several actions should be addressed to decrease them in smoked fish and meat as they are highly consumed products.

CONFLICT OF INTEREST

The authors have no conflicts of interest to declare.

ETHICAL APPROVAL

This study does not involve any human or animal testing.

ACKNOWLEDGMENTS

This work was fully supported by QualiSani project through ARES CCD (Académie de Recherche et d'Enseignement Supérieur, Commission de la Coopération au Développement).

Notes

Iko Afé, O. H., Kpoclou, Y. E., Douny, C., Anihouvi, V. B., Igout, A., Mahillon, J., Hounhouigan, D. J., & Scippo, M.‐L. (2021). Chemical hazards in smoked meat and fish. Food Science & Nutrition, 9, 6903–6922. 10.1002/fsn3.2633 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

DATA AVAILABILITY STATEMENT

All the data used in this study can be made available upon reasonable request.

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