Toxic Elements in Food: Occurrence, Binding, and Reduction Approaches

Toxic Elements in Food: Occurrence, Binding,
and Reduction Approaches

P. Hajeb, J. J. Sloth, Sh. Shakibazadeh, N. A. Mahyudin, and L. Afsah-Hejri
Abstract: Toxic elements such as mercury, arsenic, cadmium, and lead, sometimes called heavy metals, can diminish
mental and central nervous system function; elicit damage to blood composition as well as the kidneys, lungs, and liver;
and reduce energy levels. Food is considered one of the main routes of their entry into the human body. Numerous
studies have been performed to examine the effects of common food processing procedures on the levels of toxic elements
in food. While some studies have reported negative effects of processing, several have shown that processing practices may
have a positive effect on the reduction of toxic elements in foodstuffs. A number of studies have also introduced protocols
and suggested chemical agents that reduce the amount of toxic elements in the final food products. In this review, the
reported methods employed for the reduction of toxic elements are discussed with particular emphasis on the chemical
binding of both the organic and inorganic forms of each element in various foods. The molecular groups and the ligands
by which the food products bind with the metals and the types of these reactions are also presented.
Introduction consumption. Numerous studies have been carried out to exam-

Contamination with toxic elements is a global environmental ine the effects of common food processing on its contamination
concern (O’Flaherty and others 2003). Any contaminated food is with toxic elements. While some researchers have reported nega-
able to transmit toxic elements through ingestion, with the risk tive effects of processing methods, several studies have shown the
increasing as the quantity consumed increases. Marine fish at the effectiveness of certain processing practices on metal removal from
top of the aquatic food chain, for instance, contain elevated lev- foodstuffs. A number of studies have also introduced protocols and
els of certain toxic elements (Chan and others 2003). Primarily reagents that assist in the removal of considerable amounts of toxic
because of a higher concentration of some toxic metals, marine elements from different types of food. In this review, we discuss
organisms have been subjected to extensive studies compared to the published methods to reduce the toxic elements in foodstuffs
terrestrial organisms. Some toxic elements, such as mercury and and the principles that govern their removal.
methylmercury, are neurological toxicants to humans. Mercury
exposure is associated with slow mental development, blindness, Toxic Element Contamination in Foods
cerebral palsy, and other birth defects in human (Clarkson 1994; Toxic elements, mainly the heavy metals of the periodic
Coccini and others 2000). Studies indicate that the adverse health table, are normal elements found in the environment, and trace
effects of cadmium exposure, even at lowerexposure levels, are pri- amounts of them are always found in foodstuffs (Smedley and
marily in the form of bone effects and fractures as well as kidney Kinniburgh 2002); however, foods from contaminated areas may
damage. Exposure to inorganic arsenic, which occurs predomi- contain higher amounts. Toxic elements primarily enter foodstuffs
nantly through food and water intake, is primarily related to the through contact with the environment. Waterways and oceans are
risk of skin cancer as well as other skin lesions, such as hyperker- contaminated by the discharge of untreated municipal and indus-
atosis and pigmentation changes (Järup 2003). Due to the health trial wastes. Polluted air falls as precipitation with rain, contami-
effects of toxic elements, several initiatives have been set up to nating the environment, and eventually entering the food chain.
reduce the contamination of food and to make it safer for human Depending upon the exposure route, each food type may become
contaminated with different toxic elements. For instance, the high
levels of arsenic found in the groundwater of certain areas through-
MS 20131867 Submitted 12/16/2013, Accepted 2/14/2014. Authors Ha- out the world contaminates plants, including vegetables, rice, and
jeb, Mahyudin, and Afsah-Hejri are with Food Safety Research Cen- other cultivated grains (Heitkemper and others 2009). There are
tre (FOSREC), Faculty of Food Science and Technology, Universiti several reports on high arsenic levels in rice, grains, and vegeta-
Putra Malaysia, 43400, UPM, Serdang, Selangor, Malaysia. Author Sloth is with bles from different regions where the fields have been irrigated
National Food Inst, Technical Univ. of Denmark, Mørkhøj Bygade 19, DK-2860
Søborg, Denmark. Author Shakibazadeh is with Dept. of Aquaculture, Faculty of with arsenic contaminated water (Farid and others 2003; Dı́az and
Agriculture, Universiti Putra Malaysia, 43400, UPM Serdang, Selangor, Malaysia. others 2004; Signes and others 2008a, b; Bhattacharya and others
Direct inquiries to author Hajeb (E-mail: parvaneh@upm.edu.my). 2010; Anirban and others 2011). Marine organisms, especially fish
and seafood, from coastal areas associated with industrial discharge

C 2014 Institute of Food Technologists®
doi: 10.1111/1541-4337.12068 Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 457
Toxic elements in food . . .
usually contain elevated amounts of toxic elements including mer- water. Inorganic arsenic represented more than 90% of the total
cury, arsenic, cadmium, and lead (Liobet and others 2003; Falco arsenic content in rice (Torres-Escribano and others 2008; Signes
and others 2004; Marti-Cid and others 2007; Perello and others and others 2008a). High levels of arsenic, some as high as 0.55
2008; Bose-O’Reilly and others 2010; Suresh Kumar and oth- μg/g, have been reported in the most popular types of commer-
ers 2013). Furthermore, the matrix properties and the chemical cial rice from West Bengal, Spain, and Sweden (Farid and others
structure of some foods also make them more susceptible to be 2003; Torres-Escribano and others 2008; Jorhem and others 2008;
contaminated with a particularelement. Here, we review the oc- Signes and others 2008b; Azizur and Hiroshi 2011). In compar-
currence and chemistry of each element in different foods. ison to other toxic elements, rice and other grains are primarily
Heavy metal toxicity can diminish mental and central nervous contaminated with arsenic.
system function, elicit damage to blood composition, as well as Marine organisms usually contain considerable amounts of ar-
the kidneys, lungs, and liver, and reduce energy levels. Food is senic found in various inorganic and organic species with varying
considered one of the main routes of toxic element exposure toxicities. More than 50 arsenic compounds have been identified in
for humans. Numerous studies have been carried out to reduce marine organisms, where most of the organisms are common types
the amount of toxic elements in foodstuffs. Various cooking and of seafood. Some of these arsenic compounds are very important.
processing methods as well as artificial treatments using chelating They are significant metabolites (such as dimethylarsinate [DMA])
agents have been applied. Several of these methods were able to or they are notable because they are either present at high con-
remove considerable amounts of toxic elements from foods, while centrations (such as arsenosugars in algae) or have toxic properties
some were less efficient or even ineffective. In this article, the (inorganic arsenic) (Francesconi 2010). Many of the arsenic species
current state of toxic element removal from foodstuffs is reviewed, detected in seafood are trimethylated, which imparts a structure
and the various methods are evaluated. similar to trimethylamine oxide (Devesa and others 2001). The
organic forms of arsenic in fish (arsenobetaine, arsenocholine,
Occurrence of Toxic Elements in Foodstuffs dimethylarsinic acid, monomethylarsonic acid, trimethylarsine ox-
Each trace element plays a significant role in either the terres- ide, and the tetramethyl arsonium ion) show a lower toxicity or
trial or the aquatic food chain. For instance, mercury does not are considered practically nontoxic (Shiomi 1994; Conklin and
play an important role in terrestrial food chains, but it is always others 2003). The most common and abundant organo–arsenic
detected in marine organisms. While plant-based foods usually compound found in marine animals is arsenobetaine, which is
contain only trace amounts of inorganic mercury, fish and seafood harmless and is rapidly excreted in the urine following ingestion
are the main sources of mercury exposure for humans. Mercury by humans (Grotti and others 2008; Francesconi 2010). The ar-
contamination in fish and seafood is predominantly in the or- senic concentrations in marine organisms can occasionally be very
ganic form of methylmercury that is produced by marine mi- high, but most samples fall within the range of approximately 5
croorganisms (Clarkson 1994; Jures and Blanus 2003). The ratios to 100 μg/g dry matter (Francesconi 2010). Total diet studies
of methylmercury to total mercury in herbivorous fish and carniv- have shown that the highest total arsenic concentrations are in
orous fish have been reported to be approximately 70% and 100%, the seafood samples, while the concentrations of inorganic arsenic
respectively (Krystek and Ritsema 2004). Mercury concentrations in fish and most other seafood are generally low (<0.1 mg/kg)
as high as 6 μg/g have been reported in predatory fish, espe- (Munóz and others 2000; Julshamn and others 2012). Hence,
cially long-lived species such as tuna, swordfish, sharks, whales, seafood has a low contribution to the dietary exposure of inor-
and dolphins (Hueter and others 1995; Endo and others 2008; ganic arsenic. Conversely, rice grains were identified as the main
Pethybridge and others 2010). Various surveys on foodstuffs from source of dietary inorganic arsenic (Gunderson 1995; Schoof and
different countries showed that vegetables and plant food samples others 1999; Ysart and others 1999; Meharg andothers 2009).
usually contain only trace amounts of mercury (Alberti-Fidanza In contrast to mercury and arsenic, cadmium enters the hu-
and others 2002; Bordajandi and others 2004; Perello and others man diet primarily through terrestrial pathways. Edible plants are
2008; Suruchi and Khanna 2011). For instance, samples of beans, the predominant dietary source of cadmium for humans. More
potatoes, rice, and olive oils collected from local markets in Spain than 70% of our cadmium uptake comes from vegetables (Ryan
did not contain detectable levels of mercury (Perello and others and others 1982; Chen and others 2012). According to Chary
2008). Because of the elevated affinity of mercury to humic sub- and others (2008), cadmium has very high mobility and phyto-
stances, the bioavailability of this element in soil and its ability availability and relatively poor adsorption in soils. Therefore, con-
to enter plants is generally very limited (Findenegg and Haunold siderable levels of cadmium are commonly found in plant-based
1972; Tangahu and others 2011). foodstuffs. Cadmium is one of the most mobile elements among
Water serves as the main source of arsenic for humans (Guha all toxic heavy metals. Because of its high mobility, cadmium is
Mazumder and others 1998; Smith and others 1998; Tondel and readily taken up by plants from the soil and transferred to the
others 1999; Dı́az and others 2004). Inorganic arsenic is consid- aerial parts of the plant, where it can accumulate to a high level.
ered the most toxic chemical species of arsenic found in food and Because of its high mobility in soil, the bioaccumulation of cad-
drinking water. Arsenic-contaminated water used in plant irriga- mium in plant-based food is usually high compared to the other
tion and food preparation is the source of the high arsenic content trace elements (Lebeau and others 2002; Satarug and others 2003;
detected in both cooked food and cultivated grains and vegeta- Cui and others 2005; Azizur and Hiroshi 2011). According to
bles (Dı́az and others 2004). Terrestrial foods typically contain low various surveys from different countries, the range of cadmium
levels of arsenic; in fact, most samples contain less than 0.05 μg/g concentrations in rice was <0.006 to 0.01 μg/g, depending on
dry matter (European Commission 2004). However, there is an the cadmium concentration in the soil or the differences between
exception for rice, which can typically contain approximately 0.03 plant genotypes in cadmium uptake (Jung and Thornton 1997;
to 1 μg/g (Williams and others 2005; Jorhem and others 2008). Phuong and others 1999; Shimbo and others 2001; Alam and
According to Signes and others (2008a), inorganic arsenic is the others 2002; Gorbunov and others 2003; Cui and others 2004;
predominant species in vegetables (including rice) and drinking Lin and others 2004; Jorhem and others 2008). A high amount
458 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
of cadmium (0.9 to 2.5 μg/g) has been reported in mushrooms from soil has been proposed as the main reason why mercury is
from the eastern Black Sea (Tuzen and others 2007a). Tuzen and normally not accumulated in higher plants (Lorenz 1979; Tangahu
others (2007b) also reported cadmium (0.9 to 17.9 μg/kg) in and others 2011). Mercury binding to the −SH groups of pro-
honey samples from different regions in Turkey, which were cor- teins is indicated by a relatively close correlation between the mer-
related with cadmium contamination of the environment. cury concentration and the crude protein concentration in food
Cadmium ordinarily occurs only in trace levels in most aquatic (Aichberger 1977). Studies on the pathways of methylmercury ac-
organisms (Castro-González and Méndez-Armenta 2008). How- cumulation in the aqueous food chain showed that methylmercury,
ever, cadmium is predominantly accumulated in fish internal or- due to its lipophilic character, may enter any biological membrane
gans, such as the kidneys and the liver (Mansour and Sidky 2002; (Norseth and Clarkson 1971; Lorenz 1979).
Storelli and others 2005; Castro-González and Méndez-Armenta The affinity of mercury for the −SH (sulfhydryl) moiety is
2008). The cadmium content in fish depends on age, with older greater than any other single ligand. The reaction with these
animals having higher concentrations (Nordberg 1974; Kreuzer groups can result in different complexes depending on whether
and others 1976; Jezierska and Witeska 2006; Jakimska and others the metal is present as Hg2+ or R−Hg+ and whether the ligand is
2011). The main route of heavy metal accumulation in marine or- a mono- or dithiol. The resulting complex also depends on the rel-
ganisms is through the diet, but water salinity and temperature may ative concentrations of mercury and the −SH group. Most proteins
also affect the targeting of cadmium species and its bioaccumula- contain various ligands for mercury, including −SH groups. With
tion (Castro-González and Méndez-Armenta 2008). Marine clams the extraordinary affinity of the organomercurial cation (RHg+ )
and benthic fish usually accumulate high levels of cadmium in their for sulfur ligands, one would expect the simple RHgSR thiol com-
tissues (Hamza-Chaffai and others 2000; Smaoui-Damak and oth- plexes to be particularly stable molecules. However, methylmer-
ers 2003). According to Barhoumi and others (2009), cadmium cury thiomethyl (CH3 HgSCH3 ) is a white, crystalline but volatile
levels can reach 4.81 μg/g in the muscle tissue of benthic fish. compound. This material is apparently a metabolite of methylmer-
Moreover, cadmium accumulation in mollusks is due to the in- cury in biological systems and has been identified in shellfish from
herent hierarchy of the marine food web and from species-specific polluted waters in the Minamata Bay area in Japan (Nriagu 1979).
physiologic mechanisms (Honda 1990; Das and Jane 2003). In an NMR study of HgCl2 /L-cysteine complexation in a
In contrast to cadmium, lead has low transfer coefficients and strongly acidic solution, large downfield shifts of the cysteine CH2
is strongly bound to soil colloids. Studies have reported that the protons upon complexation along with only small shifts observed
accumulation of lead in plants occurs only when a high concen- for the methane proton suggested that bonding is localized at the
tration of lead is found in the soil (Chary and others 2008). Most −SH site. Plots of the molar ratio of Hg2+ :ligand versus the change
lead is retained in the roots of plants. However, food originat- in the chemical shift were interpreted in terms of both 1:1 and
ing from plants is the main source of human dietary lead intake. 2:1 complexes (Scheme 1) with no indication of bonding to other
The study by Chary and others (2008) showed that lead can be cysteine sites in either case. These solutions were strongly acidic
accumulated in cow and buffalo feeding on contaminated grass with a high Cl− ion content (Wei and others 2008).
and, hence, can also be present in their milk. Furthermore, the The binding of CH3 Hg+ to certain amino acid sites in pro-
lead concentrations were higher in buffalo milk compared to cow teins is responsible for the toxicity of methylmercury, which
milk due to its higher fat content (Leeuwen and Pinheiro 2001; drives much of the interest in the coordination chemistry of
Buechler and others 2002). organomercury RHg+ cations. CH3 Hg+ complexes with small
Lead is typically concentrated in the particulate matter in wa- −SH-containing molecules play a role in methylmercury trans-
ter surfaces. Aquatic animals that consume this particulate matter port, and CH3 Hg+ is a useful biochemical probe for active −SH
accumulate large amounts of this element (Phillips 1976; Fowler groups (Cernichiari and others 2007). The behavior of CH3 Hg+
and Oregioni 1976; Bryan and Uysal 1978; Neff 2002). The ed- toward −SH-containing amino acids is remarkably simple. For
ible species of mussels also contribute to dietary exposure to lead a 1:1 ratio of L-cysteine, D- or L-penicillamine or glutathione
in humans when consumed in large quantities. However, fish are (GSH) over the pH range of 1 to 13, the coordination to CH3 Hg+
usually not a significant source of dietary lead, presumably because is exclusively at the deprotonated sulfur site. When the number of
the kidneys and the liver, which accumulate lead, are normally dis- organomercury ions binding to a protein is in excess of the num-
carded as offal. Lead accumulation in the fish muscle tissue is very ber of readily available −SH groups, or when the −SH groups
low (Lorenz 1979; Falco and others 2006; Korai and others 2008; are absent, complexation to other sites such as the imidazole (his-
Kaoud and El-Dahshan 2010); in fact, the lead concentration in tidine) or amine (glycine) groups would occur (Yamamoto and
the edible fish muscles is usually below 0.5 μg/g (Meador and others 2007).
others 2005; Munóz and others 2005). The pH influences the molecular binding of mercury in food.
Studies on the methionine–CH3 Hg+ system, where the dynam-
Chemical Binding of Toxic Elements to Foods ics of coordination can be followed by NMR, revealed that of
Mercury the 3 locations vacant for coordination, only the thioether site
Inorganic mercury usually forms a stable bond with organic is bound at a pH below 2, when the carboxylate and amine
matter in food. However, due to the stable binding of inorganic sites are protonated (Donia and others 2008). As the pH in-
mercury with organic matter of soil, trace concentrations of mer- creases, the CH3 Hg+ ion shifts to the COO− and NH2 groups,
cury in the plants are almost merely found in the root. Mercury is with the latter strongly favored above pH 8. The Hg−N bond
assumed to be relatively strongly bound to the acidic groups of the length (2.06(4) Å) and the corresponding Hg−N bond distance
cell walls in the roots (Beauford and others 1977; Lorenz 1979; in [CH3 Hg(py)]NO3 (2.12(2) Å) demonstrate that methylmer-
Lopes and others 2013). Considerable translocation to the shoot cury can bond strongly with amine groups. Additionally, the
only takes place at extremely high levels of mercury in the soil. pH affects protein chemistry through nonsulfhydryl interactions
The relatively stable binding of inorganic mercury to the organic (Donia and others 2008). Glycine and other bifunctional amino
compounds in soils together with the plant uptake mechanisms acids lacking −SH groups are ambidentate toward CH3 Hg+ . In

C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 459
NH3+ H 3 N+ COOH
+
Hg-S-CH2-CH CH-CH2-CH2-S-Hg-S-CH2-CH2-CH
COOH HOOC NH3+
Scheme 1–The 1:1 and 2:1 complexes of Hg2+ :ligand in complexes containing cysteine.
Source: Wei and others (2008).
the pH range of 3.5 to 8, competitive binding to COO− and

NH2 is apparent, while for pH values between 1 and 3.5 the
dominant species is CH3 HgOOCCH2 + NH3 , and for pH values
between 8 and 12 most of the methylmercury is in the form of
CH3 Hg+ NH2 CH2 COO−. According to Grandjean (2008), in-
organic mercury may react with 1 or 2 −SH groups, leading to
the formation of RSHgX or RSHgSR species (Eq. 1).
R − SH + Hg2+ ↔ R − S − Hg+ +H+

Scheme 2–Proposed structure of cadmium binding to metallothioneins in
R − S − Hg+ +HS− ↔ R − S − Hg − S − R + H+ (1) mammals.
R − S − Hg − S − R + Hg2+ ↔ 2R − S − Hg+ Source: Hunt and others (1984).
The linkage of 2 macromolecules by Hg2+ is relatively com-

mon when the protein has a single, readily available −SH site. However, the stability constant for cadmium is approximately 100-
Sulfide links in proteins play a major role in maintaining the con- fold lower than that for copper (Hamer 1986). As for other metal
formation and the structure of the protein. The insertion of Hg2+ ions, the cadmium bound to metallothionein is released when the
into an −S−S− linkage to form a linear −S−Hg−S− complex pH is lowered (Kagi and Nordberg 1979). Hunt and others (1984)
is therefore an appropriate strategy to modify protein structure proposed, based on NMR data, the structures of cadmium binding
in a highly selective fashion, while observing changes in biolog- to metallothionein in mammals (Scheme 2).
ical activity (Alderson and others 2006). The reactivity of −SH In plants, cadmium is bound to several metal-binding com-
groups in proteins toward mercurial species varies based on the plexes, such as organic acids, metallothioneins, and phytochelatins.
location and accessibility of the −SH group and the size, polarity, Phytochelatins are considered the major metal-binding proteins in
and hydrophilicity of the mercurial reagents (Hasegawa and others higher plants (Wagner 1984; Grill and others 1987; Kägi and
2005). KoJima 1987; Verkleij and others 1990; Schat and others 2002).
Similar to other metal ions, mercury also binds to metalloth- Their structures consist of repeating 7-glutamylcysteine units with
ionein proteins. Metallothioneins are low-molecular-weight pro- a carboxyl-terminal glycine. The phytochelatins belong to a struc-
teins that are rich in cysteine and capable of binding to heavy metals tural class of metal-binding proteins different from the metalloth-
(Marafante and others 1972; Olafson and Thompson 1974; Noel- ioneins. However, they have certain properties in common with
Lambot and others 1978; Overnell and Coombs 1979). However, the metallothioneins, such as the ability to form the Cd-cysteine
because mercury is mostly present as methylmercury, a lipophilic complex as well as heat stability, inducibility, and synthesis from
compound with a low affinity for metallothionein, this binding GSH or the 7-glutamylcysteine precursor (Wagner 1984; Grill and
is of minor importance, whereas inorganic mercury has stronger others 1987; Verkleij and others 1990), and they are functionally
affinity for binding (Chen and others 1973). analogous to the metallothioneins (Grill and others 1987).
Cadmium Arsenic
Among the main donor atoms, such as nitrogen, oxygen, and Based on their chemical properties, the arsenic species are cat-
sulfur, that link metal ions to biological molecules, cadmium is egorized as lipid-soluble or water-soluble arsenicals (Francesconi
bound to sulfur more strongly than the other metals, except Cu 2010). The water-soluble species include both inorganic and or-
and Hg (Baes 1973; Flora and Pachauri 2010). In addition, cad- ganic compounds. Arsenobetaine is the main arsenic species in
mium is highly capable of binding to the coordination sites of most marine organisms (Maher and others 1999; Foster and others
macromolecules (DNA, RNA, and proteins), which accounts 2005). The simple methylated organic arsenic species, methylar-
for the multitude of toxic effects observed in vitro and in vivo sonate and DMA, along with other methylated arsenic species,
(Boisset and Narbonne 1996). According to the literature, in such as trimethylarsine oxide and the trimethylarsonium ion, are
aquatic and other animal foods, cadmium is generally bound to usually found as minor arsenicals in marine organisms (Sele and
metallothioneins (Lee and others 1977; Webb 1986; Kovarova and others 2012). The dimethylarsinoyl and trimethylarsonium ion-
others 2009). In metallothioneins, the metal ions are bound only containing ribosides, called arsenosugars, are dominant in marine
through thiolate coordination complexes, which involve 20 cys- algae (Francesconi and Edmonds 1997). The main arsenic species
teine residues. Therefore, the native protein contains no disulfide in marine and freshwater organisms are inorganic arsenic, arse-
bonds or free −SH groups. Zinc and cadmium are bound in each nate, and arsenite (Francesconi and Kuehnelt 2002). Conversely,
domain in the 2+ valence state and are both tetrahedrally coor- inorganic arsenic is usually only found at very low concentra-
dinated to 4 cysteine thiolate ligands (Garvey and others 1982). tions (<0.01 mg/kg) in fish and other seafood products (Sloth and
Scheme 3–Generalized reaction scheme for MMA III and a reduced dithiol.
others 2005; Julshamn and others 2012). However, some excep- A study by Meharg and others (1994) showed that arsenic is
tions have been reported in blue mussels, with concentrations of taken up, similar to phosphate, by the root systems of plants.
inorganic arsenic in the mg/kg range (Sloth and Julshamn 2008), It is transported freely throughout plants and can replace phos-
and certain types of seaweed (such as Hizikia fusiforme), where phate during oxidative phosphorylation. Arsenate is an uncoupler
concentrations above 50 mg/kg have been documented (Ichikawa of oxidative phosphorylation, while arsenite binds irreversibly to
and others 2006). −SH groups (Wachope 1983). Arsenate prevents enzyme activity
Arsenate, which is structurally analogous to phosphate, is at- and the production of photosynthesis-related enzymes (Jiang and
tached to proteins by binding to their −SH groups. These Singh 1993; Jain and Gadre 1995). Arsenite interrupts root func-
−SH groups range in size from cysteine, dimercaptosuccinic acid tion by damaging sites of protein synthesis and also by binding
(DMSA), and GSH to proteins such as hemoglobin, metalloth- irreversibly to the protein −SH groups (Wachope 1983).
ionein, and thioredoxin. Proteins with accessible reduced cysteine Arsenate and arsenite adsorption will occur, especially on A-
residues can bind with trivalent arsenicals (Raab and others 2004; type hydroxyl groups of iron oxides (Waychunas and others 1993;
Burford and others 2005; Schmidt and others 2007). The binding Manceau 1995; Sun and Doner 1996). Furthermore, arsenate and
of trivalent arsenicals to proteins can alter their structure and thus arsenite differ in terms of their use of the adjacent B- and C-type
their activity (Kitchin and Wallace 2006). Scheme 3 shows the hydroxyls. Arsenate preferentially binds with triply coordinated
mechanism of arsenic binding to −SH-containing ligands. The B-type hydroxyls, while arsenite binds with doubly coordinated
study by Jiang and others (2003) showed that 1 metallothionein, C-type hydroxyls (Sun and Doner 1996). Therefore, the surface
which contains 20 cysteine residues, could bind up to 6 arsenite, structural variations between goethite and ferrihydrite warrant a
10 monomethylarsonous acid (MMAIII ), or 20 dimethylarsinous close re-examination of their effect on competitive adsorption
acid (DMAIII ) units. reactions between arsenic and other competing ligands, such as
Lunde (1968) reported that the structure of the ar- organic acids. Arsenate is considered less phytotoxic than arsenite
senolipids in herring oil and cod liver oil are similar to as it has immediate destructive effects upon membrane contact.
known phospholipids. One of these specific arsenolipid com- The damaging effect of arsenite is attributed to its binding to the
pounds is dipalmitoylglycerophospho-2-hydroxypropyl-5-deoxy- −SH groups on the plant roots and other membranes, which effec-
5-(dimethylarsinoyl)-β-ribofuranoside, which was first isolated tively inhibits proper membrane function (Carbonell-Barrachina
from the brown alga Undaria pinnatifida and identified as a lipid- and others 1997).
soluble arsenosugar (Morita and Shibata 1988). Lunde (1972) re-
ported 2 arsenolipids in marine oils and, according to this report, Lead
the arsenic followed both the water-soluble and fatty acid frac- Lead precipitates upon interaction with sulfates and phosphates,
tions after the saponification of the oils. However, Wrench and which are chemicals generally found in the rhizosphere of plants.
Addison (1981) found 3 arsenolipids in the marine phytoplankton Therefore, it has low availability and solubility for plant uptake
Dunaliella teriolecta, where one of the arsenolipid compounds was (Blaylock and Huang 2000). Lead binds to the carboxylic groups of
a phosphatide and the other 2 were proposed to be glycolipids. the uronic acids on mucilage of the root surfaces (Morel and others
Kohlmeyer and others (2005) suggested the possibility of arsenic 1986; Sharma and Dubey 2005). Once lead enters the roots, most
binding to cholesterol or the fat-soluble vitamins because both of it is bound to the ion-exchangeable sites in the cell walls or it
of these nonarsenic-containing compounds are usually present in precipitates extracellularly as carbonates and phosphates (Blaylock
fish oil. DMA, which is the main hydrolysis product of kidney, and Huang 2000; Sahi and others 2002; Sharma and Dubey 2005).
muscle, and feces from sheep, is bound to complex lipids (Sele and Like other toxic elements, lead is complexed by cysteine-rich low-
others 2012). molecular-weight polypeptides (Cobbett 2000). It is transported
to the stems and leaves as Pb acetate, Pb nitrate, Pb sulfide, Pb

phytochelatins, and Pb citrate (Sharma and others 2004a, b; Lopez study by Sengupta and others (2006) showed that washing rice
and others 2007, 2009). Acid-soluble thiol peptides, such as GSH before cooking until the water was clear removed 28% of the ar-
and the phytochelatins, are responsible for lead uptake in aquatic senic. They claimed that the traditional rice cooking method on
plants and algae (Vymazal 1990; Gupta and others 1994; Karez the Indian subcontinent (a combination of washing until the wa-
and others 1994; Pawlik-Skowronska 2000). ter is clear, cooking at a rice:water ratio of 1:6, and discarding the
In aquatic animals, lead binds to organic matter using a large excess water) can remove 57% of the arsenic in rice. Therefore,
variety of weak metal-binding functional groups, such as carboxyl compared to the global method of cooking rice (using less wa-
and phenyl groups, as well as strong metal-binding nitrogen- and ter), this method can partially assist in removing arsenic from rice
sulfur-containing functional groups (Buffle 1988; Richards and through frequent washing and boiling with a high water-to-rice
others 2001). Unlike the other metal ions, lead ions prefer harder ratio. This reduction is likely due to arsenic solubilization from
ligands such as carboxylates, but may also become oxidized and rice to water.
bind to soft ligands more strongly. In proteins, lead binds to the Ichikawa and others (2006) introduced soaking and cooking
hard cations and the electronegative groups such as carboxylates. as effective methods for removing arsenic in edible brown algae.
For instance, in insulin and carboxypeptidase, the major site for They reported a 28.2% to 58.8% reduction of the total arsenic
lead is glutamate, but it binds to 2 aspartic acids in concanavalin following soaking with water and a 88.7% to 91.5% reduction
(Blundell and Jenkins 1977). after cooking. In studies by Laparra and others (2003, 2004) on
the bioavailability of arsenic in 3 species of algae and the effect
Methods for the Reduction of Toxic Elements in Food of cooking arsenic concentration, differences between the types
Several studies have reported that common treatments, such of algae and the use of different types of cooking treatments were
as trimming, skinning, removing fat, frying, grilling, cooking, observed. During boiling, there was a significant reduction of
breading, or microwaving, of fish do not effectively remove heavy inorganic arsenic due to its solubilization in the cooking water.
metals (Gutenmann and Lisk 1991; Morgan and others 1997; They reported that boiling could reduce up to 43% of the total
Devesa and others 2001; Burger and others 2003; Rasmussen and arsenic concentration and up to 50% of the inorganic arsenic
Morrissey 2007; Kalogeropoulos and others 2012). Furthermore, in edible seaweed. Hanaoka and others (2001) showed that the
canning and cooking can even increase the mercury content in fish traditional Japanese washing and soaking of seaweed with water
at times (Burger and others 2003; Rasmussen and Morrissey 2007). before cooking may reduce the total arsenic content by up to 60%.
However, some researchers have developed methods to remove Increasing the water temperature to 60 ◦ C assisted in the removal
heavy metals from various foods. Different reagents and media of more arsenic from the seaweed. They suggested that washing
(acidic and alkaline solutions, alcoholic solutions under heating, and boiling seaweed before cooking can remove the majority of
cysteine and homo-cysteine, organic sulfur-complexing agents, the arsenic. Heat treatment hastens breaking of bonds between
ascorbic acid, pectin solutions, and dry crushed shell membranes) arsenic and the food molecules and facilitates its solubilization in
and the combined effect of alkaline and acidic solutions with washing and/or boiling water.
metal-leaching reagents (EDTA, salt, and cysteine) have been used Dı́az and others (2004) investigated the effect of several cook-
to reduce contamination (Yannai and Saltzman 1973; Spinelli and ing treatments commonly applied to vegetables and cereals (boil-
others 1973; Suzuki 1974; Khayat and others 1975; Danesh 1976; ing, pureeing, stewing, and pie or omelet baking) on the arsenic
Schab and others 1978; Lipre 1980; Ohta and others 1982; Tetsuji concentration. Their research showed that cooking with distilled
and Miyuki 1983; Okazaki and others 1984; Aizpurua and others water significantly decreased the arsenic concentration of the raw
1997; Tomoji 1997; Semenov and others 2001a, b; Hinners 2007; products but that cooked garlic showed an increase. According to
Hajeb and Jinap 2009, 2012). Choudhury and others (1997), the presence of compounds with
sulfur moieties (allicin, alliin, and cysteine) in garlic, which are ca-
Cooking and Food Processing Methods pable of arsenic-binding, could increase the arsenic content. Fur-
A notable number of studies have been carried out to inves- thermore, the arsenic content increased after the cooking (boiling)
tigate the effect of different cooking and processing methods on of vegetables and foods that contain considerable amounts of wa-
the toxic elements in food. Different products including fish and ter (such as chard, asparagus, spinach, pumpkin, and cauliflower).
seafood, seaweeds, fruits, vegetables, and rice have been consid- Peeling beets, carrots, and potatoes also resulted in a reduction of
ered. Some studies have reported a considerable reduction of the arsenic (Dı́az and others 2004), which is due to the high concen-
heavy metals in food after cooking, while certain studies cited tration of this element in the outer layers and peels. Another study
an increase in the metal concentration. The previous studies on reported arsenic reduction (by up to 60%) in several vegetables
cooking methods that have reported a considerable reduction are after cooking (boiling) for 15 min (She and Kheng 1992). They
shown in Table 1 and discussed later. The studies that revealed stressed that the reduced concentration of arsenic was a function
a reduction of toxic elements using cooking processes depended of the boiling time.
on cooking conditions, such as time, temperature, and cooking A recent study by Houlbrèque and others (2011) showed that,
medium. although cooking processes (boiling) increased the cadmium con-
Perello and others (2008) studied the effects of common cook- centration in mussel flesh, the remaining cadmium in the cooked
ing practices used by the Spanish population on toxic heavy metals flesh was less bioaccessible compared to the cadmium occurring
(mercury, arsenic, cadmium, and lead) in a variety of foodstuffs. in the raw tissue. The same trend was observed by Metian and
They found that frying and roasting decreases the mercury con- others (2009) for cadmium, selenium, and zinc in cooked mussels.
centration in hake fish. The metal concentrations in meat also Maulvault and others (2011) showed that cooking could reduce
decreased after cooking, especially for arsenic. Cadmium was only the bioaccessibility of mercury but not the other toxic heavy met-
detected in the raw samples of veal and pork and not in the cooked als in black scabbard fish. While the concentration of mercury in
samples. Boiling significantly reduced the arsenic concentrations fried fish increased, its bioaccessibility was reduced by 24% in the
in vegetables (string bean and potato), while frying did not. A cooked samples compared to the raw samples. These differences
Table 1–Cooking and processing methods to reduce heavy metals in different foods.
Food Heavy metal Cooking/processing Reduction (%) Reference

methods
Fish Mercury Frying and roasting Considerable reduction Perello´ and others (2008)
Lambsteaks Arsenic Frying “ “
Pork “ Grilling “ “
String bean and potato “ Boiling “ “
Pasta Nickel, arsenic, lead, and Pasta-making processes 50% to 60% Cubadda and others (2003)
cadmium
Rice Arsenic Precooking wash 57% Sengupta and others (2006)
Edible brown algae “ Soaking 28.2% to 58.8% Ichikawa and others (2006)
“ “ Cooking 88.7% to 91.5% “
Edible seaweed Arsenic Boiling 43% to 50% Laparra and others (2003,
2004)
Edible seaweed “ Washing and soaking 60% Hanaoka and others (2001)
Vegetables “ Boiling 60% She and Kheng (1992)
Vegetables and cereals “ Cooking with distilled water Considerable reduction Dı́az and others (2004)
Fish Chromium and nickel Grilling and microwave “ Ersoy (2011)
cooking
Fish Lead Microwave cooking and “ Ersoy and others (2006)
baking
“ Chromium Microwave cooking “ Devesa and others (2001)
Crayfish Cadmium, nickel, and cobalt Cooking “ Jorhem and others (1994)
Fish Lead and cadmium Baking and steaming “ Atta and others (1997)
Fish and shrimp Mercury, lead, and cadmium Grilling, curing, frying, and “ Musaiger (2008)
cooking in rice
Fish Lead and cadmium Canning processes Considerable reduction Ganjavi and others (2010)
could be caused by the presence of insoluble fibers (such as those Atta and others(1997) reported significant decreases in the metal
from the wheat flour that was added before cooking), which might concentration of tilapia fish after baking and steaming. Moreover,
have affected the solubility and release of mercury or induced mer- the baking process caused a greater reduction compared to the
cury complexation with other components. steam-blanching of fish. Musaiger and D’Souza (2008) also re-
In the study by Ersoy (2011) on the effect of different cook- ported a reduction in mercury, lead, and cadmium in fish and
ing methods on heavy metals in African catfish, the grilling of shrimp after different cooking processes (grilling, frying, and cook-
the fish decreased the nickel concentration. A significant reducing both as a curry dish and in rice). The influence of cooking and
tion was also observed in the chromium concentration in grilled marinating on the metal bioaccessibility of mollusks (clams, mus-
and microwave-cooked fish. Ersoy and others (2006) investigated sels, oysters, scallops, and gastropods) was investigated by Amiard
the effect of baking, grilling, microwaving, and frying on the and others (2008). Their study showed that boiling in salted water
heavy metals in sea bass. Among the different heavy metals in- decreased the bioaccessibility of cadmium, copper, lead, and zinc
vestigated, only the lead concentration was significantly decreased from the soft tissues of gastropods. They also found that the bioac-
in microwaved and baked fish. Devesa and others (2001) reported cessibility of silver decreased with an increase in the accumulated
a lower level of chromium in African catfish fillets after grilling silver concentration in oysters, clams, and mussels, whereas the
and microwave-cooking when compared with the raw fillets. A bioaccessibility of silver, copper, and lead decreased with the ad-
study by Jorhem and others (1994) also showed that the con- dition of vinegar to oyster flesh. They claimed that the reduction
centrations of cadmium, nickel, and cobalt in crayfish decreased in the bioaccessibility of metals in cooked seafood could be due to
after cooking. The application of heat during cooking accelerates the loss of water and weight, which may be accompanied by the
protein degradation, which may affect the heavy metal content loss of the more labile fractions.
in food. Cubadda and others (2003) reported significant heavy metal re-
A study by Ouédraogo and Amyot (2011) showed that frying duction (nickel > arsenic > cadmium > lead) after milling and
and boiling reduced 40% and 60% of the bioaccessibility of mer- other technological processes involved in pasta-making. Cooking
cury in fish, respectively. They claimed that the addition of black removed considerable amounts of the toxic elements in pasta sam-
coffee and black and green tea in the boiling process could reduce ples, with an average reduction of 50% to 60%. Because most of
the bioaccessibility of mercury in raw fish by 50% to 60%. Their the heavy metal contaminations are in the outer parts of the kernel,
study reported that the combined effect of cooking and the addi- milling is expected to reduce metal contents in grains. However,
tion of tea or coffee could lead to a higher reduction in mercury the degree of reduction depends on how unevenly the element is
bioaccessibility. Frying and boiling alter protein structure by heat- distributed in the kernel. Therefore, it is expected to vary on an
ing, which can render mercury–protein complexes less available element-specific basis. Studies on the effects of canning showed
for solubilization during digestion. Tea and coffee contain con- that the levels of lead and cadmium in yellowfin tuna and skipjack
siderable amounts of catechins, theaflavins, and flavonoids, which tuna decreased throughout the processing procedure (Ganjavi and
are good natural chelators and scavengers of metals (Record and others 2010). The same study also showed that defrosting, cooking,
others 1996). The chelating role of phytochemical-rich foods, and sterilizing by autoclave reduced the concentrations of lead and
rich in phytates, may elucidate the reduction mechanism in mer- cadmium in the fish. A significant reduction in the concentration
cury bioaccessibility. Phytates form complexes with proteins at of lead and cadmium in canned tuna during defrosting can be due
both low and high pH values, which alter the protein structure to separation of the liquid from the fish meat. During the canning
and decrease its solubility (Shim and others 2009; Kumar and process, the accompanying liquids (oils or natural juices or sauces)
others 2010). may give the fish a neutral or acidic pH. The combination of

pH and temperature might lead to changes in the chemical forms A study by Hajeb and Jinap (2012) showed that more than
of metals or dissociate them from the fish proteins. Ganjavi and 90% of the mercury in mackerel fillet could be removed using
others (2010) argued that the reduction in metal concentrations a 1.25% cysteine solution, whereas Aizpurua and others (1997)
during the heating process (cooking and sterilizing by autoclave) is reported a mercury reduction of 40% to 45% in minced shark
related to the decrease in protein content and the release of heavy using a 0.5% cysteine solution. Lipre (1980) reported 40% and
metals (as free salts) with the loss of water. It is possible that the 44% mercury removal in cod fillets following treatment with 0.1%
heavy metals were bound to soluble amino acids and uncoagulated and 1.0% cysteine solutions for 24 h, respectively. Schab and others
proteins. (1978) extracted 47% of the mercury in sliced, precooked yellow
tuna using 0.1% cysteine. Kyokuyo (1976) also used dilute salt
solutions of L-cysteine or L-cysteine hydrochloride at pH 4.5 to
Chelating Agents 8 to remove mercury from fish by soaking the tissue in these
The terms chelate and chelation are taken from the Greek word solutions. Khayat and others (1975) removed heavy metals from
chelos, meaning claw. The term chelation describes the physical tuna flesh by the application of a slurry containing chelating agents
process well. It consists of the introduction of a charged molecule (cysteine or homocysteine, thiosulfate, and mercaptans) at 212 ◦ F
(usually containing one or more −SH groups) for the purpose (100 ◦ C) and pH 4 to 6 for 5 to 180 min, which resulted in
of binding specific metal ions of opposite electrical charge and a mercury removal range of 24% to 55%. However, Yannai and
facilitating the removal of the consequent complex from the body Saltzman (1973) successfully removed up to 79% of the mercury
via the urine (Risher and Amler 2005). Chelation therapy has in slices of precooked tuna using 0.33% cysteine. Schab and others
historically been used in attempts to reduce the body burden of (1978) achieved 47% mercury removal from sliced, precooked
mercury and other toxic metals in highly exposed patients with yellow tuna using a 0.1% cysteine solution. Therefore, it can be
elevated biological markers for metal poisoning (Florentine and concluded that a higher concentration of cysteine could assist
Sanfilippo 1991; Bluhm and others 1992; Guldager and others in an improved removal of mercury from fish. Danesh (1971)
1996; Baum 1999). Chelators such as calcium disodium ethylene- introduced a method to remove heavy metal ions (mercury, lead,
diaminetetraacetate (CaNa2 EDTA), D-penicillamine (DPA), 2,3 and cadmium) from seafood (swordfish and tuna) before canning.
dimercaptopropane-1-sulfonate (DMPS), and DMSA have been This method involved washing the seafood with an organic sulfur-
designed to effectively immobilize and remove toxic metal complexing agent (cysteine hydrochloride) and heating at 212 to
molecules, while limiting the disruption of the homeostatic levels 270 ◦ F (100 to 132 ◦ C) for 1 to 30 min to volatilize the heavy
of essential metals such as zinc (Fournier and others 1988; McFee metal ions. They found a 50% mercury removal from the fish using
and Caraccio 2001). Chelators have different efficacies depending a 1% solution of cysteine hydrochloride.
on the metal to which the patient was exposed (Anderson and Suzuki (1974) reported a reduction of 56% and up to 90%
others 2004). of the mercury concentration in swordfish and yellowfin tuna,
Chelators have also been applied to remove heavy metals from respectively, using a 0.5% cysteine solution. He also observed sig-
foods (Danesh 1971; Yannai and Saltzman 1973; Suzuki 1974; nificantly lower mercury removal at pH values lower than 2.0
Khayat and others 1975; Kyokuyo 1976; Schab and others 1978; because of the tendency of the fish to swell at a pH lower than
Ohta and others 1982; Aizpurua and others 1997; Hajeb and Jinap the isoelectric point of the muscle proteins. Spinelli and others
2012). The ligand atoms (usually oxygen, nitrogen, or sulfur) in (1973) and Okazaki and others (1984) agreed that the removal of
a chelating agent provide 2 electrons to form the coordinating more than 50% of the mercury would only be accomplished by
covalent bond. The metal chelation ability of organic compounds, producing changes in the protein properties. Nevertheless, Ohta
such as ethylenediaminetetraacetic acid (EDTA), nitrilotriacetic and others (1982) found a reduction by 50% and 67%, respectively,
acid (NTA), acetic acid, and citric acid, is commonly known; of the mercury in raw and preheated fish using 0.5% cysteine. The
therefore, they are often incorporated in food formulations. elimination of heavy metals using a cysteine solution depends on
the contact between the cysteine solution and the tissue, and it
Cysteine also depends on the migration of the soluble metal species. A large
Cysteine is the most common chelating agent used for the re- concentration of a toxic metal can be removed when the concen-
moval of heavy metals from foods. Various studies have shown a tration of cysteine in the solution is greater than that in the fish
significant reduction in the heavy metal concentrations in foods protein.
treated with cysteine (Table 2). Cysteine, the most reactive amino
acid with mercury, has been used in numerous studies to remove Ethylenediaminetetraacetic Acid (EDTA)
mercury from human food, particularly fish (Spinelli and others EDTA is a potent chelating agent and it forms stable complexes
1973; Yannai and Saltzman 1973; Suzuki 1974; Khayat and others with most metal ions. Because of its capability to seize metal ions,
1975; Schab and others 1978; Lipre 1980; Ohta and others 1982; EDTA is widely applied in food technology as well as the chemical
Okazaki and others 1984; Semenov and others 2001b; Hajeb and industry, medicine, agriculture, and pharmaceutical technology. In
Jinap 2012). The removal of mercury by cysteine is achieved by foods (such as canned mushrooms, canned or pickled vegetables,
splitting the bonds between the CH3 Hg− groups and the cys- mayonnaise, and salad dressings), it is added to prevent deterio-
teine sulfur atoms of the fish protein, which releases CH3 Hg into rative changes and to preserve color, taste, and aroma. EDTA is
solution. Most of the CH3 Hg is then bound by the cysteine in generally added as the disodium salt and it functions by chelating
the extraction solution (Schab and others 1978). Equilibrium will heavy metals, which often catalyze oxidation reactions, and by
then be reached between the CH3 Hg bound by the solution and inactivating enzymes that cause enzymatic browning (Shimadzu
the CH3 Hg bound by the fish protein. Once the cysteine con- 2005).
centration in the solution is higher than that in the fish, most of EDTA has also shown significant effects on heavy metal elimina-
the CH3 Hg can be removed (Aizpourua and others 1997). The tion from food, especially in fish (Table 2). Hajeb and Jinap (2012)
same mechanism is believed to occur with other heavy metals. identified EDTA as one of the most effective chelating agents to
Table 2–Artificial methods (using chelating agents) to remove heavy metals in different foods.
Food Heavy metal Method/agents used Reduction (%) Reference

Fish fillet Mercury Cysteine, EDTA, HCl, NaCl 91 Hajeb and Jinap (2012)
Fish fillet Mercury Citric acid, NaCl 83 Hajeb and Jinap (2009)
Cod fillets “ Cysteine 40 to 44 Lipre (1980)
Sliced and minced fish “ Cysteine, HCl, NaCl 40 to 45 Aizpurúa and others (1997)
Precooked yellow tuna “ Cysteine 47 Schab and others (1978)
Fish “ L-cysteine Considerable reduction Kyokuyo (1976)
Tuna flesh “ EDTA, cysteine or 24% to 55% Khayat and others (1975)
homo-cysteine, thiosulfate,
mercaptans, citric acid,
hydrochloric acid, sulfuric
acid, and phosphoric acid
Precooked tuna “ Cysteine 79 Yannai and Saltzman (1973)
Precooked yellow tuna “ Cysteine 47 Schab and others (1978)
Swordfish and tuna Mercury, lead and cadmium Cysteine hydrochloride, EDTA Considerable reduction Danesh (1971)
Yellowfin tuna Mercury Cysteine 90 Suzuki (1974)
Swordfish “ “ 56 “
raw and pre-heated fish “ “ 50 to 67 Ohta and others (1982)
Fish “ Ascorbic acid and citric acid Considerable reduction Semenov and others (2001a)
Fish “ Pectin “ Semenov and others (2001b)
Foodstuffs Lead, copper, or mercury Crushed egg shellmembrane “ Tetsuji and Miyuki (1982)
Processed fishery product Cadmium, mercury, tin, and Alcoholate under heating “ Tomoji (1995)
copper
Fish and animal roducts Cadmium, lead, and mercury Concentrated protein or “ Schwartz (2008)
phytic acid
Milk Iron Water insoluble resin 60 to 75 Feng and others (1994)
Wine and beer “ “ 70 to 85 “
Wine and wine-like beverages Different heavy metals Vinylheterocycle 79 Detering and others (1992)
Whole milk Mercury Thiolated aminoethyl 97 Roh and others (1975)
celluloses
Foodstuffs Different heavy metals HCl, hydrobromic, hydroiodic Considerable reduction Hinners (2006)
acid, and halogenated
organic acid
Shark flesh Mercury Citric acid 30 Okazaki and others (1984)
remove mercury from fish. Their study showed that maximal mer-
cury removal was achieved using an EDTA concentration of 275
mg/L. Khayat and others (1975) reported a 54% mercury removal
from fish using 2% saturated EDTA. Danesh (1976) examined dif-
ferent EDTA salts (disodium EDTA and calcium–sodium EDTA)
for mercury removal from swordfish, which resulted in some mer-
cury reduction (20% to 30%). However, Okazaki and others (1984)
stated that EDTA did not have any major effect on the mercury
reduction of shark tissue.
The degree of metal–EDTA complex formation is generally
determined by the pH (the hydrogen ion concentration of the
system) and the stability of the particular metal–ligand complex.
Therefore, it is always a competition between the hydrogen ions
Scheme 4–Metal–EDTA chelate.
and the metal ions in the system. A drop in pH results in an
Source: Puginier (1995).
increase in the deprotonation of EDTA and, therefore, an increase
in the concentration of the (EDTA)4− ion. Consequently, more
ligands are available for metal-binding (Taylor and Williams 1995). 1995; Nowack 1996; Bourg and Schindler 1979). These studies
Because the stability constant of EDTA with mercury (21.5) is show the role of EDTA in the transport of metal ions as anionic
greater than its stability with S (21.2) (Nriagu 1979), EDTA can EDTA complexes are highly mobile (Scheme 4).
chelate more mercury ions from fish. The concentration of EDTA
influences the degree of metal complexation and, subsequently, Other Chelating Agents
the concentration of free metal in solution (Escudero and others Other complexing agents have also beenapplied (Table 2). Nu-
2008). merous studies showed that salt (sodium chloride) could also con-
EDTA has 6 atoms (4 oxygen and 2 nitrogen) through which siderably promote mercury removal from fish fillets. Aizpurua and
it can bind to metal ions. EDTA forms very stable metal chelates others (1997) found a 40% removal of mercury from minced shark
with every metal ion and, almost invariably, the ratio of the metal meat that was treated with a salt solution (0.1 M). In the study by
chelated to the chelating molecule is 1:1. According to Dwyer Hajeb and Jinap (2009), an 80% mercury reduction was achieved
and Mellor (1964), the high stability of this metal chelate is due by the application of 0.5% NaCl. In another study, Hajeb and
to the formation of stable 5-membered rings where multiple rings Jinap (2012) reported a 90% removal of mercury by using a 0.5%
provide increased complex stability. The adsorption of EDTA and NaCl solution in combination with other chelating agents (cys-
metal–EDTA complexes onto artificial phases such as oxides or teine and EDTA). The method developed by Semenov and others
aluminosilicates has been the subject of numerous studies (Puginier (2001b), which involved dipping the raw fish into a solution of

Scheme 5–Chelation of a metal (M) by citric acid.
0.01% pectin for 5 min, has successfully removed heavy metals, water-insoluble resins to chelate iron from food beverages includ-
especially mercury, from fish tissue. ing milk, wine, and beer. The water-insoluble resin used was able
Plant phenolic compounds are also potent metal ion chelators to remove 70% to 85% of the iron content from wine and beer
due to their numerous hydroxyl groups (van Acker and others and 60% to 75% from milk. Feng and others (1994) also stated
1996; Moran and others 1997; Khokhar and Apenten 2003). A that the rate/degree of iron removal from beverages is dependent
double bond between the C2 and C3 carbons of the flavones is on the pH and the concentration of the soluble chelators added.
important for the binding and chelation of metal ions (Mira and Detering and others (1992) developed a process for removing 97%
others 2002). Tannins, the polyphenolic compounds in plants, are of the heavy metal ions from wine and wine-like beverages by
also good chelators for metal ions (Mehansho and others 1987). treating the beverage with a polymer-containing vinyl heterocy-
The presence of several catechol and galloyl groups in their struc- cle. Roh and others (1975) removed up to 70% of the mercury in
ture enables tannin molecules to chelate heavy metal ions (Karamac raw whole milk by treatment with thiolated aminoethyl celluloses.
and Pegg 2009). Cellulose, hemicelluloses, lignin, and pectins from
fiber-containing foods have the ability to bind heavy metal com- Acidic and Alkaline Solutions
pounds as well (Casterline and Yuoh 1993; Borycka and others As previously mentioned, the absorption of heavy metal ions
1996; Sangnark and Noomhorm 2003). Their chemical binding by chelating agents depends on the pH of the solution. The pH
is through the phenolic groups from the fibers and the carboxyl affects the speciation of metal ions in solution and the metal-
groups of the uronic acids (Hu and others 2010). Of the fibrous binding sites of the chelating agent (Bayramoglu and Arica 2008).
components of fruits, pectins have the highest binding capacity for For instance, the mercury in organomercurials can be replaced by
copper, cadmium, and lead. Additionally, the polyphenols bind hydrogen through reaction with acids or reducing agents (Ebadian
considerable amounts of lead ions (Nawirska 2005). 2001). Chelation is a chemical reaction that involves the bind-
Tetsuji and Miyuki (1982) proposed using novel heavy metal- ing of dissolved metals with an organic ring-forming compound.
removing agents such as dried and crushed eggshell membrane. These organic ring compounds include many organic acids such
They claimed that eggshell membrane powder, when used directly as lactic acid, acetic acid, citric acid, and ascorbic acid. All of these
or in a mixture with other food additives, would have the capacity natural acids, which are classified as weak acids, have the ability
to remove harmful metals, such as lead, copper, or mercury, from to sequester or seize metal atoms such as mercury, cadmium, and
food. Tomoji (1995) patented an industrial protocol to remove lead.
toxic metals, such as cadmium, mercury, tin, and copper, contained The pH has always been one of the factors investigated in studies
in a processed fishery products. He extracted heavy metals from a performed on heavy metal reduction in foods. Various pH ranges,
processed fishery product using alcohol under heating, electrolysis, adjusted using different acids and alkalis, have been evaluated for
and desalination of a salted food. Schwartz (2008) also developed the reduction of each heavy metal; however, most researchers
a method to remove and manage the heavy metals in foods. His applied hydrochloric acid (Yannai and Saltzman 1973; Khayat and
method is applicable to food processing (fish, shellfish, and other others 1975; Aizpurua and others 1997; Hinners 2007; Hajeb
animal products) to remove mercury, cadmium, lead, chromium, and Jinap 2012). Hajeb and Jinap (2012) reported a greater than
manganese, copper, nickel, barium, zinc, selenium, and silver. In 90% mercury removal from a mackerel fillet at pH 3.75. At pH
this method, the food is exposed to a heavy metal-binding ligand, 2.0 to 2.2 and pH 1.5, Yannai and Saltzman (1973) managed
such as phytic acid or concentrated protein, to form a heavy metal to remove 55% and 79% of the mercury in precooked slices of
chelate, and then the chelate is allowed to separate from the food. tuna, respectively. They used dilute hydrochloric acid containing
Using phytic acid disodium salt as the heavy metal-binding ligand 0.33% cysteine hydrochloride to treat the fish slices. Aizpurua and
in fish, 50% mercury removal was obtained (Schwartz 2008). others (1995)achieved 45% mercury removal from minced shark at
The method for removing heavy metals from beverages using pH 7. Ohta and others (1982) and Spinelli and others (1973) used
water-insoluble calcium salts (calcium chelates) that exchange cal- extraction solutions containing cysteine at pH levels above 4.5 and
cium for the metal ions in the food was invented by Bersworth 1.4, respectively. Schab and others (1978) found a 47% reduction
(1958). Using this method, copper and iron were successfully re- of mercury in precooked yellow tuna at pH 2.2. Additionally,
moved from wine. In another study, Feng and others (1994) used they claimed that there was no advantage to a pH below 0.5 when
using cysteine solutions because it strongly protonates the sulfur bond by a 6-center cyclic process (Di Michele and others 2009).
to form −SH groups, which blocks their availability for binding The cleavage of aryl groups from mercury by reagents, such as
to mercury ions. hydrogen chloride in partially aqueous media, appears to resemble
Hinners (2007) used strong acid solutions (hydrochloric, hy- aromatic substitution and likely proceeds via the formation of an
drobromic, hydroiodic acid, and halogenated organic acids) and σ -complex (Eq. 3).
sodium bicarbonate to adjust pH. He reported the removal of
aluminum, beryllium, calcium, cadmium, copper, lead, magne- Slow H Fast
ArHgCl + H+ ←→Ar+ ←→ ArH + HgCl2 (3)
sium, manganese, mercury, potassium, iron, nickel, sodium, and HgCl (C1− )
zinc from different foods (fish, shellfish, vegetables, and fruits) at
pH values between 4 and 8. Treating bovine liver samples with The carboxyl and hydroxyl groups of citric acid can each lose
0.16 N nitric acid for 24 h at ambient temperature removed 99% a proton and coordinate to a metal ion to form a metal chelate.
of the calcium, 97% of the copper, 40% of the iron, and 100% Metals form stable complexes with citric acid (Fennema 1996),
of the cadmium, magnesium, manganese, potassium, sodium, and and the typical structure of citric acid with a metal is shown in
zinc (Hinners 2007). Treatment with a 0.16 N nitric acid solution Scheme 5.
for 21 h at ambient temperature removed 89% of the lead and
52% of the nickel from other animal tissues. Using 2 N nitric Conclusion
acid for 20 h at ambient temperature can remove 97% and 50% of The concentration of toxic elements may be reduced in a food-
the mercury from flaked swordfish and sliced shark muscle, respec- stuff by choosing a suitable method for preparation. Precooking
tively (Hinners 2007). Khayat and others (1975) also used different treatments such as the peeling of plant products as well as some
acids (citric, hydrochloric, sulfuric, and phosphoric) in combina- cooking methods can remove some of the heavy metals. Cooking
tion with complexing agents to remove mercury from fish flesh. methods such as boiling and frying can alter the content of a toxic
Their study showed that pH is very important for the thiosulfate element through the loss of water and volatiles, the solubilization
ion to remove mercury from fish muscle, and the optimal pH to of the metal, and, to some extent, metal binding to macronutrients
remove 55% of the mercury was 4.25. such as carbohydrates, lipids, and proteins. Since toxic elements
Citric acid is one of the organic acids commonly used as a are not evaporated or broken down to safer compounds, the ele-
chelating agent. Semenov and others (2001a) used a 0.1% citric ments which are removed from foodstuff during frying, boiling,
acid solution to remove heavy metals from fish. They reported or canning processes definitely migrate from food to the frying
increased amounts of mercury removed from fish in a shorter time oil, boiling water or cooking stocks. However, some of cooking
due to the reductive property of citric acid. The application of methods and herbal marinating reduce bioaccessibility of toxic
citric acid has also been utilized by Okazaki and others (1984), elements through binding of elements to other compounds and
and they reduced 30% of the mercury in shark flesh at pH 1 to forming unbioaccessible complexes. Mercury can be eliminated
2. However, Hajeb and Jinap (2009) achieved a 75% reduction from food using acids because an acidic medium assists in the re-
of mercury in mackerel fillets at pH 1 to 2 using citric acid and moval of mercury bound to the protein in fish tissue. EDTA and
sodium hydroxide. In their study, Hajeb and Jinap (2009) also cysteine are the chelating agents with the highest potential for
found that the optimum pH to remove 83% of the mercury from application to the industrial removal of toxic elements in fish.
a fish fillet was 2.79. They identified pH as the most effective
factor in mercury reduction.
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Toxic Elements in Food: Occurrence, Binding, and Reduction Approaches

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Toxic Elements in Food: Occurrence, Binding, and Reduction Approaches

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Toxic Elements in Food: Occurrence, Binding,

and Reduction Approaches

Introduction consumption. Numerous studies have been carried out to exam-

the pH range of 3.5 to 8, competitive binding to COO− and

R − SH + Hg2+ ↔ R − S − Hg+ +H+

The linkage of 2 macromolecules by Hg2+ is relatively com-

Food Heavy metal Cooking/processing Reduction (%) Reference

Food Heavy metal Method/agents used Reduction (%) Reference

Scheme 5–Chelation of a metal (M) by citric acid.

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