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1 s2.0 S0147651311004155 Main
1 s2.0 S0147651311004155 Main
Nicolaus Copernicus University, Collegium Medicum in Bydgoszcz, Department of Ecology and Environmental Protection, Sk!odowska-Curie St. 9, PL 85-094 Bydgoszcz, Poland
ra, Faculty of Biological Sciences, Institute of Biology and Environmental Protection, Department of Biotechnology, Prof. Szafran St. 1, PL 65-516
University of Zielona Go
ra, Poland
Zielona Go
c
Institute of Soil and Plant CultivationGovernment Scientic Institute, Department of Soil Structure, Czartoryskich St. 8, PL 24-100 Pu!awy, Poland
d
Nicolaus Copernicus University, Collegium Medicum in Bydgoszcz, Department of Laboratory Diagnostics, Sk!odowska-Curie St. 9, PL 85-094 Bydgoszcz, Poland
b
a r t i c l e i n f o
abstract
Article history:
Received 30 May 2011
Received in revised form
2 November 2011
Accepted 16 November 2011
Available online 12 December 2011
The aim of this study was to prove whether anthropogenic pollution affects antioxidant defense
mechanisms such as superoxide dismutase (SOD) and catalase (CAT) activity, ferritin (FRT) concentration and total antioxidant status (TAS) in human serum. The study area involves polluted and salted
environment (Kujawy region; northern-middle Poland) and Tuchola Forestry (unpolluted control area).
We investigated 79 blood samples of volunteers from polluted area and 82 from the control in 2008 and
2009. Lead, cadmium and iron concentrations were measured in whole blood by the ICPMS method.
SOD and CAT activities were measured in serum using SOD and CAT Assay Kits by the standardized
colorimetric method. Serum TAS was measured spectrophotometrically by the modied Benzie and
Strain (1996) method and FRT concentrationby the immunonefelometric method. Pb and Cd levels
and SOD activity were higher in volunteers from polluted area as compared with those from the control
(0.0236 mg l 1 vs. 0.014 mg l 1; 0.0008 mg l 1 vs. 0.0005 mg l 1; 0.137 U ml 1 vs. 0.055 U ml 1,
respectively). Fe level, CAT activity and TAS were lower in serum of volunteers from polluted area
(0.442 g l 1 vs. 0.476 g l 1; 3.336 nmol min 1 ml 1 vs. 6.017 nmol min 1 ml 1; 0.731 Trolox-equivalents vs. 0.936 Trolox-equivalents, respectively), whilst differences in FRT concentration were not
signicant (66.109 mg l 1 vs. 37.667 mg l 1, p 0.3972). Positive correlations between Pb (r 0.206),
Cd (r 0.602) and SOD in the inhabitants of polluted area, and between Cd and SOD in the control
(r 0.639) were shown. In volunteers from both studied environments TASFRT (polluted: r 0.625 vs.
control: r 0.837) and FeFRT (polluted area: r 0.831 vs. control: r 0.407) correlations, and PbFRT
(r 0.360) and PbTAS (r 0.283) in the control were stated.
The higher lead and cadmium concentrations in blood cause an increase of SOD activity. It suggests
that this is one of the defense mechanisms of an organism against oxidative stress caused by
environmental factors, whilst non-enzymatic mechanisms marked by TAS are the main antioxidant
defense system in relation with Pb concentration in humans from unpolluted area. Simultaneously, the
higher CAT activity and TAS can indicate that these mechanisms play a key role in the antioxidant
protection in non-stressed environments.
& 2011 Elsevier Inc. All rights reserved.
Keywords:
Anthropogenic pollution
Human serum
Environmental stress
Superoxide dismutase
Catalase
Ferritin
Total antioxidant status
n
Corresponding author at: Nicolaus Copernicus University, Collegium Medicum in
Bydgoszcz, Department of Ecology and Environmental Protection, Sk"odowska-Curie
St. 9, PL 85-094 Bydgoszcz, Poland. Fax: 48 52 585 38 07, 48 68 3287875.
E-mail addresses: monicjus@wp.pl (M. Wieloch), piotr.kaminski@cm.umk.pl,
p.kaminski@wnb.uz.zgora.pl (P. Kaminski),
anna.ossowska@cm.umk.pl (A. Ossowska),
beata.koim@cm.umk.pl (B. Koim-Puchowska), ts@iung.pulawy.pl (T. Stuczynski),
magdalenakuligowska@wp.pl (M. Kuligowska-Prusinska),
grazyna.dymek@op.pl (G. Dymek), anetha7@poczta.onet.pl (A. Mankowska),
odes@cm.umk.pl, grazynaodes@interia.pl (G. Odrowaz-Sypniewska).
1
Fax: 48 68 328 78 75.
2
Fax: 48 81 886 45 47.
3
Fax: 48 52 585 36 03.
0147-6513/$ - see front matter & 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.ecoenv.2011.11.017
1. Introduction
Reactive oxygen species (ROS) takes part in pathogenesis of
many diseases correlated with environmental factors. The relationships between ROS in humans and the morbidity on many diseases
(cancers, rheumatoid arthritis, arteriosclerosis, diabetes, diseases of
central nervous and alimentary system, hematids, etc.) have been
proved (Nohl and Stolze, 1998; Olinski and Jurgowiak, 1999; Schulz
et al., 1999; Siems et al., 2000; Beisswenger et al., 2001; Buonocore
et al., 2001; Darlington and Stone, 2001; Kawanishi et al., 2001;
Sayre et al., 2001).
196
197
Table 1
Age and gender structure (Ffemales, Mmales) of volunteers from Mogilno
neighborhood (polluted area) and Tuchola Forestry (unpolluted control area).
There was no signicant difference in age structure in examined environments
(chi-square Pearson test: p 0.088109).
Environment
Polluted area 20
Control area 31
37
26
22
25
63
52
16
30
79
82
198
2. Study area
Studies were carried out in Mogilno (521400 11.2000 N;
521370 4.6400 S; 181110 50.2100 E; 171560 35.1400 W, central Poland) neighborhood (polluted and salted region) and in Tuchola Forestry
(531420 40.6800 N; 531320 51.0900 S; 171590 3.0600 E; 171470 45.8100 W, N
Poland), which serves as a control (unpolluted areas). Mogilno
district is situated on the south-west of KuyavianPomeranian
province and sits next to Inowroc"aw Region of Ecological Danger
(Fig. 1). Since heavy metals from industrial plants get through to the
atmosphere, the pollution involves not only areas directly adjoining
but also neighbor districts (Senczuk, 2002; Kaniuczak, 2004).
The control areas were chosen on the basis of earlier research
carried by Ossowska et al. (2009), in which metals concentrations in
blood of humans resident in the Tuchola district were measured.
Tuchola Forestry and landscape parks district are situated in the
northern part of the province (Fig. 1) and most of this territory is
determined by forests and forest-lands. This area serves as a control
also for the reason of lack of heavy industry.
3. Material and methods
3.1. Human population
The study material included blood samples of volunteers from polluted
Mogilno neighborhood and unpolluted Tuchola Forestry. The number of humans
studied in 2008 and 2009 was 79 and 82 for Mogilno and Tuchola Forestry,
respectively. The volunteers were at the age below 60 years because of depletion
of antioxidants (Sulochana et al., 2002). The age structures (Table 1) of volunteers
from polluted (Mogilno neighborhood) and control (Tuchola Forestry) were
similar. The volunteers divisions depending on the nicotinic habits from polluted
and the control were also similar (Table 2).
Blood samples were collected in tubes to receive blood serum for antioxidant
enzymes activity, ferritin and total antioxidant status detection (test-glasses with
accelerator of blood coagulating in the vacuum-system for biochemical research
on the serum) and to the tubes with heparin for elements concentration analysis.
Table 2
Volunteers depending on smoking cigarettes in Mogilno neighborhood (polluted
area) and Tuchola Forestry (unpolluted area). There were no signicant differences
in numbers of smokers and non-smokers in examined environments (chi-square
Pearson test: p 0.301307). NP1: non-smokers since 1 year; NP5: non-smokers
since 5 years; NP10: non-smokers since 10 years; NP: non-smokers all life; P1:
smokers since 1 year; P5: smokers since 5 years; P10: smokers since 10 years;
P15: smokers since 15 years; P20: smokers since 20 years; N: total number of
smokers and non-smokers in polluted and unpolluted environments.
Environment
NP1
NP5
NP10
NP
P1
P5
P10
P15
P20
Polluted area
Control area
3
2
3
3
5
11
47
43
58
59
2
1
3
4
1
4
5
3
10
11
21
23
Blood samples in tubes for receiving blood serum were centrifuged at 2000g for
15 min at 4 1C for SOD and CAT activity measurements serum aliquots were stored
at 80 1C until analysis. All of the above procedures were adopted in accordance
with the methodology specied by Johansson and Borg (1988), Wheeler et al.
(1990), Liu (1996), Sherwood et al. (1998), Andrews (1999), Cook (1999), Kricka
(1999), Van den Bosch et al. (2001)and Maier and Chan (2002).
4. Statistical analyses
By the central terminal statement for the number of cases
above 50, to nd whether essential differences in Pb, Cd, Fe and
FRT concentrations, and SOD and CAT activities and TAS exist, the
z test was used, and a value of p o0.05 was considered to be
signicant. To show what kinds of interactions between studied
parameters exist, the multiple regression analysis was used
(Stanisz, 2006). Arithmetic means with standard deviations,
minimum and maximum values of analyzed parameters and p
value for z test for comparison were described in the tables,
while the correlations were demonstrated on scattering graphs
(3 W for three parameters with the surface tted method of least
squares, 2 W for two parameters with lineal or multinomial
match). The results were presented as arithmetic means7SD
for volunteers from studied environments.
This study was undertaken following the Guidelines of the
European Union Council and the current laws in Poland, according
to the Ethical Commission No. 05/2005. The work required a
permit from the Local Committee for Bioethical Research of
Nicolaus Copernicus University, Collegium Medicum in Bydgoszcz
(No. KB/153/2008).
5. Results
Lead, cadmium and iron concentrations in blood, and antioxidant enzymes activity and total antioxidant status in serum were
found to be different in volunteers from studied areas. We have
stated signicant higher lead and cadmium concentrations in blood
samples of volunteers from polluted area as compared with
those from the control (0.0236 mg l 1 vs. 0.014 mg l 1 and
0.0008 mg l 1 vs. 0.0005 mg l 1, respectively), but a lower iron
concentration (0.442 g l 1 vs. 0.476 g l 1; Table 3). The activity of
SOD in serum of volunteers from polluted area was over two times
higher than in serum of volunteers from unpolluted (0.137 U ml 1
vs. 0.055 U ml 1), whilst CAT activity in serum of volunteers from
polluted area was lower than in serum of those from the control
(3.336 nmol min 1 ml 1 vs. 6.017 nmol min 1 ml 1; Table 3).
Simultaneously, we have demonstrated no signicant differences
in FRT concentration (66.109 mg l 1 vs. 37.667 mg l 1, p0.3972)
and signicant lower TAS in serum of volunteers from polluted area
compared with those from the control (0.731 Trolox-equivalents vs.
0.936 Trolox-equivalents, respectively); Table 3. The interactions
between analyzed parameters were examined and we stated
199
Table 3
Superoxide dismutase (SOD) and catalase (CAT) activities, lead (Pb), cadmium
(Cd), iron (Fe) and ferritin (FRT) concentrations, and total antioxidant status (TAS)
in serum of volunteers from Mogilno neighborhood (polluted area) and Tuchola
Forestry (unpolluted control area); p for z test of comparisons, Nnumber,
xarithmetic mean, SDstandard deviation, min. and max.minimum and
maximum values, respectively.
Parameter
Polluted area
Control area
Polluted vs.
control area
SOD [U ml 1]
N
x 7 SD
min.max.
Median
79
0.137 7 0.077
0.0470.346
0.106
82
0.055 70.018
0.0110.100
0.057
p 0.0000
82
6.017 7 3.000
2.10114.476
4.587
p 0.0000
FRT [mg l 1]
N
x 7 SD
min.max.
Median
82
37.6677 22.710
9.20093.200
31.200
p 0.3972
TAS [Trolox-equivalents]
N
79
x 7 SD
0.731 7 0.174
min.max.
0.2171.135
Median
0.695
82
0.936 7 0.180
0.5231.304
0.924
p 0.0000
Pb [mg l 1]
N
x 7 SD
min.max.
Median
79
0.0236 7 0.027
0.0100.079
0.020
82
0.014 70.007
0.0030.038
0.013
p 0.0000
Cd [mg l 1]
N
x 7 SD
min.max.
Median
79
0.0008 7 0.0005
0.00040.0035
0.0006
82
0.0005 70.0003
0.00020.0014
0.0005
p 0.0000
Fe [g l 1]
N
x 7 SD
min.max.
Median
79
0.442 7 0.077
0.2360.854
0.438
82
0.476 7 0.071
0.2380.884
0.479
p 0.0028
79
66.109 7 39.944
20.800161.000
50.900
Table 4
Parameters of multiple regression for the dependence between superoxide
dismutase (SOD) activity in serum and lead (Pb) and cadmium (Cd) concentrations
in the blood of volunteers from polluted area, involving partial correlation
coefcient and semipartial correlation coefcient, p for F test and value of
F test (model of multiple regression essentiality) and model equation (N 79).
Element
Partial
correlation
Semipartial
correlation
Cd
Pb
0.833225
0.256971
0.602094
0.206850
0.0001
11.418
200
Fig. 4. Correlation between iron (Fe) concentration in blood and ferritin (FRT)
concentration in serum of volunteers from polluted area.
Fig. 5. Correlation between iron (Fe) and lead (Pb) concentrations in blood and
ferritin (FRT) concentration in serum of volunteers from unpolluted area.
Table 5
Parameters of multiple regression for dependence between ferritin (FRT) in serum
and iron (Fe) and lead (Pb) concentrations in the blood of volunteers from control
area, involving partial correlation coefcient and semipartial correlation coefcient, p for F test and value of F test (model of multiple regression essentiality)
and model equation (N 82).
Element
Partial
correlation
Semipartial
correlation
Fe
Pb
0.462010
0.418763
0.406606
0.359933
0.0000
16.678
blood was also positively correlated with TAS (r 0.283) in volunteers from unpolluted area (Fig. 7). Positive correlations between
FRT concentration and TAS in serum in volunteers from both
environments were also stated (polluted: r0.625 vs. control:
r0.837; Fig. 6).
6. Discussion
Our research allows proof of the effect of actual lead, cadmium
and iron exposure, marked by these elements level in blood, upon
defense antioxidant mechanisms in humans (Tables 3 and 5).
Environmental factors are essential either for human health or for
the condition of any living organism, because the increase of
concentration of toxic metals plays signicant role in disorders
involving macro- and microelements homeostasis in the organism. It causes disorders of physiological balance of an organism
and serious danger of many abnormalities or diseases, including
cancer, and weakens defense mechanisms (Nohl and Stolze, 1998;
Olinski and Jurgowiak, 1999; Schulz et al., 1999; Siems et al.,
2000; Beisswenger et al., 2001; Buonocore et al., 2001; Darlington
and Stone, 2001; Kawanishi et al., 2001; Sayre et al., 2001).
There are many antioxidant mechanisms targeting to control
physiological level of reactive oxygen species and to protect
human organism against oxidant damage. We tried to estimate
the impact of environmental stress, which is determined by the
magnitude of lead and cadmium concentrations in blood, on the
antioxidant enzymes activity (CAT, SOD), FRT concentration and
TAS in serum (this study). We can thus evaluate this impact;
however there is lack of similar environmental studies carried on
humans. Nevertheless, many publications concerning occupational exposure on lead and its inuence on the antioxidant
enzymes activity exist. They found the impact of lead upon
antioxidant enzymatic mechanisms in relation to doses and time
of exposure (Monteiro et al., 1985; Sugawara et al., 1991; Aydinn
et al., 2004; Han et al., 2005; Patil et al., 2006). It is supported by
studies in which plasma oxidant and antioxidant statuses, in cement
plant workers who were in the profession over the last 10 years
ranging in age between 29 and 54 years, were measured; e.g., SOD
activity was decreased in cement plant workers compared with
control group (Aydinn et al., 2004). The investigations by Han et al.
(2005) involved measurements of oxidative stress biomarkers in
serum of shipyard welders with 133 yr of exposure history in a
large ship-building industry, full-time employed and used a gas
metal arc-welding process with carbon dioxide as shielding gas. The
measurements of ambient air samples taken outside the welding
helmet had a mean welding fume particulate load (13.21.8 mg/m3)
signicantly higher than the Occupational Safety and Health Administration American Conference of Governmental Industrial Hygienists occupational exposure limits (5 mg/m3), and there was no
signicant difference between SOD activity in serum of exposed
workers and the control group (Han et al., 2005). In the other
research, antioxidant enzymes activity was measured in the erythrocytes from workers occupationally exposed to lead, e.g., there
was signicant decrease in SOD and CAT activities in the erythrocytes from workers exposed to lead compared with those from
control group. When a direct effect of lead on both puried enzymes
was tested, SOD activity was inhibited by about 10% and CAT
activity by about 20% at a lead concentration of 400 mg/dl
(Sugawara et al., 1991). The relation between the exposure time
201
202
Taking into account the results of our studies (this work) and
data from abovementioned authors, we can assume that the
changes of SOD activity depend on the condition of an organism
and environmental determinations. Thus our studies (this paper)
show an increase in SOD activity, as an important mechanism of
antioxidant defenses against environmental stress. Our environmental research analyzes the changes in the antioxidant enzymes
activity in humans living under conditions of environmental
stress, which considers the magnitude of Pb and Cd concentrations in blood. On the basis of our studies we can thus conclude
that signicant increase of SOD activity in serum of volunteers
from polluted areas can be one of the defense systems of an
organism against oxidative stress caused by environmental factors (Tables 3 and 4, Figs. 2 and 3). It is also supported by positive
correlation between Pb and Cd concentrations in blood and SOD
activity in serum of volunteers from polluted area, which can be
interpreted as SOD activity increase together with toxic metals
concentrations (Tables 3 and 4; Fig. 2). On the other hand, we
indicated that CAT activity was signicantly higher in serum of
volunteers from unpolluted area (Table 3). We could thus conclude that, as it is connected from our research (this paper), CAT
might be more sensitive upon environmental impact. Simultaneously we should emphasize that the lack of correlation
between CAT activity and Pb or Cd level in serum of volunteers
from studied areas may suggest however that CAT may not meet
the essential role in the protection of an organism against the
toxic metals in the areas studied in this study. Simultaneously,
our environmental investigations showed the increase of TAS and
positive correlation between Pb concentration in blood and TAS in
serum of volunteers from unpolluted areas. This can be interpreted as saying that together with lead height concentration, TAS
in serum also increases (Fig. 7). These results suggest that nonenzymatic antioxidants, marked by total antioxidant status in
serum, play signicant role in the protection against lead blood
increase in volunteers from unpolluted areas.
Analysis of the results of this study shows a positive correlation
between serum FRT and serum iron in the blood of people living in
county of polluted (Fig. 4) and control areas (Table 5, Fig. 5). The
strength of FRTFe correlation was stronger at the Mogilno countys
residents (polluted) than in the controls, where the highest Fe
concentration was stated (Tables 3 and 5, Figs. 4 and 5). In addition,
a positive correlation has been demonstrated in the case of
dependences between FRT and lead in the control (Table 5, Fig. 5).
Furthermore, determination of serum FRT is used as a valuable
parameter, providing both a shortage and excess of iron in the body
(Nielsen et al., 2000). In healthy individuals, approximately 15% of
the total amount of iron ions are associated with this protein, and
65% with hemoglobin (Bauminger and Harrison, 2003). Therefore, it
Fig. 7. Correlation between lead (Pb) concentration in blood and total antioxidant
status (TAS) in serum of volunteers from unpolluted area.
203
7. Conclusions
1. Environmental pollution makes for increase of actual lead and
cadmium exposure, which manifests with lead and cadmium
blood concentrations increase.
2. Superoxide dismutase is resistant to the inuence of environmental factors. Thus increase of SOD activity in serum of
inhabitants from polluted areas is one of the defense mechanisms of an organism against oxidative stress caused by
environmental lead and cadmium exposure.
3. The higher catalase activity and total antioxidant status
indicate that these mechanisms play a key role for antioxidant protection in the unpolluted areas.
4. Non-enzymatic mechanisms marked by a total antioxidant
status are the main antioxidant defense in relation with lead
concentration in humans of unpolluted areas.
5. Ferritin and total antioxidant status are related to each other;
thus antioxidant mechanisms can strengthen one other.
Acknowledgments
This work was supported by a grant from funds of the European
Social Fund and State budget within the framework of the Integrated
Program of Operating-Regional Development (the Activity 2.6
Regional Innovative Strategies and knowledge transfer of individual project of the KuyavianPomeranian Province: Scholarships
for graduate students of 2008/2009-ZPORR) and Nicolas Copernicus
University in Torun within the framework of Rector Magnicus
Grant no. 24/2009.
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