Trends in Food Science & Technology 75 (2018) 36–45

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Trends in Food Science & Technology

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Review

Occurrence of trace metals in foodstuffs and their health impact T

∗
Ahmed A. El-Kady, Mosaad A. Abdel-Wahhab
Food Toxicology & Contaminants Department, National Research Centre, Dokki, Cairo, Egypt

A R T I C LE I N FO A B S T R A C T

Keywords: Background: Unlike organic pollutants, heavy metals are not created nor are biodegradable materials. They
Heavy metals naturally occur in earth crust and many of them reach the environment via anthropogenic activities, which
Sources belonged to mining, smelting, production of fertilizers, pesticide applications and others.
Foodstuffs Scope and approach: Due to their water solubility and bioaccumulative tendency in different matrices of the
Health impact
environment, some heavy metals are extremely toxic even at low exposure levels and can be transported into the
food chain.
Key findings and conclusions: Many criteria are defined to identify heavy metals based on their specific gravity,
weight and atomic number, chemical properties and their toxicity, therefore the heavy metals term is still very
loose. Dietary exposure is a significant route for trace metals to the humans and constitutes about 90% of
exposure. Long term exposure to metals via food consumption, drinking water or other occupational sources
leads to serious problems, e.g., hepatotoxicity, kidney failure and neurotoxicity. Analysis of the current situation
concluded that the concentrations of heavy metals declined over the years, but they are still hot spots suffering
from domestic wastes, agrochemicals like pesticides, fertilizers and industrial wastes. Due to the contamination
sources in those hot spots, levels of some metals exceeded the approved permissible limits and become sources of
severe problems to humans. Almost comprehensive hazard assessment of these metals is missing due to in-
sufficient data corresponding to body burden for groups potentially exposed to high concentration of metals and
their concentrations in foodstuffs.

1. Introduction essential metals, which are necessary for human health, such as copper,
zinc, iron, cobalt … etc. For instance, cobalt has a major role in pro-
Several scientific definitions were established for heavy metals, ducing red blood cells and is a component of Vit. B12 (Klotz, Kröncke,
which have been reviewed through literature and scientific publications Buchczyk, & Sies, 2003). Non-essential metals are those that have no
with multitude of identification according to different criteria. positive role in a biological system and are toxic even at low level ex-
Confusion and considerable debate and argument on the exact identi- posure. These metals include lead, cadmium, mercury and uranium.
fication of heavy metals have occurred until now. The definition in Metals are different from persistent organic pollutants since they are
terms of specific gravity is most popular since several criteria had been not created or destroyed. They are not subjected to the biodegradation
approached according to the density of metals. These reference points process such organic pollutants. Once they released into the aquatic
ranged from 3.5 to 7 g/cm3 (Duffus, 2002; Hodson, 2004). Another environment, they are adsorbed by sediments, re-released into the
definition criterion depends on the atomic weight, which sets the aquatic environment and begin to biomagnify in the aquatic food chain
number at 23 and 40 for heavy metals. The third method identified (Nfon et al., 2009).
heavy metals as having an atomic number above 20. This category in- Due to their characteristics as non degradable and resistant to nat-
cludes essential metals such as potassium and magnesium (Duffus, ural biodegradation, the tendency of their accumulation in all media
2002). Other definitions are set based on chemical properties or toxicity including soil and aquatic environments is, therefore very high (Gilbert
of metals (Duffus, 2002; Klaasen, 2001). So, the terminology of the & Weiss, 2006). The bioconcentration process, which describes the
heavy metals is very loose and there is an inexact scientific term. abstracting of metals from the surrounding environment into the or-
While all metals are considered toxic at a certain level of exposure, ganism is the primary step in food chain contamination. Such bio-
many metals are essential and have an important role in biological concentration and biomagnifications are becoming a significant source
systems. In this concern, metals are classified into two main groups: of health hazards once they exceed the safe limits (Khan, Cao, Zheng,

∗
Corresponding author.
E-mail address: [email protected] (M.A. Abdel-Wahhab).

https://doi.org/10.1016/j.tifs.2018.03.001
Received 9 January 2018; Received in revised form 1 March 2018; Accepted 2 March 2018
Available online 06 March 2018
0924-2244/ © 2018 Elsevier Ltd. All rights reserved.
A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

Huang, & Zhu, 2008). More than one thousand million tons of metals and porcelain by the ancient Egyptians and Chinese who applied a thin
are produced from the age of stone as estimated by Lu and Wang film of lead oxide as a waterproof layer (Ye & Wong, 2006). In this case,
(2012). In mining process, each ton produces 420 kg of worthless ma- lead ions (Pb2+) become a source of contamination within a short time
terials, which is called mullock, 520 kg of tailing (separated during of contact with acidic food based on this reaction:
preparation of the final product), 40 kg of wastes and finally 20 kg of
PbO(s) + 2 H+(aq) → Pb2+(aq) + H2O
useful metals (Ripley, Redmann, & Crowder, 1996, pp. 1–356). There-
fore the natural occurrences of heavy metals together with anthro- Lead acetate is another example that is used in direct contact with
pogenic sources induce the accumulation of these metals in the food humans to convert white or grey hair to a dark color as a result of lead
web (Zhang, Huang, Dong, Hu, & Akhtar, 2017). ion (Pb2+) reacting with the sulfur group (SH) of hair protein.
The toxicity of metals can be divided into chronic or acute toxicity. Moreover, lead acetate is used as a dye for cottons, pigments of chrome,
Most metals have a high affinity with the sulfhydryl group and can pesticides and paint productions (Asaduzzaman et al., 2017). Moreover,
inhibit more than two hundred enzymes in the biological system (Jan lead nitrate has many applications in several products, e.g., matches,
et al., 2015). Long term exposure to trace metals induces toxicity in printing of textiles, oxidizer, sensitizer, and rodenticides (García-Lestón
many organs of human body such as hepatonephrotoxicity and neuro- et al., 2010). Nowadays, traditional lead pipes, which are manufactured
toxicity (Caito & Aschner, 2014). From the practical standpoints of the from polyvinyl chloride (PVC), have been replaced by other kinds of
above presentation, this review explores the concept of heavy metals, polymers (polypropylene, polyethylene), free of lead stabilizers and
identify the origin and anthropogenic sources of trace metals and ex- accounting for 54% of pipes worldwide (Lasheen, Sharabym, El-Kholy,
plain the transfer of heavy metals from different origins to humans Elsherif, & El-Wakeel, 2008). Drinking water represents one-fifth of
through the food chain as well as the health hazards associated with the lead total daily intake in the United States since the vast majority of
exposure and intake of these metals via foodstuffs. lead intake is from food (Levin, Schock, & Marcus, 1989). In Egypt,
Lasheen et al. (2008) tested the lead content of water released from
2. Sources of heavy metals three kinds of pipes manufactured from different materials and found
that water released from polyvinyl chloride (PVC) pipes had the highest
2.1. Natural sources concentration of lead (0.113 mg/L) followed by pipes made from gal-
vanized iron (GI) (0.062 mg/L), and then polypropylene (PP) pipes
Heavy metals such as aluminium, iron and magnesium occur (0.040 mg/L).
naturally in the environment and constituted 7.4%, 4.7% and 2.1%,
respectively of the earth's crust (Manahan, 2000). The releasing and
4. Mercury (Hg)
distribution of heavy metals from rocks to various environmental media
is affected by many erosion factors, e.g., rainfall intensity, amount,
Mercury is a toxic metal that exists in the environment in different
frequency of rains, vegetation and physical properties of soil
forms including; elemental form (Hg0), which is liquid at ambient
(Rodríguez, Ramos-Miras, Boluda, & Gil, 2013). Volcanic activities,
temperature; inorganic forms like mercury chloride (HgCl2), mercury
continental weathering and forest fires are also considered natural
bromide (HgBr2), mercury oxide (HgO); and organic form such as
sources of heavy metals that together with anthropogenic sources in-
methyl mercury, which is considered to be highly toxic to humans
duce the accumulation of heavy metals in the food chain (Zhang et al.,
(Wang, Kim, Dionysiou, Sorial, & Timberlake, 2004). The three primary
2017).
sources of Hg are natural, anthropogenic and re-emission. Natural
sources, mainly come from degassing of the terrestrial system con-
2.2. Anthropogenic sources
taminated with Hg, volcanic activities and forest fires (Camargo, 2002).
More than two thousand metric tons of Hg were used during 1960s all
Besides the natural sources of heavy metals as mentioned above,
over the world (Wang et al., 2004). Moreover, a wide range of mercury
anthropogenic activities play an important role in transporting and
emission (590–930 metric tons) is estimated annually from pyrolysis of
spreading metals in all components of the environment, including the
biomass worldwide (Brunke, Labuschagne, & Slemr, 2001). In the
aquatic environment and food and feeds. In this respect, there are two
United States, due to the pressure of environmental groups, the total
main categories of contamination with trace metals. The first is
emission of mercury has dropped from 48 to 38 tons annually and is
smelting, mining and the other activities related to the mining industry
expected to be reduced to 15 tons. The anthropogenic sources resulted
as point sources. The second category includes non-point sources that
from the combustion of coal and oil and incineration of solid waste,
affect agricultural soils, which contaminate by the application of fer-
which have high contribution compared to other sources for the world
tilizers, organic manures, agrochemicals and composts (Goretti,
emission (Pirrone, Keeler, & Nriagu, 1996). Mercury exists in soil due to
Pallottini, Ricciarini, Selvaggi, & Cappelletti, 2016; Islam, Ahmed, Al-
the extensive use of pesticides and fungicides that contain mercury in
mamun, & Masunaga, 2014). Additionally, it was reported that foliar
their formulas.
uptake of metals emission is considered as sources of heavy metal
contamination in agricultural products (Islam, Ahmed, Al-Mamun, &
Raknuzzaman, 2015). 5. Cadmium (Cd)
The main five metals, namely, lead (Pb), mercury (Hg), cadmium
(Cd), chromium (Cr) and arsenic (As) will be discussed in more detail Cadmium is classified as carcinogenic metal and most of cadmium
based on their extensive applications, toxicity, distribution and occur- in the environment is considered as a by-product. Usually cadmium is
rence in all environmental media including foods and feeds. not found as a pure metal and high concentrations of Cd are found in
association with lead and zinc ores (Satarug, Vesey, & Gobe, 2017).
3. Lead (Pb) Phosphate fertilizers are the major sources of Cd in the soil and culti-
vated areas since phosphate rock contains ionic cadmium as a natural
Lead is a toxic metal that occurs naturally in the earth's crust and contaminant (Roberts, 2014). Huge amounts of cadmium are commonly
can be combined with other chemicals to form lead salts that have used in rechargeable nicad (nickel-cadmium) batteries used in many
many applications due to their physicochemical characterizations, e.g., devices, as a pigment and anticorrosion agents (Järup, 2003). Cadmium
softness, bad conductivity, resistance to corrosion (García-Lestón, is used as stabilizers for PVC in a form of Stearate Ba-Cd-Zn (Folarin &
Méndez, Pásaro, & Laffon, 2010; Wani, Ara, & Usmani, 2015). It is Sadiku, 2011). Tobacco also is a major source of Cd beside other metals
known that lead oxide (PbO) was used extensively in glazing pottery including Hg, Ni, and Pb. The concentration of Cd in whole tobacco

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A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

leaves ranges from 0.46 to 4.41 μg/g as stated by Rickert and Kaiserman between 20 and 300 μg/day according to the food type, agricultural
(1994). In addition, Cd can enter the aquatic environment through in- conditions and food processing (IARC, 2012). Water is the common
dustrial and agrochemical wastes, which discharge into surface water source of metal exposure through direct consumption of drinking water
bodies and then be available by aquatic organisms (Zang & Bolger, or indirect way by eating the edible parts of contaminated vegetables
2014). with trace metals, which are absorbed and accumulated in the leafy
parts of vegetables (Arora et al., 2008).
6. Chromium (Cr)
10. Inhalation
Chromium exists into the environment in three statuses: elemental
chromium (0); trivalent chromium (Cr3+); and hexavalent chromium Inhalation is considered as a primary pathway of occupational ex-
(Cr6+). Trivalent naturally occurs, while elemental and Cr6+ are typi- posure. Some metals have an important impact on its potential for in-
cally generated by industry (Zhitkovich, 2011). Cr is commonly used for halation exposure and exist in the environment as vapors. Mercury is
electroplating, corrosion protection and leather tanning. In tanning, one of this category, which exists in the atmosphere in gaseous state
trivalent binds to protein in animal skin to form leather that is resistant constituting 80% of total atmospheric mercury (Wang et al., 2004). In
to water and bacteria. Elemental chromium is mainly used in manu- the same regards, IARC together with EPA classified Cr (IV) as carci-
facturing stainless steel and alloy production. However, hexavalent nogenic material (Group 1) which has sufficient evidence to cause
chromium has several applications as an anti corrosive measure in cancer in humans via inhalation route (IARC, 2012; Waseem & Arshad,
manufacturing textile dyes and wood protection (Saha, Nandi, & Saha, 2016).
2011). The contamination of drinking water with Cr6+ is a great con-
cern due to the health risk associated with exposure of Cr6+. Ground 11. Dermal exposure
water bodies are contaminated by chromium during the production of
stainless steel, textile dyes and wood saving (Kaprara et al., 2015). Ir- Generally, skin is the effective barrier against absorption due to the
rigation practices that use wastewater consider the primary source of structure of the outer most keratinized layer of epidermal cells
this heavy metal in soil. This practice increases levels of Cr in soil and (O'Flaherty, 2000). So, exposure via skin route is only a concern for
then increases the uptake by plants (Ying-ping et al., 2011). some metals. Some metals have the ability to penetrate skin when
combined with other compounds. Nowadays, metals have become most
7. Arsenic (As) popular contact sensitizers in humans, particularly nickel, which leads
to increase the rate of nickel allergy in children, especially in developed
Arsenic is classified as a metalloid and occurs naturally as it reach countries (Brandão & Gontijo, 2012).
the environment from volcanic activities or from anthropogenic sources One of the primary sources of contamination with heavy metals is
like smelting and mining of gold, lead, copper and nickel, manu- street dust, which is characterized by fine particles with huge surface
facturing steel, or consuming of coal and fossil fuels (IARC, 2012). areas that are easily transferred and deposits the micro-pollutants such
Another source of As in soil is the continuing use of the arsenical pes- as heavy metals (Li & Zuo, 2013; Keshavarzi, Tazarvi, Rajabzadeh, &
ticides (Islam et al., 2014). As is found in ground water, affects the Najmeddin, 2015). Human beings are exposed to these fine particles
agricultural products irrigated by this type of water. As exists in ar- containing heavy metals via three main routes: oral ingestion, which is
senite As(III) or arsenate As(V), but As(III) is the most abundant form in associated unintentionally with foodstuffs and/or drinking water
the ground water where reducing conditions are available underground (Mohmand et al., 2015); inhalation via the respiratory system; and
(Kesici, 2016). dermal adsorption (Li et al., 2017).

8. Route of human exposure to heavy metals 12. Occurrence of heavy metals in human food

Human exposure to heavy metal mainly occurs through three major 12.1. Mercury (Hg)
routes, including the inhalation, the oral ingestion and the dermal ex-
posure (Asaduzzaman et al., 2017; Li et al., 2017). The primary route of Although Hg does not play any critical role in food chains, it is
heavy metals exposure depends on the metal characteristics. For ex- mainly detected in the marine organisms. However, plant-based foods
amples, oral ingestion is the primary pathway of copper intake due to sometimes contain trace amounts of the inorganic mercury. Fish and
its solubility in water. Also, ingestion is the primary pathway of mer- other seafood are considered the principal sources of human exposure
cury (Hg) via the consumption of marine organisms in which organic of Hg since more than 75% of total Hg in fish exists in the form of MeHg
forms of Hg like methyl mercury (MeHg) have bioaccumulated at a high (Gochfeld, 2003) that is produced by marine microorganisms (Jures &
concentration level in their tissues (Horvat et al., 2003). In this respect, Blanus, 2003). Krystek and Ritsema (2004) reported that the ratios of
Boudou, Maury-Brachet, Coquery, Durrieu, and Cossa (2005) stated MeHg to the total Hg in the carnivorous fish and herbivorous fish are
that dietary fish is the main source of mercury intake for many popu- approximately 70% and 100%, respectively. It was reported that the
lations. Other heavy metal such as arsenic is characterized as volatile concentration of Hg reaches up to 6 μg/g in the predatory fish, mostly
metals and present in the atmosphere. In the current section, the ex- the long-lived species including, swordfish, tuna, whales, sharks and
posure routes mentioned above are discussed in more details. dolphins (Pethybridge, Cossa, & Butler, 2010). Once the elemental Hg
or inorganic Hg enters aquatic ecosystem, they are biomethylated by
9. Ingestion the microorganisms to form MeHg (Fig. 1), which is bioconcentrates
and biomagnifies in the food chain (Gochfeld, 2003). The MeHg ab-
Several factors affect the absorption of trace metals via gastro- sorbed by the fish from the aqueous media through their gills in a
intestinal track, e.g., metal solubility, chemical forms and occurrence of process called bioconcentration or through other available marine or-
other compounds. Compared with inhalation and dermal exposures, ganisms in a process called biomagnifications. The concentration ratio
food consumption is considered as the primary route of these heavy of MeHg between fish tissue (flesh, the edible part) and the surrounding
metal exposures (Loutfy et al., 2006) since it constitutes greater than environment can reach one million to one. Previous surveys conducted
90% of daily intake of total trace metals in humans. For instance, water in several countries on foodstuffs revealed the plant food and vegetable
and food contaminated with arsenic (As) are considered to be the major samples commonly contain trace concentrations of Hg (Perello, Marti-
source of exposure, since WHO (2010, pp. 1–5) estimated daily intake Cid, Liobet, & Domingo, 2008; Suruchi & Khanna, 2011). In this

38
A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

found in certain types of seaweed (Hizikia fusiforme) (Ichikawa et al.,

2006). Recently, Islam, Rahman, Rahman, and Naidu (2017) reported
that different types of Australian rice contain significant levels of ar-
senic since more than 90% of the investigated samples, including baby
rice contained up to 456 μg/g for total As and up to 270 μg/g for in-
organic arsenic. These levels exceeded the maximum recommended
levels for both children and infants (100 μg/kg) or the limits stated for
adults (200 μg/kg) suggested by EFSA (2009). A critical situation oc-
curred in the United Kingdom regarding levels of inorganic or total
arsenic in rice and rice-based products intended for infants or adults
(Signes-Pastor, Carey, & Meharg, 2016). Based on the medical records
and observations of spreading lung cancer in European countries, the
European Food Safety Authority decreased the Provisional Tolerable
Weekly Intake of As from 15 to just 3 μg/kg b.w./W (Škrbić, Živančev,
& Mrmoš, 2013).

12.3. Chromium (Cr)

Fig. 1. Mercuric cycle and distribution of mercury forms between atmosphere and hy-
drosphere.
Cr can reach the food grains, mainly from contaminated soil or
through grinding the whole grain using stainless steel equipments or
processing of foodstuffs using aluminum or steel equipments which is
concern, Perello et al. (2008) reported that samples of potatoes, beans, considered a significant source of Cr in foods (Cubadda, Raggi, &
olive oils and rice collected from Spanish local markets contain un- Marconi, 2005). It was reported that the level of total chromium and
detectable levels of Hg. The bioavailability of Hg in soil and the ability Cr6+ in whole grains intended for bread production in South Africa
to absorb by plants is very limited due to its high affinity to the humic reached 19–63 μg/kg for Cr6+ while the total chromium was
substances (Tangahu et al., 2011). However, some cereal and cereal 57–156 μg/kg (Mathebula, Mandiwana, & Panichev, 2017). In a study
based products, particularly rice, are considered a great source of conducted by the French Agency of Food Safety, fatty foods were found
mercury since high concentrations of total Hg (569 μg/kg) and MeHg to contain high concentrations of Cr (810 μg/kg) followed by sweet-
(144 μg/kg) were found in rice without husks (Horvat et al., 2003). eners (chocolate, sugar and their products). Moreover, dark chocolate
These concentrations reflect the effect of both atmospheric mercury was found to have the highest level of Cr reaching 2000 μg/kg, which
deposition and absorption of Hg from the soil due to the extensive may be due to the use of stainless steel and aluminum equipment and
applications of mercury as fungicides and pesticides (Patra & Sharma, sample milling equipment (Noël et al., 2012). The distribution of Cr
2000). concentration levels in different group of foodstuffs is presented in
Dietary habits have been found to affect the extent of Hg in humans Fig. 3.
as reported by Renzoni, Zino, and Franchi (1998). In this report strong
correlation is found between number of seafood meals and the levels of 12.4. Cadmium (Cd) and lead (Pb)
mercury in human hair as presented in Fig. 2.
Food can be contaminated by Cd primarily through the terrestrial
pathways and the edible plants are considered the predominant source
12.2. Arsenic (As)
of dietary Cd for humans. At least 70% of Cd uptake comes through
vegetables (Chen et al., 2012). Due to its high mobility, phytoavail-
Due to the chemical properties of the arsenic species, they are ca-
ability and relatively poor adsorption in soils, considerable amounts of
tegorized as lipid-or water-soluble arsenicals which include both or-
Cd are usually found in the plant-based foodstuffs. The high mobility of
ganic and inorganic compounds (Francesconi, 2010). The marine or-
Cd makes it easily absorbed by the plants from the soil, transferred and
ganisms usually contain methylarsonate and DMA beside other
accumulate in the aerial parts in a high concentration (Chary, Kamala,
methylated organic and methylated arsenic species, such as the tri-
& Raj, 2008) compared to other trace elements (Azizur & Hiroshi,
methylarsonium ion and trimethylarsine oxide (Sele et al., 2012). On
2011). Several surveys were conducted in different countries and re-
the contrary, inorganic arsenic is commonly found at very low con-
ported that Cd concentrations in rice was in the range of <
centrations ( < 0.01 μg/g) in fish and other seafood (Julshamn et al.,
0.006–0.01 μg/g depending on the Cd concentration in soil or the
2012) although there are some exceptions for blue mussels which
variation of Cd uptake for different plant genotypes (Jorhem et al.,
contain inorganic arsenic in the range of mg/kg (Sloth & Julshamn,
2008). Moreover, mushrooms from the eastern Black Sea were reported
2008). However, high concentrations of arsenic (50 μg/g or more) were
to contain high concentrations of Cd reached 0.9–2.5 μg/g (Tuzen,
Sesli, & Soylak, 2007a). Honey samples collected from different regions
in Turkey were found to contain Cd in concentrations ranged from 0.9
to 17.9 μg/kg, which were correlated with Cd contamination in the
environment (Tuzen, Silici, Mendil, & Soylak, 2007b). On the other
hand, Cd is mostly accumulated in internal organs of fish such as the
liver and kidneys (Castro- González and Méndez-Armenta 2008;
Storelli, Giacominelli-Stuffler, Storelli, & Marcotrigiano, 2005) de-
pending on age since the older fish have the highest concentrations
(Jakimska, Konieczka, Skora, & Namiesnik, 2011). The benthic fish and
marine clams usually accumulate the highest levels of Cd in their tissues
and organs (Smaoui-Damak, Hamza-Chaffai, Berthet, & Amiard, 2003).
Barhoumi, Messaoudi, Deli, Säıd, and Kerkeni (2009) reported that Cd
Fig. 2. Correlation between the number of sea food meals and the concentration levels of levels may reach 4.81 μg/g in the muscle of the benthic fish. In general,
mercury in human hair (Adapted from Renzoni et al., 1998).
Satarug et al. (2017) reported that there is a strong correlation between

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A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

Fig. 3. Levels of Chromium in different consumed foodstuff (μg/kg wet weight) in France. (adapted Noël et al., 2012).

food and Cd exposure. In Vietnam, 93–97% of dietary cadmium is

mainly coming from the consumption of rice. However, cereals and
breads constitute 31–38% of dietary Cd in Denmark, France, Spain and
Chile. In Sweden, Potatoes and cereals represented 40–50% of dietary
Cd, while Potatoes constitute 23%, 26% and 9% in Denmark, France
and Chile, respectively.
In contrast to Cd, Pb has low transfer coefficients but strongly bound
to the soil colloids and its accumulation in plants occurs with the
highest levels in the soil (Chary et al., 2008). Although most of Pb is
retained in the plant roots, food originating from plants is still the main
source of human dietary Pb intake. Pb was reported to be accumulated
in lactating animals fed contaminated grass consequently; it appears in
their milk (Chary et al., 2008). Pb is adsorbed onto the suspended
particles in the water surfaces, and then the aquatic organisms accu-
mulate large amounts of this element once they consume these particles
(Neff, 2002, pp. 161–174). Although the edible parts of mussels con-
tribute to the dietary exposure of Pb in humans consumed in large
quantities, fish generally are not a major source of dietary Pb, pre-
sumably because of the livers and kidneys, which accumulate Pb are
normally discarded as offal and the accumulation of Pb in the fish
muscle is too low (less than 0.5 μg/g) (Kaoud & El-Dahshan, 2010;
Korai, Sahato, Kaziand, & Lashari, 2008).
In Egypt, several studies were conducted to estimate the levels of Cd
and Pb in fish samples collected from different regions and concluded
that extremely high concentrations were detected in the fish samples
(Oreochromis niloticus and Oreochromis zilli) collected from illegal fish Fig. 4. Food consumption in Egypt towards European Countries (FAO, 2002).

farms, which suffer from domestic wastes and agrochemicals such as

pesticides, fertilizers and industrial wastes (Table 1). Comparison with from the permissible limits (Table 1).
other data reported by Abumourad, Authman, and Abbas (2013) for Food habits are very important issue to have a good figure about the
fish farms and ElKady, Wade, Klein, and Sweet (2015) for the same levels of these toxic metals in body burdens. Fig. 4 illiterate the food
species of fish (Oreochromis niloticus) in Lake Manzala, the concentra- habits for Egyptian ass estimated by FAO (2002) and suggested that
tions of these metals and others were very low and the levels were so far cereals provide the main source for energy for Egyptians and constitute

Table 1
Concentration Levels (mg/kg ww) of Cd, Pb and Hg in tilapia fish collected from different places in Egypt.

Locations Cd Pb Hg Reference

Illegal fish farm in Sabal drainage canal (Oreochromis niloticus) 4.35 3.02 2.33 Authman, Abbas, and Gaafar (2012)
(O. niloticus)
Sabal Drainage Canal, Al-Minufiya Province (Oreochromis niloticus) 3.4 31.9 39.1 Authman (2008)
Illegal fish farms near Sabal Drainage Canal (Tilapia Zillii) – 3.88 – Alne-na-ei (1998)
Shanawan drainage canal, Al-Minufiya Province (Oreochromis niloticus) 5.3 48.7 67.1 Khallaf, Galal, and Authman (1998)
River Nile (Shoubra El-Kheima, Cairo sector) (Oreochromis niloticus) 0.04 1.22 – Elghobashy, Zaghloul, and Metwally (2001)
Manzala Lake (Oreochromis niloticus) BDL 0.012–0.039 0.002–0.006 ElKady et al. (2015)
Drainage canals in Nile Delta (Tilapia zillii) – 6.20 – Alne-na-ei (2003)
Al-Abbasa (Sharkia) (O. niloticus) 0.0005 0.0038 NA Abumourad et al. (2013)
Kafr El-Sheikh (Oreochromis niloticus) 0.0005 0.0013 NA Abumourad et al. (2013)
El-Fayoum (Oreochromis niloticus) 0.0008 0.0017 NA Abumourad et al. (2013)
Permissible Limit 0.500 2.00 0.300 WHO (1993)

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A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

33% of the total food consumption followed by vegetables (24.6%); tissue including the brain (Tahir et al., 2017). Ultimately, lead deposits
however fish meals account only 2.1%. Milk and dairy products re- in the bone and replaces calcium since Pb2+ and Ca2+ ions are similar
presented about a quarter of European food consumption, while cereals in size. There is evidence that children with lower calcium content in
and vegetables constituted just 11.5 and 11.9%, respectively. their body have a high blood lead (Al-Saleh, Al-Rouqi, Elkhatib,
Abduljabbar, & Al-Rajudi, 2017). Also, children with a deficiency of
13. Health hazards associated with the exposure to heavy metals iron had high levels of Pb in their blood (Lanphear et al., 2002). The
high level of Pb in blood in children is associated with neurotoxicity
13.1. Mercury (Hg) symptoms, e.g., attention, deterioration in communication skills
(Counter, Buchanan, & Ortega, 2008).
The toxicity of mercury depends on mercuric form ingested. Alkyl The high concentration of Pb in the blood stream blocks the re-
mercury compounds such as methyl mercury are extremely more toxic ceptors (N-methyl-D-aspartate), which have an important role for the
than the inorganic form (Karri, Schuhmacher, & Kumar, 2016). The cognitive functions and neuronal synaptic plasticity and ultimately
absorption of MeHg via the gastrointestinal tract represented 90% of disrupts the region of hippocampus that specific for memory acquisition
total absorbed mercury. The neurotoxicity of MeHg is high in com- (Snyder, Hong, McDonald, & Wojtowicz, 2005). This action leads to
parison with inorganic mercury since it is transferred from the blood limitation of permanent intake and learning skills (Lasley, Green, &
into the central nervous system through the blood brain barrier by the Gilbert, 2001). Furthermore, chronic exposure to Pb can inhibit both
L-neutral amino acid carrier transport (LAT). MeHg concentrates enzymes δ-aminolevulinic acid synthetase and dehydratase (ALAS &
mainly in the cells of gill origin, resulting in the induction of neural ALAD), which are necessary for heme biosynthesis and lead to anemia
inflammation and oxidative stress (Farina, Rocha, & Aschner, 2011). It (Johnson, 1998). Additionally, Pb has a toxic effect on reproductive
disturbs the metabolism of amino acid and the breakdown of membrane system since the sperm count is decreased with increasing the abnormal
phospholipid. Epidemiological studies revealed that pregnant women occurrence of sperm in males (Brochin et al., 2008). Like most xeno-
ingested fish-heavy diet contained significant amounts of MeHg became biotics, Pb acts as prooxidant and has direct actions in plasma mem-
at risk and gave birth of neurological deficit children (Julvez et al., brane cells as oxidative stress, reducing the activities of antioxidants.
2016). Once MeHg enters the brain, it binds with cysteine to form cy- There is a strong correlation between the accumulation and elevation of
steine complex (MeHg-Cys), mimicking the structure of methionine, a Pb levels in humans and the hazard of Parkinson's disease, which has
substrate for LAT amino acid transport system (Farina et al., 2011). It is long been characterized as a central nervous system disorder
directly disturbed the mitochondrial activities through the releasing of (Weisskopf et al., 2010).
uncontrolled calcium ions (Ca2+) from mitochondria (Farina et al.,
2005). Moreover, Karri et al. (2016) reported that exposure to MeHg 13.3. Chromium
inhibits the activities of glutathione peroxidase, increases lipid perox-
idation, and decreases the uptake of glutathione into cerebrocertical Trivalent Cr (Cr3+) is an essential element for humans. However, Cr
slices (Fig. 5). (VI) is toxic and induces several health risks due to its solubility, mo-
It was reported that several crises have resulted from the con- bility and ability for reduction. The reduction of Cr (IV) to Cr (V) by
sumption of foods contaminated by mercury. More than two thousand NADPH leads to increase the hydroxyl radical (•OH), which enhanced
of Japanese people were affected and about one thousand died due to P53 activation in human lung epithelial cells (A549). Moreover the
Minamata disorder during 1980s and 1990s, resulting from mercury prolonged and continued exposure to Cr(VI) through smoking and/or
pollution by a chemical plant (Rafati-Rahimzadeh, Rafati-Rahimzadeh, occupational exposure prevents cell growth arrest although it activates
Kazemi, & Moghadamnia, 2014). In Iraq during 1956, 1960, and 1972, p53 leading to the DNA damage and trigger p21 degradation; conse-
hundreds of deaths occurred and some cases in the United States and quently, cells will undergo apoptosis as shown in Fig. 6 (Hill et al.,
China due to consumption of bread made from grain treated by a fun- 2008).
gicide containing mercury as these seeds were prepared for cultivation Cr is well known to induce genotoxicity in animals. It induces
(Risher, Murray, & Prince, 2002). DNAeprotein crosslinks, DNA inter- and intra-strand crosslinks, DNA
adducts, DNA-strand breaks, dysfunctional DNA replication and tran-
13.2. Lead (Pb) scription, dysregulated DNA repair mechanisms, genomic instability,
alteration of survival signaling pathways, oxidized bases, microsatellite
Once the lead is ingested by humans, it initially presents in blood instability, abasic sites and the epigenetic/genetic changes (Shahid
and then distributed to the whole body and organs, particularly the soft et al., 2017). Cr is unlike other metals due its ability to interact mainly
and directly with DNA to form DNA-DNA cross links and DNA-protein
(Nickens, Patierno, & Ceryak, 2010).

13.4. Cadmium (Cd)

Inhalation exposure to CdO fumes of dust cause severe irritation to

the respiratory system. It is estimated that about 50% of cadmium in
tobacco is reabsorbed by lung and the body burden of Cd in smokers is
about 4–5 times of non-smokers. The kidney is the target of Cd since it
affects the proximal renal tubular function and is characterized by the
presence of low molecular weight protein in urine called proteinuria
(Satarug et al., 2017). Tubular disorder starts to develop once the level
of Cd reaches the threshold level in renal cortex, which was estimated
as 200 μg/g renal cortex (Zang & Bolger, 2014). Consumption of Cd for
long term, mostly from food intake like rice, resulted in serious pro-
blems including kidney failure. A very famous disease called Itat-itai,
which appeared due to human activities related to mining industries in
Fig. 5. Flow chart explains the mechanism of mercury toxicity (adapted from Karri et al., the Toyama County in Japan, caused softening of the bones, e.g., os-
2016).
teomalacia and osteoporosis, bone deformities and finally renal

41
A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

Fig. 6. Proposed mechanism for chromium-mediated carcinogenesis (Hill et al., 2008).

within the group (1) as carcinogenic agent. The consumption of food-

stuffs contaminated by inorganic arsenic may be a concern to the world
cancer burden (Oberoi, Barchowsky, & Wu, 2014). A good example of
arsenic exposure of contaminated foods is the consumption of rice by
Asian people since rice is considered an essential diet for about 2 billion
people (Praveena & Omar, 2017). The arsenic toxicity depends on its
chemical form, the route and duration of exposure. Inorganic forms of
As [arsenite, As(III) and arsenate, As (V)] are extremely toxic compared
with organic forms (Feldmann & Krupp, 2011). Organoarsenicals
compound constituted the vast majority of total arsenic found in sea
foods and are mostly non-toxic (Feldmann & Krupp, 2011). Inhalation is
a significant route for inorganic arsenic, causing nausea and skin irri-
tation. Also, lung cancer is increased due to the exposure to inorganic
arsenic (Kesici, 2016). Many toxic compounds are formed during the
metabolism of arsenic; e.g. dimethylarsonic acid (DMA V), dimethy-
larsinous acid (DMA III), monomethylarsonous acid and arsenic-glu-
tathione (As-GSH) (Kesici, 2016). Arsenic exposure also affects the
metabolism of nerve-impulse transmitters such as monoamines, acet-
ylcholine, gamma-aminobutyric acid (GABA) and glutamate by en-
hancing the acetylcholine esterase activity and glutamate decarbox-
ylase (GAD) mRNA expression (Patlolla & Tchounwou, 2005). The toxic
impact of arsenic is extended to have a direct effect on oxidative stress.
Free radicals, which are released after exposure to inorganic arsenic,
Fig. 7. Arsenic-induced carcinogenesis and signaling pathways (Flora, 2011). reduce glutathione, glutathione peroxidase and glutathione synthase
activities and increase the levels of malondialdehyde (MDA) (Karri
et al., 2016). The generation of ROS by arsenic (Fig. 7) increases the
dysfunction (Zang & Bolger, 2014). In this prevalence, women were
expression of different proapoptotic molecules (Bid and Bax), decrease
affected directly due to the contamination of Jinzu River, which is the
the expression of antiapoptotic molecules (Bcl-1 and Bcl-XL). Moreover,
main source of irrigation (Aoshima, 2016). Liver fibrosis is common in
ROS decrease the mitochondrial membrane potential and induce cal-
Itai-itai patients; however; the liver function still intact due to the
cium imbalance inside the cells leading, open the membrane pore and
protective role of metallothionein to minimize the hepatotoxicity of Cd
increase release of cytochrome c leading to apoptosis (Gao, Li, Xu, Liu,
(Baba et al., 2013). Reducing the activity of metallothionein and brain
& Liu, 2018).
derived neuronal factor, followed by Cd exposure increase the level of
ROS and induce oxidative stress in the brain cells (Lopez, Arce, Oset-
Gasque, Canadas, & Gonzalez, 2006).
14. Conclusion

13.5. Arsenic (As) Due to chemical stability, bio-accumulative tendency, large pro-
duction, and excessive consumption, heavy metals are considered per-
Consumption of contaminated food together with drinking water is sistent pollutants that are still found in every environmental compo-
the major routes of As in humans. Moreover, the As-contaminated nent, including foods and feeds and are also still detected in human
ground and surface water used for planting become major routes for As tissues, blood and hair. Exposure to heavy metals results in various
uptake via contaminated crops. IARC (2012) classifies inorganic arsenic harmful effects, including reproductive toxicity, neurotoxicity, immune

42
A.A. El-Kady, M.A. Abdel-Wahhab Trends in Food Science & Technology 75 (2018) 36–45

suppression, birth defects, cancer, are behavioral and developmental and nickel) in childhood. The Journal Brazilian Annals of Dermatology, 87, 269–276.
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