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To assess cookware�s influence on the concentration of essential and non-essential trace metals and on the lipid peroxidation process in pork muscle during heat treatment, meat samples were cooked without the addition of oil, salt or spices, at a temperature of 200�C � 2�C for 50 minutes, in pans made of aluminium, ceramic-coated aluminium, brass and stainless steel. Fe, Cu, Zn, Mn, Sn, Ni, Cr, Ti, Al, Pb, Cd and U in samples were subsequently determined by optical emission spectrometry (OES). In order to assess the intensity of lipid peroxidation, peroxide value (PV) and thiobarbituric acid reactive substances (TBARS) were determined by colorimetric methods.
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http://www.revistadechimie.ro REV.CHIM.(Bucharest)68No. 7 2017
1476
The Influence of Cookware on the Concentration of Trace Metals and
Lipid Peroxidation in Pork Muscle
CAMELIA PAPUC, IRINA CHERA, CORINA PREDESCU*, VALENTIN NICORESCU, IULIANA GAJAILA,
GHEORGHE VALENTIN GORAN
University of Agronomic Sciences and Veterinary Medicine of Bucharest, 59 Marasti Blvd, 011464, Bucharest, Romania
To assess cookware’s influence on the concentration of essential and non-essential trace metals and on the
lipid peroxidation process in pork muscle during heat treatment, meat samples were cooked without the
addition of oil, salt or spices, at a temperature of 200°C ± 2°C for 50 minutes, in pans made of aluminium,
ceramic-coated aluminium, brass and stainless steel. Fe, Cu, Zn, Mn, Sn, Ni, Cr, Ti, Al, Pb, Cd and U in
samples were subsequently determined by optical emission spectrometry (OES). In order to assess the
intensity of lipid peroxidation, peroxide value (PV) and thiobarbituric acid reactive substances (TBARS)
were determined by colorimetric methods.
Key words: meat, trace elements, peroxide value, thiobarbituric acid reactive substances
The term
trace element
is used for an element occurring
at levels lower than 0.01% (< 100 µg/g) [1]. Trace metals
can be classified in essential trace metals, essential for a
normal life (Fe, Zn, Cr, Co, Ni, Cu, Mn, Mo, Se) and non-
essential trace metals [1]. Human diet is rich in essential
trace metals but, due to industrialization, may also contain
non-essential trace metals with toxic effects on the human
body. The presence of essential trace metals above certain
concentrations in food can have negative effects on both
human health and the quality of foods. The negative effects
on human health may be due to the fact that inadequate
intake of any essential trace metal may result in specific
biochemical lesions within cells of the body and
development of characteristic clinical symptoms [1]. Most
kitchen utensils used for food thermal cooking are made
of different metals, alone or in combination. During heat
preparation, cookware metals can leach into food.
In food systems, transition metals can act as catalysts
of lipid peroxidation process. Thus, iron act as promoter of
lipid oxidation in the presence of hydroperoxides. Iron, like
other transition metal ions, is involved in one-electron redox
reaction, which leads to hydroperoxide decomposition to
generate alkoxyl and peroxyl radicals, which are initiators
in chain reactions of the autoxidation [2, 3, 4]. Lipid
oxidation products (e.g., 4-hydroxynonenal and
malondialdehyde) ingested along with food represent a
risk for body health. Chronic uptake of large amounts of
such substances is reported to increase tumour frequency
and incidence of atherosclerosis in animals [5].
This study aimed at assessing to what extent cookware
made of aluminium, ceramic-coated aluminium, brass and
stainless steel influence the concentration of some trace
metals and lipid peroxidation in meat cooked at 200°C. To
evaluate the effect of cookware on the concentration of
trace metals and lipid peroxidation, the concentrations
obtained for heat-treated meat were compared with
concentrations found in raw meat.
Experimental part
Materials
Fresh pig meat was purchased from a farm around the
city of Bucharest, Romania. The animal was slaughtered
after electrical stunning and the meat was refrigerated at
* email: durduncorina@yahoo.com; Phone: 0744.867.527
4°C. The cookware was purchased from a local store
(Bucharest), excepting the brass and aluminium pans,
which were purchased from a craftsman.
Preparation of meat samples
At 24 hours after slaughtering, semimembranosus
muscle was excised, external fat and epimysial connective
tissue were removed and muscles were divided
perpendicularly to their longitudinal axis into five equal
fractions, and every fraction was cut into three even
portions with an average weight of 250 – 260 g. The first
fraction was heat-untreated and the other 4 parts were
cooked in a preheated oven at 200°C in pans made of
aluminium, ceramic-coated aluminium, brass and
stainless steel. Meat samples were heat treated without
the addition of oil, salt or spices, at a temperature of 200°C
± 2°C for 50 min; the temperature was controlled by a
Eurotherm thermoregulator. After cooking, the meat was
taken out of the oven and then allowed to cool to room
temperature. Both raw and cooked meat samples were
homogenised in a glass blender and each group was further
analysed.
Chemical analysis
Determination of trace metals in meat
Drying of samples.
Meat samples were weighed with
an accuracy of 0.0001 g in weighing vials brought to
constant weight, at a temperature of
105 ± 2°C, and then
were dried in an oven at 105 ± 2°C for 8 h.
Calcination of samples.
After drying, the samples were
weighed with an accuracy of 0.0001 g in porcelain
crucibles brought to constant mass. The crucibles were
heated in the flame of a gas burner for two hours and then
were placed in a furnace at 450°C for 48 h. The resulting
ash was weighed on analytical balance and then subjected
to disaggregation with HCl 37% diluted with bidistilled water
1:4 (v/v). After disaggregation, the samples were brought
to 25 mL in volumetric flasks and then were used to
determine the trace metals.
Determination of trace metals.
Fe, Cu, Zn, Mn, Sn, Cr, Ni,
Ti, Al, Cd and Pb were determined by
Inductively-coupled
argon plasma - Optical emission spectrometry (ICP-OES),
REV.CHIM.(Bucharest)68No. 7 2017 http://www.revistadechimie.ro 1477
using a spectroflame ICP model P (SPECTRO Analytical
Instruments, U.S.A.). The determinations were performed
in accordance with [6]. Uranium was assessed by Direct
coupled plasma - Optical emission spectrometry (DCP-
OES), using a SpectraSpan V (Beckman Instruments,
U.S.A.) spectrometer and a standardized method was
applied [7].
Determination of lipid oxidation parameters
Determination of peroxide value
(PV).
PV was
determined according to the method of [8], modified by
[9]. Ground sample (1.00 g) was homogenized with 11
mL of chloroform/methanol (2:1, v/v) mixture. The
homogenate was filtered and 2 mL of 0.5% NaCl solution
were added to 7 mL of the filtrate. The mixture was vortexed
at a moderate speed for 30s and then centrifuged at
3,000×g for 3 min at 4°C, using a refrigerated centrifuge to
separate the sample into two phases. The lower phase (3
mL) was carefully pipetted out, and 2 mL of cold
chloroform/methanol (2:1) mixture were added. Then, 25
µL of 30% (w/v) ammonium thiocyanate and 25 µL of 20
mM iron (II) chloride were added to the mixture. The
reaction mixture was allowed to stand for 20 min at room
temperature prior to reading the absorbance at 500 nm.
The blank sample was prepared in the same manner,
except that chloroform/methanol mixture was used
instead of sample extract. A standard curve was prepared
using cumene hydroperoxide at concentrations ranging
from 0.5 to 2 mg/L. PV was expressed as milligrams of
cumene hydroperoxide per kilogram wet weight (mg CHP/
kg WW).
Determination of 2-thiobarbituric acid reactive
substances
(
TBARS) value.
TBARS value of uncooked and
cooked meat was measured using the method described
by [10]. Wet sample (0.5 g) was mixed with 2.5 mL of TBA
solution containing 0.375% thiobarbituric acid, 15%
trichloroacetic acid, and 0.25 N HCl. The mixture was
heated in boiling water for 10 min to develop a pink colour,
cooled with running tap water, sonicated for 30 min,
followed by centrifugation at 5,000×g at 25°C for 10 min.
The absorbance of the supernatant was measured at 532
nm. Standard curve was prepared using 1,1,3,3-
tetramethoxypropane at concentrations ranging from 0 to
10 ppm, and TBARS were expressed as milligram of
malondialdehyde equivalents per kilogram wet weight (mg
eq MDA/kg WW).
Statistical analysis
Analysis of variance was used to evaluate experimental
data, and significant differences among means were
determined by one-way analysis of variance (ANOVA) and
Duncan’s multiple range test (p = 0.05) (SPSS 10.0 for
Windows).
Results and discussion
Determination of trace metals
The concentrations of trace metals as means ±
standard deviation are shown in table 1.
In all cooked pork samples, the mean concentrations of
trace metals Fe, Cu Zn, Mn, Sn, Ni, Cr, Ti, Al and Pb were
increased compared to average levels for control (raw
meat) and in some cases they significantly (p<0.05)
depended on the pan type used for cooking.
The highest iron mean concentrations were registered
in the meat cooked in brass pans (27.72 mg/kg DW),
stainless steel pans (16.67 mg/kg DW), and ceramic-
coated aluminium pans (16.64 mg/kg DW). Compared to
Fe mean concentrations in raw meat (control), Fe average
levels in meat cooked in brass pan were 3.13 times higher,
and they were increased 1.88 times in meat cooked in
stainless steel and ceramic-coated aluminium pans. The
iron levels found in this study showed that meat thermal
treatment at 200°C in ceramic-coated aluminium, brass,
stainless steel and aluminium pans respectively
determined the leaching of iron into the meat, but this fact
was found as significant (p<0.05) only for brass pans.
About 70% of the iron in mammals is found in haemoglobin,
and about 5% to 10% is found in myoglobin. 25% of iron in
Table 1
MEAN CONCENTRATION OF TRACE METALS IN PORK (mg/kg, DRY WEIGHT) COOKED AT 200°C FOR 50 min IN PANS MADE OF ALUMINIUM,
CERAMIC-COATED ALUMINIUM, BRASS AND STAINLESS STEEL
http://www.revistadechimie.ro REV.CHIM.(Bucharest)68No. 7 2017
1478
the body is stored in hemosiderin, ferritin, and transferrin in
the liver, spleen, and bone marrow [11].
Also, there are some nonheme iron-containing enzymes
such as peroxidases, catalases and cytochrome-
c
. Iron
excess is associated to hepatic injury, fibrosis and
ultimately cirrhosis. Iron can initiate lipid peroxidation
process by two different iron-mechanisms. First is Fenton
reaction, iron forming with hydrogen peroxide the hydroxil
radical (HO•), the most reactive oxygen species, which
eventually initiates lipid peroxidation. In the second
mechanism, iron forms with oxygen iron-oxygen
complexes such as perferryl or ferryl ions with reactivities
approaching to that of HO•. Lipid peroxidation produces
damages in lipid membranes of cellular organelles
resulting in structural and functional alterations of cell
integrity [12].
Copper mean concentration in meat cooked in brass
pan was 13.58 mg/kg DW, 150.89 times higher than Cu
average level in raw meat. In meat cooked in ceramic-
coated aluminium pans, Cu mean concentration was 2.44
mg/kg DW (27.11 times higher compared to its average
level in raw meat samples), while Cu mean concentrations
in meat cooked in stainless steel and aluminium pans were
1.69 and 1.73 mg/kg DW respectively (approximately 19
times higher than the values found for raw meat). The
copper levels determined in this study showed that
cookware type significantly influenced (p<0.05) the leach
of copper into the meat, but this aspect was significant
(p<0.05) only in case of brass pans. Cu is an essential
trace element present in all tissues and it is needed for
cellular respiration, peptide amidation, neurotransmitter
biosynthesis, pigments formation and connective tissue
strength [13]. Copper is a functional component of several
essential enzymes, known as copper enzymes, and plays
an important role in central nervous system development
[13, 14]. Nevertheless, the other side of the coin is the
prooxidant activity of copper in lipid oxidation. Like iron
and other transition metals, Cu ions facilitate the transfer
of electrons leading to increased rates of free radicals
formation [15] and are effective in absorbing oxygen when
added to meat [16].
Mean concentrations of zinc in cooked meat were
significantly (p<0.05) dependent on the pan type used for
cooking. In all cooked meat samples, Zn mean
concentrations were increased compared to those
registered in raw meat samples, and the values were
significantly (p<0.05) higher only in case of meat samples
cooked in brass pan. Zn is an essential trace element in
the body and it is essential as a catalytic, structural and
regulatory ion. It is involved in homeostasis, in immune
responses, in oxidative stress, in apoptosis and in ageing
[17]. Zn is involved in the activity of about 100 enzymes,
e.g. RNA polymerase, carbonic anhydrase, Cu–Zn
superoxide dismutase, angiotensin I converting enzyme.
Also, it is present in Zn-fingers associated with DNA [18].
Zn toxicity has been highlighted in both acute and chronic
forms; intakes of 150–450 mg of Zn per day have been
associated with low Cu status, altered Fe function, reduced
immune function, and reduced levels of HDL [19].
All cooked meat samples showed increased mean
values of manganese compared to those found for the
same element in raw meat samples, but the Mn mean
concentrations were significantly (p<0.05) higher only in
meat samples cooked in brass and aluminium pans. Mn is
associated with bone development, and with amino acid,
lipid, and carbohydrate metabolism [18] Manganese is
component of a number of enzymes, as manganese
containing superoxide dismutase Mn-SOD [20], and
activates other enzymes (ex., glycosyl transferases) [21].
High doses of manganese are able to produce neurotoxicity,
that may develop in human Parkinsonian syndrome [22,
23], cardiac dysfunction by blocking calcium channels [24],
liver toxicity [25], fertility decreasing and increased of fetal
abnormalities [26-29].
All cooked meat samples registered significantly
(p<0.05) increased mean concentrations of tin compared
to its average levels in raw meat samples. Sn is believed to
be an essential trace element in some organisms,
potentially including humans, although its function has not
been exactly determined. It has been suggested that tin
may contribute to tertiary structure of proteins and may
participate in redox reactions in biological systems because
the Sn2+ Sn4+ + 2e- potential of 0.13 volt is within the
physiological range [30]. Inorganic tin salts are poorly
absorbed (5%) and rapidly excreted in the faeces.
Mutagenic studies on metallic tin and its compounds have
shown fewer malignant tumours in animals exposed to tin
than in controls [31].
Nickel mean concentrations in cooked meat
significantly (p<0.05) depended on the pan type used for
cooking. In all cooked meat samples, Ni mean
concentrations were increased compared to its average
levels found in raw meat samples, but the mean values
were significantly (p<0.05) higher for meat samples
cooked in ceramic-coated aluminium, brass and stainless
steel pans. Nickel is considered a nutritionally essential
trace metal for at least several animal species [32], but Ni
overdoses may cause toxic effects in the respiratory tract
and immune system. The exposure of the general
population to nickel mainly concerned oral intake, primarily
through water and food, as a contaminant in drinking water
or as both a constituent and contaminant of food [32, 33].
The pan type used for cooking significantly (p<0.05)
influenced chromium mean concentrations in cooked
meat. All cooked meat samples showed increased mean
values of Cr compared to those registered for the same
element in raw meat samples, but its average levels were
significantly (p<0.05) higher in meat samples cooked in
ceramic-coated aluminium, brass and stainless steel pans.
If chromium is an essential trace element is questionable.
Some studies suggested that chromium is an essential
trace element associated with carbohydrate metabolism,
and chromium deficiency causes an impaired glucose
tolerance [34]. Anyway, it was concluded that chromium
is not an essential trace element [35], because feeding
with a severely low-chromium diet (0.016 ìg/g) does not
impair glucose tolerance, and the amount of Cr absorbed
by humans is less than 1 ìg/day, which is much lower than
the level for an essential trace element. Also, chromium
intake seems to be dependent on chromium contamination
during food processing and cooking.
All cooked meat samples presented significantly
(p<0.05) increased mean concentrations of titanium
compared to its average levels in control samples. The
highest Ti average level was found in meat samples cooked
in brass pan (0.40 mg/kg DW), and its lowest average value
was found in meat samples cooked in aluminium pan (0.20
mg/kg DW).
Aluminium content varied from a mean value of 4.53
mg/kg DW in meat samples cooked in ceramic-coated
aluminium pan to 21.62 mg/kg DW in meat samples
cooked in brass pan. All cooked meat samples showed
increased Al mean concentrations compared to its average
levels determined in raw meat samples, but Al average
levels were significantly (p<0.05) higher in meat samples
cooked in brass, stainless steel and aluminium pans. In
meat cooked in aluminium pan, Al mean concentration
REV.CHIM.(Bucharest)68No. 7 2017 http://www.revistadechimie.ro 1479
was 10.15 mg/kg DW, 10 times higher compared to raw
meat (0.99 mg/kg DW). It was found that the leach of Al
into meat was the most intense in case of brass pan,
determining the increase of Al levels by 21.83 times. Other
studies showed that aluminium is implicated in several
serious conditions, such as dialysis dementia and
osteodystrophy, amyotrophic lateral sclerosis, and
Alzheimer’s disease [36]. Previous researches
demonstrated that aluminium foil used in cooking provides
an easy channel for the metal to enter into the human
body, the increase of cooking temperature causing more
leaching. The leaching is also highly dependent on the
p
H
value of the food solution, as well as salt and spices added
to the food [37].
Lead mean concentrations in all cooked meat samples
were increased compared to its average levels found in
raw meat samples, but the only Pb average level
significantly (p<0.05) increased was registered in case of
meat samples cooked in brass pan (0.94 mg/kg DW, 5.88
times higher than control). Also, Pb mean concentrations
for meat samples cooked in aluminium and ceramic-
coated aluminium pans were 3.3 times higher compared
control. Pb, as Cd, is a toxic metal with numerous negative
effects on health such as neurotoxicity, carcinogenicity,
reproductive toxicity and renal dysfunction [38, 39].
Cadmium mean concentrations in cooked meat (when
detected) were higher than in raw meat samples (not
detected), but they were not significantly (p>0.05)
dependent on the pan type used for cooking. In case of
meat samples cooked in ceramic-coated aluminium and
stainless steel pans, Cd was detected in mean
concentrations of 0.07 mg/kg DW and 0.06 mg/kg DW
respectively. Cd is one of the most toxic elements to which
humans can be exposed at work or in the environment
[40]. Once absorbed, Cd is efficiently retained in the human
body, in which it accumulates throughout life [41]. Cd is
toxic for kidney, is responsible for bone damage and itai-
itai disease, alteration of reproductive biology and cancer
[41, 42].
The only sample in which uranium was detected and its
mean value was significantly (p<0.05) increased was the
meat cooked in ceramic-coated aluminium pan (0.026
mg/kg DW). In raw meat samples and in the other cooked
meat samples, U was below the method detection limits.
The leach of U into food from glass and ceramics was
reported by [43]. From a uranium-glazed plate, vinegar
could leach up to 31,800µg/L of uranium, and nitric acid
leached 304,000 µg/L of uranium [43]. Uranium
compounds were used in the colouring of ceramics and
glass until the middle of the 20th century. Twenty percent of
15 uranium-glazed dinnerware samples tested contained
easily removable surface compounds of natural uranium
[44].
Evaluation of lipid oxidation process
Peroxide value
Lipid hydroperoxides are primary oxidation products that
may break down to a variety of volatile and non-volatile
secondary products. PV is an indicator of the initial stages
of lipid oxidation. PV for the analysed samples as means
± standard deviation is shown in table 2.
The mean PV for raw meat was 1.271 mg CHP/kg WW,
which indicates the presence of lipid peroxidation process
during meat handling and refrigeration. The largest amount
of lipid peroxides was found in meat cooked in ceramic-
coated aluminium pan (1.974 mg CHP/kg WW). In the
case meat heat-treated in other cookware, PV was lower
than in uncooked meat, the lowest value being found in
meat cooked brass pan (0.378 mg CHP/kg WW).
Compared to uncooked meat (control), the concentration
of lipid peroxides was significantly (p<0.05) higher in meat
heat-treated in ceramic-coated aluminium pan and
significantly (p<0.05) lower in meat heat-treated in the
other cookware. For heat-treated meat, between PV and
the concentration of Al a significant negative correlation
was found (r = -0.555). Statistical correlations were not
significant (p>0.05) between the concentration of the
other metals and PV.
The lower PV found in meat heat-treated in the brass
pan could be due to the higher thermal conductivity of
brass, which causes a faster achievement of a temperature
in meat which favours thermal decomposition of lipid
peroxides. According to The Engineering Tool Box, thermal
conductivity for brass is 64, for aluminium bronze is 44 and
for stainless steel is 7 – 26 Btu/(hr0F ft). The difference
between PV for ceramic-coated aluminium pan and
aluminium pan can be explained also by the difference in
thermal conductivity, the ceramic-coated aluminium pan
having a thickness of about 3 times higher, and the ceramic
layer decreases thermal conductivity as well.
TBARS value
Thiobarbituric acid reactive substances (TBARS) are
secondary oxidation products formed via the
decomposition of primary lipid peroxidation products.
TBARS value is an indicator of the second stages of lipid
oxidation. Changes in TBARS value of meat cooked in
aluminium, ceramic-coated aluminium, brass and
Table 2
PEROXIDE VALUE (PV) AND THIOBARBITURIC ACID REACTIVE SUBSTANCES VALUE (TBARS) IN MEAT COOKED AT 200°C FOR 50 MIN IN PANS
MADE OF ALUMINIUM, CERAMIC-COATED ALUMINIUM, BRASS AND STAINLESS STEEL
http://www.revistadechimie.ro REV.CHIM.(Bucharest)68No. 7 2017
1480
stainless steel pans are shown in Table 2. In all samples of
cooked meat, TBARS values were higher than the one of
uncooked meat. The lowest TBARS value was found in
meat cooked in ceramic-coated aluminium pan (0.406
mg eq MDA/kg WW), while the highest TBARS value was
found in meat cooked in brass pan (0.764 mg eq MDA/kg
WW). Compared with heat-untreated meat, TBARS values
were significantly (p<0.05) higher in cooked meat,
regardless of the type of cookware used. TBARS value
determined for meat cooked in brass pan was also
significantly (p<0.05) higher than TBARS values
determined for aluminium, ceramic-coated aluminium and
stainless steel pans. Between TBARS values of cooked
meat and Fe, Cu, Zn, Cr, Ti, Al and Pb concentrations were
found significant correlations (p<0.05). TBARS values were
significantly (p<0.05) and strongly positively correlated
with concentrations of Fe (r = 0.809), Cu (r = 0.814), Zn (r
= 0.874), Cr (r = 0.842), Ti (r = 0.920), Al (r = 0.867) and
Pb (r =0.777).
The results demonstrate that metal ions leaked from
cookware favour lipid oxidation process. The meat cooked
in brass pan showed the highest concentrations of Fe, Cu,
Zn, Ti, Al and Pb, but also the highest concentration of
secondary products of lipid peroxidation. Some researchers
argued that lipid oxidation is enhanced by metals such as
iron, cobalt and cooper which facilitate the transfer of
electrons leading to increased rates of free radical
formation [15]. It was suggested that lipid peroxidation in
minced turkey muscle is primarily affected by
free
metal
ions [45]. It was stated that free ionic iron plays an important
role in the catalysis of lipid peroxidation and the status of
ionic iron is more important than the total amount of iron
[46].
Conclusions
The concentration of trace metals leaked from
cookware into meat significantly depends on the type of
cookware used. The highest leakage of metals was found
in meat cooked in brass pan. Brass, stainless steel and
aluminium pans caused significant (p<0.05) leakage of
Al into the meat. The ceramic-coated aluminium pan
caused significant (p<0.05) leakage of U into the meat.
Metal ions leaked from cookware favour lipid
peroxidation process in meat. Between TBARS mean
values found in heat-treated meat and the concentrations
of Fe, Cu, Zn, Cr, Ti, Al and Pb, significant correlations were
found.
Acknowledgements. This work was carried out through Partnerships
in priority areas Program – PN II, implemented with the support of
MEN – UEFISCDI, project nr. 149/2014
.
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