Food Research International 56 (2014) 159–165

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Food Research International

journal homepage: www.elsevier.com/locate/foodres

Review

Health risks of human exposure to chemical contaminants through egg

consumption: A review
José L. Domingo ⁎
Laboratory of Toxicology and Environmental Health, School of Medicine, IISPV, Universitat “Rovira i Virgili”, 43201 Reus, Catalonia, Spain

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

Article history: It is well known that by a number of reasons such as low cost, general availability, nutritional characteristics, and
Received 3 November 2013 multiple possibilities of consumption, avian eggs in general, and hen eggs in particular, are an important compo-
Accepted 20 December 2013 nent of the human diet over the world. Until recently, it was assumed that the egg cholesterol content implied an
increased risk for coronary heart disease (CHD). However, recent studies have suggested that a frequent consump-
Keywords:
tion of eggs (up to one egg per day) is not associated with increased risk of CHD or stroke. The nutritional benefits
Eggs
Nutrients
of eggs are due to the content of proteins and several essential nutrients, particularly vitamins D and B12, choline,
Chemical contaminants and selenium among others. However, various studies have also detected the presence of several chemical pollut-
Dietary intake ants in eggs, whose exposure could also mean certain health risks for the consumers. The human health risks
Human health risks derived from exposure to a number of chemical contaminants through the regular consumption of eggs are here
reviewed. It is concluded that the health risks derived from exposure to these contaminants must be considered
in the context of each specific diet, which besides eggs, includes numerous foodstuffs, and chemical pollutants.
© 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
2. Eggs and diet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160
3. Chemical pollutants in eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160
4. A case-study: Catalonia, Spain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
4.1. Trace elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
4.2. Hexachlorobenzene (HCB) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
4.3. Polychlorinated naphthalenes (PCNs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
4.4. Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
4.5. Polychlorinated biphenyls (PCBs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
4.6. Polybrominated diphenyl ethers (PBDEs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
4.7. Polychlorinated diphenyl ethers (PCDEs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
4.8. Polycyclic aromatic hydrocarbons (PAHs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
4.9. Summary of results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
4.10. Perfluoralkyl substances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
5. The CONTEGG study, Belgium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163
6. Eggs and the “Belgian PCB/dioxin crisis” . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
Funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164

1. Introduction

The socio-economic status of the general population influences their

⁎ Tel.: +34 977 759380; fax: +34 977 759322. dietary habits, and consequently the health. A proper balance of the
E-mail address: joseluis.domingo@urv.cat. intake of nutrients, concurrently with the avoidance of their excess or

0963-9969/$ – see front matter © 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodres.2013.12.036
160 J.L. Domingo / Food Research International 56 (2014) 159–165
deficiency, is basic to maintain a good health status, as well as to prevent
a number of diseases. There are three basic parameters influencing the
socio-economic status: occupation, education, and income (Vlismas,
Stavrinos, & Panagiotakos, 2009). Income is likely to mirror the avail-
ability of economic and material resources. Therefore, it influences
the dietary quality, making healthy food more or less affordable and
accessible.
In recent years, a number of studies that focused on the potential
association between certain dietary habits and the risks of various
diseases have been performed. These are some interesting examples:
antioxidant vitamins and coronary heart disease risks; dietary antioxi-
dant nutrients; fruit and vegetable intakes and total mortality; Mediter-
ranean diet and mortality; fruit and vegetable consumption, and renal
and breast cancer; meat intake and risk of stomach and esophageal
adenocarcinoma; cereal fiber intake and reduced risk of gastric adeno-
carcinomas; health benefits and risks of regular fish consumption;
dairy consumption and risk of prostate cancer; meat, fish and fat intake
and risk of colorectal cancer, etc.
On the other hand, it has been demonstrated that certain dietary
habits can also contribute to compromised health by being a source of
potential exposure to toxic contaminants. Consequently, caution in the
consumption of certain foodstuffs, depending on their concentrations
of chemical pollutants, is also another nutritional key issue. This paper
specifically reviews the potential health risks derived from exposure
to a number of chemical contaminants through a regular dietary con-
sumption of hen eggs. Eggs, whose nutritional content is well established,
are generally accessible to most individuals over the world, even for
populations whose incomes are low.
2. Eggs and diet
In recent decades, a number of studies regarding dietary fat and cho-
lesterol intake have reported a strong and positive correlation with
heart disease (Fernandez, 2006; Jones, 2009; Kratz, 2005; Spence,
Jenkins, & Davignon, 2010). However, the results of various epidemio-
logical investigations performed in recent years do not support a rela-
tionship between cholesterol intake and cardiovascular disease (CVD)
(Barona & Fernandez, 2012; Baum et al., 2012; Rong et al., 2013). Even
various recent clinical trials assessing the effects of long-term egg
consumption (as a vehicle for dietary cholesterol) did not find negative
impacts on several indices of cardiovascular health and disease (Barona
& Fernandez, 2012; Baum et al., 2012), noting that the existing epidemi-
ological data clearly demonstrate that dietary cholesterol is not correlat-
ed with increased risk for coronary heart disease (CHD) (Fernandez,
2012; Rong et al., 2013).
In the human diet, the avian egg is an important source of nutrients,
containing proteins, lipids, vitamin D, vitamin B12, selenium and other
minerals, choline, and growth factors required by the developing em-
bryo, as well as a number of defense factors to protect against bacterial
and viral infection. In addition, eggs contain substances with biological
functions beyond basic nutrition (Ruxton, Derbyshire, & Gibson,
2010). A medium-sized egg provides approximately 78 kcal, containing
about 6.5 g of protein and 5.8 g of fat, being 2.3 g monounsaturated fat.
The lipids are found almost exclusively in the egg yolk, mainly as lipo-
proteins, while the majority of proteins are found in the egg yolk and
the egg white, and only a small proportion in the eggshell and the
shell membrane (Kovacs-Nolan, Phillips, & Mine, 2005). Notwithstand-
ing, eggs, as a large number of other food items, are also a source of
dietary cholesterol.
On the other hand, it is also important to take into account that eggs
are an inexpensive and low calorie source of many other nutrients,
including minerals, proteins and unsaturated fatty acids, which could
lower the risk of cardiovascular disease (Fernandez, 2012; Rong et al.,
2013). Moreover, in populations following a carbohydrate restricted
diet, dietary cholesterol from eggs could increase plasma concentrations
of HDL cholesterol, which has been suggested to protect against
vascular disease. Consequently, in recent years some health organiza-
tions have recommended that reducing egg intake might not be impor-
tant for healthy people with normal levels of cholesterol in the blood
(Better Health Channel-BHC Australia, 2009; Fernandez, 2012; Rong
et al., 2013).
Because globally eggs may be a healthful food, it is important that
sensible strategies be recommended for inclusions of eggs in a healthy
diet. Consequently, the daily consumption of avian eggs is being
reconsidered based on the recent recommendations for dietary choles-
terol for health populations. Eggs are also a good source of several
nutrients, such as high-quality protein, choline, selenium, and lutein.
The current American Heart Association (AHA) recommendations are
the following: to balance caloric intake and physical activity to achieve
and maintain a healthy body weight; consume a diet rich in vegetables
and fruits; choose whole-grain, high-fiber foods; consume fish,
especially oily fish, at least twice a week; limit intake of saturated fat
to b7% of energy, trans fat to b 1% of energy, and cholesterol to
b300 mg/day by choosing lean meats and vegetable alternatives,
fat-free (skim) or low-fat (1% fat) dairy products, and minimize intake
of partially hydrogenated fats; minimize intake of beverages and foods
with added sugars; choose and prepare foods with little or no salt.
3. Chemical pollutants in eggs
Certain dietary habits can also contribute to compromised health by
being a source of exposure to environmental contaminants. Many of
these potentially toxic pollutants are fat soluble, and thus, any fatty
food (including eggs) often may contain high levels of persistent organic
pollutants (POPs). A number of studies have shown that eggs as many
other food items, especially those with a high fat content, can be a po-
tential source of human exposure to environmental contaminants,
whose potential toxicity is well known. Among these pollutants that
stand out are metals, polychlorinated dibenzo-p-dioxins and dibenzofu-
rans (PCDD/Fs), or polycyclic aromatic hydrocarbons (PAHs), but also
other organohalogenated contaminants such as polybrominated
diphenyl ethers (PBDEs), polychlorinated diphenyl ethers (PCDEs),
polychlorinated naphthalenes (PCNs), and perfluorinated compounds
(PFCs). Information on exposure and adverse effects for most of these
organic pollutants in humans is still relatively limited.
Next, the results of various recent international studies, in which the
concentrations of chemical contaminants in eggs were determined, are
summarized. In a survey of residues of organochlorine pesticides (OPs)
in hen eggs of Uganda (Ejobi, Muller, Opunda-Asibo, & Kruger, 2000), it
was concluded that egg contamination with residues of OPs from areas
of Uganda included in the study presented a low health risk to the con-
sumers. It was remarked that organochlorine residue levels in hen eggs
of Uganda were relatively lower than those previously found in other
African countries. Sasamoto et al. (2006) estimated the dietary intake
of dioxins (PCDD/Fs and dioxin-like PCBs) through foods retailed in
the metropolitan Tokyo area from 1999 to 2004. The study was carried
out by the total diet-market basket method on the basis of food classifi-
cation (14 groups), the data on food consumption in the Tokyo region
being obtained from the Japan Nutrition Survey. It was found that
more than 90% of the daily intake of dioxins proceeded from the groups
of fish and shellfish, meat and eggs, and milk and dairy products. More-
over, high levels of PCDD/Fs in eggs, among other foodstuffs, were also
detected in an assessment of the dietary exposure to some POPs in the
Republic of Karakalpakstan, Uzbekistan (Muntean et al., 2003). In turn,
when the levels of PCDD/Fs and PCBs were determined in the blood of
non-occupationally exposed residents living in the vicinity of a chemical
plant in the Czech Republic (Cerná et al., 2007), a positive correlation of
the PCDD/F and PCB blood levels with age and with consumption of
locally produced eggs was found.
Polder et al. (2010) analyzed residues of several POPs in 70 selected
food items from Northwest Russia in 1998–2002. The levels of PCBs in
eggs ranged from 0.5 to 16 ng/g wet weight (ww). Mean levels in
 J.L. Domingo / Food Research International 56 (2014) 159–165
eggs of sum TEQs of dioxin-like mono-ortho PCBs: PCBs 105, 118, 156
and 157 (∑mo-PCBs-TEQs) were 0.245 pg/g ww, respectively, being
eggs, together with fish, dairy products and meat, as the main contribu-
tors to the estimated daily intake (EDI) of ∑ mo-PCBs-TEQs. In
Romania, Dirtu and Covaci (2010) estimated human exposure to
organohalogenated contaminants, including OPs such as hexachlorocy-
clohexanes, DDT and metabolites, HCB and chlordanes, and also PCBs,
PBDEs, and hexabromocyclododecane (HBCD), through food consump-
tion (mainly food of animal origin including eggs) and indoor dust
ingestion. It was highlighted that concentrations of DDTs above the cur-
rent European maximum residue levels (MRLs) were recorded in eggs
from rural areas. On the other hand, in a Swedish market basket study
performed in 2005 and focused on analyzing the levels of various
POPs and their dietary estimations, the relative contribution to the
dietary intake of PCDD/Fs and PCBs (total-TEQ), as well as that of
∑ PBDEs was found to be 1% (Törnkvist, Glynn, Aune, Darnerud, &
Ankarberg, 2011).
Song et al. (2011) measured the levels of PCDD/Fs and DL-PCBs in
selected foods from Zheijang Province, China, where electronic waste
is being recycled. Hen eggs were among the foodstuffs showing
the highest WHO-TEQ values (2.80 pg/g ww). In another electronic
waste recycling region of China (South), the concentrations of three reg-
ulated halogenated flame retardants (HFRs) were measured in home-
produced eggs. Mean levels of HFRs in eggs from the recycling sites
ranged 2640–14,100, 700–1620, 44–350, and 720–3920 ng/g lipid
weight for ∑PBDEs, ∑PBBs (polybrominated biphenyls), ∑ HBCDs
(hexabromocyclododecanes) and ∑AHFRs (several alternative HFRs),
respectively, which were one to two orders of magnitude higher than
those found in the reference site (Zheng et al., 2012).
Recently, Rawn et al. (2012) assessed the impact of production type
and region on PCB and PCDD/F concentrations in Canadian chicken egg
yolks. WHO-TEQ ranged from 0.089 pg TEQ (PCDD/F + dioxin-like
[DL]-PCB)/g lipid to 12.8 pg TEQ (PCDD/F + DL-PCB)/g lipid (median
0.342 pg TEQ (PCDD/F + DL-PCB)/g lipid). PCB and PCDD/F concentra-
tions were significantly different in egg yolks from different regions of
collection. Median PCB dietary intake estimates based on consumption
of eggs were less than 10 ng/day, while median PCDD/F intakes were
less than 45 pg/day. In Ireland, Fernandes et al. (2011) determined
the concentrations of selected PCN congeners in 100 commonly con-
sumed foods. The average sum of PCNs was 0.62 ng/kg whole weight.
Luzardo et al. (2013) investigated the influence of the method of pro-
duction of eggs on the daily intake of PAHs and organochlorine con-
taminants in the Canary Islands (Spain). Analysis of 16 PAHs, 20 OPs
and 18 PCBs were performed on eggs from three different production
types (conventional, free-run and organic). It was found that the
mean dietary intake estimates of the organochlorine contaminants
based on consumption of eggs, regardless of the type chosen, was
negligible for the Canary Islands' population. However, the median
dietary intake estimates of PAHs greatly depended on the type of
eggs chosen, being much lower when free-run and organic eggs are
consumed. On the other hand, the transfer of dioxins from contami-
nated soils to eggs was recently assessed by Piskorska-Pliszczynska,
Mikolajczyk, Warenik-Bany, Maszewski, and Strucinski (2014) in
Poland. The sum of the WHO-PCDD/F/PCB-TEQ concentrations,
exceeding two-fold the European Union's maximum level, was de-
tected in eggs from a free-range farm (12.55 ± 2.37 pg WHO-
PCDD/F/PCB-TEQ/g fat). The weekly intake of dioxins for an adult
would be 3.5 pg WHO-TEQ/kg body weight (24.9% of the tolerable
weekly intake TWI).
4. A case-study: Catalonia, Spain
In 2000, we initiated in our laboratory an extensive program aimed
at determining the daily intake of various chemical contaminants by
the general population of Catalonia, Spain. The first survey of that
program was performed between 2000 and 2002. In the summer of
161
2000, food samples were randomly obtained in local markets, large su-
permarkets, and grocery stores from seven cities of Catalonia, with pop-
ulations between 150,000 and 1,800,000 inhabitants. A total of 11 food
groups were included in that study, constituting hen eggs as one of
these groups. The following contaminants were analyzed: As, Cd, Hg
and Pb (Llobet, Falcó, Casas, Teixidó, & Domingo, 2003), hexachloroben-
zene (Falcó et al., 2004), PCNs (Domingo et al., 2003), PCDD/Fs (Llobet
et al., 2003), PCBs (Llobet et al., 2003), PBDEs (Bocio et al., 2003),
PCDEs (Bocio, Llobet, & Domingo, 2004), as well as a number of PAHs
(Falcó et al., 2003). The daily intakes of these pollutants were calculated
by multiplying the concentration in each specific food item by the esti-
mated daily consumption of the respective food group. Finally, the total
dietary intake of each pollutant was calculated by summing each prod-
uct over all the food groups.
In 2006–2008, we carried out the second survey of the program.
There were some differences with the design of the previous study: a)
an increase in the number of cities in which food samples were pur-
chased, 12 in total, b) the inclusion of a new food group, bakery prod-
ucts, and c) an increase in the number of fish and seafood species
analyzed. We measured the same chemical pollutants as those deter-
mined in the previous survey. Food samples were collected between
March and June of 2006.
The most recent study of the program was initiated in 2008. The
samples were purchased in the same 12 Catalan cities during Novem-
ber–December of 2008, being also divided into the same 12 food groups
than those of the previous survey. The results corresponding to hen eggs
in the three surveys of the program are next summarized.
4.1. Trace elements
In our first study (BF1), As, Cd, Hg and Pb concentrations were 0.015,
0.008, 0.001 and 0.015 μg/g wet weight, respectively. Based on an aver-
age consumption of eggs by the male adults in Catalonia, 34 g/day, the
intakes of As, Cd, Hg and Pb for male adults were 0.51, 0.27, 0.27
and 0.51 μg/day, respectively (Llobet, Falcó, Casas, Teixidó, &
Domingo, 2003). In the second survey (BF2), As, Cd, Hg and Pb con-
centrations were b0.100, b 0.025, b0.100 and 0.042 μg/g wet weight,
respectively. Based on a daily consumption of eggs of 31.07 g, the in-
takes of As, Cd, Hg and Pb for a male adult were 0.00, 0.00, 0.00 and
1.31 μg/day, respectively (Martí-Cid, Bocio, Llobet, & Domingo,
2008). Finally, in the most recent study (BF3), As, Cd, Hg and Pb con-
centrations were b0.100, b 0.025, b0.100 and 0.076 μg/g wet weight,
respectively (ND was assumed to be zero, ND = 0). Based on the same
daily consumption of eggs (31.07 g), the intakes of As, Cd, Hg and Pb
for a male adult were 0.00, 0.00, 0.00 and 2.35 μg/day, respectively
(Martorell et al., 2011).
4.2. Hexachlorobenzene (HCB)
The mean HCB concentrations in eggs were 0.182 (Falcó et al., 2004),
0.175 (Martí-Cid, Llobet, Castell, & Domingo, 2008a, 2008b, 2008c,
2008d) and 0.038 ng/g (Perelló, Gómez-Catalán, Castell, Llobet, &
Domingo, 2012a, 2012b) of fresh weight for the BF1, BF2 and BF3 sur-
veys, respectively. The estimated intakes of HCB through hen egg
consumption by the adult population of Catalonia were respectively,
6.26, 5.47 and 1.19 ng/day.
4.3. Polychlorinated naphthalenes (PCNs)
The mean concentrations of PCNs (∑ PCNs tetra-octa) in the BF1
and BF2 studies were respectively, 23 (Domingo et al., 2003) and
4.3 ng/kg wet weight (Martí-Cid, Llobet, Castell, & Domingo, 2008a,
2008b, 2008c, 2008d). No data corresponding to BF3 are available. In
turn, the estimated intakes of PCNs through hen egg consumption by
the adult population of Catalonia were 0.80 and 0.13 ng/day in the
BF1 and BF2, respectively.
162 J.L. Domingo / Food Research International 56 (2014) 159–165

4.4. Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) corresponded again to phenanthrene (2.43 μg/kg wet weight), and
naphthalene (1.54 μg/kg wet weight), the mean total PAH concen-
The mean PCDD/F concentrations (WHO-TEQ values) in eggs in the tration being 8.56 μg/kg wet weight, and the mean dietary intake
BF1, BF2 and BF3 surveys were, respectively, 0.58 (ng/kg fat) (Llobet, of PAHs through hen egg consumption, 0.27 μg/day (sum of 16 PAHs)
Domingo, et al., 2003), 0.014 (ng/kg fresh weight) (Llobet, Martí-Cid, (Martí-Cid, Llobet, Castell, & Domingo, 2008a, 2008b, 2008c, 2008d).
Castell, & Domingo, 2008) and 0.032 (ng/kg fresh weight) (Perelló Finally, in the BF3 study, the highest concentration corresponded to
et al., 2012a, 2012b). The estimated intakes of PCDD/Fs through hen naphthalene (1.20 μg/kg wet weight), the mean total PAH concen-
egg consumption by an adult male in Catalonia were 2.37, 0.43 and tration being 3.62 μg/kg wet weight and the mean dietary intake of
1.09 pg WHO-TEQ/day, for the BF1, BF2 and BF3 surveys, respectively. PAHs through egg consumption was 0.11 μg/day (sum of 16 PAHs)
(Martorell et al., 2010).
4.5. Polychlorinated biphenyls (PCBs)
4.9. Summary of results
In the BF1 study, the levels of 11 PCB congeners (IUPAC No. 28, 52,
77, 101, 105, 118, 126, 138, 153, 169 and 180) were measured. The The above results are summarized in Table 1. A detailed assessment
mean concentration of all PCBs in hen eggs was 475.2 ng/kg fresh of our more recent data (BF2 and BF3 studies) shows that, assuming an
weight, or 24.82 pg WHO-TEQ/kg fresh weight (Llobet, Domingo, average daily consumption of 31 g of eggs by the male adult (70 kg of
et al., 2003), while the estimated intake of PCBs through egg consump- body weight) population of Catalonia, the percentages of contribution
tion for 70-kg (body weight) adult males (20 to 65 years old) living in to exposure for the analyzed pollutants through the consumption of
Catalonia was 0.84 pg WHO-TEQ/day. In the BF2 study, the mean PCB hen eggs would be the following (always referred to the 100% of
concentration (18 congeners, including 12 dioxin-like (DL) PCBs) and the ingested contaminant in the total consumed foodstuffs): about 0%
the adult male dietary intake of the DL-PCBs were, respectively, 18 (negligible) for inorganic As, Cd and Hg, and 2.36% for Pb (Martorell
.0 pg WHO-TEQ/kg fresh weight and 0.55 pg WHO-TEQ/day (Llobet et al., 2011); 3.16% for hexachlorobenzene (Perelló et al., 2012a,
et al., 2008). Finally, in the BF3 survey the mean PCB concentration 2012b); 1.79% for PCNs (Martí-Cid, Llobet, Castell, & Domingo, 2008a,
(18 congeners, including 12 dioxin-like (DL) PCBs) and the adult male 2008b, 2008c, 2008d); 6.93% for PCDD/Fs (Perelló et al., 2012a,
dietary intake of the DL-PCBs were, respectively, 15.0 pg WHO-TEQ/kg 2012b); 1.85% for PCBs (Perelló et al., 2012a, 2012b); 3.98% for PBDEs
fresh weight and 0.48 pg WHO-TEQ/day (Perelló et al., 2012a, 2012b). (Domingo et al., 2008); 0.10% for PCDEs (Martí-Cid, Llobet, Castell, &
Domingo, 2008a, 2008b, 2008c, 2008d), and 1.69% for PAHs (sum of
4.6. Polybrominated diphenyl ethers (PBDEs) 16 different PAHs) (Martorell et al., 2010). Interestingly, exposure to
these environmental contaminants through egg consumption, given in
The mean concentrations of PBDEs (∑PBDEs tetra-octa) in the BF1 percentages of the total dietary exposure to each pollutant, was for
and BF2 studies were respectively, 333.9 (Bocio et al., 2003) and most contaminants lower than 2.52%. This is the percentage of the
94.8 ng/kg wet weight (Domingo, Martí-Cid, Castell, & Llobet, 2008). daily consumption of eggs on the total daily intake of all foodstuffs
No data corresponding to BF3 are available. In turn, the estimated in- here analyzed. The only exceptions were PCDD/Fs, with a 6.93% in BF3
takes of PBDEs through hen egg consumption by the adult (males, vs. the previous 1.67% (BF2) (Llobet et al., 2008) and 2.48% (BF1)
70 kg body weight) population of Catalonia were 2.2 and 3.0 ng/day (Llobet, Domingo, et al., 2003), PBDEs in BF2 (no BF3 data are available),
in the BF1 and BF2, respectively. and HCB, with a 3.16% in BF3, but decreasing since the previous 7.64%
(BF2) and 3.77% (BF1) (Perelló et al., 2012a, 2012b). It is particularly
4.7. Polychlorinated diphenyl ethers (PCDEs) important to know the trend in PCDD/Fs, as well as to pursue with the
PBDE analysis.
In the BF1 study, the mean concentrations of PCDEs were for all ho-
mologues (tetra- to octaCDE) under the respective detection limits 4.10. Perfluoralkyl substances
(Bocio et al., 2004). To estimate the PCDE intake by the adult male
(70 kg body weight) population of Catalonia, for the groups of homo- Recently, we also assessed exposure to perfluoroalkyl substances
logues below the detection limit, it was assumed that the concentration through the diet. In a preliminary study (Ericson et al., 2008), we deter-
would be equal to one-half of the respective limit of detection. Thus, mined the dietary intake of 11 perfluorinated chemicals (PFCs) by the
exposure to PCDEs through hen egg consumption was estimated to be
0.04 ng/day. A similar assumption was done in the BF2 study, the Table 1
∑ PCDEs (tetra to octa) in eggs being 1.5 ng/kg fresh weight, and Daily intake of a number of chemical contaminants through the consumption of eggs by
the estimated intake was 0.05 ng/day (Martí-Cid, Llobet, Castell, & the male adult population of Catalonia, Spain.
Domingo, 2008a, 2008b, 2008c, 2008d). No data corresponding to BF3
Chemical contaminant BF1 (2000–2002) BF2 (2006–2008) BF3 (2008–2011)
are available.
Trace elements
(μg/day)
4.8. Polycyclic aromatic hydrocarbons (PAHs) Arsenic 0.51 0.00 0.00
Cadmium 0.27 0.00 0.00
In our BF1 study, we determined the levels of 16 PAHs (naphthalene, Mercury 0.27 0.00 0.00
acenaphthylene, acenaphthene, fluorene, phenanthrene, anthracene, Lead 0.51 1.31 2.35
Hexachlorobenzene 6.26 5.47 1.19
fluoranthene, pyrene, benz[a]anthracene, chrysene, benzo[b]fluoran- (ng/day)
thene, benzo[k]fluoranthene, benzo[a]pyrene, dibenz[a,h]anthracene, PCNs (ng/day) 0.80 0.13 Not determined
benzo[g,h,i]perylene and indeno[1,2,3-c,d]pyrene) in a number of PCDD/Fs 2.37 0.43 1.09
foodstuffs including hen eggs. The highest concentrations corresponded pg WHO-TEQ/day
PCBs 0.84 0.55 0.48
to phenanthrene (0.827 μg/kg wet weight) and naphthalene
pg WHO-TEQ/day
(0.620 μg/kg wet weight), the mean total PAH concentration being PBDEs (ng/day) 2.2 3.0 Not determined
2.423 μg/kg wet weight (Falcó et al., 2003). For male adults living PCDEs (ng/day) 0.04 0.05 Not determined
in Catalonia, the mean dietary intake of PAHs through egg consump- ∑PAHs (16) 0.083 0.27 0.11
tion was 0.083 μg/day (sum of 16 PAHs). In the BF2 study, when the Average body weight: 70 kg. Average consumption of eggs: BF1, 34.0 g/day; BF2 and BF3,
same 16 PAHs were also determined, the highest concentrations 31.07 g/day.
 J.L. Domingo / Food Research International 56 (2014) 159–165
population of Tarragona County (Catalonia). PFC levels were deter-
mined in 36 composite samples of foodstuffs randomly purchased in
various locations. Samples of hen eggs were included. Perfluorooctane
sulfonate (PFOS), perfluorocarboxylate perfluorooctanoate (PFOA),
and perfluoroheptanoic acid (PFHpA) were the only compounds detect-
ed in foodstuffs, with only PFOS being specifically found in eggs
(0.082 ng/g of fresh weight). For male adults, it would mean an average
intake of 2.8 ng/day. On a total daily intake of 74.2 ng/kg of body weight
for PFOS, the contribution of the egg consumption would mean 2.8%. In
a recent study (Domingo et al., 2012), we assessed the levels of 18
perfluoroalkyl substances (PFASs) in the most widely consumed
foodstuffs in Catalonia, as well as the total dietary intake of these com-
pounds. Among the 18 analyzed compounds, only PFHpA was detected
in eggs (0.20 ng/g of fresh weight), while PFOS levels (b5.3 ng/g of
fresh weight) were under the detection limit for this compound. For
male adults, these values would mean intakes of 3.12 and 1.84 ng/kg
of body weight for PFHpA and PFOS, respectively. However, the intake
of both compounds through hen egg consumption was notably lower
than that from the consumption of fish and shellfish, the group contain-
ing the highest PFC concentrations, but also lower exposure from con-
sumption of meat and meat products, milk, and other widely consumed
foodstuffs (Domingo et al., 2012).
5. The CONTEGG study, Belgium
Home-produced eggs from Belgian private owners of hens were
included in a large study aimed at determining the concentrations of
various environmental contaminants. The study was conducted for the
Belgian Federal Public Service of Health, Food Chain Safety and Environ-
ment during 2006–2007. Eggs were analyzed for PCDD/Fs, PCBs (includ-
ing dioxin-like PCBs), organochlorine pesticides, trace elements, PAHs
and PBDEs. In addition to these chemical contaminants, mycotoxins
were also analyzed (van Overmeire et al., 2009; van Overmeire et al.,
2009). The mean fresh weight concentrations in eggs in autumn 2006
and spring 2007, respectively, were b8.0 and b8.0 μg/kg for arsenic,
0.5 and b 0.5 μg/kg for cadmium, 116 and 74 μg/kg for lead, 0.43 and
0.52 mg/kg for copper, 20.3 and 19.2 mg/kg for zinc, and 3.15 and
4.44 μg/kg for mercury. The average Pb concentrations were higher
than those found in eggs from other countries. The Pb concentrations
correlated well with those found in soils, which shows that soils are
an important source of Pb contamination for eggs. Other pollution
sources of trace elements in eggs might be home-grown vegetables
and forage, but also, indirectly, air pollution (Waegeneers, Hoenig,
Goeyens, & de Temmerman, 2009). When the levels of PCBs and persis-
tent organochlorinated pesticides (OC) were measured in home-
produced eggs, the mean and median values of the sums of DDTs
were 457.2 and 63.4 ng/g fat, respectively. Hexachlorohexane, endosul-
fan, endrin, methoxychlor and nitrofen were not detected in any sam-
ple. In turn, the median PCB concentrations in eggs for the whole set
of data were 15.0 and 32.6 ng/g, for eggs collected in spring and au-
tumn, respectively. The sum of marker PCBs (IUPAC No. 28, 52, 101,
118, 153, 138 and 180) showed a minimum value of 0.0 ng/g fat and a
maximum value of 345.6 ng/g fat (Windal et al., 2009). On the other
hand, the total WHO-TEQ levels in eggs, determined by HRGC-HRMS,
ranged from 3.29 to 95.35 pg TEQ/g fat in autumn, and from 1.50 to
64.79 pg TEQ/g fat in spring. The minimum and maximum values, de-
termined by CALUX, were 1.52 and 12.77 pg WHO-TEQ/g fat, respec-
tively. All these levels included PCDD/Fs and dioxin-like PCBs. From a
point of view of human health risks, a consumption of the analyzed
eggs would mean 5–79% of the tolerable weekly intake (TWI) of 14 pg
TEQ/kg body weight for PCDD/Fs and dioxin-like PCBs by exposure to
their home-produced eggs only (van Overmeire, Waegeneers, et al.,
2009). Finally, the concentrations of PBDEs (sum of 13 congeners, in-
cluding BDE-209) ranged between not detected (ND) and 32 ng/g
lipid weight, with medians of 3.0 and b2.0 ng/g lipid weight for the au-
tumn 2006 and spring 2007 surveys, respectively. BDE-209 was the
163
major PBDE congener (45% of sum PBDEs) when it could be detected,
while when BDE-209 was not detected, the PBDE profile was composed
of pentaBDE (BDE-99 and BDE-47) and octaBDE (BDE-183 and BDE-
153), the contribution of the last higher being in certain cases (Covaci
et al., 2009).
The above results indicate that, in general terms, home-produced
eggs show higher levels of chemical contaminants than commercially
produced eggs. Previous studies to assess chemical contamination
(trace elements including the toxic elements As, Cd, Hg and Pb, PCDD/
Fs, marker and dioxin-like PCBs, and DDT and other OCs) of free-range
eggs from Belgium showed that eggs from private owners were more
contaminated than those from commercial farms (van Overmeire
et al., 2006). The reason was mainly due to the fact that chickens
foraging on soils contaminated with environmental pollutants accu-
mulate these compounds into their eggs. The transfer of soil contam-
inants to home-produced eggs was assessed with PCDD/Fs and Pb. It
was shown that soils were the major source of PCDD/Fs and Pb in
home-produced eggs. The main goal of the study was to formulate
preventive measures, which might reduce the contamination of
such eggs (Waegeneers et al., 2009). It is important to remark that
contamination levels in soil should be kept low and should be con-
trolled in areas with free foraging chicken. However, all modifying
factors potentially influencing uptake of PCDD/Fs and PCBs from
the environment and transfer into eggs are not well understood yet
(Schoeters & Hoogenboom, 2006).
6. Eggs and the “Belgian PCB/dioxin crisis”
In February of 1999, a poisoning episode broke out in several poultry
farms in Belgium. A mixture of PCBs contaminated with PCDD/Fs was
accidentally added to a stock of recycled fat used in the production of
animal feeds. Although the first signs of poultry poisoning were noticed
by February, 1999, the source and the extent of the contamination were
not discovered until May 1999, when it appeared that more than 2500
farms could have been supplied with contaminated feeds (Bernard
et al., 1999; Bernard et al., 2002). The study of PCB levels and profiles
in contaminated feeds delivered to poultry or pig farms confirmed
that the Belgian PCB incident was due to a single source of PCB oil intro-
duced into the food chain at the end of January 1999. This PCB oil had a
congener pattern closely matched to a mixture of Aroclor 1260/1254 in
the proportion 75/25. The total amount of PCBs added to recycled fats
was estimated at 50 kg (sum of the seven markers), or approximately
150 kg total PCBs, which corresponded to about 100 l of PCB oil
(Bernard et al., 2002). Seven million chickens and 50,000 pigs were
slaughtered and discarded. Many farms were closed down for months
and animal food products were banned from the market. During the in-
vestigation, questions were raised as to whether the costs for destroying
the food and feedstock were necessary, as it seemed obvious that the
contaminated food had already passed through the food market during
the period from January to May. At the end of December 1999, the data-
base contained the results of more than 55,000 PCB and 500 dioxin
analyses. Specifically concerning whole eggs, the mean PCBs value
was 839 (range 515–1631) ng/g fat, while the mean PCDD/Fs values
was 3.8 (range 1.2–19.6) ng/g fat (Bernard et al., 2002), while according
to van Larebeke et al. (2001) the means ± SDs and the maximum
concentrations of PCDD/Fs (expressed in TEQ) and PCBs observed per
gram of fat in contaminated eggs were 32.0 ± 104.4/713.3 pg, and
392.7 ± 2883.5/46,000.0 ng, respectively. For comparative purposes
only, the current maximum values of PCDD/Fs and PCBs in hen eggs
and egg products established by the European Union are these: sum of
dioxins (WHO-PCDD/F-TEQ), 3.0 pg/g fat; sum of dioxins and dioxin-
like PCBs (WHO-PCDD//F–PCB-TEQ), 6.0 pg/g fat, and sum of PCB 28,
PCB 52, PCB 101, PCB 158, PCB 153 and PCB 180 (ICES 6), 40 ng/g fat
(EU, 2011). With respect to human health risk assessment following
that serious incident, the results were rather contradictory. It was sug-
gested that, since only a limited proportion of the food chain was
164 J.L. Domingo / Food Research International 56 (2014) 159–165
contaminated, it would be unlikely that adverse effects affected the
Belgian population. However, another assessment suggested that neu-
rotoxic and behavioral effects in neonates, together with an increase
in the number of cancers, might be observed (Covaci et al., 2008).
7. Conclusions
The scientific data here reviewed show that, in general terms, the
nutritional benefits of the regular consumption of hen eggs by the gen-
eral population, clearly outweigh the potential health risks derived from
potential exposure to a number of chemical pollutants through that
consumption. Recent studies have suggested that frequent consump-
tion of eggs (up to one egg per day) is not associated with increased
risk of coronary heart disease or stroke (Rong et al., 2013). However,
the increased risks of coronary heart disease among diabetic patients,
and reduced risk of hemorrhagic stroke associated with higher egg
consumption in subgroup analyses, would require further studies for
specific population groups (Rong et al., 2013). Regarding exposure to
chemical contaminants, it must be highlighted that the human health
risks will derive from all the general dietary habits of each individual, in-
cluding especially the regular consumption of fish and seafood, meat
and meat products, vegetables and fruits, milk and dairy products, etc.,
and not only on the specific consumption of a certain food item such
as eggs. Because they are the most consumed foods, the frequency of
their consumptions, and the meal sizes, are essential issues for the
balance of the health benefits and risks of the dietary habits of a certain
subject (Martí-Cid, Bocio, Llobet, & Domingo, 2008).
Finally, I would like to call the attention of the readers on some
limitations of this review, taking into account that it basically focused
on the risks of environmental pollutants only. For example, it is well
known that poultry treated with pharmaceutical products can produce
eggs contaminated with drug residues, which could pose a risk to con-
sumer health. This is an important issue requiring probably an addition-
al review of the scientific literature much broader than the current one.
For those particularly interested in the role of veterinary drugs in laying
hens and residues in eggs, I would suggest to consult the reviews on that
topic by Donoghue (2003), Pompa, Arioli, and Fracchiolla (2005),
Anadón et al. (2009), and Goetting, Lee, and Tell (2011). Outside the
purpose of the current review was also the potential exposure of laying
hens to mycotoxins through naturally contaminated feed, another issue
of notable concern (Awad, Ghareeb, Böhm, & Zentek, 2013; Yunus,
Razzazi-Fazeli, & Böhm, 2011).
Conflict of interest statement
None.
Funding source
None. This is a Review article and no funding is necessary for prepar-
ing this paper.
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