Food Control 21 (2010) 606610

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Determination of polycyclic aromatic hydrocarbons in grilled meat

Afsaneh Farhadian, S. Jinap *, Faridah Abas, Zaidul Islam Sakar
Centre of Excellence for Food Safety Research (CEFSR), Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia

a r t i c l e i n f o a b s t r a c t

Article history: Polycyclic aromatic hydrocarbons (PAHs) are primarily formed as a result of thermal treatment of food,
Received 28 March 2009 especially grilling or barbecuing. In this study nine types of Malaysian popular grilled meat dishes were
Received in revised form 28 August 2009 analyzed for toxic PAHs, i.e. uoranthene, benzo(b)uoranthene and benzo(a)pyrene using HPLC-FD. The
Accepted 9 September 2009
differences in PAH concentrations among (charcoal, gas and oven grilling) were found to be signicant
(p < 0.05), ranging from 3.51 to 106 ng/g. Fluoranthene was found in all samples; the highest concentra-
tion of total PAHs was 132 ng/g found in beef satay and the lowest was 3.51 ng/g in oven grilled chicken.
Keywords:
2009 Elsevier Ltd. All rights reserved.
Polycyclic aromatic hydrocarbons (PAHs)
Grilled meat
Carcinogen

1. Introduction
Polycyclic aromatic hydrocarbons (PAHs) are a group of com-
pounds comprised of fused aromatic rings. PAHs containing up to
four fused benzene rings are known as light PAHs and those con-
taining more than four benzene rings are called heavy PAHs. Heavy
PAHs are more stable and more toxic than light ones (Wenzl, Si-
mon, Kleiner, & Anklam, 2006). Light PAHs are more volatile, water
soluble and less lipophilic than the heavy PAHs (Ferrarese, Andre-
ottola, Irina, & Oprea, 2008; Wild & Jones, 1994). According to the
Scientic Committee on Food (2002), 15 PAHs showed clear evi-
dence of mutagenicity/genotoxicity in somatic cells in experimen-
tal animals in vivo. They may be regarded as potentially genotoxic
and carcinogenic to humans their carcinogenicity is initiated by
their metabolic conversion in mammalian cells to diolepoxides
that bind covalently to cellular macromolecules, including DNA,
causing errors in DNA replication and mutation (Phillips & Grover,
1994).
PAHs are formed by the incomplete combustion of organic mat-
ter and are thus generated whenever fossil fuels or vegetation is
burned, and they are one of several classes of carcinogenic
chemicals present in tobacco smoke. They are also present in food
(Phillips, 1999). Cooking and food processing at high temperatures
have been shown to generate various kinds of genotoxic sub-
stances or cooking toxicants, including PAHs (Agerstad & Skog,
2005). Many studies have demonstrated that carcinogenic PAHs
are present in food, being formed through the grilling and smoking
of foods (Chen & Chen, 2005; Chen & Lin, 1997; Mottier, Parisod, &
Turesky, 2000; Ova & Onara, 1998; Phillips, 1999; Swallow, 1976;
* Corresponding author. Tel.: +60 38946 8367; fax: +60 38948 5970.
E-mail addresses: jinap@food.upm.edu.my, sjinap@gmail.com (S. Jinap).
Wu, Wong, Lee, Shi, & Ong, 1997). Cooking methods involving grill-
ing can produce marked differences in the concentrations of car-
cinogens. Grilling (broiling) meat, sh or other foods with
intense heat over a direct ame results in fat dripping on the hot
re and yielding ames containing a number of PAHs (Agerstad
& Skog, 2005). These chemicals adhere to the surface of the food.
The more intense the heat, the more PAHs are present. (Jgerstad
& Larsson, 1986). Although according to (Chen & Chen, 2005;
Madhavan & Naidu, 1995; McLachlan, 1997; Roeder, Garber, &
Schelling, 1998), PAHs migrate through the food chain into hydro-
phobic compartments, and thus, accumulate in lipid components
due to their lipophilic nature, but according to Lawley, Curtis, &
Davis, 2008 signicant levels of PAHs do not usually accumulate
in the meat, milk, or egg of food animals because PAhs are rapidly
metabolized in these species. PAHs are present in grilled meat or
sh in varied amounts (0130 ng/g). The concentration of the
benzo(a)pyrene [B(a)P] in these foods ranges from 0.2 to 50 ng/g
(IARC International Agency Research on Cancer, 1983). Grilled
meat in general is estimated to contain ca. 10.5 ng/g B(a)P (IARC
International Agency Research on Cancer, 1993).
Some of the highest concentrations of PAHs have been found in
food cooked over open ames. For example, in barbecued meat to-
tal PAHs were found to be present at concentration up to 164 ppb
and B(a)P being present at levels as high as 30 ppb (Panalaks,
1976). In Italy, it was found that the highest concentrations of
PAHs were observed in pizza baked in wood-burning ovens and
barbecued beef and pork (Lodovici, Dolara, Casalini, Ciappellano,
& Testolin, 1995). Since grilled foods are popular both at home
and in restaurants, these foods may present a health risk to the
population due to higher concentrations of carcinogens found in
such products in comparison to foods prepared by alternative
cooking methods (Sundararajan, Ndife, Basel, & Green, 1999).

0956-7135/$ - see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2009.09.002
 A. Farhadian et al. / Food Control 21 (2010) 606610
Some Malaysian popular dishes (various grilled meats) such as
satay (grilled beef), ayam bakar (grilled chicken), and ikan bakar
(grilled sh) are prepared at high temperature that may generate
PAHs. Malaysia has one of the highest per capita consumption rates
in the world for chicken. Per capita consumption of poultry, beef
and sh is respectively reported at 33.8, 5.8 & 60.5 kg. (Hajeb
et al., 2008; Tey, Mad Nasir, Alias, Zainalabidin, & Amin, 2008).
On the other hand, cancer has become increasingly important as
a public health concern in Malaysia (Lim, 2002). Therefore, the
objective of this study was to evaluate the occurrence of PAHs in
Malaysian grilled foods.
2. Materials and methods
2.1. Standards and reagents
PAHs standards (uoranthene [Fln], benzo(b)uoranthene
[B(b)Fln] and benzo(a)pyrene [B(a)P]) were purchased from Supe-
lco (Bellefonet, PA, USA). The solvents (acetonitrile, dichlorometh-
ane, and n-hexane) used throughout this study were of HPLC grade,
obtained from Merck (Darmstadt, Germany). Diatomaceous earth
(Extrelut, 20 mL) was obtained from International Sorbent Tech-
nology Hengoed Mid Gleam, UK), while the propylsulphonic (PRS,
500 mg) SPE and silica gel columns were from Silica Chemical Divi-
sion (Quebec City, Canada).
2.2. Samples
The list of meat, chicken and sh dishes and details of cooking
conditions are shown in Table 1. The cooking methods were classi-
ed into charcoal grilling, ame-gas grilling and oven grilling. Sam-
ples (three portions for each sample) of each of the dishes was
purchased at three different days from six local restaurants, all
within a 25 km radius of Serdang, Selangor, Malaysia. A composite
sample was made by pooling the meat, chicken and sh samples
(without bones) from each restaurant (Kazerouni, Sinha, Hsu,
Greenberg, & Rothman, 2001; Knize et al., 1995). The samples were
Table 1
Malaysian meat dishes sampled in this study and their cooking method.
Cooking method Meat Cooking condition
(degree of cooking) dishes
1. Charcoal grilled Ayam 45 pieces of chicken were grilled for 6
(well done) bakar 7 min on each side using garden-type
(chicken) grill fuelled by charcoal
Ikan bakar 1 whole gutted sh (250300 g) were
(sh) grilled for 78 min on each side using
garden-type grill fuelled by charcoal
Beef satay 45 small pieces of beef were grilled for
56 min on each side using satay-type
grill fuelled by charcoal
Chicken 45 small pieces of chicken were grilled
satay for 45 min on each side using satay-
type grill fuelled by charcoal
2. Gas grilled Beef Sliced beef skewered onto the vertical
direct heat (well kebab rotisserie with a vertical gas heat
done) element
Chicken Sliced chicken skewered onto the
kebab vertical rotisserie with a vertical gas
heat element
Grilled 1 large piece of chicken were grilled for
chicken 810 min on each side using gas stove
3. Oven grilled Tandoori 2 pieces chicken cooked in a clay oven
indirect heat (chicken) (Tan door) heat source was gas and
(well done) under a clay surface
Grilled 1 whole chicken (1 kg) cooked in an
chicken electric oven
607
blended using a Waring blender (Milford, MA, USA) and kept at
18 C prior to extraction and analysis.
2.3. Extraction and clean up of PAHs samples
Extraction and clean up procedures were based on the method
described by Janoszka, Warzecha, Blasz czyk, and Bodzek (2004).
Each meat sample (5 g) was homogenized for 36 h in 15 mL of
cold NaOH solution (1 M). Each sample was mixed with Extrelut
rell material, diatomaceous earth, as stationary phase (17 g) and
the mixture obtained was placed in a 20 mL Extrelut column. Then
the column was connected to a PRS SPE column and the PAH
fraction was eluted with dichloromethane (60 mL). The dichloro-
methane extract was evaporated to dryness and the residue was
re-dissolved in n-hexane (1 mL), the residue was then placed on
the top of the column which was packed with deactivated silica
gel (10 g) and preconditioned by using n-hexane (25 mL). The col-
umn was eluted with 60:40 (v/v) n-hexane and dichloromethane
(60 mL) to collect the PAH fraction. The solvent was evaporated
and the PAH residue was dissolved in acetonitrile (250 ll).
2.4. PAHs determination by HPLC
PAHs analysis was carried out using an HPLC apparatus (Waters,
Massachusetts, USA) equipped with a 600 controller pump, uo-
rescence detector, Waters 2475 (kex = 360 nm, kem = 460 nm)
and a 20 ll loop injector. A PAH column (250 mm  4.6 mm,
5 lm particle size) (Hichrom, Reading, UK) was used. The mobile
phase consisted of 84% acetonitrile and 16% water at a ow rate
of 1 mL/min. Separation was performed under isocratic conditions.
Each PAH sample solution was passed through a 0.45 lm lter
(Whatman, Maidstone, UK) prior to injection onto the HPLC sys-
tem. The quantication of PAHs was performed by the use of an
external calibration curve method.
2.5. Recovery study
Recovery experiments were carried out for seven replicates by
spiking 40 ng of each of the PAH standards, Fln, B(b)Fln and
B(a)P, in each of the grilled dish samples, using the unspiked sam-
ple as control; all spiked samples were mixed for 1 h before extrac-
tion. Recoveries were calculated from the differences in total
concentrations between spiked and unspiked samples.
3. Results and discussion
Identication of three PAHs, Fln, B(b)Fln and B(a)P was achieved
on the basis of comparison of HPLC retention times of PAHs stan-
dards and those of spiked and unspiked meat samples. Typical
HPLC chromatograms of PAH are presented in Fig. 1. The selected
PAHs compounds increased after spiking the sample. The calibra-
tion curve, linear equation, coefcients of regression (R2) and limits
of detection and quantication (LOD and LOQ) obtained using the
signal-to-noise ratio as S/N = 3 and S/N = 10, respectively (Juan,
Zinedine, Molto, Idrisi, & Manes, 2008) for PAHs quantication
and presented in Table 2. The limits of detection and quantication
(LOD and LOQ) were 0.02 and 0.09; 0.01 and 0.04; and 0.03 and
0.10 for Fln, B(b)Fln and B(a)P, respectively, which showed enough
sensitivity for the detection of the compound in the samples. Pre-
cision and recovery are presented in Table 3. Recoveries obtained
for different PAH standards ranged from 68.2% to 118% and their
relative standard deviation ranged from 15.9% to 21.3%. Based on
the AOAC manual guidelines, these recovery values are acceptable
(AOAC Association of Ofcial Analytical Chemists, 1993).
608 A. Farhadian et al. / Food Control 21 (2010) 606610

Fig. 1. Typical HPLC chromatograms: (A) mixed standard, (B) spiked chicken satay and (C) unspiked chicken satay.

Table 2
Linear equation, limits of detection and quantitation (LOD and LOQ) obtained for quantication of PAHs.

Standards Concentration range (ng/g) Linear equation Regression coefcient LOD (ng/g) LOQ (ng/g)
Fluoranthene 0.210 Y = 1.6311X+ 0.0282 0.999 0.02 0.09
Benzo(b)uoranthene 0.210 Y = 3.6586X 1.3827 0.999 0.01 0.04
Benzo(a)pyrene 0.210 Y = 5.1752X 2.3397 0.998 0.03 0.10

Table 3
Precision and recovery of PAHs in Malaysian grilled food, determined by HPLC with uorescence detector.

Standards Replication Spiked conc. (ng/g) Conc. found (ng/g) Mean recovery (%) Range of recovery (%) RSD (%)
Fluoranthene 7 8 4.07.6 84.6 68.3118 21.3
Benzo(a)pyrene 7 8 5.19.3 88.6 71.1104 15.9
Benzo(b)uoranthene 7 8 4.97.4 88.6 68.3110 18.4

Table 4 shows the determination of PAHs in grilled meat dishes
by HPLC. The results showed that Fln was detected in all samples,
in the range of 3.51106 ng/g. The minimum concentration of Fln
(3.51 ng/g) was detected in oven grilled chicken, and the maximum
concentration (106 ng/g) was detected in beef satay. In total, the
maximum concentration of individual PAHs were detected in four
dishes that were grilled on charcoal.
Table 4 also shows that there was a signicant difference
(p < 0.05) between this group of dishes (charcoal gilled) and two
other groups (gas grilled and oven grilled dishes) (p < 0.05). Fur-
thermore, the concentration of each of the three PAHs in the sec-
ond group of dishes (ame-gas grilled) was signicantly
difference (p < 0.05) as compared to the third group of dishes (oven
grilled). The study indicates that the thermal process and method
 A. Farhadian et al. / Food Control 21 (2010) 606610 609

of grilling has a signicant effect on the concentration of PAHs gen-

Sum of three PAHs

erated in the food samples. These ndings are in agreement with

(ng/g) (minmax)
those has mentioned by Phillips (1999): normal roasting or frying
food does not produce copious quantities of PAHs, some of the

3.517.14
4.659.66
4.6312.4
8.2320.4
9.3615.0
9.3615.0

14.337.6
28.951.1

81.0132
highest levels of PAHs reported in foods have been detected in food
cooked over open ames. For example, in barbecued meat total
PAHs were found to be present at levels up to 164 ppb with Ben-
zo(a)pyrene being present at levels as high as 30 ppb. And also
Benzo(a)pyrene

Chen and lin (1997) in Their study found that For total PAHs, smok-
(ng/g) (mean)

ing contained the highest amount (154 ng/g), followed by charcoal

grilling (151 ng/g), roasting (88.5 ng/g) and steaming (4.4 ng/g). In

1.57
4.35

7.35
1.95
0.37

0.40
0.76

0.40
addition as it has showed in Table 4, dishes of the second group

nd
(ame-gas grilled) had the lower concentration of PAHs than the
rst group (charcoal grilled). And Masuda, Mori, and Kuratsune
Benzo(a)pyrene

(1966) also, in their study showed, sh samples which were grilled

(ng/g) (range)

in an electric broiler produced only minimal concentrations of PAH

2.576.46

7.3412.5
1.612.67

nd2.83
nd1.23

nd0.87
nd0.84

nd0.80

while those grilled using gas yielded somewhat higher concentra-

tions. And in this group, the lower concentration of PAHs could be
nd

due to the vertical source of heat as well, that prevented the drop-
ping of the fat from meat into the ame (Lijinsky & Shubik, 1964).
Benzo(b)uoranthene

Tandoori and grilled chicken samples (Table 2) in the last group of

samples (oven grilled) had the lowest concentration of PAHs. In
(ng/g) (mean)

comparison to the other two group of samples (gas & charcoal grill-
ing). This can be probably due to the oven grilled that foods were
indirect contact with the ame (Agerstad & Skog, 2005). In a study
0.42
0.32

0.40
3.81

9.67
1.16
1.07

by Rey-Salgueiro, Garcia-Falcon, Nez-Carballo and SimalGandara

nd
nd

(2008), direct toasting (ame-toasting, coal-grilling or gas oven-

toasting) and indirect toasting (electric oven-toasting) of bread
Benzo(b)uoranthene

samples were investigated to evaluate the levels of PAHs. No sam-

ples obtained by electric oven and toaster were polluted; other-
(ng/g) (range)

wise the samples toasted by charcoal and ame grilling

1.556.23

6.2213.8
0.621.74

presented very high levels and 350 ng/g of total PAHs were de-
nd2.21

nd0.92
nd0.96

nd1.1

tected in toasted samples by wood ame. And their results conrm

nd
nd

our results.
In the study by Janoszka et al. (2004), Fln and B(a)P were found
(ng/g) (mean)
Fluoranthene

at concentrations of 0.57 ng/g and 0.15 ng/g, respectively, in grilled

chicken breast on charcoal. In addition, Kazerouni et al. (2001)
found that B(a)P was present in 200 different meat dishes, of which
5.35
6.72
13.55
7.64
10.65
9.90
86.3
22.5
32.0

very well-grilled or barbecued meat had the highest concentra-

tions of PAH, ranging from 0.40 to 1.15 ng/g. When comparing
our results with the other studies, some Malaysian dishes such
(ng/g) (range)
Fluoranthene

3.517.14
4.659.66
4.6312.5
8.1611.8

7.3018.6
7.408.60

as chicken grilled on charcoal had higher concentration of PAHs

12.133.2
24.838.4

67.4106

(Fln (36.3 ng/g) and B(a)P (6.46 ng/g)). The authors are now carry-
ing out a study on the inuence of ingredients used to marinate
these grilled dishes. Some ingredients, especially those used in
grilled satay, may be responsible for generating high concentration
Polycyclic aromatic hydrocarbon concentration of meat samples (ng/g).

number of

of PAHs. It is known that recoating with sauces can often result in

samples

burned meat surface (Agerstad & Skog, 2005). Fat content of the
Total

18
18
18
18
18
18

18
18
18

sample is also an important factor for PAHs formation in grilled

meat (Fretheim, 1983).
Number of

purchased
samples

3
3
3
3
3
3
3
3
3

4. Conclusions
Number of
restaurant

The PAHs concentrations between the three groups of grilled

dishes were found to be signicantly different (p < 0.05). The high-
est concentration of PAHs was detected in charcoal grilled followed
6
6
6
6
6
6
6
6
6

by ame-gas grilled and oven grilled dishes. In charcoal grilled

Oven grilled chicken

dishes, beef satay had the highest concentration of PAHs. PAHs

Tandoori (chicken)

concentrations of ame-gas grilled dishes was found to be low

Grilled chicken

nd: Not detected.

Chicken kebab
Chicken satay
Food samples

when the gas-ame source was vertical. Furthermore, there were

Ayam bakar

Beef kebab
Ikan bakar
Beef satay

no signicant difference in PAH concentrations (p < 0.5) between

beef & chicken grilled by a vertical source. Since grilled meat dishes
Table 4

are popular in the Malaysian diet, conducting more studies on the

effects of different heat sources, fat content of meat and marinating
610 A. Farhadian et al. / Food Control 21 (2010) 606610
ingredients are necessary in an effort to possibly reduce the PAH
contamination in these foods.
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