504

Journal o f Food Protection, Vol. 77, No. 3, 2014, Pages 504-509

doi: 10.4315/0362-028X. JFP-13-223
Copyright © , International Association for Food Protection

Research Note

Evaluation of Heavy Metals and Polycyclic Aromatic

Hydrocarbons in Honeys from Different Origins
LOURDES CORREDERA,1* SUSANA BAYARRI,1 CONSUELO PEREZ-ARQUILLUE,1 REGINA LAZARO,1
FRANCISCO MOLINO,2 a n d ANTONIO HERRERA1

lDepartamento de Produccion Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Facultad de Veterinaria, Calle Miguel Servet 177,
50013 Zaragoza, Spain; and 2Centro de Investigacion y Tecnologla Agroalimentaria de Aragon, Avenida de Montanana 930, 50059 Zaragoza, Spain

MS 13-223: Received 29 May 2013/Accepted 29 September 2013

ABSTRACT

A survey of honey samples from different geographical and botanical origins, including some samples collected from a fire-
affected area in Spain, was conducted to assess their content of heavy metals and polycyclic aromatic hydrocarbons (PAHs). The
levels of the determined toxic elements (Pb, Cd, As, and Sn) were low and were in the range of those reported by other studies. In
our work the total amount of heavy metals and Pb was higher in dark honeys than in pale honeys. In the collected samples, no
detectable levels of the 15 PAHs studied were found. The obtained data served to assess the levels of heavy metals and PAHs in
honey samples from different geographical and environmental origins and to contribute to the scarce data about pollutant content
of this matrix. In light of these results, the analyzed samples do not pose any serious concern to human health, and the data
obtained in this study could serve to contribute to the establishment of specific maximum limits for honey.

Honey, one of the most complex foodstuffs produced in
nature, has valuable nourishing, healing, and prophylactic
properties ( 19, 21). It contains a mixture of different
nutrients and is often consumed without processing, but it
must be free of any objectionable contents and should not
contain significant amounts of pollutants (21, 29).
In the past few years, investigation of the pollutant
content in honey has mainly studied heavy metal concen­
trations (4 , 5 , 24 , 28). These pollutants may come from
external sources (mines and steelworks, industrial and urban
areas, or highways near the bees’ forage area) or may be
introduced by incorrect procedures during honey processing
and storage. Due to the acidic nature of honey, metallic tools
or containers may release elements such as Cr, Pb, or Sn.
Metal content in honey is also closely associated with its
botanical origin, the geographical area in which it originated
(melliferous flora, different minerals arising from soil, dust,
etc.), but it can also be influenced by the feeding of the bees
and other anthropogenic activities (3 ). The mineral
composition and botanical origin of honey correlate with
its color ( 10, 14, 18). Dark and amber honeys (avocado,
chestnut, and heather) contain higher amounts of certain
major, minor, and trace metals than do pale honeys.
Interestingly, dark honeys have been associated with
concentrations of Cd, Fe, and Pb and light honeys with
concentrations of A1 and Mg ( 14).
Bee products may also be contaminated by other kind
of chemical pollutants, such as polycyclic aromatic
* Author for correspondence. Tel: ( + 34) 976761543; Fax: (+ 3 4 )
976761590; E-mail: corredera.lourdes@gmail.com.
hydrocarbons (PAHs). PAHs are mainly the products of
incomplete combustion and pyrolysis of organic matter,
formed from anthropogenic and natural sources. The
presence of PAHs in the environment has received much
attention over the past decades due to their persistent, toxic,
mutagenic, and carcinogenic properties (25). Honey can be
contaminated with these kinds of substances as a result of
environmental pollution (forest fires, stubble burning,
location of beehives near industrial sites, etc.) or beekeeping
practices, such as blowing smoke into the beehives during
handling to calm the bees and keep them from attacking the
beekeeper. Wood chips, pine needles, and other vegetable
materials usually can be used safely for bee smoking, but oil
petroleum products or contaminated materials must be
avoided.
In spite of these possibilities of contamination, there is
little information on the levels of PAHs in honeys from
Spain (2 , 7) and from other European countries (9 , 16, 17).
The control of compounds that can damage health,
including heavy metals and PAHs, could be essential, since
the effects of pollution, the increased use of pesticides, and
the loss of the flower-rich habitat on which bees depend for
food could be responsible for behavior disorders in the bee
colony and could be to blame for “ honeybee depopulation
syndrome.” Also, in studies from around the world,
honeybees and their products have been proposed as
suitable bioindicators of chemical pollution ( 17, 20 , 21 ,
26). Because honey is the result of a bioaccumulative
process, and because there is a large foraging area
associated with an apiary, honey is also useful for collecting
information about the surrounding environment ( 19).
J. Food Prot., Vol. 77, No. 3
TABLE 1. Description o f the origins o f the analyzed honey samples
Sample no. Geographical origin
1-6 Ainsa (Huesca)
7-11 Luesma (Zaragoza)
12-14 Chiprana (Zaragoza)
15-18 Loscos (Teruel)
19-24 Zuera (Zaragoza)
25-30 (commercial) Blend of EU and non-EU honeys
The European Union regulates the concentration of
heavy metals and PAHs in various food products using
international criteria for maximum tolerable limits (11), but
honey has not yet been included in this regulation.
An analytical methodology for analysis of PAHs in
honey was developed and validated in previous work in our
laboratory ( 7). Following this research line and considering
all the above points, the present study measured heavy metal
and PAH concentrations in honey samples from different
geographical and environmental origins to detect variations
among them and also looked at the effects of a huge forest
fire in August 2008 in the region of Zaragoza (Spain). This
study could also be used as part of a risk assessment to
establish maximum tolerable limits in honey and to
contribute to the scarce data about pollutant contents in
this matrix.
MATERIAL AND METHODS
Reagents. Nitric acid (H N 03) was of suprapure quality
(J. T. Baker, The Netherlands) and ultrapure water was obtained
from a Milli-Q plus apparatus (Millipore, Bedford, MA). High-
performance liquid chromatography analysis grade ethyl acetate,
methanol, and acetonitrile were used. All the organic solvents
were supplied by Labscan (Dublin, Ireland). To prepare element
standard solutions o f heavy metals used for calibration, stock
solutions of 1,000 mg/liter Pb, Cd, As, and Sn (Sigma Aldrich, St.
Louis, MO) were diluted in H N 0 3.
PAH standards in acetonitrile (10 mg/liter) originated from
Dr. Ehrenstorfer (Augsburg, Germany): cyclopenta[c,<7]pyrene
(CPP) 99.0%, benz[a]anthracene (BaA) 99.5%, chrysene (CHR)
99.0%, 5-methylchrysene (5MC) 99.8%, benzo[b]fluoranthene
HEAVY METALS AND PAHs IN HONEY 505
Botanical origin
Multifloral
Labiatae (Thymus + Rosmarinus)
Fruit tree (Prunus)
Multifloral
Thyme (Thymus)
Multifloral (as indicated in labeling)
(BbF) 99.0%, benzo[/]fluoranthene (BjF) 99.0%, benzo[L]fluor-
anthene (BkF) 99% , benzo[a]pyrene (BaP) 99.5%, dibenz[a,/i]an-
thracene (DbA) 99.0% , dibenzo[a,/]pyrene (DIP) 99.5% ,
benzo[g/!/']perylene (BgP) 99.5%, indeno[l,2,3-c,d]pyrene (IP)
99.5%, dibenzo[a,e]pyrene (DeP) 99.0%, dibenzo[a,t]pyrene
(DiP) 99.9%, dibenzo[a,/z]pyrene (DhP) 99.0%.
Sample collection. Thirty honey samples of different
botanical origins and sampling sites were collected between 2009
and 2012 in the region o f Aragon (Spain), to study their levels of
heavy metals and PAHs. Eighteen o f them came from four
locations away from roads and industrial sites, and six were
collected in a region affected by a huge forest fire that took place
in August 2008, which burned 2,513.60 ha o f the Province of
Zaragoza (Aragon). The affected area was mainly composed of
rosemary, juniper, oak, and especially Aleppo pine (Pinus
halepensis). The zone has a semiarid climate with dry summers,
during which temperatures reach 40°C. The zone has a scanty
average precipitation o f 310 mm, with abundant sunny days and a
dry wind blowing from the northwest, conditions that could
intensify fire.
The other six samples were commercial honeys (labeled as
blends o f European and non-European honeys, without specifying
origin). Table 1 specifies the geographical and botanical origin of
each sample, and Figure 1 shows the distribution o f the different
sampling sites in the northeast of Spain.
Honeys were collected directly from the beekeepers; the
keepers used vegetable combustibles to smoke the beehives,
avoiding the use o f contaminated materials. The samples presented
a homogeneous appearance, without phase separation, and all of
them were kept at 4 to 5°C in a dark place until the analysis.
Commercial honey samples were purchased in several Spanish
supermarkets.
FIGURE 1. Honey sampling points in
northeast Spain.
506 CORREDERA ET AL.
Heavy metal determination. Concentrations of Pb, Cd, Sn,
and As were determined by inductively coupled plasma mass
spectrometry (Elan 6000, Perkin-Elmer, Norwalk, CT), providing
limits of detection (LODs) of 1.5 pg/liter for Pb, As, and Sn and
1 pg/liter for Cd (7.5 and 7 pg/kg of honey, respectively). The
samples were digested using a methodology based on that of
Fredes and Montenegro (12). All material used in this assay was
made of plastic, in order to prevent contamination from metal or
glass; material was soaked in H N 03 diluted with water (1:10) and
rinsed with distilled water prior to use. Five grams of each sample
was placed in porcelain crucibles, and 12.5 ml of concentrated
H N 03 was added. The mixture was stirred on a heating plate (100
to 120°C) to almost complete dryness and was made up to 25 ml
with ultrapure water. Blank solutions were prepared under identical
conditions to check for possible cross-contamination due to
laboratory practices, reagents, or apparatus. Accuracy of the
analytical method (recovery and precision) was evaluated using
spiked samples that contained concentrations of the analytes of
interest that were similar to those expected in the samples, since
there is not certified reference material for heavy metals in this
food matrix. The recovery was found to be over 90% for all the
elements, with relative standard deviation below 10%, which
indicates that the results are reliable.
A honey color analyzer (C221, Hanna Instruments, Guipuz-
coa, Spain) was used to classify the samples. This measurement,
expressed directly in mm Pfund, is based on the percent light
transmittance of the sample compared to analytical reagent
glycerol. A melissopalynological study of the crude honey samples
was performed in order to guarantee their botanical origins.
Statistics. Analysis of variance (ANOVA) was performed to
process the obtained results and to detect significant differences
among groups (according to sampling site and color of the
samples).
PAH determination. The analytical method applied in this
study was based on a solid-phase extraction with a C18 cartridge
(500 mg), using ethyl acetate as the elution solvent, and high-
performance liquid chromatography with fluorescence and diode
array detection with five different wavelengths. The mobile phase
was a gradient of acetonitrile-water. The methodology was
developed and validated in agreement with Commission Regula­
tion (EC) No 333/2007 and Commission Decision 2002/657/EC as
in a previous work ( 7), focusing on the 15 PAHs included in the
EU list of priority compounds and regarded as probably or possibly
carcinogenic to humans: (CPP, BaA, Chr, 5MC, BbF, BjF, BkF,
BaP, DbA, DIP, BgP, IP, DeP, DiP, DhP). It enabled, for the first
time, reliable results in this type of food matrix with good
sensitivity (LODs varying between 0.08 and 0.84 pg/kg), accuracy,
and ruggedness.
RESULTS AND DISCUSSION
Determination of pollutants in honey is of great interest,
not only for quality control, but also as an indicator of
environmental pollution and of good beekeeping practices.
Heavy metal concentrations in the samples are reported in
Tables 2 and 3, with percentage of detection, mean,
standard deviation (SD), and maximum levels shown for
each element. For all samples with concentrations below the
LOD, LOD/2 was used in the mean concentration
calculation (15). Only three of the investigated samples
were free of heavy metals; one of them was collected near
the fire area. The most common element was Pb, detected in
J. Food Prot., Vol. 77, No. 3
80% of the samples. Cd and As were the second and third
most abundant (46.7 and 33.4%, respectively), whereas Sn,
which, according to the scientific literature, may originate
mainly from containers where honey is stored, was less
frequent (only 5 of the 30 samples contained detectable
levels). Statistical analysis showed no significant differences
among the sampling sites. Mean values were very similar in
the six groups, except for Pb, which was present at higher
concentrations in commercial honeys. No great differences
were found for the other three elements in any of the
honeys, with average values of 5.98 pg/kg for As, 6.72 pg/kg
for Cd, and 4.80 pg/kg for Sn. However, it is remarkable that
maximum levels were all detected in commercial honeys,
except for Cd. In the samples from the fire-affected area,
the mean Cd content was lower than in the other groups
(3.55 pg/kg), and Sn was not detected in any of the six
samples. However, As concentrations were higher in
this sampling site. In general, regarding the total metal
concentrations, dark honeys had higher levels than lighter
ones; the three highest values were obtained by samples
with more than 90 mm Pfund. ANOVA testing showed no
statistical differences in As, Cd, and Sn as related to color
of the samples, whereas Pb and total metal concentrations
were related to color (P < 0.05), with higher contents in
dark amber honeys. No statistical differences in degree of
environmental pollution were found in our laboratory
among the sampling sites, but metal concentrations were
related to the color of the samples. In this study, it was not
possible to correlate the presence of specific elements with
the botanical origin of the honey because the melisso­
palynological analyses showed that the majority of the
samples were multifloral honeys.
Of toxic elements in bee products, Pb and Cd have been
the most frequently analyzed in the scientific literature,
probably because they are considered to be the most
dangerous to human health. The concentrations in our study
are low, in the range of those found in other Spanish studies,
which reported levels of Pb from 30 to 260 pg/kg (27), 2
to 49 pg/kg (23), and 31 to 46 pg/kg (13). Cd levels
were lower in these studies, with values between 0.7 and
50 pg/kg. In Italian honeys, Pb concentrations varied from 4
to 304 pg/kg and Cd from 0.5 to 15 pg/kg (6,18)-, in Polish
and Turkish honeys, Pb concentrations varied from 8 to
106 pg/kg and Cd from 0.9 to 27 pg/kg (21, 29). In India
and Egypt, contamination in honey reached higher levels,
up to 4,200 pg/kg for Pb and 500 pg/kg for Cd (5, 22).
Analysis of As and Sn is less common in honey samples,
but some studies reported levels up to 20 pg/kg for As (1,6,
18) and 27 pg/kg for Sn (6), higher than the levels obtained
in our laboratory.
In the 30 honey samples collected, no detectable levels
of the 15 PAHs studied were found; this absence indicates
that the forest fire did not contaminate the honeys collected
in the affected area. It is possible that climate conditions
dispersed the pollutants from the fire to other nearby zones.
As far as we know, this is the first time this matrix has been
studied with regard to PAHs after a forest fire. In a similar
study, Costopoulou et al. (8) looked at the presence of these
kinds of pollutants in olive and olive oil samples from areas
J. Food Prot., Vol. 77, No. 3 HEAVY METALS AND PAHs IN HONEY 507

TABLE 2. Color and concentration o f heavy metals in honey samplesa

Sample Color (mm Pfund) As Cd Pb Sn Total

1 36 ND 5.10 7.80 ND 20.40

2 72 ND 25.60 16.70 ND 49.80
3 17 ND 5.10 8.50 ND 21.10
4 46 ND 8.90 ND ND 20.15
5 26 ND ND 11.80 ND 21.80
6 27 10.10 ND 19.20 ND 35.55
Mean 4.81 8.28 11.29 ND 28.13
SD 2.59 8.80 5.81 — 12.15
Maximum 10.10 25.60 19.20 ND 49.80
7 41 ND 8.90 12.20 ND 28.60
8 83 ND 36.80 14.50 ND 58.80
9 13 7.60 5.30 ND 8.00 24.65
10 70 ND ND ND ND ND
11 94 ND 13.80 67.32 ND 88.62
Mean 4.52 13.46 20.30 4.60 42.88
SD 1.72 13.71 26.73 1.90 30.54
Maximum 7.60 36.80 67.32 8.00 88.62
12 118 18.30 8.70 8.80 10.50 46.30
13 126 8.90 ND 67.80 8.45 87.65
14 66 ND ND ND ND ND
Mean 10.32 4.57 26.78 7.57 66.98
SD 7.38 3.58 35.61 3.46 29.24
Maximum 18.30 8.70 67.80 10.50 87.65
15 39 ND ND 9.30 ND 19.30
16 36 ND ND 22.80 ND 32.80
17 24 7.70 ND 22.60 ND 36.55
18 21 ND ND 10.60 10.03 26.88
Mean 4.74 ND 16.33 5.32 28.88
SD 2.28 — 6.99 3.63 4.88
Maximum 7.70 ND 22.80 10.03 36.55
19 65 ND 8.82 29.52 ND 45.84
20 53 9.60 ND 16.40 ND 32.25
21 44 13.30 ND 8.50 ND 28.05
22 17 ND ND ND ND ND
23 22 10.20 ND 9.70 ND 26.15
24 30 ND ND 8.30 ND 18.30
Mean 7.39 3.55 12.70 ND 30.12
SD 4.18 2.58 9.19 — 10.14
Maximum 13.30 8.82 36.40 ND 45.84
25 22 ND 7.30 8.10 ND 22.90
26 150 7.70 15.80 21.80 ND 49.05
27 90 10.95 ND 125.50 ND 142.70
28 85 ND ND 46.70 13.20 66.15
29 67 ND 6.20 ND ND 17.45
30 100 ND 5.20 43.10 ND 55.80
Mean 5.61 6.58 41.49 5.33 59.01
SD 3.06 4.92 44.75 3.86 45.16
Maximum 10.95 15.80 125.50 13.20 142.70

° Concentrations are expressed in micrograms per kilogram. ND, not detected.

TABLE 3. Percentage of detection, mean, standard deviation, and maximum levels of the studied heavy metals in the 30 honey samples

As Cd Pb Sn Total

% of detection 33.40 46.70 80.00 16.70 93.30

Mean 5.98 6.72 21.33 4.80 40.62
SD 3.69 7.67 26.16 2.50 28.27
Maximum 18.30 36.80 125.50 13.20 136.45
508 CORREDERA ET AL.
affected by forest fires in Greece. For the same PAHs that
we studied, they reported levels that were considerably
lower than those found in samples of extra virgin olive oil
that came from olive oil mills or from the retail market
(most of the compounds were below the LODs, and BaP
levels were always below 1 pg/kg). Our results are in
agreement with those published in other studies that
analyzed Spanish honeys ( 2 , 7). In a study of honey
samples from two regions of Italy to study the different
degrees of environmental pollution, Perugini et al. ( 17) did
not detect BaP, and phenanthrene, anthracene, and Chr were
detected at very low concentrations (the average levels were
always below 1 pg/kg and were often lower than the LODs
established in our study). All sampling sites showed the
presence of PAHs; however, no significant differences were
detected among the eight sites. Furthermore, the mean PAH
concentration in honey samples was lower than that reported
in honeybees of the same regions, and no positive
correlation was found between the compounds detected in
bees and those in honey. Similarly, Lambert et al. ( 16)
concluded that bees are better bioindicators of PAH
pollution than honey, since they are sensitive to low
concentrations of PAHs. As to peaks of contamination, the
beehive matrix is the best to differentiate apiary and period
effects. In contrast, Dobrinas et al. ( 9) reported the presence
of BaP (with concentrations of 0.5 to 141 pg/kg) and 13
other hydrocarbons (concentrations up to 665 pg/kg
depending on the compound) in several honey samples
from Romania, noting significantly higher concentrations of
PAHs in urban sites than in mountain and rural sites. The
data obtained in our study cannot be compared with that
from other works carried out in the same matrix in similar
situations. In the present case, it is possible that the strong
winds and climate conditions during the fire immediately
dispersed pollutants to a wider area, so that they were not
absorbed in the honey next to the burning site. On the other
hand, PAHs are highly hydrophobic and tend to adsorb on
lipophilic matrices, whereas honey is a polar matrix.
Generally speaking, most of the literature indicates-
that, at these levels of contamination and taking into
account daily honey intake, no significant danger to human
health would be expected and honey products could be
marketed without any risk. The data from this study could
contribute to the establishment of specific maximum limits
for honey.
ACKNOWLEDGMENT
The authors thank the Government of Aragon for giving a scholarship
to Lourdes Corredera and for its financial support (Grupo de Investigation
Consolidado A01, Fondo Social Europeo and Ayudas Apt'colas).
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