jnasci-2015-394-403

Journal of Novel Applied Sciences
Available online at www.jnasci.org
©2015 JNAS Journal-2014-4-3/394-403
ISSN 2322-5149 ©2015 JNAS
Examination of Mercury concentration in the hair,
milk and Saliva mothers, and relation to number
of dental amalgam filling and mother feeding
Sanaz Khammar1*, Alireza Pourkhabbaz1 and Reza Dahmardeh Behrooz2
1- Department of Environmental Sciences, Faculty of Natural Resources and Environmental, University of
Birjand, Birjand, South Khorasan, Iran
2- Department of Environmental Sciences, Faculty of Natural Resources, University of Zabol, Zabol, Sistan,
Iran
Corresponding author: Sanaz Khammar
ABSTRACT: in this study we aimed to evaluate the maternal factors [including dietary habits and dental
care, during pregnancy and number of children] that influence milk, hair and saliva mercury concentration.
Forty healthy mothers were enrolled in the study in order to take milk, hair and saliva samples. The mean
mercury concentration milk, hair and saliva of mothers were 1.23 (μg / g), 1.81 (μg / g) and 1.10(μg / g)
respectively.The analysis showed that fish consumption, chewing gum, maternal weight and number of
dental amalgam fillings were the factors which had positive correlation with mercury concentration of
mothers. The effect of the factors number of children, during pregnancy, fruit consumption and birth weight
infants had negative relation on mercury levels of mothers. Preventive strategies for mercury exposure
should include, consume appropriate amounts of fishes with low mercury, more of the dental care and
proper nutrition during the pregnancy period.
Keywords: Maternal Factors, Mercury, Milk, Hair, Saliva.
INTRODUCTION
Mercury is a heavy metal that is widespread in the environment and has important adverse health effects (Fok
et al., 2006). The contamination sources of mercury consist of industrial waste water, use of fossil fuels and
fungicides, and burning wastes (Hernandez et al., 1999). The amount of mercury is transformed into methylmercury
and transferred up in the food chain through bio-accumulation (UNEP,1999; EPA, 2000 ; FDA, 2004). Infants may
be exposed to Methyl mercury via breast-milk (Dorea, 2004; Gundacker et al., 2002). Generally, there is a low transfer
of toxic metals through milk when maternal exposure levels are low (Dorea, 2004; Bjornberg et al., 2005). To diminish
maternal and infant exposure to mercury, it is necessary to establish guidelines based on an understanding of the
environmental occurrence of these metals and the manner in which they reach the developing human organism
(Ünüvar et al., 2007; Passos et al., 2007). A mother's diet affect on her breast-milk metal concentrations and the
transfer of mercury through breast-milk in relation to other trace elements (Oskarsson et al., 1996; Sharma and
Pervez, 2005).
Previous studies have shown that a diet rich in fish is the primary pathway of human exposure to MeHg and that
statistical differences in MeHg intake exist between high and low fish consumption groups (Oskarsson et al.,19961;
Foo and Tan, 1998 ). WHO reduced the MeHg provisional tolerable daily intake from 0.47 to 0.23 μg/kg body
weight/day (FAO/WHO, 2003). In addition to milk, hair and saliva of the mother, the most important indicators of
exposure to methyl mercury. Hair contains the thiol (- SH) group for which mercury cations have high affinity (Boischio
and Henshel, 2000) and mercury levels in hair have been shown to reflect mercury level in internal organs (Clarkson,
1992; Pfeiffer et al., 1993) as well as dietary intake (Clarkson, 1992).
J Nov. Appl Sci., 4 (3): 394-403, 2015
in recent years because of the benefits, Saliva, including easy access, is a non-invasive method to collect the liquid
that has been unrivaled as a diagnostic agent (Shiran, 1996).
In this study, we calculate the total concentration of mercury in breast milk, hair and saliva in mothers in this
region and also we examined the relationship between mercury levels of mothers with regard to their factors.
Characteristics of the study area
The city of Zahedan , with an area of 36581Km2 is the most important town in the South East of Iran. The city is
located in terms of the geographical coordinates in 60 degrees 51 minutes and 25 seconds east longitude and 29
degrees 30 minutes 45 seconds north latitude and its height from sea level is 1385 meters. In the last census had a
population of 660,575. Due to the proximity of the city of Zahedan to the Chahnimeh of Zabol and Gulf of Oman, the
people of this area, generally consumed fishes of Zabol Chahnimeh and Gulf of Oman, this city was selected to
perforrm the research.
Figure 1. The map of Iran showing sampling site in South East of Iran
MATERIALS AND METHODS
This prospective study was conducted between January 2013 and March 2014, in Zahedan. A number of 40
mothers (15 to 35 years) without any systemic disease and levels of dental amalgam restorations, were selected.
Mothers were informed about the purpose of the study and completed a questionnaire with respect to weight prior to
pregnancy, height, gestational age, environmental factors, maternal nutrition (fish consumption), amalgam fillings
and lactation period. Infants were examined, their birth weight and height were recorded. To analyze mercury
exposure, about (5-10) ml milk, (5-10)ml saliva and(1gr) hair from each of the mothers of were collected.
In order to avoid contamination to the extent possible, milk was expressed in the morning, 2 hours after the last
breast-feeding by hand. Hair was sampled from occipital area, cut close to the scalp with stainless still scissors, and
placed in an envelope properly labeled. Milk and saliva samples were put directly into polyethylene bottles previously
immersed in nitric acid (65%) for one day and well rinsed with deionized water and were frozen at 20 C. All samples
were evaluated in the environmental analysis laboratory of Natural Resources Faculty of Birjand University.
Analysis
At first, the amount of 3 mg of milk and saliva were accurately weighed and poured into nickel pipes washed with
deionized water. Then the hair samples were washed with distilled water (3 times) and finally with acetone
(UNEP,1987) After drying, the samples became into very small pieces as possible by using special scissors.
In this study, atomic absorption spectrometer model ContrAA300 (Analytik Jena, Germany) was used with
continuous light equipped with a flame, hydride generation and continuous mercury lamp .
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J Nov. Appl Sci., 4 (3): 394-403, 2015
Statistical analysis
The statistical analysis was performed by SPSS software (version 16). Data were tested for normality using
Kolmogorov–Smirnov test. One-way ANOVA was used to compare between mercury concentrations with maternal
weight and birth weight infants factors. A paired t-test was used to determine significant differences in fish and fruit
consumption, chewing gum and number of children. Pearson rank correlation coefficients were used to test
correlations among various mercury levels with amalgam fillings and during pregnancy and also to study the relation
between mercury of mothers’ breast milk, hair and saliva. A p-value < 0.05 indicated statistical significance.
RESULTS AND DISCUSSION
Results
The concentrations of mercury in milk, hair and saliva are summarized in Table 1 for mothers.
The mean concentrations of mercury in milk, hair and saliva of mothers were 1.23 μg / g , 1.81 μg / g, and 1.10 μg /
g respectively.
Tbable 1. Mercury concentration (μg / g) in milk, hair and saliva of mothers
Characteristic
Milk
Hair
Saliva
N
40
40
40
Minimum
0.21
0.67
0.20
Maximum
1.70
3.00
1.99
Mean
1.23
1.81
1.10
Std. Deviation
0.306
0.54
0.50
In our study, there was a significant correlation between mercury concentration in saliva and hair of mothers(R=
0.25 , P= 0.02) and there was a weak correlation between mercury concentrations found in milk and hair (R= 0.064,
P= 0. 69) with milk and saliva (R= 0.059, P= 0.71) (Table 2).
The most influential independent variables for mercury contamination have been shown in Tables 3,4 and 5.
Concentration of mercury of breast milk, hair and saliva of this study has been compared with other countries in
Table 6, 7 and 8.
consumption of fish had increasing effect on mercury concentration in hair (p=0.001) and saliva(p=0.002) of
mothers and only the number of dental amalgam fillings had positive association on mercury concentration in
maternal hair(p=0.002).
Furthermore, chewing gum (p=0.001) and weight of mothers (p=0.000) had a positive association on mercury
content in saliva of the mothers. The analysis showed that consumption of fruits(p=0.004 ), birth weight babies(p
saliva=0.007 ) and (p hair=0.002 ), number of children(p=0.001 ) and during pregnancy(p=0.003 ), respectively,
had negative effects on mercury levels in hair, saliva and hair, milk, and saliva of mothers .
Table 2. The correlation between mercury in the milk, hair and saliva of mothers
Variables
Hair
Milk
Saliva
R
1
0.064
0.250
Hair
P
0.695
0.02
N
40
40
40
R
0.064
1
0.059
Milk
P
0.695
0.719
N
40
40
40
R
0.250
0.059
1
Saliva
P
0.02
0.719
N
40
40
40
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J Nov. Appl Sci., 4 (3): 394-403, 2015
Table 3. Associations between Hg concentration(μg / g) in the milk of mothers and independent factors in mothers
Characteristic
Number of dental amalgam fillings
Variable
N
Mean±S.D
Range
P value
<1 per month
40
37
1.38±1.07
1.53±1.28
1-4
1-9
0.38
1-2 per week
3
1.46±1.24
9-17
2 children
36
1.20±0.73
1-4
> 2 children
4
0.85±0.71
4-7
1 per month
36
0.49±0.29
0-4
1 per week
4
1.08±0.26
4-8
1 per week
27
1.41±1.08
1-4
4-5 per week
13
1.62±1.47
4-7
45-60
11
1.54±1.15
38-55.33
61-75
17
1.7±1.63
55.33-72.66
76-90
12
1.50±1.37
72.66-89.99
1600-2500
18
1.10±1.00
1.75-2.8
2600-3400
16
1.12±1.04
2.8-3.85
3500-4300
6
1.25±0.49
3.85-4.9
-
40
1.60±1.48
0-769
Chewing gum
0.58
0.001
Number of Children
Fish consumption
0.72
Fruit consumption
Mother's weight
0.18
0.21
Birth weight infants
0.92
During pregnancy
0.000
Table 4. Associations between Hg concentration(μg / g) in the hair of mothers and independent factors in mothers
Characteristic
Number of dental amalgam fillings
Variable
N
Mean±S.D
Range
P value
<1 per month
40
37
2.18±0.79
1.81±1.26
1-4
1-9
0.002
1-2 per week
2 children
3
36
2.67±1.85
2.33±0.76
9-17
1-4
> 2 children
1 per month
4
36
1.41±1.72
0.73±2.18
4-7
0-4
1 per week
1 per week
4
27
2.66±1.27
2.92±1.85
4-8
1-4
4-5 per week
45-60
13
11
1.55±1.42
2.26±1.23
4-7
38-55.33
61-75
17
2.91±0.85
55.33-72.66
76-90
1600-2500
12
18
1.47±1.30
2.30±1.96
72.66-89.99
1.75-2.8
Birth weight infants
2600-3400
16
1.75±1.34
2.8-3.85
0.002
During pregnancy
3500-4300
-
6
40
0.75±0. 69
2.62±2.17
3.85-4.9
0-769
0.083
Chewing gum
0.64
Number of Children
0.27
0.001
Fish consumption
0.004
Fruit consumption
Mother's weight
0.90
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J Nov. Appl Sci., 4 (3): 394-403, 2015
Table 5. Associations between Hg concentration(μg / g) in the saliva of mothers and independent factors in mothers
Characteristic
Number of dental amalgam fillings
Variable
<1 per month
N
40
37
Mean±S.D
1.74±1.46
1.43±1.29
Range
1-4
1-9
1-2 per week
2 children
3
36
1.75±0.64
1.58±1.44
9-17
1-4
> 2 children
1 per month
4
36
2.8±1.4
1.25±0.56
4-7
0-4
1 per week
1 per week
4
27
0.64±0.22
1.52±1.41
4-8
1-4
4-5 per week
13
1.96±1.66
4-7
45-60
11
0.59±0.35
38-55.33
61-75
17
1.49±1.1
55.33-72.66
76-90
1600-2500
12
18
1.6±1.25
1.75±1.87
72.66-89.99
1.75-2.8
Birth weight infants
2600-3400
16
1.64±1.47
2.8-3.85
0.007
During pregnancy
3500-4300
-
6
40
1.92±1.21
1.81±1.12
3.85-4.9
0-769
0.003
0.001
Chewing gum
Number of Children
0.81
0.002
Fish consumption
Fruit consumption
Mother's weight
P value
0.20
0.094
0.000
Discussion
In our study The mean concentration of breast milk mercury was 1.23μg /g. mean Concentrations of mercury
vary widely in human milk samples around the world: 2.02-9.50 μg / g (Dorea, 2004 ; Da Costa et al., 2005; Chien et
al., 2006 ; Drasch et al., 1998 ; Bose-O'Reilly et al., 2008; Sakamoto et al.,2002; Sandborgh-Englund et al., 2001;
Klemann et al., 1990). The mercury concentration in breast milk of mothers in the area was higher than mercury
concentration in Sweden (Oskarsson et al., 1996),Canada (Vimy et al., 1997) and Germany (Drexler and Schaller,
1998) and this amount was lower than mercury concentration in Brazil (Barbosa and Dorea, 1998), Zimbabwe and
Tanzania (Bose-O'Reilly et al., 2008). Milk mercury concentrations may differ depending on sampling day and time
during each feeding session and exposure concentrations of the mothers(Dorea, 2004 ; Bjornberg et al., 2005;
Drexler and Schaller 1998; Abadi et al 1997).
Analysis showed that increase in the number of children had a statistically significant differences in milk mercury
concentrations in our study population(p = 0.001).
Some studies observed a negative correlation between mercury concentration in the breast milk and the number
of children (Oskarsson et al., 1996; Drexler and Schaller, 1998) .
The mean concentration of mercury in all tested hair samples in this study was (1.81 μg / g).
In this study, the mean for hair mercury concentrations was lower than Mahshahr port (South of Iran) ,(2.95μg/g)
(Fakour et al., 2010) but, this amount was higher than the Southern shores of the Caspian Sea(North of Iran)
,(0.19μg/g) (Ghasempouri et al., 2010).
Also in the present study, hair mercury concentrations was higher than New Jersey(Stern et al., 2001), Sweden
(Bjornberg et al., 2005), Japan (Yasutake et al., 2003) and Florida (Adam et al., 2014) and this amount was lower
than mercury concentration in Brazil(Santos et al., 2002) and Seychelles (Cernichiari et al., 1995) .
In the heavily polluted Mina Mata Bay (1953-1971), where the villagers consumed mercury contaminated fish
(11.4-39.0 μg g-1), the level of mercury in their hair was 191-705 μg / g (Koos and Longo, 1976 ; Harada, 1982).
In Zahedan, a good positive correlation between fish consumption and accumulation of toxic mercury was found
in hair (p=0.001) and saliva (p=0.002) of mothers. Fish is the most important food bio-concentration of mercury
(Pinheiro et al., 2002) . The mercury content in hair and saliva reflects mainly the uptake of organic mercury
compounds via fish consumption.
Mothers were classified in two groups in relation to fish consumption (1per week and 1per month) in this region.
The mean mercury concentration was significantly higher in hair and saliva samples obtained from mothers with
1 meal per week of fish consumption compared to mothers with 1 per month of fish consumption.
A statistically significant difference were found between the concentration of mercury in hair and saliva and fish
consumption.
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J Nov. Appl Sci., 4 (3): 394-403, 2015
Fish consumption influenced mercury levels in the hair and saliva of mothers and with more fish consumption,
mercury concentration increased.
Based on our questionnaires, people of the region often consume fishes such as salmon, cod, grouper and trout
although we did not examine the effects of different fishes on mercury contamination.
Dahmardeh Behrooz et al, examined mercury levels of fishes of Chahnimeh of Zabol and Gulf of Oman,
concluded that fish is by far the most important dietary item consumed by people in South East of Iran and one of
the main sources of mercury to the body is consumption of seafood (Dahmardeh Behrooz et al.., 2013).
In order to decrease the risk of perinatal mercury exposure, mothers should be advised to consume appropriate
amounts of fishes that are low in mercury (Gerbersman et al., 1997).
In the present study, a significant positive correlation between the number of dental amalgam fillings and hair
mercury levels in women was demonstrated (p=0.002). These results are compatible with the findings in pregnant
Italian women reported by Luglie et al. (Luglie et al., 2005). They have demonstrated that the number of amalgam
fillings positively influenced the mercury concentration in the amniotic fluid of pregnant Italian women. These findings
suggest that in addition to dietary mercury intake, dental amalgam fillings also contribute to mercury accumulation in
the body.
The amount of mercury absorbed into the human body through the amalgam is about 1.2 to 1.10 of the absorbed
mercury through food.
The mean mercury in the hair of women who had a number of amalgam surfaces was 2.18±0.79 μg / g.
According to the results of Fakour et al., individuals who have many amalgam fillings and consume large amounts of
fish have higher levels of mercury than others (Fakour et al., 2010).
The number of maternal dental amalgam fillings and amalgam placements or removals during pregnancy and
the lactation period were reported to determine the mercury concentration of mothers (Oskarsson et al., 1996 ;
Drasch et al., 1998).
The mean concentration of saliva mercury found (1.10 μg/g) in Zahedan women.The mean mercury levels of
saliva was higher from Germany (Pesch et al., 2002) and Finland (Leistevuo et al., 2002). In addition, the
concentrations of saliva mercury in this study was lower than reported from Fakour et al in North of Iran 4.14 μg/g
(Fakour et al., 2010 ).
We noticed positive correlation between chewing gum(p=0.001) and mercury levels in the saliva of mothers. The
mean mercury concentration was significantly higher in saliva samples generated from mothers with 1-2 per week
chewing gum 1.75± 0.64μg / g compared to mothers with <1 per month chewing gum 1.43± 1.29 μg /g.
Amalgam continuously releases mercury into the oral cavity, that is releasing in activities such as chewing gum
increases (Brune,1988, Sällsten et al., 1996).
Pesch et al stated behavioral peculiarities such as bruxism and chewing gum increase the saliva mercury
concentration ( Pesch et al., 2002).
The analysis showed a positive relation in mercury levels in saliva with maternal weight (p=0.000). In a study
conducted by Al-Majed et al found that the weight of the control group and the group of fishermen are the most
important factors influencing on mercury levels (Al-Majed and Preston, 2000). Also observed low during pregnancy
significantly increased the saliva(p=0.003) and milk(p=0.000) mercury levels.
Gundacker et al.( Gundacker et al., 2002) reported elevated mercury levels prematurity (<37 weeks gestation),
frequent consumption of cereals, maternal use of vitamins, and residence in either urban or industrial areas of Austria.
Research on the effects of mercury suggests there is good reason to limit exposure. For women of child-bearing age,
mercury can be passed on to a developing fetus at its most sensitive stage posing neurological risks to the child.
While fish consumption is often encouraged to increase gestation in pregnancy and bolster developing children’s
neurodevelopment, high mercury exposure in mothers may lead to very preterm delivery and counter beneficial
effects for children’s neurodevelopment.
In the present study, the mothers with higher fruit consumption had low concentration of mercury in their hair
(p=0.004) .
Interestingly, Passos et al.( Passos et al., 2007) reported an association between fruit consumption and lower
Hg levels in Amazonian riparians, thus showing the protective effect of fruit consumption against mercury exposure
via dietary intake of fish.
The results showed mercury levels of mothers had no effect on the weight and height of five-month old children
and of two-year-old children ,but, mercury concentrations in hair (p=0.002) and saliva (p=0.007) of mothers had a
significant influence in infants of low birth weight.
The mean of mercury in mothers’milk and hair in the South East of Iran is lower than the normal WHO
recommended limits (2 μg / g) and (7.2 μg / g), respectively (WHO, 2008). But the concentration of mercury in milk
399
J Nov. Appl Sci., 4 (3): 394-403, 2015
8.5 % and the concentration of mercury in hair was 12.5 % of mothers’milk and hair samples were higher than the
normal WHO recommended limit.
In this study, the mean of mercury in saliva was lower than breast milk and the mean of mercury in breast milk
was lower than that of mothers’ hair.
According to the correlation between indicators of milk, hair and saliva was found a significant correlation
between hair and saliva (R= 0.25 , P= 0.02) and there was a weak correlation between mercury concentrations found
in milk and hair (R= 0.064, P= 0. 69) with milk and saliva (R= 0.059, P= 0.71) (Table 2).
The analysis of hair cannot be considered as an alternative method to the analysis of milk, though the sampling
procedure is much easier than milk collection.
Nevertheless, both methods contribute to a comprehensive estimation of the total mercury exposure, since
mercury analysis in hair is preferred concerning the estimation of the body burden related to organic mercury
compounds, whereas the results of the analysis of mercury in milk are a better indicator for exposure to inorganic
mercury . In fact, hair is established as a screening matrix specially targeted for determination of organic mercury,
but also of inorganic mercury (Schweinsberg and Kroiher, 1994 Wilhelm and Idel 1996).
In the present study, saliva was tested as a substitute matrix for assessing the mercury load. Saliva as a readily
collectable material has also been discussed for use as a diagnostic fluid (Jaffe et al., 2005).
Conventional saliva sampling is a noninvasive procedure and saliva mercury analysis may be of importance in
HBM studies. A disadvantage of mercury determination in saliva is that the analytical method has not yet been
standardized and the interpretation of the obtained data remains unclear (Pesch et al., 2002).
The explanation is that breast-milk is not the primary pathway of exposure for infants,
and that prenatal transplacental exposure is a much greater concern. It should be noted that the trans-lactational
barrier is more effective than the transplacental barrier in preventing the transfer of these toxic metals to infants
(Bjornberg et al., 2005; Sharma and Pervez, 2005).
The transfer of mercury from the mother to the fetus is through the placenta and breastfeeding and occurs at
different rates, depending on the source of mercury (Bjornberg et al., 2005).
Mercury concentrations in maternal milk are a function of age, body mass, time of sampling, nutritional status,
lactation period, and fat content of milk (IPCS, 2000).
Anyway there is no study concerning dangers of mercury for health as a bio-environmental toxic material and
the advantages of breast milk in the developing countries to contribute in studies like this (Pronczuk et al., 2002).
At the community level, publicbased information and risk factors should be investigated and at the individual
level, the physician could provide advices on reducing the toxicological burden to the expectant mothers and their
children.
In this study, it is determined that maternal dietary habits, dental care and other factors have an important role
on mercury levels in mothers, but we should not ignore the effects of other factors, such as the use of drugs containing
mercury like Thimer Thimerosalm and Mercurochome, pesticides containing mercury in agricultural activities may
be used and the use of some cosmetics that contain mercury.
Table 6. Comparison of mercury levels in breast milk (μg/g) in different populations
Country/location
N
-
0.25
0.24
Subjects
Mothers at the first week after
birth
After 2 months of breast feeding
Amalgam filling
72
30
30
20
40
0.15
5.8
0.6
48.50
4.20
1.23
Control
Mothers—high eaters
Women 6 week after delivery
Amalgam burner
Former miner
Mothers in South East of Iran
118
Mean
0.90
Germany
82
References
Drexler and Schaller
Vimy et al
Canada
Brazil
Sweden
Tanzania
Zimbabwe
Iran
Barbosa and Dorea
Oskarsson et al
Bose-O’Reilly et al
Bose-O,Reilly et al.
Present study
400
J Nov. Appl Sci., 4 (3): 394-403, 2015
Table 7. Comparison of mercury levels in hair (μg/g) in different populations
Country/location
Brazil
New Jersey
Sweden
Seychelles
N
-
Japan
Florida
Iran
-
189
127
-
135
40
Mean
15.7
0.53
0.35
6.85
Subjects
Indigenous women aged 14-44 years
pregnant women
pregnant women
Women with frequent fish consumption
References
Oliviera Santos et al
Stern et al
Björnberg et al
Cernichiari et al
1.43
0.96
1.81
adult females residing
Women with dietary fish
Mothers in South East of Iran
Yasutake et al
Adam et al
Present study
Table 8. Comparison of mercury levels in saliva (μg/g) in different populations
Country/location
N
Mean
Finnish
187
0.46
Subjects
amalgam fillings
inorganic mercury
References
Leistevuo et al
organic mercury
Germany
239
0.27
0.24
Indigenous population
Pesch et al
North of Iran
-
4.14
Iranian women: amalgam exposure
Fakour et al
South East of Iran
40
1.10
Mothers in South East of Iran
Present study
ACKNOWLEDGEMENT
Special thanks to Engineers Abdolali Khammari, SaeedReza Khammar, Esmat Shahriary, Razieh Khaksefidi
and Mrs Zeynab Naseri for assistance in preparing and following up this study.
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