Article

Toxicology and Industrial Health

2018, Vol. 34(7) 459–467
The biochemical effects of occupational © The Author(s) 2018
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exposure to lead and cadmium on markers DOI: 10.1177/0748233718769526
journals.sagepub.com/home/tih
of oxidative stress and antioxidant
enzymes activity in the blood of glazers
in the tile industry

Maryam Hormozi1, Ramazan Mirzaei1,

Alireza Nakhaee2, Shahrokh Izadi3
and Javid Dehghan Haghighi4

Abstract
The aim of the present study was to evaluate the effects of occupational exposure to lead (Pb) and cadmium
(Cd) on markers of oxidative stress in glazers in tile industries. Total antioxidant capacity (TAC), mal-
ondialdehyde (MDA), and the activity of antioxidant enzymes superoxide dismutase (SOD), catalase (CAT),
and glutathione peroxidase (GPx) were determined in the blood of 80 subjects, including 40 glazers and 40
nonexposed subjects. Mean levels of blood Cd (8.90 + 2.80 mg/L) and blood Pb (62.90 + 38.10 mg/L) of glazers
showed a significant increase compared with the control group. In the serum of glazers, the level of MDA was
significantly higher and the level of TAC was significantly lower than the control group. We have noted a
disturbance in the levels of antioxidants by a significant increase in the CAT activity and a significant decrease in
the activities of SOD and GPx in the serum of glazers compared with the controls. Correlation analysis
demonstrated that the serum MDA level and CAT activity were positively associated with the blood levels of
Pb and Cd. Also, GPx and SOD were negatively correlated with blood Cd levels. The study clearly indicated
that co-exposure to Cd and Pb can induce oxidative stress in glazers, resulting in increased lipid peroxidation
and altered antioxidant enzymes.

Keywords
Occupational exposure, heavy metals, oxidative stress, glazers, antioxidants

Received 4 October 2017; Revised 27 January 2018; Accepted 23 February 2018

Introduction
In the ceramic tile industry, heavy metals such as lead
(Pb) and cadmium (Cd) are employed as coloring
powders to improve the strength of the products and
polish them, as well as in the manufacture of various
types of colored glaze (Cepriá et al., 2005). Glazers
are heavily exposed to these toxic metals in glazing
departments (Shouroki et al., 2015a, 2015b). There is
the possibility of occupational exposure during activ-
ities such as weighing, unloading, mixing, and storing
bags containing powder of metal components when a
lot of respirable dust is generated (Shouroki et al.,
2015a). The International Agency for Research on
1
Department of Occupational Health, School of Health, Health
Promotion Research Center, Zahedan University of Medical
Sciences, Zahedan, Iran
2
Department of Clinical Biochemistry, School of Medicine,
Zahedan University of Medical Sciences, Zahedan, Iran
3
Department of Epidemiology and Biostatistics, School of Health,
Health Promotion Research Center, Zahedan University of
Medical Sciences, Zahedan, Iran
4
Department of Community Medicine, School of Medicine,
Zahedan University of Medical Sciences, Zahedan, Iran
Corresponding author:
Ramazan Mirzaei, Department of Occupational Health, School of
Health, Health Promotion Research Center, Zahedan University
of Medical Sciences, Zahedan 9816743175, Iran.
Email: rammir277@gmail.com
460
Cancer (IARC) has classified Cd (Godt et al., 2006)
and Pb (Landrigan et al., 2000) as, respectively, car-
cinogenic and a possible carcinogen in humans. Also,
the technical guide report has recently warned of the
potential health risk of heavy metals such as Pb and
Cd existing in pigments (Awodele et al., 2013).
Numerous studies have shown that oxidative stress,
as a major mechanism, plays an important role in both
toxicity of Pb and Cd and prooxidant/antioxidant
imbalance (Hunaiti and Soud, 2000; Sugawara et al.,
1991; Wang and Fowler, 2008). By increasing reactive
oxygen species (ROS) and impairing the cellular anti-
oxidant defense system, Pb and Cd can cause oxidative
damage to the body (Garçon et al., 2004; Patrick,
2006). These metals are capable of diminishing the
level of major cellular antioxidant compounds, espe-
cially enzymes, and causing lipid peroxidation (LPO)
and DNA damage (Valko et al., 2005).
Malondialdehyde (MDA), a marker of LPO, is the
result of the interaction between ROS and cell mem-
brane (Klaunig et al., 2011). Besides, it is one of the
sensitive and reliable markers that has many applica-
tions, under oxidative stress conditions, in determin-
ing the amount of damage to cell membranes in the
human body (Guichardant et al., 2004).
On the other hand, antioxidant enzymes, including
catalase (CAT), superoxide dismutase (SOD), and glu-
tathione peroxidase (GPx), are the most essential com-
ponents of the endogenous antioxidant defense system.
These enzymes are the potential targets of Pb and Cd
and are regarded as the first line of defense against the
toxic effects of heavy metals. In fact, by decreasing the
production of free radicals and peroxides decomposi-
tion, they have an important role in protecting cell mem-
branes against oxidative damage (Flora et al., 2013).
The total antioxidant capacity (TAC) proposes a
complete panorama of antioxidant system function
in the organism under oxidative stress (Kusano and
Ferrari, 2008). In addition, this test has become an
important tool in evaluating occupational and envi-
ronmental exposure to toxic chemicals. In this regard,
it has been noted that exposure to trace elements such
as Pb, Cd, aluminum, arsenic, and mercury could
reduce the level of TAC in the body (Ferrari, 2012).
Previous studies have provided evidence suggest-
ing that occupational exposure to Pb and/or Cd is
correlated with increasing levels of MDA (Ściskalska
et al., 2014) as well as changes made in the level of
activity of antioxidant enzymes such as CAT, SOD,
and GPx (Babu et al., 2006; Bizoń et al., 2013;
Kasperczyk et al., 2004).
Toxicology and Industrial Health 34(7)
To the best of our knowledge, no study has so far
been conducted on glazers in order to consider the
effects of occupational co-exposure to Pb and Cd and
their relationship with oxidative stress markers as
well as the status of antioxidants. Hence, the purpose
of this study was to determine the blood concentra-
tions of Pb and Cd of glazers and explore the effects
of occupational exposure to these heavy metals on
TAC, MDA, and the activities of SOD, CAT, and GPx
in blood serum.
Materials and methods
Subjects
This study was performed using blood samples from 80
subjects; 40 male glazers (aged 31.83 + 4.97 years),
who were exposed to both Pb- and Cd-containing pig-
ments, compared with 40 office employees; 31 males
and 9 females (aged 32.30 + 8.00 years) as a control
group who were unexposed occupationally to these two
heavy metals. The exposed group was composed of all
the tile glazers who were working at least 1 year or
more in the glazing section of tile factories in Birjand,
Iran. The study protocol was approved by the Ethics
Committee on Medical Research of Zahedan Univer-
sity of Medical Sciences in Zahedan, Iran (no.
IR.ZAUMS.REC.2016.85). The studied groups were
of similar age, body mass index (BMI), and smoking
status. About 5% of the glazers (two subjects) and 7%
of the controls (three subjects) were smokers. None of
the studied subjects consumed alcohol. The data such
as age, smoking habit, alcohol consumption, BMI,
blood pressure, and years of work in the tile industry
were collected by a questionnaire.
Blood sampling
To measure the serum levels of TAC, MDA, and
antioxidant enzyme activities (SOD, GPx, and
CAT), 10 mL samples of venous blood from both
glazers and control subjects were collected at the
beginning of the work shift. Blood sampling was
carried out by trained personnel according to a stan-
dard procedure using gel-containing tubes without
anticoagulant and centrifuged at 3500  g/10 min
to separate the serum. Then, the serum samples were
divided into aliquots and stored at 70 C until ana-
lyzed. To assess the blood levels of Pb and Cd, 1 mL
of whole blood from all the subjects was collected
in heparinized blood collection tubes and stored at
4 C until analyzed.
Hormozi et al.
Informed consent
All participants gave written informed consent to par- activities
ticipate in the study.
Metals concentration
The Pb levels in whole blood (Pb-B) were determined
using a Perkin Elmer AAnalyst 700 (Perkin Elmer,
Waltham, MA, USA) graphite furnace atomic absorp-
tion spectrometer and graphite Massmann cuvettes,
with the absorbance measurement at wavelength 
¼ 283.3 nm. The Cd levels in whole blood (Cd-B)
were determined by the same method at wavelength 
¼ 228.8 nm. Preparation of the samples for the quan-
tification of Cd and Pb in blood was done according to
the method proposed by Andresen (1986). In this
method, the samples were diluted to 1:5 with a sur-
factant solution containing 0.1% Triton X-100 (v/v) in
deionized water. The concentrations of Cd and Pb in
blood were expressed as micrograms per liter.
Determination of MDA levels
Concentration of MDA in serum was determined
spectrophotometrically by measuring the thiobarbitu-
ric acid reactive substances (TBARS), according to
the method of Uchiyama and Mihara (1978). In this
method, an aliquot (3 mL) of 1% phosphoric acid and
1 mL of 0.6% thiobarbituric acid solution w/v was
added to 0.5 mL of serum. The mixture was heated
for 45 min in a boiling water bath. After cooling, the
mixture was centrifuged at 3000  g/10 min, and the
absorbance was measured at  ¼ 535 nm against a
blank sample. The concentration of TBARS was cal-
culated using the MDA standard curve and was
expressed as micromoles per liter in serum.
Determination of TAC levels
The assessment of TAC level in serum was carried out
by the method of Benzie and Strain (1999). Totally,
1.5 mL of working ferric reducing–antioxidant power
reagent (25 mL 0.3 M sodium acetate buffer, pH 3.6;
2.5 mL 0.01 M tripyridyl-triazine (TPTZ) in 0.04 M
hydrochloric acid; 2.5 mL 0.02 M FeCl36H2O; pre-
heated to 37 C) was mixed with 50 mL of serum; the
absorbance was measured at  ¼ 593 nm after a 5-min
incubation at 37 C. Ferrous sulfate solutions were
used for calibration. Concentration of TAC was
expressed as micromoles per milliliter in serum.
461
Determination of SOD, CAT, and GPx
The activity of antioxidant enzymes of SOD, CAT,
and GPx in the serum of subjects was measured using
commercially available assay kits (ZellBio GmbH,
Germany, CAT no. ZB-96A) according to the manu-
facturer’s instructions. In this assay, the SOD activity
unit was considered as the amount of the enzyme that
will catalyze the decomposition of 1 mmole of O2 to
H2O2 and O2 in 1 min. The CAT activity unit was
considered as the amount of the enzyme that will
catalyze the decomposition of 1 mmole of H2O2 to
water and O2 in 1 min and the GPx activity unit was
considered as the amount of the enzyme that will
catalyze the decomposition of 1 mmole of glutathione
reduced form (GSH) to glutathione disulfide (GSSG)
in 1 min. The absorbance of SOD, CAT, and GPx was
read with an ELISA reader at wavelengths of 420,
405, and 412 nm, respectively. Activity of these
enzymes was expressed as units per milliliter in
serum.
Biochemical parameters
Uric acid values in serum was determined by an enzy-
matic colorimetric method (Roche/cobas c6000 ana-
lyzer; Roche, Basel, Switzerland), and the
hemoglobin level in erythrocytes was measured by
flow cytometry and analyzed by high-pressure liquid
chromatography. The hematocrit was calculated from
the complete blood cell count using the Coulter impe-
dance principle by automatic cell count analyzers.
These blood parameters were performed by a trained
operator in a hematology laboratory.
Statistical analysis
Statistical analyses were carried out using Stata ver-
sion 11. The data were expressed as mean + standard
deviation. The normality of the variables was tested
by the Shapiro–Wilk test. Independent samples t-tests
were used to compare the mean values of continuous
variables between two groups. Linear multiple regres-
sion models were fitted to compare the means of out-
comes between study groups controlling for gender
effect as confounder. Furthermore, Spearman’s corre-
lation coefficient test was employed to assess the rela-
tionship between continuous variables such as blood
Pb, blood Cd, TAC, MDA, SOD, CAT, and GPx with
nonparametric distributions. The differences were
considered significant at p < 0.05.
462 Toxicology and Industrial Health 34(7)

Table 1. Summary of characteristics in the unexposed Table 2. The comparison of the concentrations of Pb and
control group and glazers.a Cd and selected oxidative stress parameters of glazers and
control subjects.a
Control group Glazers p
Variables (n ¼ 40) (n ¼ 40) Valueb Controls Glazers p
Variables (n ¼ 40) (n ¼ 40) Valueb
Age (years) 32.30 + 8.00 31.83 + 4.97 0.751
BMI (kg/m2) 24.57 + 3.94 23.93 + 3.25 0.425 Pb in blood (mg/ 23.40 + 9.28 62.90 + 38.10 <0.001
Work years in the 8.60 + 6.39 6.70 + 2.47 0.090 L)
tile industry Cd in blood (mg/ 3.96 + 1.95 8.90 + 2.80 <0.001
(years) L)
Smoking; number 3 (7.5) 2 (5.0) 0.643 MDA (mmol/L) 4.82 + 0.67 6.73 + 1.76 <0.001
(%) TAC (mmol/mL) 1.12 + 0.23 1.03 + 0.21 0.003
Male; number (%) 31 (77.5) 40 (100.0) 0.002 SOD (U/mL) 38.24 + 8.41 31.44 + 5.67 <0.001
Uric acid in serum 5.62 + 1.11 5.68 + 1.05 0.805 GPx (U/mL) 171.06 + 35.24 133.98 + 31.81 <0.001
(mg/dL) CAT (U/mL) 12.60 + 5.54 17.44 + 6.71 0.001
Hemoglobin (g/dL) 15.17 + 1.23 15.12 + 1.07 0.847
Hematocrit (%) 45.49 + 3.43 44.61 + 3.28 0.246 Pb: lead; Cd: cadmium; MDA: malondialdehyde; TAC: total anti-
oxidant capacity; SOD: superoxide dismutase; GPx: glutathione
Systolic blood 112.50 + 9.81 110.50 + 9.66 0.361
peroxidase; CAT: catalase.
pressure a
Data are represented as mean + standard deviation.
(mmHg) b
Adjusted for gender effect using multiple linear regression
Diastolic blood 71.10 + 9.42 71.84 + 7.63 0.651 models.
pressure
(mmHg)
BMI: body mass index. were positively and GPx activity (r ¼ 0.408; p <
a
Data are represented as mean + standard deviation. 0.001) negatively associated with blood Pb levels.
b
Independent samples t-test. Moreover, the correlation coefficients between blood
Cd levels and MDA level (r ¼ 0.519; p < 0.001) as
Results well as enzymes activities of SOD (r ¼ 0.264;
p ¼ 0.018), CAT (r ¼ 0.318; p ¼ 0.004), and GPx
Demographic characteristics and some of the hemato- (r ¼ 0.235; p < 0.036) were estimated. We also
logical parameters for the glazers and control subjects indicated that confounding factors such as age, BMI,
are shown in Table 1. Mean levels of blood pressure, and smoking did not show any statistically significant
uric acid, hematocrit, and hemoglobin showed no sta- relationship with the levels of LPO and activity of
tistically significant differences in glazers as compared antioxidant enzymes.
with the unexposed group (p > 0.05). However, there
was a significant difference between the two groups in
terms of gender (p ¼ 0.002). The results of the com-
parison of oxidative stress markers in the exposed Discussion
group (glazers) and unexposed subjects are shown in The present study examined the effects of occupa-
Table 2 and Figure 1. As may be seen in Table 2, the tional exposure of glazers on the activity of antioxi-
results of multiple regression models adjusting for gen- dant enzymes and the markers of oxidative stress in
der indicated that the mean blood Pb and blood Cd the ceramic tiles industry, an industrial sector which
levels in glazers were significantly higher than unex- has always been considered hazardous because of the
posed control subjects (p < 0.001). A statistically nota- use of toxic metals–rich glazes, especially Pb and Cd.
ble increase in the MDA levels and CAT activity as In this research, an increase of almost 2.5-fold in
well as a significant reduction in the activities of blood Cd (Cd-B) and blood Pb (Pb-B) levels occurred
SOD and GPx in the serum of glazers was demon- in glazers as compared with the unexposed group
strated (p < 0.001). The findings also showed a sig- (p < 0.0001). However, in the glazers group, the blood
nificant decrease in the TAC levels of glazers as Cd levels were 1.78-fold higher and blood Pb levels
compared with control subjects (p ¼ 0.003). were below the values recommended by the American
The results of Spearman’s correlation analysis for Conference of Governmental Industrial Hygienists
all participants indicated that MDA levels (r ¼ 0.508; (ACGIH). These results are similar to those reported
p < 0.001) and CAT activity (r ¼ 0.267; p ¼ 0.017) higher concentrations of urinary Pb (Shouroki et al.,
Hormozi et al. 463

Figure 1. (a) Blood levels of lead and cadmium (micrograms per liter), (b) serum levels of malondialdehyde (micromoles
per liter) and total antioxidant capacity (micromoles per milliliter), and (c) oxidants serum levels of glutathione perox-
idase, catalase, and superoxide dismutase (units per milliliter).

2015a) and urinary Cd (Shouroki et al., 2015b) in
glazers in tile industries.
In the present study, the authors noted higher con-
centrations of MDA in the serum of glazers compared
with controls (p < 0.0001). Wasowicz et al. (2001)
reported that occupational co-exposure to Pb and Cd
in the workplace caused a significant increase in the
plasma level of MDA in workers exposed to both of
these metals, as compared to those exposed to Cd alone.
The results of the present research displayed a signifi-
cantly positive correlation between MDA concentration
and Cd-B level (r ¼ 0.519; p < 0.001) and Pb-B level
(r ¼ 0.508; p < 0.001). Our results are consistent with
previous studies that have clearly demonstrated occu-
pational exposure to Pb and Cd is associated with an
increased MDA concentration in plasma (Bizoń et al.,
2013; Garçon et al., 2004; Ściskalska et al., 2014).
In comparison to controls, the current study also
showed that exposure of glazers to Pb (62.9 + 38.1
mg/L) and Cd (8.90 + 2.80 mg/L) concentrations in
blood decreased SOD and GPx activities (p < 0.001)
and increased the CAT activity in serum (p ¼ 0.001).
Studies investigating the impact of co-exposure to Pb
and Cd on the activity of antioxidant enzymes at dif-
ferent levels of exposure have reported mixed results.
The authors have indicated that, compared with the
control group, exposure of nonsmoking smelters to
high Pb-B concentrations (27.33 + 12.19 mg/dL) and
low Cd-B concentrations (0.54 + 0.44 mg/L)
increased the activity of Cu/Zn SOD and GPx in
erythrocytes. They reported a significant positive cor-
relation between the Pb-B level and the activities of
Cu/Zn SOD and GPx in erythrocyte of smelters, while
no significant correlation was noted between the
Cd-B levels and the activity of these enzymes (Bizon
et al., 2013).
Other authors have suggested that moderate expo-
sure levels of Pb-B ¼ 395.71 mg/L and Cd-B ¼ 5.83
mg/L are significantly associated with a decrease of
the GPx activity (r ¼ 0.35); however, no significant
relationship was found between the levels of Cd-B
and the activities of GPx and SOD (Garçon et al.,
2004). Different responses of these enzymes in the
blood of workers occupationally exposed to heavy
metals, such as Pb and Cd, might be related to the
degree of oxidative stress (Imamoglu et al., 2008). It
has been demonstrated that increased levels of GPx
protect cells against low levels of oxidative stress,
whereas CAT can be increased in situations of
extreme stress. This could reflect the important role
464
of these enzymes in the accurate regulation of ROS
levels (Cuypers et al., 2010).
Cytotoxicity of Cd is mediated by both apoptosis
and necrosis. These two mechanisms are caused by
oxidative stress resulting from increased accumula-
tion of ROS (Fleury et al., 2002; Hossain et al.,
2009) and increased LPO after exposure to Cd
(Kotelnikova et al., 2008; Slyuzova et al., 2008;
Tezcan et al., 2012).
Both occupational (Babu et al., 2006; Bizoń and
Milnerowicz, 2014; Moitra et al., 2014; Nzengue
et al., 2011) and experimental (Ikediobi et al., 2004;
Tezcan et al., 2012; Uchida et al., 2004) studies have
provided extensive evidence corroborating that oxida-
tive damage caused by Cd is associated with
decreased SOD and GPx enzymes activity. SOD
enzyme is responsible for catalyzing dismutation of
the superoxide anion (O2) to H2O2. This is the first
step of the antioxidant defense system against oxida-
tive stress. Due to the production of ROS interacting
with the cellular defense system, Cd can have a dama-
ging effect on cellular enzymes and thus considerably
depletes the antioxidants level, particularly SOD
(Ogunrinola et al., 2016).
Studies have shown that Pb can cause both an
increase and a decrease in the blood level of anti-
oxidant enzymes of CAT and GPx (Chiba et al.,
1996; Han et al., 2005; Sugawara et al., 1991).
Incremental changes in these enzymes have been
seen at lower levels of exposure, while reduction
can occur at higher levels of exposure and longer
periods of time. In this study, the authors showed
that the range of Pb-B concentrations in the sub-
jects (9.21–210 mg/L) was significantly correlated
with an increase in the serum levels of MDA and
CAT activity and a decrease in GPx activity. The
results of experimental and clinical studies have
indicated that, depending on the concentration, Pb
can either stimulate or has no effect on the activity
of GPx (Kasperczyk et al., 2004).
In the present study, a disturbance occurred in the
level of antioxidants that reduced the activities of
SOD and GPx and increased the activity of CAT in
glazers. CAT is an enzyme that directly contributes to
antioxidant defense in neutralizing the harmful effects
of free radicals (Nakhaee et al., 2010). Increased CAT
activity in glazers may be due to direct enzyme acti-
vation by Cd and Pb as a consequence of overproduc-
tion of ROS and the compensatory mechanism
developed to balance the excess of LPO. These results
were confirmed by both occupational studies (Gurer
Toxicology and Industrial Health 34(7)
and Ercal, 2000; Rendón-Ramı́rez et al., 2014) and
experiments (Gong et al., 2008; Tandon et al., 2003)
where an increase in blood CAT activity was
observed after exposure to metals such as Pb or Cd.
The present study also noted lower TAC levels
in glazers compared to control subjects. The rela-
tionship between occupational exposure to heavy
metals and TAC has not yet been explored. Only
a few studies have reported that an increase in
blood Pb level was associated with decreased TAC
levels in plasma (Alghasham et al., 2011). In con-
trast, the plasma TAC level was increased in work-
ers who were occupationally exposed to chemicals
such as Pb and Cd (Arinola and Akiibinu, 2006;
Han et al., 2005; Malekirad et al., 2010). Given
that TAC can be severely affected by uric acid in
the sample (Ferrari, 2012), our results showed no
significant difference in blood uric acid levels
between glazers and the controls. Cd exerts dual
effects on antioxidant capacity; on the one hand,
it can induce oxidative stress via inhibiting antiox-
idants, but on the other hand, it activates many
antioxidative components as a result of redox
imbalance as well as a consecutively induced sig-
nal transduction cascade (Cuypers et al., 2010).
A number of studies have reported that the levels
of LPO and the activities of SOD and GPx are asso-
ciated with age (Bizon et al., 2013; Chia et al., 2008)
and BMI (Ohmori et al., 2005). In the current study,
the age of the subjects ranged from 25 to 44 years
and in line with the study of Babu et al. (2006), we
did not observe any association between age as well
as BMI with the serum levels of MDA, TAC, SOD,
GPx, and CAT in correlation analysis. Also, this
research did not discover any similar relationship
with respect to work years in the tile industry. This
could be because of the small number of study sub-
jects and the low average of work years (6.70 +
2.47) in the tile industry.
The present study indicated that co-exposure to
Cd and Pb significantly influences the level of
LPO, a marker of oxidative stress, and the activity
of antioxidant enzymes. The authors concluded that
oxidative stress appears to occur in glazers even at
very low levels of exposure to Pb (62.90 mg/L) that
are considered safe by the current standards recom-
mended by the ACGIH. This may be due to an
interaction between Pb and Cd as a possible under-
lying mechanism of stress oxidative. Therefore,
monitoring Cd and Pb blood levels of glazers is
Hormozi et al.
helpful in identifying and following up affected
glazers in the tile industry.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest
with respect to the research, authorship, and/or publication
of this article.
Funding
The author(s) disclosed receipt of the following financial
support for the research, authorship, and/or publication of
this article: This study was supported by a dissertation grant
(Ph.D thesis, project no.: 7615) to first author from Zahe-
dan University of Medical Sciences, Zahedan, Iran.
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