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Buzała M., Słomka A., Janicki B. 2016. Heme iron in meat as the main
source of iron in the human diet. J. Elem., 21(1): 303-314. DOI: 10.5601/
jelem.2015.20.1.850
Journal of Elementology ISSN 1644-2296
REVIEW PAPER
HEME IRON IN MEAT AS THE MAIN SOURCE
OF IRON IN THE HUMAN DIET
Mateusz Buzała1, Artur Słomka2, Bogdan Janicki1
1Department of Animal Biochemistry and Biotechnology
UTP University of Science and Technology, Bydgoszcz
2Department of Pathophysiology
Nicolaus Copernicus University in Toruń
Ludwik Rydygier Collegium Medicum in Bydgoszcz
Abstract
Iron is a trace element involved in many cardinal metabolic processes of almost all living
organisms. It is well known that iron participates in oxygen transport as well as it is a cofactor
in many fundamental enzymatic and nonenzymatic processes. Accordingly, disturbances of iron
homeostasis can cause serious clinical consequences. In humans, dietary iron can enter the body
in two main forms: heme and nonheme. The former is a component of many hemoproteins
(including myoglobin, hemoglobin, cytochromes b and c) and is easily absorbed in the duodenal
enterocytes. Red meat is an excellent source of heme iron, while the less bioavailable nonheme
form is found in large amounts in milk products and vegetables. For this reason, consumers of
meat have a better iron status than vegetarians and vegans. Heme iron found in muscle protein
should be supplied to humans to prevent iron deciency, which can lead to anemia. It is easily
absorbed and its main source is red meat. In addition, heme iron, which is mainly found in my-
oglobin in meat, contributes to the desirable bright red color and to the most undesirable brown
color of meat. Both heme and nonheme iron are catalysts of lipid oxidation in meat. This process
lowers the nutritive value through oxidation of polyunsaturated fatty acids, which produces an
undesirable avor and aroma. The aim of this paper was to discuss the role of heme iron in the
human diet.
Keywords: iron, meat, lipid oxidation, metabolism, meat color.
Mateusz Buzała, MSc, Department of Animal Biochemistry and Biotechnology, UTP University
of Science and Technology, Mazowiecka 28, 85-084 Bydgoszcz, Poland, e-mail: buzala@utp.edu.pl
304
INTRODUCTION
Iron is crucial for many of the body’s metabolic processes, such as oxygen
transport and storage, and electron transfer. Iron is also necessary for normal
development of the central nervous system, cell proliferation, synthesis and
the repair of genetic material. As a component of catalase and peroxidase,
iron represents a protective mechanism against reactive oxygen species (Mar-
tınez-navarrete et al. 2002, PaPanıkolaoua, PantoPoulos 2005, Mcafee et al.
2010, Słomka et al. 2012). For this reason, prenatal and postanatal iron de-
ciency may affect adversely the cognitive processes and thus lead to neuropsy-
chological disorders (conrad, uMbreıt 2000, taPıero et al. 2001, Mancını,
Hunt 2005). Iron deciency is one of the most common nutritional decien-
cies, affecting around 20% of the world’s population. Deciency of this ele-
ment is more prevalent in less industrialized countries (20-50% of the popula-
tion) than in more developed countries (2-28%) (Martínez-navarrete et al.
2002). The most signicant consequence of iron deciency is sideropenic (iron
deciency) anemia. It is mostly caused by insufcient dietary intake of iron,
often when the demand is high. The disease is most commonly found in in-
fants and in women of childbearing age, often as a result of heavy menstrual
bleeding. It is also stressed that iron deciency can induce many abnorma-
lities in fetal and neonatal development (Słomka et al. 2012). In adolescence
the demand for iron increases, due to the growth and development of muscles
and increasing blood volume. This results in an intensication of erythropoie-
sis, for which iron is necessary to produce myoglobin and hemoglobin (Mesías
et al. 2013). Although iron plays a signicant role in the human body, an ex-
cessive intake of this element may contribute to intestinal mucosal damage
and be a risk factor in cardiovascular diseases, neurodegenerative diseases,
infections and colorectal cancer (Pereıra, vıcente 2013). The results of the
meta-analysis suggest that the intake of heme is associated with an increased
risk of coronary heart disease. In individuals who consume more heme iron a
31% increase in the risk of the disease was found compared with those with
a lower consumption of this type of element (Yang et al. 2014).
The present review is focused on role of heme iron, which is mainly fo-
und in meat and is the principal source of iron in the human diet.
Iron as a component of meat myoglobin
Myoglobin (17 kDa) is the main proteins of muscle tissue sarcoplasm,
containing a centrally located heme (Figure 1), which is a complex of proto-
porphyrin IX with Fe(II). Globin is a single chain of 153 amino acid residues
with 80% of the polypeptide chain existing in a-helical conformations, which
makes protein structure highly compact. Heme in the hydrophobic pocket of
this molecule is protected from oxidation to Fe(III) (brewer 2004, Mancını,
Hunt 2005, PaPanıkolaoua, PantoPoulos 2005). The fth coordination position
of the iron atom is occupied by the imidazole nitrogen atom of histidine resi-
305
due (His 93). The sixth coordination position of the iron atom on the opposite
side of the heme is the main binding site for oxygen and also for nitric oxide
and carbon oxide. In addition, differences in the occupancy of the sixth coor-
dination position enable myoglobin to exist in three physiological forms. In
deoxymyoglobin, this position remains empty; in oxymyoglobin, it is occupied
by oxygen, and in ferrimyoglobin, the site is occupied by water (brewer 2004,
Mancını, Hunt 2005).
The myoglobin content of skeletal muscles can be inuenced by an ani-
mal’s breed, age and muscle activity (kołczak 2008). Red meat owes its dark
red color to the presence of large amounts of heme, the content of which in
this meat is 10-fold higher than in white meat (bastıde et al. 2011). Beef has
the highest amount of myoglobin per gram of fresh meat (15 mg) compared
to mutton (10 mg), pork (5 mg), poultry and rabbit meat (≤ 5 mg) (valenzu-
ela et al. 2011). Heme iron content in beef may depend on the type of musc-
le, breed and storage time (raMos et al. 2011). Physical activity of animals
may increase the amount of heme iron, especially in muscles having high
oxidative activity. A greater degree of physical tness increases the muscle
oxidative capacity by increasing the number of mitochondria in the white -
bers, hence turning them into red bers (castellını et al. 2002). The muscles
of heifers, young bulls and steers contain less myoglobin than the muscles of
cull cows, while calf muscles have less pigment than steer muscles (kołczak
2008). In addition, the content of total iron, heme iron and myoglobin in the
muscles of animals on low level feeding is higher than in those on high fe-
eding level (PurcHas, busbooM 2005, calkıns, Hodgen 2007). Furthermore,
the above parameters of iron homeostasis are lower in older animals than in
younger ones (calkıns, Hodgen 2007).
Effect of iron on meat color
Meat color is primarily determined by its content of myoglobin, but also
hemoglobin and cytochrome c. The binding of an oxygen molecule to myoglo-
Fig. 1. The structure of heme
306
bin makes it oxygenated (oxymyoglobin), thus giving the desired bright red
color of meat. During the oxygenation, iron’s valence does not change and the
sixth coordination position is occupied by an oxygen molecule. In addition,
the distal histidine (His 64) in myoglobin interacts with bound oxygen, alte-
ring the oxygen’s structure and stability. As exposure to oxygen increases,
the oxymyoglobin penetrates deeper beneath the meat’s surface. The depth of
oxygen penetration depends on the meat’s temperature, oxygen partial
pressure, pH and competition for oxygen by other processes that require this
cofactor (Mancını, Hunt 2005, kołczak 2008).
Under anaerobic conditions, most often during the vacuum packaging of
meat, oxymyoglobin is converted to deoxymyoglobin, because the sixth coor-
dination position for oxygen is unoccupied and iron is present in the form of
Fe(II). In this case, meat becomes purple red or purple pink, because very
low oxygen partial pressure (<1.4 mm Hg) maintains myoglobin as deoxymy-
oglobin (myoglobin without oxygen).
Metmyoglobin is a molecule between the oxymyoglobin present on the
surface of meat and the deoxymyoglobin present in meat, as a result of a
change in valency of from Fe(II) to Fe(III). Metmyoglobin is formed inside
meat and extends towards the surface, producing the undesirable brown co-
lor of the meat. Metmyoglobin formation depends on many factors, including
oxygen partial pressure, temperature, pH, the reducing activity of meat com-
ponents and in some cases the growth of microorganisms. Metmyoglobin re-
duction is essential to meat color and largely depends on the enzymatic acti-
vity and pool of NADHs (reduced nicotinamide adenine dinucleotide), which
are constantly depleted with the increasing time after slaughter. Lactate
dehydrogenase, which catalyzes the interconversion of pyruvate and lactate
with concomitant interconversion of NADH and NAD+, injected postmortem
into meat was found to oxidize lactate to pyruvate and to reduce the amount
of metmyoglobin, thus improving the color of meat (Mancını, Hunt 2005, koł-
czak 2008).
Iron as a catalyst of lipid oxidation in meat
During postmortem changes, the natural antioxidant system that pre-
vents living cells from lipid oxidation becomes increasingly weaker, which
accelerates the lipid oxidation processes. The cessation of blood circulation in
the body shifts metabolism from oxidative to glycolytic during the conversion
of muscle to meat. This results in lactic acid accumulation, which reduces pH
from 7.4 to approx. 6.0-5.5. This is when the structural integrity of muscle
cells is compromised as a result of proteolysis and protein denaturation, re-
leasing iron ions from hemoproteins and low-molecular-weight compounds,
which may become catalysts. Iron initiates lipid oxidation by generating, via
the Fenton reaction, reactive oxygen species capable of abstracting a proton
from unsaturated fatty acids. Free iron ions may bind to negatively charged
phospholipids (such as phosphatidylcholine) in cell membranes and catalyze
307
the breakdown of pre-formed lipid hydroperoxides. The lipid hydroperoxides
are further decomposed oxidatively to form peroxide radicals or, by reduc-
tion, to produce alkoxyl radicals. These radicals may initiate new chain reac-
tions, and alkoxyl radicals may further decompose to produce aldehydes and
other secondary products of lipid oxidation (carlsen et al. 2005, Mın, aHn
2005, orıno, watanabe 2008). One such short-chain aldehyde is malondialde-
hyde (taPıero et al. 2001, Hęś, korczak 2007, danesHYar 2012). This compo-
und is often used to evaluate the degree of lipid peroxidation and may produce
a rancid avor and aroma, undesirable for the consumer (taPıero et al.
2001, faustMan et al. 2010, danesHYar 2012). Malondialdehyde may induce
DNA damage, leading to mutations, and can react with DNA to form adducts
with deoxyguanosine, deoxyadenosine and deoxycytidine. The major DNA
adduct formed by the reaction of malondialdehyde with DNA is 1,N2-malon-
dialdehyde-deoxyguanosine (M1dG) (bastıde et al. 2011). In addition, heme
proteins that initiate lipid oxidation in biological membranes may impair
membrane function, decrease uidity, inactivate membrane-bound recep-
tors and enzymes, and increase permeability to ions such as Ca2+ (baron,
andersen 2002).
Free iron ions released from heme and ferritin may be considered as the
main catalysts of lipid peroxidation in both raw and cooked meat. Ferritin is
a ubiquitous intracellular protein (consisting of 24 protein subunits) that
stores iron and releases it in a controlled fashion. Ferritin releases iron in
the presence of reducing agents such as superoxide anion and ascorbate
(Mın, aHn 2005). Hydrogen peroxide, present in the muscle cell cytosol, rele-
ases free iron from heme as a result of oxidative cleavage of the porphyrin
ring, whereas ascorbate releases iron ions from ferritin, which catalyzes lipid
peroxidation in meat. Ascorbic acid can exhibit both antioxidant and prooxi-
dant properties, depending on its concentration and the amount of iron pre-
sent. In low concentrations, ascorbic acid most often contributes to lipid pe-
roxidation in muscle tissue by reducing iron, and in high concentrations it
transforms some of peroxide radicals directly into lipid hydroperoxides, as a
result of breaking the free radical reaction by donating a hydrogen atom to
the free radical. Ascorbic acid also regenerates a-tocopherol in biological
membranes (Mın, aHn 2005).
In addition, iron in muscle can be chelated by low-molecular-weight com-
pounds, such as organic phosphate esters, inorganic phosphates, amino acids
and organic acids. Low-molecular-weight, water-soluble iron-chelating agents
may be responsible for catalyzing the oxidation of tissue lipids by iron. What
is more, the conversion of ferritin to hemosiderin in the body is biologically
benecial because it decreases the availability of iron for promotion of lipid
peroxidation. Therefore, the body’s iron metabolism should be strictly regu-
lated by iron-binding proteins to ensure that no free iron exists (Mın, aHn
2005). Ferritin is a ubiquitous and highly conserved iron storage protein,
which plays a major role in iron metabolism by storing iron ions and protec-
308
ting tissues from its toxic effect. Furthermore, owing to the enzymatic activi-
ty, ferritin molecules are able to oxidize Fe(II) to Fe(III) (orıno, watanabe
2008, Słomka et al. 2012). Non-transferrin-bound iron (NTBI) can be highly
toxic because it facilitates reactive oxygen species generation, which contri-
butes to the damage of all biomolecules. Non-transferrin-bound iron may be
involved in the pathogenesis and progression of many hematological disor-
ders, as well as in the etiopathogenesis of the central nervous system in
neonates, neurodegenerative diseases and diabetes (Słomka et al. 2011, koba
et al. 2013).
The susceptibility of raw meat to lipid oxidation depends on the animal
species, muscle type, activity of antioxidant enzymes, fat content, fatty acid
prole and other factors (Mın et al. 2008). Muscles with a higher number of
red bers (type I or type IIa) are more sensitive to lipid oxidation because
they contain more iron and phospholipids compared to muscles that mostly
contain white bers (faustMan et al. 2010, saMuel et al. 2012). Muscles with
more red bers generate more hydrogen peroxide during auto-oxidation of
this protein compared to meat with a lower content of this pigment. Hydro-
gen peroxide may react with metmyoglobin to form ferrylmyoglobin, which
initiates lipid oxidation by abstracting a hydrogen atom from polyenoic fatty
acids and generates lipid hydroperoxides. Additionally, heating reduces the
activation energy for lipid peroxidation and breaks down initially formed
hydroperoxides to free radicals, which stimulate auto-oxidation processes and
the development of undesirable avor and aroma (Mın et al. 2008). Nonheme
iron plays a greater role in this process, especially in an acidic environment
and in cooked meat. In turn, heme iron may initiate lipid oxidation in both
raw and cooked meat (Hęś, korczak 2007). Additionally, the meat cooking
process inhibits the activity of antioxidant enzymes and releases iron from
heme, leading to its oxygenation.
Source of iron in the human diet
Iron in the human diet has two forms: heme iron (II), which is easily ab-
sorbed, and nonheme iron (III), which is much less readily absorbed by the
body (carPenter, MaHoneY 1992, beard, Han 2009, valenzuela et al. 2009,
scHonfeldt, Hall 2011). Red meat, in particular beef, mutton and goat meat,
is regarded as a richer source of heme iron (Table 1) than poultry meat and
sh (taPıero et al. 2001, uMbreıt 2005, valenzuela et al. 2009, Mcafee et al.
2010, scHonfeldt, Hall 2011, zotte, szendro 2011). Heme iron, although con-
sumed in smaller amounts, is two- or threefold more easily absorbed (50-87%)
than nonheme iron. Nonheme iron, which is found mainly in vegetables and
milk products, forms the majority of all dietary iron (approx. 60%), but its
absorption is low (2-20%) (carPenter, MaHoneY 1992, benıto, Mıller 1998,
valenzuela et al. 2009, 2011). The absorption rate of nonheme iron depends
on the presence of dietary components that increase or inhibit its bioavailabi-
lity (taPıero et al. 2001, uMbreıt 2005, scHonfeldt, Hall 2011, Pereıra et al.
309
2013). Its absorption is facilitated by factors such as ascorbic acid, citric acid
and some amino acids. Citric acid enhances the absorption of nonheme iron
through chelation, preserving it in the solution of ascorbic acid and some ami-
no acids such as cysteine, which reduce iron to a more readily available form
of Fe(II), thus facilitating its intestinal absorption (carPenter, MaHoneY 1992,
benıto, Mıller 1998, conrad, uMbreıt 2000, uMbreıt 2005, beard, Han 2009,
Pereıra, vıcente 2013). Other organic acids, such as malic and tartaric acid,
can also improve the absorption of iron (lıM et al. 2013). Infants and approx.
one-third of the elderly have low secretion of hydrochloric acid by gastric pa-
rietal cells, which may lead to iron malabsorption (benıto, Mıller 1998). The
absorption of nonheme iron is inhibited by factors such as phosphates, phyta-
tes, dietary ber, lignins, polyphenols and tannins. These inhibitors generally
bind most iron ions into complexes and make them unavailable to transport
proteins. In turn, heme iron, which is easily soluble in the alkaline environ-
ment of the duodenum, is immediately absorbed by enterocytes (conrad,
uMbreıt 2000, 2005, beard, Han 2009). Minerals such as zinc, calcium, copper
and manganese can also inhibit the bioavailability of iron by competing
for the same carrier in enterocytes, modifying the oxidation state of iron or
interfering with metabolism (Mesías et al. 2013). Studies have shown that
calcium chloride also inhibits the absorption of heme iron (lóPez, Martos
2004). As a result, iron in a diet which is high in cereal products and
thus has a substantial bre content will be less bioavailable than in a diet
containing meat, regardless of other factors affecting iron absorption in the
human body (benıto, Mıller 1998, uMbreıt 2005, beard, Han 2009).
Table 1
Iron content in meat of different species of animals
Type
of meat
Iron content
(mg kg-1)Source
Beef 8-220 (Mın et al. 2008, valenzuela et al. 2009, scHonfeldt, Hall 2011,
HoffMann et al. 2010)
Veal 5.5-23 (scHonfeldt, Hall 2011, zotte, szendro 2011)
Mutton 33 (zotte, szendro 2011)
Lamb 9.6-26 (scHonfeldt, Hall 2011, HoffMann et al. 2010)
Goat 21-44 (webb et al. 2005)
Game 33-47 (sales, kotrba 2013, trıuMf et al. 2012)
Pork 5.5-17 (Mın et al. 2008, zotte, szendro 2011, HoffMann et al. 2010)
Poultry 5.9-20 (Mın et al. 2008, zotte, szendro 2011, Buzała et al. 2014)
Rabbit 1-13 (zotte, szendro 2011, cYgan-szczegıelnıak et al. 2012)
Fish 1.2-5 (stanek et al. 2012, grela et al. 2010)
310
Iron metabolism in the human body – short presentation
The average intake of meat is 41-72 g day-1 in men and 24.2-45.5 g day-1
in women, which supplies the body with 14.5±5 mg and 20.2±28 mg of iron,
respectively (Pereıra, vıcente 2013). Daily dietary iron requirements are
approx. 8 mg for adult men and approx. 18 mg for adult women with men-
strual iron losses (ganz, neMetH 2012). During pregnancy, total iron require-
ment is approx. 1,040 mg (Słomka et al. 2012). However, iron deciency often
occurs in young women in Poland (Hamułka et al. 2011, WaśkieWicz, SygnoW-
ska 2011). Consequences of iron deciency and iron overload in humans are
shown in Figure 2.
Iron is stored mainly in the liver, containing around 60% of the body’s
iron pool, of which around 95% is stored as ferritin in hepatocytes. Small
amounts of iron (around 5%) can also be stored as hemosiderin, apparently a
degradation product of ferritin, which is mainly found in Kupffer cells. The
amount of ferritin, an easily available source of iron, is mainly regulated by
iron regulatory proteins (IRP1 and IRP2). These proteins are key regulators
of iron cell homeostasis in higher eukaryotes. A single ferritin molecule can
hold up to 4,500 iron atoms, which may participate in erythropoiesis. Ery-
Fig. 2. Summary of the consequences of iron deciency and iron overload in human
(koHgo et al. 2008, falkowska, ostrowska 2010, Słomka et al. 2012)
311
thropoiesis requires around 30 mg of iron/day, and erythrocytes contain aro-
und 80% of the body’s total iron. The remaining content of iron in the body
(around 40%) is found in muscle tissue myoglobin, epithelial reticular cells,
cytochromes and iron-containing enzymes (catalase, peroxidase). Only very
small amounts of iron are excreted and the body’s iron cycle is nearly closed.
A human with around 4 g of iron stored in the body loses only 1 mg per day
(0.025% of the body’s iron) and consumes a similar amount daily with food.
Body iron is lost, among others, through iron found in sloughing epidermal
and intestinal epithelial cells, and as a result of menstrual bleeding in wo-
men (conrad, uMbreıt 2000, taPıero et al. 2001, PaPanıkolaoua, PantoPoulos
2005, uMbreıt 2005, beard, Han 2009, Słomka et al. 2012).
Iron ions in food are absorbed mainly in the duodenum. The transport of
iron ions into enterocytes occurs through the divalent metal transporter
DMT-1, which is located at the apical membrane of intestinal enterocytes.
DMT-1 works in concert with duodenal cytochrome b (Dcytb) (ganz, neMetH
2012). Heme iron passes through the apical membrane of the duodenal ente-
rocytes with the help of the heme transporter HCP1 protein (heme carrier
protein 1). Next, heme is released from the porphyrin ring by the action of
the heme oxygenase enzyme and divalent iron is released. The porphyrin
ring may be responsible for the high absorption of heme iron (lóPez, Martos
2004). In turn, globin degradation metabolites facilitate the absorption of
nonheme iron. Next, iron leaves the cell through the basolateral membrane
of the enterocyte and enters the bloodstream via ferroportin, which works in
combination with hephaestin. Ferroportin is a key iron transporter found on
duodenal enterocytes. It is also subject to molecular control. After binding to
hepcidin, ferroportin decreases the export of iron from cells to the blood.
Hepcidin is a peptide hormone that inhibits duodenal iron absorption and its
synthesis is regulated by iron. Large amounts of iron in the hepatocytes
(inammation) contribute to higher hepcidin production in the liver, thus
reducing iron absorption and release in the body. In turn, iron deciency
decreases or inhibits hepcidin production by hepatocytes, allowing more iron
to enter blood plasma (lóPez, Martos 2004, ganz, neMetH 2012). Following
release from enterocytes, the ferrooxidase enzymes hephaestin and cerulopla-
smin, which contain atoms of copper, can oxidize Fe(II) to Fe(III). In the
blood, two atoms of oxidized iron bind to transferrin, which is a 78 kDa gly-
coprotein. This protein is responsible for transporting iron to most cells and
normally about 25-30% of transferrin is saturated by iron. The transferrin-
-Fe(III) complex in blood is taken up by transferrin receptors (TfR1 and
TfR2) located in the target cell membrane. The rate and site of iron uptake
from plasma depends on the number of transferrin receptors, which are hi-
ghly expressed in all diving cells, especially erythroid cells. Transferrin re-
ceptor 1 binds two molecules of transferrin, as a result of which iron ions are
released into the cell cytoplasm. The role of the second receptor (TfR2)
in iron metabolism has received less attention. Probably, this receptor is
responsible for binding non-transferrin-bound iron (NTBI). Iron ions are
312
transported into the cell via endocytosis. In the resulting endosome, which
maintains an acidic pH, iron is separated from transferrin. Next, iron enters
the cytoplasm via DMT-1 present in the endosome membrane. Iron ions in
the cytosol are incorporated into ferritin and hemosiderin to form a storage
pool or are used for producing heme and nonheme proteins. After release of
iron, apotransferrin is recycled to the membrane, leaves the cell and enters
circulation to transport the next iron ions again (benıto, Mıller 1998, con-
rad, uMbreıt 2000, taPıero et al. 2001, uMbreıt 2005, beard, Han 2009,
Słomka et al. 2012).
SUMMARY
Heme iron found in muscle protein should be supplied to humans to pre-
vent iron deciency, which can lead to anemia. Heme iron, whose main sour-
ce is red meat, is easily absorbed by the human body. In addition, heme iron,
which is mainly found in myoglobin in meat, contributes to the desirable
bright red color and to the most undesirable brown color of meat. Both heme
and nonheme iron are catalysts of lipid oxidation in meat. This process lo-
wers the nutritive value through oxidation of polyunsaturated fatty acids,
which produces an undesirable avor and aroma.
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