D0006NF
D0006NF
net
1
Department for Management of Science and Technology Development, Ton Duc Thang University, Ho Chi Minh City,
Vietnam; 2Faculty of Environment and Labour Safety, Ton Duc Thang University, Ho Chi Minh City, Vietnam
Abstract: Objective: Polycyclic aromatic hydrocarbons (PAHs) are well researched chemicals in
foods that have been found to exhibit mutagenic and carcinogenic potentials. This study examined
available literature on polycyclic aromatic hydrocarbons in foods, sources, effects and remediation.
Method: Available literature on polycyclic aromatic hydrocarbons in foods, sources, effects and
remediation was critically reviewed.
Results: The review showed that carcinogenicity of PAHs varies from the potent to moderately
Current Nutrition & Food Science
1. INTRODUCTION very low aqueous solubility [2, 3]. It has been found that
their vapour pressure and aqueous solubility tend to decrease
Polycyclic aromatic hydrocarbons (PAHs) are groups of
with increasing molecular weight, while their resistance to
hydrocarbons which consist of compounds with a certain
oxidation and reduction increases [2, 3]. Most of PAHs have
number of aromatic rings joined by two or more carbon at-
been found to be very soluble in organic solvents and also
oms [1]. They are widely studied organic compounds includ-
they exhibit high lipophilic characteristics. Other characteris-
ing benzo[a]pyrene. They have been found to be mutagenic
tics of PAHs include light sensitivity, heat resistance, and
and carcinogenic in laboratory animals. Several PAHs have
conductivity; emit ability, corrosion resistance, and physio-
been detected but only a few of them, typically between 14
logical action [2, 3].
and 20 individual PAH compounds are of significant im-
portance due to their carcinogenicity [1]. Several researchers have reported that PAHs could be
formed during the combustion of coal, mineral oil, and oil
PAHs are characterized by high melting and boiling
shale and other organic matter. However, the consumption of
points and are mostly solid, with low vapour pressure, and
smoked and charred foods, well cooked meat and fish prod-
ucts prepared on open flame remains a major source of
*Address correspondence to this author at the Department for Management PAHs to consumers. Several studies have revealed that many
of Science and Technology Development, Ton Duc Thang University, Ho
Chi Minh City, Vietnam and Faculty of Environment and Labour Safety,
PAHs are carcinogenic in animal studies, and PAH exposure
Ton Duc Thang University, Ho Chi Minh City, Vietnam; in humans has been associated with lung, skin, stomach and
Tel: +2347067004902; E-mail: samuel.adeyeye@tdtu.edu.vn urinary cancers and so on. The carcinogenic potential of
PAHs varies and could range from potent to moderately car- composition under intense heat and low oxygen resulting in
cinogenic or mutagenic. Potent to moderately carcinogenic the formation of low molecular weight fat intermediate.
PAHs include 3-methylcholanthrene, B[a]P, dibenz[a,h] Pyrogenic PAHs are found in large proportions in grilled,
anthracene, 5-methylchrysene, and dibenz[a,j]anthracene, smoked and barbecued meat and fish products (Fig. 1)
whereas benzo[e]pyrene, dibenz[a,c]anthracene, chrysene, [4, 5, 15].
benzo[c]phenanthrene and fluoranthene are relatively weak Biological PAHs are formed as a result of bio-synthesis
or inactive carcinogens [3]. However, because humans are by certain plants and bacteria or during the degradation of
exposed to mixtures of PAHs that are produced during com- vegetative matter as a result of decomposition. According to
bustion, smoked fish and meat, the carcinogenic potential of Zelinkova and Wenzl [15] this type of PAHs formation could
PAHs is due to combined effects of several exposure scena- be natural or anthropogenic.
rios and is highly variable because of a mixture of PAHs that
are involved [3-5]. It has been found that a high amount of PAH compounds
are emitted from processing coal, during incomplete com-
In the last few decades, several researchers have carried bustion of organic matter as well as from motor vehicle ex-
out studies on PAHs in foods because of their carcinogenic haust and cigarettes. Howsam and Jones [3] also observed
and mutagenic properties [5, 6]. It has been observed that the that forest fires, volcanoes and hydrothermal processes are
presence of PAHs in foods could be from natural sources or also natural emission sources of PAHs that could contami-
as a result of environmental contamination for example nate foods of plant or animal origin. Cooke [16] stated that
deposition of air particulates on vegetables, foods or intake PAH contamination of vegetation from industrial areas is
of contaminated water by fish. PAHs have been found in higher than in rural areas.
food through cooking, grilling and frying; traditional curing
and drying have also been found to be a contributing factor Food contaminations with environmental PAHs have
[7] along with packaging materials treated with contaminated been found to be dependent on physical and chemical
mineral oils [8]. properties of the concerned PAHs [17, 18]. Phillips [14]
stated that the concentrations of PAHs in plant foods are
Tamakawa [7] and Moret and Conte [9] have reported the higher on the plant surface (outer leaves, peel) than in inter-
presence of PAHs in edible oils and fats and attributed this to nal tissue. Oil spillage has been identified as a major source
contamination by environmental pollution and/or during pro- of seafood and fish contamination with PAHs. Harvey [2]
cessing steps preceding refining. While Moreda et al. [10] and Afolabi et al. [19] reported that contamination of PAHs
reported that the processes of decolorization and deodoriza- and the PAH content in aquatic organisms is influenced by
tion with activated carbon, charcoal and clay could signifi- their ability to metabolize them. They were of the opinion
cantly reduce PAH levels in vegetable oil. that bivalve mollusks have the ability to filter large volumes
Ravindra et al. [11], Ramesh et al. [12] and Choi et al. of water and but could not metabolize high molecular mass
[13] have reported that human exposure to PAHs varies and PAHs thus, efficiently stored more PAHs.
depends on factors such as smoking rates, fuel types in cook- Several authors [4, 19-23] have established that pro-
ing, and pollution controls on power plants, industrial pro- cessing of food such as drying, smoking, baking and cooking
cesses, and vehicles. They also observed that developed at high temperatures has been found to be the major sources
countries have lower levels of PAH exposure as a result of of food contamination by PAHs. Moreda et al. [10] reported
stricter air and water pollution controls, cleaner sources of that the seed oils and raw products for vegetable oil produc-
cooking, and prohibitions of public smoking while develop- tion may be contaminated with PAHs through artificial dry-
ing and undeveloped countries tend to have higher levels as ing and heating during processing, especially if care was not
aresult of poor pollution control. taken such as indirect drying and good temperature control.
Philip [14] discovered that the major source of PAHs ex- Moreda et al. [10] also reported that drying of seeds and ker-
posure is through diet particularly from smoking or grilling nels is thought to be one of the prominent sources for the
meat. He observed that people also consume PAHs from contamination of edible vegetable oils with PAHs.
especially broad-leafed vegetables. However, Choi et al. [13] Simko [24] reported that industrial smoking of meat and
reported that PAHs are consumed at low concentrations in dairy products without precautionary measures is the major
drinking water. source of food contamination with PAHs. He suggested that
This study reviewed and examined polycyclic aromatic the PAH contamination of smoked foods can be significantly
hydrocarbons in food: sources, detection and health implica- reduced by preventing foods from having direct contact with
tions to the consumers. smoke. Houessou et al. [25] and Pincemaille et al. [26] have
also suggested that roasting and drying processes of coffee
2. SOURCES OF POLYCYCLIC AROMATIC HYDRO- beans, cocoa beans and tea leaves are the major sources of
CARBONS IN FOODS PAH contamination.
Foods have been found to be contaminated with PAHs
3. OCCURRENCE OF PAHS IN FOODS
from different sources such as air, soil, or water, or during
food processing and cooking. Foods for human consumption Foods are identified as an important pathway for human
could also be contaminated through pyrogenic and biological exposure to PAHs. Scientific Committee on Food (SCF)
processes. Pyrogenic PAHs are formed as a result of fat de- [27], Mastral and Callén [1] and Edwards [17] studied the
868 Current Nutrition & Food Science, 2020, Vol. 16, No. 6 Samuel A.O. Adeyeye
Fig. (1). Sources of PAH compounds.
contributions of food consumption to the total intake of meat or fish near the fireplace for several days. It was also
PAHs in some countries of Europe. They discovered that discovered that, “commercial smoked cheese is of lower
food consumption was shown to be the main source of PAH contamination (sum of PAHs 2.3-57 μg/kg) than the tradi-
intake and thus stated the need for research on PAHs in food tionally “home-made” cheese (sum of PAHs 73-114 μg/kg)”
and the development of appropriate strategies to mitigate or [28-31]. “Higher contamination of traditional cheese with
reduce their contents in foods. PAHs was observed as a result of solid particles from the
smoke”. This has been found to be greatly reduced by the
Several authors [3, 8] have reported the presence of
use of purified smoke generated in industrial smoking pro-
PAHs in fats and oils such as sunflower, olive, soybean,
palm, and rapeseed oils. They were of the opinion that PAHs cesses according to Tamakawa [7] as this allows only
flavouring compound to reach the products while most of the
contamination of fats and oils occurred during heating pro-
hazardous compounds of wood pyrolysis are removed
cesses or extraction with organic solvents or through air or
through the purification process.
contact with smoke from fuel combustion. Howsam and
Jones [3] and Moffat and Whittle [8] reported the use of ac- Zelinkova and Wenzl [15] and Simko [24] studied the ef-
tive carbon or steam distillation processes to remove PAHs fects of frying, grilling, roasting, toasting, and barbecuing on
from fats and oils. Moret and Conte [9] reported that the sausages, beef, burgers, chicken, and lamb. Their studies
content of benzo[a]pyrene in vegetable oils is very low and revealed that barbecued beef burgers contained the highest
usually below 2 μg/kg. levels of PAHs, with up to 29 μg/kg benzo[a]pyrene concen-
It has been reported by Zelinkova and Wenzl [15] that trations. They also discovered that distance between foods
meat or fish products exposed to direct smoke result in higher and sources of fire affect the level of PAHs in barbecued or
PAH contents when compared to indirect smoking methods. smoked foods. Simko [24] observed that differences in the
They also observed that hot smoking has been found to result surface area, the surface texture and the manner in which fat
in higher PAH levels than cold smoking. It has also been is lost during cooking affect PAH levels.
well established that smoking, if precautionary steps are not
Several researchers [15, 25, 26] have worked on roasting
taken, could lead to the formation of higher levels of PAHs
of coffee. The outcome of research showed that the presence
of low molecular weight in smoked food products [15].
of PAHs may be attributed to the formation of PAHs to the
Smoking meat or fish in the smoldering fire has been found
roasting process. They discovered that the common PAH
to give the highest levels of low molecular weight PAHs
compounds in roasted coffee arephenanthrene, fluoranthene,
while the use of liquid smoke gives the lowest levels of low and pyrene with concentrations in the range 3-50 μg/kg.
molecular weight PAHs in smoked foods [15].
Houessou et al. [25] discovered that benz[a]anthracene and
Several researchers [4-6, 23, 24] have reported higher chrysene were the most abundant in roasted coffee with con-
levels of low molecular weight PAHs in products, where centrations near 13 μg/kg for both compounds. However,
smoking was carried out in a traditional way, putting the Zelinkova and Wenzl [15], Houessou et al. [25], and Pince
Polycyclic Aromatic Hydrocarbons in Foods: A Critical Review Current Nutrition & Food Science, 2020, Vol. 16, No. 6 869
Phenanthrene Pyrene Benzo[a]pyrene
maille et al. [26] have reported Benzo[a]pyrene in Several researchers [15, 32-35] have found that cereals
commercially ground and instant coffees in the range from and cereal-based products are the main sources of human
<0.01 μg/kg to 1.2 μg/kg. exposure to PAHs due to the high amounts consumed. Con-
Pincemaille et al. [26] detected a wide variety of PAHs in tamination of bread by PAHs according to Ciecierska and
tea leaves, particularly in smoked and non-smoked leaves. Obiedziński [32] may be attributed to the contamination of
They also found that benzo[a]pyrene (Fig. 2) in non-smoked bakery raw materials, especially flour, and the baking pro-
tea leaves ranges from 0.6 μg/kg to 5.6 μg/kg and in smoked cess. However, benzo[a]anthracene, chrysene, benzo[b]
leaves from 2.8 μg/kg to 21.9 μg/kg. fluoranthene, and benzo[k]fluoranthene were reported at low
Contamination of vegetables with PAHs has been found levels by Ciecierska and Obiedziński [32]. They detected
to be through gas and particle deposition, and uptake from benzo[a]pyrene only in the crust of wholemeal rye bread at
soil [27, 28]. the baking temperature of 260°C.
Borokovcova et al. [31] and Davídek [22] in their study
showed that the common PAHs in vegetables are PAHs with 4. DETECTION OF POLYCYCLIC AROMATIC
two and three rings. They also found a higher accumulation HYDROCARBONS IN FOODS
of these PAHs on the large surface area of vegetable leaves. Collaborative studies on the Association of Official Ana-
They discovered that vegetables that were grown in highly lytical Chemists (AOAC) and International Union of Pure
industrialized areas or near roadways or irrigated with
and Applied Chemistry (IUPAC) led to the release of the
wastewater generally showed higher levels of PAHs when
first official method for the analysis of benzo[a]pyrene in
compared with those grown in rural areas. Zelinkova and
Wenzl [15], Howsam and Jones [3] observed that vegetables food products such as smoked foods, meat, cheese, total diet
grown at the vicinity of a power plant site in India had composites and beverages. This method uses ultraviolet
significantly more PAHs when compared to vegetables spectrophotometry confirmed by spectrophotofluorometry to
grown in an environment far away from a power plant. The detect benzo[a]pyrene or general PAHs in different food
common PAHs found in vegetables from this site were products. However, the method was released by AOAC in
acenaphthene, fluoranthene, fluorene, and pyrene according 1972 as its official first method and recommended by
to Zelinkova and Wenzl [15] and Howsam and Jones [3]. IUPAC in 1975 [35].
870 Current Nutrition & Food Science, 2020, Vol. 16, No. 6 Samuel A.O. Adeyeye
In 1998, a standard technique to determine benzo[a] to the health and the well-being of humans. Among these
pyrene in animal and vegetable fats and oils was released by PAHs is benzo[a]pyrene which serves as a biomarker for the
International Organization for Standardization (ISO/IEC presence of carcinogenic PAHs in processed foods.
17025) [36] The technique uses reverse phase HPLC-
fluorescence detection (FLD) after clean-up on alumina. 6. REGULATORY LIMITS IN FOOD
However, the technique has been revised (ISO 2007:15302)
Regulating PAHs in processed foods has received
[35, 36].
attention that it deserves by numerous organizations such as
Several other methods of analysis like ISO 2009:22959 the USEPA), IACR, SCF, the Joint FAO/WHO Expert
[37] have been released and used in the determination of Committee on Food Additives (JECFA), the International
PAHs in edible fats and oils. This could be used in determin- Programme on Chemical Safety (IPCS), and the (EFSA).
ing total 17 PAHs (including 14 EPA PAHs) by on-line cou- This could be observed in the following examples based on
pling of donor-acceptor complex chromatography to re- legislation on PAHs in foods from different countries. How-
versed phase HPLC-FLD (ISO 2009:22959) [38]. ever, the list of these countries and the legislation is not ex-
Another method, gas chromatography coupled to mass haustive [46].
spectrometry (GC-MS) was published in 2004 (PD ISO/TR The U.S. Federal Government has set up several regula-
24054) [38]. GC-MS is being used on animal and vegetable tory standards and guidelines to protect people from the pos-
fats and oils and is able to determine up to 27 PAHs (PD sible health effects caused by eating, drinking, or breathing
ISO/TR 24054) [39]. PAHs. Several legislations like Safe Drinking Water Act,
In recent time, HPLC-FLD and GC-MS are the two main USEPA has set legal maximum limits on the level of
instrumental analysis techniques used in determining PAHs benzo[a]pyrene in drinking water to be 0.2 μg/L. Likewise,
in foods. Mass spectrometric methods are commonly used NIOSH and OSHA have set the maximum limit of a legally
because of the high selectivity of their detectors, enabling the enforceable exposure limit of 0.2 mg/m3 air averaged over an
confirmation of analyte identity based on the mass spectrum 8-h period of workplace exposure based on the evaluation of
[40]. Likewise, HPLC/FLD has been extensively used to occupational exposure to coal products. However, in the
determine PAHs in foodstuffs and beverages, because it is United States, no maximum limits for PAH contents of food-
cheap and simple, in comparison with other detection sys- stuffs have been set by U.S. legislation till now [4, 6, 47, 48].
tems [40]. Wise et al. [41] observed that low concentrations
of anthracene and perylene are best measured by the use of The EC has continued to set the pace in PAH regulation
HPLC/FLD because of their selective and sensitive fluores- in foods. The EC in 2005 set maximum levels for
cence-detection characteristics. GC/MS, however, has been benzo[a]pyrene for the first time through Regulation (EC)
found to provide more accurate results for the determination No. 208/2005 amending Regulation (EC) No. 466/2001 [47,
of benzo[ghi]perylene because of its low fluorescence [41-44]. 48]. Later, in 2006, the maximum levels for benzo[a]pyrene
were laid down in Regulation (EC) No. 1881/2006 setting
Schiewek et al. [45] reported that the use of time-of- maximum levels for certain contaminants in foodstuffs.
flight (TOF) MS with GC and LC has become increasingly However, the most recent legislation was a maximum level
popular in food analysis in recent years. It has been found for the sum of the four PAHs (benzo[a]pyrene, benz[a]anth-
that through these methods, accurate mass measurements and racene, benzo[b]fluoranthene, and chrysene) which was
full-scan data of the analytes can be acquired. This method included in Regulation (EU) No. 835/2011 amending Regu-
through its high mass resolving power can enable better lation (EC) No. 1881/2006 [49]. The EC used this approach
structural conformation and better signal-to-noise ratios than to ensure that PAH levels in food are kept at levels that do
single quadrupole analyzers, especially with complex sam- not cause health concerns and that foods in which
ples. benzo[a]pyrene is not detectable, but where other PAHs are
present are prevented from entering the market. The EC
5. HEALTH IMPLICATIONS OF PAHS maintained through these legislations separates maximum
Several research works have identified PAHs especially level for benzo[a]pyrene to ensure comparability of previous
the 17 PAHs of greatest concern with regard to potential and future data. However, the EC intends to lower some of
exposure and adverse health effects on humans. Research the maximum levels as from 2014/2015 [50].
agencies such as EFSA [46] have found that biological moni- In Asia, China has led regulation on PAHs contamination
toring of exposure to PAHs could be of utmost importance to of foods and related products. The Standardization Admin-
reduce possible effects of these toxicants on humans. How- istration of China issued the National Standards, which in-
ever, EFSA [46] has classified PAHs into three (3) groups. clude a set of mandatory and recommended standards.
These are known, possibly, or probably to be carcinogenic to According to Bugang and Woolsey [50], Chinese food safety
humans (Group 1, 2A or 2B). Among the known carcinogens national standard GB 2762-2012 (Maximum Levels of con-
are benzo[a]pyrene (Group 1), the possible carcinogens are taminants in Foods) was issued by the Ministry of Health to
naphthalene, chrysene, benz[a]anthracene, benzo[k]fluoran- replace the preceding 2005 edition (GB 2762-2005).
thene and the probable carcinogens are benzo[b]fluoranthene GB2762-2012 came into force as of June 1, 2013. Zelinkova
(Group 2B) [46]. Some PAHs are well-known carcinogens, and Wenzl [15] and Bugang and Woolsey [51] reported that
mutagens, and teratogens and therefore pose a serious threat GB Standard sets maximum levels of certain contaminants in
Polycyclic Aromatic Hydrocarbons in Foods: A Critical Review Current Nutrition & Food Science, 2020, Vol. 16, No. 6 871
foods including benzo[a]pyrene. However, the maximum Research on Cancer (IACR), the Scientific Committee on
limits for benzo[a]pyrene are set for four food categories in Food (SCF), the Joint FAO/WHO Expert Committee on
China [51]. Food Additives (JECFA), the International Programme on
Chemical Safety (IPCS), and the European Commission and
Several regulations have been set by various government
the European Food Safety Authority (EFSA). Care must be
agencies in Brazil to regulate and control the amounts of
taken for adequate process and quality control of the
PAHs in foods for human consumption. Regulations estab-
processed food products, in order to reduce the ingestion of
lishing maximum levels for benzo[a]pyrene in foods include
Resolução RDC No. 281/2003 [29] for smoke flavorings these chemical contaminants and the burden of cancer in
(30 μg/kg), Resolução RDC No. 2/2007 [28] for olive oil humans.
(2.0 μg/kg), and Portaria MS No. 518/2004 [30] for drinking
water (0.7 μg/L). CONSENT FOR PUBLICATION
Not applicable.
7. CLINICAL TRIALS ON THE EFFECTS OF PAHS
ON HUMANS FUNDING
Although PAHs carcinogenicity and toxicity have been None.
extensively discussed, several studies are available which are
in human clinical trials. However, laboratory animal studies CONFLICT OF INTEREST
have shown that PAHs at high doses could be fatal. But
Perera et al. [52] revealed that the dose of PAHs in the order The authors declare no conflict of interest, financial or
of 10th of the fetus to the mother could result in PAH- otherwise.
induced carcinogenesis during the fetal and infancy periods.
They then “compared the levels of benzo[a]pyrene-DNA ACKNOWLEDGEMENTS
adducts as a proxy for PAH-DNA damage measured in Declared none.
maternal blood and newborn cord blood obtained at delivery
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