Science of the Total Environment 677 (2019) 466–473

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Science of the Total Environment

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Concentration of mercury, cadmium, and lead in breast milk from

Norwegian mothers: Association with dietary habits, amalgam and
other factors
Marie Vollset a, Nina Iszatt b, Øyvind Enger a, Elin Lovise Folven Gjengedal a,⁎, Merete Eggesbø b
a
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Aas, Norway
b
Department of Environmental Exposure and Epidemiology, Norwegian Institute of Public Health, P.O. Box 4404, N-0403 Oslo, Norway

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Cadmium and mercury was detected in

100% and lead in 87% of breast milk
samples from Norwegian mothers.
• Levels of cadmium and lead in breast
milk are among the lowest reported
globally.
• Maternal seafood intake and amalgam
fillings explained 46% of the observed
variation in breast milk mercury con-
centrations.
• Cadmium showed no significant rela-
tion with any factor investigated.
• Maternal intake of liver and kidneys
from game was associated with levels
of lead in breast milk.

a r t i c l e i n f o a b s t r a c t

Article history: Mercury (Hg), cadmium (Cd), and lead (Pb) are of great concern for food safety and infants are especially sensi-
Received 13 February 2019 tive to exposure to the maternal body burden. We quantified these elements in breast milk from Norwegian
Received in revised form 12 April 2019 mothers and determined their association with dietary habits, maternal amalgam fillings, and smoking. Breast
Accepted 16 April 2019
milk (n = 300) from the Norwegian Human Milk Study (HUMIS) was analyzed using triple quadrupole induc-
Available online 19 April 2019
tively coupled plasma mass spectrometry, after an acidic decomposition using microwave technique. We used
Editor: Filip M.G. Tack multiple linear regression to examine predictors of Hg and Cd in breast milk, and logistic regression to test pre-
dictors of Pb above the quantification limit. The median breast milk concentrations (minimum - maximum) were
Keywords: 0.20 μg Hg/kg (b0.058–0.89), 0.057 μg Cd/kg (0.017–1.2), and b0.67 μg Pb/kg (b0.2–7.5). Cadmium showed no
Dental filling significant relation with any exposure variable investigated. Lead was associated with intake of liver and kidneys
Human milk from game. For Hg concentration in breast milk, number of amalgam fillings and high fish consumption were sig-
Dietary intake nificant predictors (p b 0.001). We detected a significant association (p b 0.01) between Hg in breast milk and
Seafood maternal consumption of Atlantic halibut, lean fish, mussels and scallops and lifetime consumption of crab. Sea-
Toxic metal
food intake alone explained 10% of variance, while together with amalgam explained 46% of variance in Hg con-
centration in breast milk. Our findings emphasize the importance of following consumer advice with respect to
fish and seafood and points to amalgam as an important source for Hg exposure.
© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).

⁎ Corresponding author.
E-mail addresses: marie.vollset@nmbu.no (M. Vollset), nina.iszatt@fhi.no (N. Iszatt), elin.gjengedal@nmbu.no (E.L.F. Gjengedal), Merete.Eggesbo@fhi.no (M. Eggesbø).

https://doi.org/10.1016/j.scitotenv.2019.04.252
0048-9697/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473
1. Introduction
Breast milk contains nutrients that are important to growth and de-
velopment of infants; simultaneously, breast milk contains potentially
toxic elements and compounds. The content of persistent organic pol-
lutants in breast milk from Norwegian mothers has been documented
in previous studies (Eggesbø et al., 2009; Polder et al., 2009; Thomsen
et al., 2010); yet knowledge of the composition and level of toxic ele-
ments is lacking.
Mercury occurs as elemental mercury (Hg0), inorganic mercury
(Hg2+) and organic mercury (e.g. methyl, ethyl and phenyl mercury)
(Holmes et al., 2009). In the Northern Hemisphere, mercury is
transported north and naturally transformed into methylmercury, one
of the most common organic mercury compounds (Guzzi and La
Porta, 2008) and also one of the most harmful and bioavailable forms
of mercury. Methylmercury biomagnifies in the aquatic food web, mak-
ing fish a predominant source (Holmes et al., 2009). Amalgam fillings
are a source of elemental mercury, with limited evidence for adverse
health effects (Park and Zheng, 2012; Rathore et al., 2012). Methylmer-
cury and elemental mercury can pass the blood/brain barrier (Clarkson,
2002), and pass through the placenta and enter the fetus (Guzzi and La
Porta, 2008). The elimination half-life of Hg in humans is estimated up
to 80 days (Clarkson, 2002; Jo et al., 2015; Park and Zheng, 2012).
Neurodevelopmental toxicity is the most sensitive endpoint for Hg
(Clarkson, 2002), although the association is uncertain at low doses
(Poulin and Gibb, 2008). More recent research indicate that even low
dose exposure may cause early childhood neurocognitive effects
(Karagas et al., 2012).
Cadmium can accumulate in aquatic organisms and agricultural
crops. Tobacco is an important source of Cd for humans, through
smoking (Järup, 2003) or snuff (Pappas et al., 2008). Non-smokers are
primarily exposed through their diet in foods such as grains, shellfish
and fish (Llobet et al., 2003). Cadmium has a long biological half-life
(10–30 years) in humans (Järup, 2003). Women may have higher
blood concentrations of Cd than men, and in utero exposure to Cd has
been associated with adverse neurodevelopmental effects (Schoeters
et al., 2006). Cadmium does not, however, readily excrete into human
milk (Hallén et al., 1995; Vahter et al., 2002).
Atmospheric deposition of Pb in Norway has declined following the
ban of leaded gasoline in 1990 (Steinnes et al., 2011). However, Pb is still
present in the ocean floor and in contaminated soil, and thus available
for uptake through the food web. The intestine of young children ab-
sorbs Pb 4–5 times more effectively than that of adults, and once in
the body, Pb is transported to other organs, finally accumulating in
bones and teeth (WHO, 2010). Lead can be mobilized from the bones,
and subsequently pass into breast milk (Ettinger et al., 2006). Lead has
an estimated half-life of 20 days in adults, however, infants have slower
elimination (National Research Council, 1993). Lead exposure can dam-
age the nervous system, resulting in a reduced intelligence quotient (IQ)
and learning disabilities among children (Lanphear et al., 2005), and
may negatively influence growth (Fleisch et al., 2013).
Infants are especially sensitive to exposure to toxic elements, due to
their immature kidneys and liver, rapid growth, and development of
their nervous system during this period (Goudarzi et al., 2013). Since in-
fants may be exposed to toxic elements through breastfeeding, we de-
termined the total concentration of Hg, Cd, and Pb in breast milk from
Norwegian mothers and investigated factors that may affect the con-
centration of these elements in the breast milk.
2. Materials and methods
2.1. Study population and sampling procedure
The HUMIS study, is a multi-center birth cohort with 2606 mothers
and their children. (Eggesbø et al., 2009; Eggesbø et al., 2011). During
2002–2009, public health visitors recruited mothers to the HUMIS
467
study during routine postnatal care home visits, in six counties in
Norway representing coastal and inland areas. In one region, Østfold
County, recruitment took place at the maternity ward by a pediatrician,
and two consecutive term births for every preterm birth were enrolled.
Mothers collected 25 mL of breast milk every morning on eight consec-
utive days, between the third and eight week postpartum in line with
recommendations (WHO, 2007), but milk sampled otherwise was also
accepted. Mothers recorded date and time of collection for each sample,
as well as whether they had used a breast pump. Breast milk was col-
lected at a median 33 (interquartile range [IQR]: 26–43) days after
birth. The frozen samples were sent to the Norwegian Institute of Public
Health and kept frozen at minus 20 °C. Mothers completed a question-
naire on pregnancy factors and maternal characteristics including infor-
mation on maternal consumption of seafood, number of maternal
amalgam fillings, maternal smoking, maternal age, parity, maternal
body mass index (BMI), maternal education, and proportion of meals
given through breastfeeding. Mothers who were fluent in Norwegian
were eligible for the study. For the present study, we selected 300 sam-
ples of breast milk collected from Norwegian mothers living in six dif-
ferent counties, located in the south-west, south-east and northern
parts of Norway, in the period 2002–2009: 157 samples were from
those with the highest intake of fish and shellfish (N95th percentile)
and 143 sampled randomly (Table 1).
Informed consent was obtained prior to the study and the study was
approved by the Norwegian Data Inspectorate (Ref: 2002/1398-2 and
02/01398-7) and the Regional Committees for Medical and Health Re-
search Ethics (Ref: S-02122).
2.2. Exposures (questionnaire data)
We obtained information on exposures and other covariates from
the Medical Birth Registry of Norway (maternal smoking during preg-
nancy), and the questionnaires that the mothers answered at time of
breast milk sampling. We tested a number of exposure variables as de-
terminants of Hg, Cd, and Pb: number of maternal amalgam fillings,
smoking at the end of the pregnancy, intake of seafood N95th percentile,
last year's consumption of individual seafood (number of meals per year
of each: Atlantic halibut, northern pike, shrimp, mussels, and scallops,
fatty fish, lean fish, fishliver/−roe (“Svolværpostei”), and cod liver oil
Table 2). In addition, we assessed lifetime consumption of liver and kid-
ney from game (never, yes) and different types of seafood: northern
pike (yes/no), seagull (Larinae) eggs (yes/no), and crab (never, 1–10
times, 11–100 times, N100 times).
2.3. Analysis of breast milk
2.3.1. Sample preparation
After thawing from storage at minus 20 °C, the breast milk was ho-
mogenized in a Thermoshake incubator shaker (Gerhardt GmbH & Co.
KG, Königswinter, Germany) at 37 °C. By means of an electronic
100–5000 μL pipette (Biohit, Helsinki, Finland), 3.00 mL-aliquots of
breast milk were transferred into Teflon tubes (Milestone Srl, Sorisole,
Italy) and accurately weighed (Mettler Toledo PG4002-S Delta Range;
Mettler-Toledo GmbH, Greifensee, Switzerland). Subsequently,
3.00 mL ultra-pure nitric acid (69% weight (w)/w, Merck KgaA,
Darmstadt Germany, was purified by distillation using a Milestone
duoPUR, Milestone Srl, Sorisole, Italy) was added to each sample prior
to microwave digestion using the Milestone UltraClave IV (Milestone
Srl, Sorisole, Italy); hold time 25 min at the maximum temperature
260 °C. In order to stabilize Hg, 0.30 mL ultra-pure hydrochloric acid
(37% w/w, Merck KgaA, Darmstadt Germany, sub-boiled, Milestone
duoPUR) was added to each sample. Further on, the samples were
quantitatively transferred into polypropylene centrifuge tubes
(Sarstedt, Nümbrecht, Germany), and finally diluted to 15 mL with de-
ionized water (N18 MΩ).
468 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473

Table 1 mass (Q1 = Q2) at the following masses: 202Hg, 111Cd, and Pb as the
Demographic characteristics of the study population by selected variables. sum of mass 206, 207, and 208, indium (115In), and gold (197Au). The in-
Characteristic n Mothers with Mothers with a high intake of fish ternal standards (Spectrascan, certified elements standards, Teknolab
variable amalgam and A/S, Drøbak, Norway) used were 115In with respect to Cd and 197Au
fillings shellfish (N95% percentile of the with respect to Hg and Pb. Oxygen (O2) was the chosen gas modes for
(%) whole
all three analytes. See Supplementary Table S1 for further information
HUMIS) (%)
on instrumental settings. Detection limits (LOD) and quantification
Maternal age
limits (LOQ) were standard deviation of the blank samples (n = 6) mul-
b28 85 22 40
≥28 and b 33 114 44 53 tiplied by three and ten, respectively (Supplementary Table S2). Blank
≥33 101 52 62 samples were taken through the whole measurement procedure, in-
cluding the sample preparation steps.
Parity
None 118 28 47
One or more 181 49 56
2.3.3. Quality control
Pre-pregnancy BMI (≥ 25 kg/m3)
No 195 42 56 We assessed blank samples for contamination of reagents and
Yes 96 40 43 equipment used, and checked accuracy by concurrent analysis of
European Reference Materials (Joint Research Center, European com-
Education
b12 years 30 33 53
mission, Geel, Belgium), the skimmed milk powders ERM® - BD150
12 years 38 45 47 and ERM® - BD151, certified for the mass fractions of the respective el-
N12 years 229 41 53 ements (Supplementary Table S3). The obtained data were within a 95%
Previous breastfeeding
confidence level of the certified values issued. The within-laboratory re-
No 100 36 57 producibility (RSD) of the method was 11% and 9% for Cd and Pb (n =
Yes 143 59 70 12), respectively, and 3% for Hg (n = 6); results obtained by carrying
County
out measurements on replicate samples of the HUMIS breast milk.
Østfold 36 50 44
Akershus 5 60 60
Oppland 11 45 27 2.4. Statistical analysis
Telemark 19 53 53
Rogaland 87 48 55
Nordland 12 50 75 We imputed concentrations below LOQ as a random number be-
Troms 62 53 97 tween 0 and LOQ. We assessed the distributions of the three elements
Finnmark 10 30 80 and found the distribution of all three elements was left-skewed with
Urban-rural long tails towards high concentrations. We therefore assessed the bivar-
City 34 59 74 iate associations between the toxic elements and the exposure variables
Outer city 87 49 68 using non-parametric tests (Mann-Whitney, Wilcoxon rank-sum or
Villages 54 43 56 Kruskal-Wallis). In multiple linear regression models, we investigated
Rural 64 50 61
the associations between 1) Hg and independent variables amalgam
Particular diet fillings and high intake of seafood (Model 1); 2) Hg and respective
High intake of 235 39 – types of seafood and self-catching of fish (Model 2); and 3) Cd and ma-
seafooda
ternal smoking and high intake of seafood. We log-transformed the Hg
Lifetime intake of liver & kidney from gameb concentrations due to skewed distributions. Due to the high percentage
No 190 75 47 of indecisive determinations (64% b LOQ) for Pb, we made a variable
Yes 102 75 65
showing above LOQ (yes/no), and assessed the odds of having quantifi-
a
Being in the 95th percentile of the HUMIS cohort for total seafood consumption. able Pb in breast milk and from consumption of high intake of seafood,
b
Lifetime consumption of liver and kidneys from game.
and liver and kidneys from game using logistic regression.
We selected covariates using DAGitty (Textor et al., 2011) (Supple-
mentary Fig. S1), and also tested additional co-variates such as birth
2.3.2. Analysis of samples weight, sample collection age, residence in urban versus rural area
Quantification of the total element concentrations in breastmilk was and county of residence.
conducted by inductively coupled plasma mass spectrometry using the Additional adjustment for the additional co-variates above did not
Agilent 8800 Triple Quadrupole (QQQ) ICP-MS (Agilent, Santa Clara, CA, significantly improve the fit of the models and were not included in
USA). All three analytes and the internal standards were quantified on- the final models.

Table 2
Seafood consumption frequency (number of meals per year) by breast feeding mothers.

Seafood n Mean ± SD Median Minimum 25p 75p Maximum

Fatty fisha 293 40 ± 47 24 0 10 58 379

Lean fishb 294 50 ± 46 48 0 12 104 208
Atlantic halibut (Hippoglossus hippoglossus) 291 5 ± 12 0 0 0 4.0 104
Northern pike (Esox lucius) 288 0.2 ± 1.2 0 0 0 0 12
Crab (Brachyura) 286 4 ± 11 0 0 0 3.3 99
Shrimp (Cardidea) 293 10 ± 17 5.0 0 2.0 12 120
Mussels (Mytilus edulis) and scallops (Pecten maximus) 290 3 ± 17 0 0 0 2.0 240
“Svolværpostei”c 292 5 ± 20 0 0 0 0 156
a
Fatty fish such as mackerel (Scomber scombrus), salmon (Salmo salar), brown trout (Salmo trutta) and herring (Clupea harengus), shrimp, mussels, and scallops.
b
Lean fish such as cod (Gadus morhua), pollock (Pollachius virens), flounder (Pleuronectidae), and haddock (Melanogrammus aeglefinus).
c
“Svolværpostei” is a pâté, spread/sandwich filling containing cod roe and cod liver.
 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473 469

We tested for interactions between Hg and consumption of self-
caught fish using a product term and Wald value of p b 0.10 as indicating
interaction. The multiple linear regression models were tested for ho-
moscedasticity, normality, linearity, and influential data points. Due to
heteroscedasticity and left-tail in the distribution of the residuals, we re-
stricted regression analyses to those with Hg above LOQ. The linearity
assumptions held and there were no point of high influence. Additional
adjustment for potential confounders such as county of residence
(Models 1 and 2) and maternal age and education (Model 2) did not sig-
nificantly improve the fit of the models and were not included in the
final models. Statistical analysis was performed in STATA version 14
(Stata Corporation, College Station, Texas, USA).
3. Results
3.1. Characteristics of the participants
Mothers had a mean age of 30.4 years, pre-pregnancy BMI of
24 kg/m2 and were multiparous (60.5%), and this was not significantly
different across the regions. Other characteristics of the participants
can be found in Table 1.
explained 46% of variance in breast milk Hg. Of the seafood variables,
lifetime consumption of crab was associated with a percentage increase
in Hg of 40% and 65% going from never eating to 11–100 times or N100
times, respectively. An IQR increase (92 meals per year) in lean fish was
associated with a 32% increase in Hg relative to mean Hg. We found no
association between those who had eaten pike during their lifetime and
Hg concentration in breast milk (Table 4). We found no interaction be-
tween eating self-caught fish and any seafood variable (p-
interactionN0.15).
Cadmium showed a significant association with lifetime consump-
tion of crab in the bivariate analyses (Table 4), however, the multiple
linear analysis did not show any significant relations with lifetime con-
sumption of crab or with any other dietary habits or other factors inves-
tigated (not shown).
Compared to never eating liver and kidneys from game, reported
consumption was associated with an odds of having Pb breast milk con-
centrations above LOQ of OR = 2.03 (95% CI: 1.19–3.49) after adjust-
ment for maternal age, maternal body mass index (BMI), education
and number of siblings, and high seafood intake (pseudo R2 = 0.025).
Individual seafood variables were not associated with Pb above LOQ in
breast milk (data not shown).

3.2. Level of Hg, Cd, and Pb in breast milk of Norwegian mothers 4. Discussion

Table 3 shows the distribution of concentrations of Hg, Cd, and Pb in We detected Hg, Cd, and Pb in the breast milk of Norwegian mothers.
breast milk of Norwegian mothers. Cadmium and Hg were detected in In particular, high intake of seafood and amalgam fillings were associ-
100% and Pb in 87% of breast milk samples. Cadmium had no values ated with Hg concentrations, whereas intake of liver and kidneys from
below LOQ, while Hg and Pb had 2% and 64% b LOQ, respectively. game was associated with Pb.

3.3. Factors associated with the concentration of Hg, Cd, and Pb
We found that the number of amalgam fillings in the mother's teeth
significantly increased the concentration of Hg in breastmilk (Tables 4
and 5). In addition, there was a significant association between high in-
take of seafood and concentration of Hg in breast milk (Tables 4 and 5).
High seafood intake alone explaining 8% of variance in Hg concentration
in breast milk, while together with amalgam these two factors ex-
plained 38% of variance in Hg concentration in breast milk (Model 1).
This corresponds to a 9% (95% CI: 7% - 12%) increase in Hg relative to
mean Hg per amalgam filling increase (i.e. exp.(0.09) = 1.094), while
there was a 42% (95% CI: 22% - 65%) increase in mean Hg going from
low to high seafood consumers.
Among the individual seafood variables tested in the bivariate anal-
yses, lean fish, Atlantic halibut, shrimp, mussels and scallops, fishliver−/
roe pate (Svolværpostei), lifetime consumption of seagull-egg, and life-
time consumption of crab showed a significant relationship with the
concentration of Hg in breast milk (Table 4). In the multiple linear re-
gression analysis (Model 2), only lean fish, Atlantic halibut, mussels
and scallops, and lifetime consumption of crab showed a significant as-
sociation after adjustment for potential confounders (Table 5). The sea-
food variables in Model 2 explained 10%, and with amalgam fillings
Table 3
Concentrations of mercury, cadmium, and lead in breast milk of Norwegian mothers
(n = 300).
Element Mean ± SDa Median Percentiles Min – max
(μg/kg)
10% 25% 75% 90%
4.1. The level of Hg, Cd, and Pb in breast milk of Norwegian mothers com-
pared to other countries
The concentration of Hg, Cd, and Pb in breast milk from Norwegian
mothers are among the lowest levels reported globally (Table 6). Aver-
age or median Hg in breast milk from the Faroe Islands (Grandjean et al.,
1995), Austria (Gundacker et al., 2002), Slovakia (Ursinyova and
Masanova, 2005), Iran (Goudarzi et al., 2013), and Turkey (Yalçın
et al., 2010) are higher than the maximum value in the Norwegian
mothers (0.89 μg/kg). In the present study, only total mercury was de-
termined, while it is methylmercury (MeHg) which is of great concern
to childbearing and breast-feeding women. A recent study reveals
higher levels of MeHg in human milk in Norway compared to Slovakia
and the Netherlands (Čechová et al., 2017). The Cd concentrations in
breast milk from Norwegian mothers are comparable with that from
Swedish mothers (Björklund et al., 2012) and Austria (Gundacker
et al., 2007), while Cd in breast milk from Iran (Goudarzi et al., 2013)
and Spain (García-Esquinas et al., 2011) is substantially higher than
our maximum value (1.2 μg/kg). All countries report higher breast
milk concentrations of Pb compared to Norway, in particular Spain
(García-Esquinas et al., 2011), Turkey (Örün et al., 2011), and Iran
(Vahidinia et al., 2019). However, one explanation could be that most
of the participants in our subset reported to be living in a rural setting.
Among the studied elements, Pb in breast milk is the one with the
highest variability between studies (Table 6). The concentration of Cd,
Pb, and Hg in breast milk varies with time of day, stage of lactation, ma-
ternal factors and exposure (Örün et al., 2011), nevertheless, the huge
variation indicates different exposure levels between countries
(Rebelo and Caldas, 2016; Sharma et al., 2019).

Hg 0.2 ± 0.17 0.20 0.069 0.11 0.32 0.45 b0.058b–0.89 4.2. Factors associated with the concentration of Hg, Cd, and Pb
Cd 0.08 ± 0.10 0.057 0.027 0.036 0.089 0.13 0.017–1.2
Pb – b0.67b b0.2c b0.67b 0.46 0.87 b0.2c–7.5
We found a significant positive association between maternal amal-
a
Standard deviation of the mean. gam fillings and concentration of Hg in breast milk, in agreement with
b
LOQ: wet-weight concentrations were determined on the basis of the mean sample
weight of breast milk.
the majority of studies on breast milk and amalgam fillings (Björnberg
c
LOD: wet-weight concentrations were determined on the basis of the mean sample et al., 2005; Da Costa et al., 2005; Drasch et al., 1998; Oskarsson et al.,
weight of breast milk. 1996; Ursinyova and Masanova, 2005; Vimy et al., 1997), although
470 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473

Table 4
Concentrations of mercury and cadmium in breast milk of Norwegian mothers (median, interquartile range (IQR)), according to maternal exposures.

Hg Cd

Exposures nf Median IQR p Median IQR p

Amalgam fillings
None 61 0.11 0.056–0.19 0.049 0.032–0.085
1–3 61 0.14 0.097–0.22 0.060 0.040–0.089
4–6 53 0.23 0.15–0.35 0053 0.038–0.076
≥7 68 0.34 0.24–0.43 *** 0.059 0.037–0.095
a
Smoking
No 189 0.20 0.10–0.32 0.056 0.036–0.085
Yes 109 0.22 0.12–0.33 0.058 0.037–0.092

Last year's eating habits

High intake of seafoodb
No 143 0.15 0.089–0.24 0.054 0.034–0.091
Yes 157 0.25 0.17–0.36 *** 0.058 0.040–0.088
Fatty fishc
Never 32 0.17 0.088–0.39 0.075 0.038–0.10
Monthly or less than monthly 74 0.19 0.11–0.32 0.053 0.036–0.085
Monthly or twice a month 47 0.23 0.13–0.33 0.068 0.042–0.093
Less than weekly 67 0.20 0.11–0.31 0.050 0.033–0.085
Weekly or more often 74 0.22 0.14–0.31 0.054 0.037–0.081
Lean fishd
Never 19 0.11 0.064–0.32 0.046 0.033–0.084
Monthly or less than monthly 73 0.13 0.087–0.23 0.056 0.036–0.091
Twice or more a month 62 0.21 0.11–0.32 0.054 0.029–0.089
Weekly or more often 140 0.23 0.17–0.35 *** 0.061 0.040–0.086
Halibut
Never 147 0.18 0.09–0.32 0.055 0.035–0.090
Less than monthly 93 0.19 0.12–0.30 0.054 0.036–0.084
Monthly or more often 51 0.27 0.18–0.38 ** 0.069 0.040–0.089
Crab
Never 148 0.19 0.096–0.32 0.058 0.035–0.085
Less than monthly 109 0.20 0.12–0.32 0.057 0.038–0.091
Monthly or more often 29 0.24 0.17–0.35 0.045 0.036–0.081
Shrimp
Never 54 0.13 0.063–0.22 0.06 0.034–0.093
1–10 meals per year 130 0.19 0.11–0.28 0.054 0.035–0.086
N10 meals per year 109 0.26 0.16–0.38 *** 0.058 0.040–0.086
Mussels and scallops
Never 192 0.19 0.098–0.315 0.058 0.037–0.085
Less than monthly 85 0.22 0.16–0.31 0.056 0.035–0.095
Monthly or more often 13 0.38 0.22–0.43 ** 0.042 0.036–0.073
Svolværposteie
Never 246 0.19 0.11–0.31 0.055 0.036–0.088
Less than monthly 19 0.28 0.21–0.33 0.060 0.035–0.089
Monthly 13 0.22 0.19–0.27 0.062 0.037–0.089
Weekly 14 0.31 0.13–0.61 * 0.071 0.044–0.084
Self–catching of fish
No 151 0.18 0.10–0.29 0.057 0.036–0.091
Yes 149 0.22 0.13–0.34 ** 0.057 0.038–0.085

Earlier eating habits

Lifetime consumption of northern pike
No 227 0.20 0.11–0.32 0.055 0.036–0.085
Yes 63 0.21 0.10–0.33 0.062 0.039–0.095
Lifetime consumption of seagull egg
No 221 0.19 0.10–0.31 0.058 0.036–0.091
Yes 70 0.26 0.18–0.37 *** 0.049 0.035–0.073
Lifetime consumption of crab
Never 53 0.18 0.087–0.3 0.062 0.037–0.085 *
1–10 times 99 0.19 0.11–0.29 0.045 0.032–0.079
11–100 times 103 0.21 0.12–0.33 0.062 0.040–0.091
N100 times 38 0.26 0.17–0.36 * 0.062 0.042–0.093

Significance testing based on Kruskal-Wallis and Mann-Whitney (Wilcoxon rank-sum) *p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001.
a
Smoking at the end of pregnancy.
b
Being in the 95th percentile of the HUMIS cohort for total seafood consumption.
c
Fatty fish such as mackerel, salmon, brown trout and herring.
d
Lean fish such as cod, pollock, flounder, and haddock.
e
“Svolværpostei” is a pâté, spread/sandwich filling containing cod roe and cod liver.
f
Due to lack of information in the questionnaire the number of participants (n) is b300.

three studies found no significant association (García-Esquinas et al., amalgam fillings, compared with total number of participants.
2011; Gundacker et al., 2002; Yalçın et al., 2010). The discrepancy Gundacker et al. (2002) and García-Esquinas et al. (2011) had few
could be due to insufficient number of mothers without, or with few, mothers without amalgam fillings, n = 3 and n = 8, respectively,
 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473 471

Table 5 albeit, not statistically significant, between fish consumption and con-
Factors associated with the natural log of mercury in breast milk. centration of Hg in breast milk. In populations with low fish intake,
Explanatory variable Coefficient (β) 95% confidence interval p there is no association between fish in the diet and Hg in breast milk
Model 1a (Adjusted R2 = 0.38h, N=229g)
(Björnberg et al., 2005; Oskarsson et al., 1996). In the Faroe Islands, eat-
Amalgam fillings 0.09 0.07–0.11 0.000 ing pilot whales (which have a high Hg content) (Grandjean et al.,
High intake of seafoodb 0.35 0.20–0.50 0.000 1994) but not quantity of fish meals, was significantly association with
Model 2c (Adjusted R2 = 0.46i, n=226g)
Hg concentrations in breast milk (Grandjean et al., 1995).
Lean fishd, f 0.003 0.001–0.005 0.001 We investigated which types of seafood were associated with Hg
Atlantic halibutf 0.01 0.003–0.02 0.005 concentrations in breast milk and found significant associations with
Shrimpf 0.003 −0.002– 0.01 0.226 lean fish, Atlantic halibut, mussels and scallops, and lifetime consump-
Mussels and scallopsf 0.01 0.002–0.02 0.016
tion of crab. A study on total Hg in the blood of Norwegian adults ranked
Svolværposteie,f −0.001 −0.004–0.003 0.784
Lifetime consumption of crab Atlantic halibut, northern pike and crab among the species with the
1–10 times 0.19 −0.01–0.39 0.062 highest average Hg concentrations (Jenssen et al., 2012). This corre-
11–100 times 0.28 0.073–0.48 0.008 sponds well with our findings that there was a significant positive asso-
N100 times 0.43 0.175–0.69 0.001 ciation between consumption of halibut and the concentration of Hg in
Self-catching of fish 0.13 −0.01–0.27 0.076
breast milk. There was, however, no association between those who
a
Adjusted for maternal age, maternal body mass index (BMI), education and number of during their lifetime had eaten pike and concentration of Hg in breast
siblings.
b milk. This may be due to few high consumers of pike in our study,
Being in the 95th percentile of the HUMIS cohort for total seafood consumption.
c
Adjusted for amalgam fillings, maternal age, maternal BMI, education, number of with only nine mothers having eaten pike N11 times in their lifetime.
siblings, and includes all seafood variables in the same model. This is consistent with recommended dietary advice of no consumption
d
Lean fish such as cod, pollock, flounder, and haddock . e “Svolværpostei” is a pâté, of pike especially by pregnant or breastfeeding mothers (Norwegian
spread/sandwich filling containing cod roe and cod liver. Food Safety Authority, 2015). Lifetime intake of crab, but not eating
f
Meals per year.
g
Due to missing information the number of participants (n) in the regression analyses
crab during the last year, was significantly positively associated with
is b300. the concentration of Hg. Consumers with higher intake of both shrimp
h
R2 from just fish = 0.08; R2 from fish plus amalgam = 0.37. and “Svolværpostei” had significantly higher concentrations of Hg in
i
R2 from seafood variables = 0.10; R2 from seafood plus amalgam = 0.46. the bivariate analysis, but not in the multiple linear regression model,
while mussels and scallops were significant in both. Shellfish and cod
liver and roe (ingredients in “Svolværpostei”) have low Hg concentra-
while Yalçın et al. (2010) had mothers with a small number of amalgam tions compared to other seafood such as halibut and crab claws
fillings only (b6). Since 1991, due to Hg risk, guidelines to reduce the use (Jenssen et al., 2012), and consumers of these foods may have generally
of dental amalgam, have been introduced in Norway, with a ban imple- higher consumption of other seafood with higher Hg concentrations,
mented in 2008 (Skjelvik, 2012). However, it will take a number of confounding the relation and giving rise to the bivariate, non-adjusted
years until all existing amalgam fillings are removed. relation.
We also found a significant association between high intake of sea- Mercury concentrations in breast milk were not associated with con-
food and Hg in breast milk, consistent with a large study (n = 1058) sumption of fatty fish such as mackerel, salmon, brown trout, and her-
from Greece, Italy, Croatia, and Slovenia, in which fish consumption ring, but were associated with consumption of lean fish (i.e. cod,
was associated with Hg concentrations in breast milk (Miklavčič et al., pollock, flounder, and haddock). This is consistent with the study in
2013). García-Esquinas et al. (2011) also reported a positive association, Norwegian adults where lean fish consumption had the highest impact

Table 6
Mercury, cadmium, and lead in human breast milk in different countries and regions (μg/kg or μg/L).

Country/region n Hg Cd Pb Sampling time Reference

b b c
Norway 301 0.2. ± 0.17 0.08 ± 0.10 b0.67 1 month (26–43 days IQR) (The present work)
0.20c 0.057c
Sweden 30 0.6 ± 0.4b 6 weeks (Oskarsson et al., 1996)
60 0.086 ± 0.045b 1.5 ± 0.90b 2–3 weeks (Björklund et al., 2012)
0.075c 1.2c
Faroe Islands 88 2.45c (8.7)d 4–5 days (Grandjean et al., 1995)
Austria 116 1.59 ± 1.21b 1.63 ± 1.66b (n = 138) 2–14 days (Gundacker et al., 2002)
0.086 ± 0.085b 2–14 days (Gundacker et al., 2007)
0.063c
Slovakia 158 0.94 ± 0.77b 0.43 ± 0.27b 4.7 ± 4.1b 4 days (Ursinyova and Masanova, 2005)
Germany 46 0.37c b7 days (Drasch et al., 1998)
Greece 95 0.13c NDa 14 days (Leotsinidis et al., 2005)
Italy 605 0.2c (b0.045–28)e 1 month (Miklavčič et al., 2013)
Slovenia 284 0.2c (b0.045–2.9)e 1 month
Croatia 125 0.2c (b0.045–2.4)e 1 month
Greece 44 0.6c (b0.045–12)e 3–8 months
Spain 98 0.61c 1.41c 16.64c 3 weeks (García-Esquinas et al., 2011)
Iran 37 0.92 ± 0.54b 1.92 ± 1.04b 7.11 ± 3.96b 1–6 weeks (Goudarzi et al., 2013)
100 2.8c b1 41.9 c 1–12 months (Vahidinia et al., 2019)
Turkey 144 0.67c 20.6c 2 months (Örün et al., 2011)
44 3.42 ± 1.66b 10–20 days (Yalçın et al., 2010)
a
ND: Not detected.
b
Mean ± standard deviation.
c
Median.
d
Maximum.
e
Range (minimum-maximum).
472 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473
on total Hg blood concentrations (Jenssen et al., 2012). They also found
that catching N50% of their seafood themselves was associated with in-
creased total Hg blood concentrations, however, in our study self-
catching fish was only borderline significant after adjustment for other
seafood variables and confounders.
Seafood is rich in essential long-chain polyunsaturated fatty acids,
which are important for brain development and functions (Bazinet
and Layé, 2014) and breastfeeding mothers in Norway are recom-
mended to eat lean fish (Norwegian Directorate of Health, 2019). In
general, N90% of Hg in fish is found as methylmercury; however, the
concentrations of methylmercury can vary considerably between spe-
cies (Morel et al., 1998). Substantial underestimation of the effects of
Hg toxicity and of fish benefits may occur from the lack of adjustment
for confounders and imprecision of the exposure parameters (Choi
et al., 2008). The European Food Safety Authority recommends that
each country needs to consider its own pattern of fish consumption, es-
pecially the species of fish consumed, and carefully assess the risk of ex-
ceeding the tolerable weekly intake of methylmercury while obtaining
the health benefits from consumption of seafood (European Food Safety
Authority, 2014).
We found no significant relation between Cd and any exposure var-
iables. Accordingly, García-Esquinas et al. (2011) found no association
between Cd in breast milk and consumption of fish and shellfish. How-
ever, maternal smoking has been significantly associated with Cd con-
centrations in other countries (Bassil et al., 2018; Gundacker et al.,
2007; Ursinyova and Masanova, 2005; Örün et al., 2011), a discrepancy
probably due to a deficiency of heavy smokers among the mothers in-
cluded in this study. Norway currently has one of the highest rankings
in a European index of tobacco control activities (Joossens and Raw,
2006), with consumption of cigarettes per woman (age 15–74 years)
peaking around 1990 (Lund and Lund, 2014). The percentage of female
daily smokers halved to 12% from 2006 to 2016, while the use of snuff (a
smokeless tobacco) among young woman increased (SSB, 2017). We
did not include snuff in this study, and it should be considered in future
investigations.
The majority of women in our study had Pb below the LOQ. Lifetime
consumption of liver and kidneys from game, was associated with a
doubling of the odds of having quantifiable Pb in breast milk compared
to never eating it, although the explained variance was only 3%. In a
group of 147 adult Norwegians, Meltzer et al. (2013) found that lead-
shot cervid game meat consumption once a month or more was associ-
ated with approximately 31% increase in blood Pb concentrations. Fish
muscle normally have low levels of Pb (Julshamn et al., 2004), whereas
shellfish show substantially higher values even in unpolluted waters
(Julshamn et al., 2008). However, we found no indication that high in-
take of seafood, or specific seafood types was associated with quantifi-
able levels of Pb in breast milk in this study.
4.3. Strengths and limitations of the study
Current knowledge on element concentrations and the association
with dietary habits and other factors are scarce. The strengths of this
study include a relatively large sample size with participants from
eight counties from south to north in Norway, including a large selection
of mothers with high intake of seafood. We had substantial information
on maternal diet from the previous year and lifetime consumption of
high-risk foods from questionnaires, however, we missed information
on snuff. We were able to quantitatively determine the Cd and Hg in
100% and 98% of the samples, respectively. However, for Pb, the major
limitation was the LOQ which was not sufficient low and consequently
resulted in 36% quantitative determinations only.
5. Conclusion
The concentrations of Cd and Pb in breastmilk from Norwegian
mothers are among the lowest reported globally. Breastmilk Cd and
Pb concentrations were not strongly associated with dietary habits or
other factors investigated. However, Hg concentrations in breast milk
significantly increased with the number of maternal amalgam fillings
and high intake of seafood. This points to the importance of dietary
guidelines for fish and seafood consumption for women of child-
bearing age.
Author contributions
Establishing the cohort on which the study was based, identifying
high fish eaters and pulling their samples, M.E.; Methodology, M.E.,
E.L.F.G., N.I., Ø.E., and M.V.; Chemical analysis, M.V., Ø.E., and E.L.F.G.;
Statistical analysis, M.V. and N.I.; Writing-Original Draft Preparation,
M.V.; Writing-Review & Editing, M.V. E.L.F.G., N.I. and M.E.; Supervision,
E.L.F.G., N.I., and M.E.; Project Administration, M.E. and E.L.F.G.; Funding
Acquisition, M.E. and E.L.F.G.
Acknowledgments
We are grateful to all the breast feeding mothers participating in this
study. A special thanks to the public health visitors and the pediatrician
for recruiting mothers to the HUMIS study. This work was supported by
the Research Council of Norway (NevroNor, grant number 226402), and
the Norwegian University of Life Sciences (own funding).
Conflicts of interest
The authors declare no conflict of interest.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2019.04.252.
References
Bassil, M., Daou, F., Hassan, H., Yamani, O., Kharma, J.A., Attieh, Z., Elaridi, J., 2018. Lead,
cadmium and arsenic in human milk and their socio- demographic and lifestyle de-
terminants in Lebanon. Chemosphere 191, 911–921. https://doi.org/10.1016/j.
chemosphere.2017.10.111.
Bazinet, R.P., Layé, S., 2014. Polyunsaturated fatty acids and their metabolites in brain
function and disease. Nat. Rev. Neurosci. 15 (12), 771–785. https://doi.org/10.1038/
nrn3820.
Björklund, K.L., Vahter, M., Palm, B., Grandér, M., Lignell, S., Berglund, M., 2012. Metals and
trace element concentrations in breast milk of first time healthy mothers: a biological
monitoring study. Environ. Health 11 (92). https://doi.org/10.1186/1476-069X-11-
92.
Björnberg, K.A., Vahter, M., Berglund, B., Niklasson, B., Blennow, M., Sandborgh-Englund,
G., 2005. Transport of methylmercury and inorganic mercury to the fetus and
breast-fed infant. Environ. Health Perspect. 113 (10), 1381–1385. https://doi.org/
10.1289/ehp.7856.
Čechová, E., Scheringer, M., Seifertová, M., Mikeš, O., Kroupová, K., Kuta, J., Forns, J.,
Eggesbø, M., Quaak, I., de Cock, M., van de Bor, M., Patayová, H., Palkovičová
Murínová, Ľ., Kočan, A., 2017. Developmental neurotoxicants in human milk: com-
parison of levels and intakes in three European countries. Sci. Total Environ. 579,
637–645. https://doi.org/10.1016/j.scitotenv.2016.11.046.
Choi, A.L., Cordier, S., Weihe, P., Grandjean, P., 2008. Negative confounding in the evalua-
tion of toxicity: the case of methylmercury in fish and seafood. Crit. Rev. Toxicol. 38
(10), 877–893. https://doi.org/10.1080/10408440802273164.
Clarkson, T.W., 2002. The three modern faces of mercury. Environ. Health Perspect. 110
(Suppl. 1), 11–23. https://doi.org/10.1289/ehp.02110s111.
Da Costa, S.L., Malm, O., Dórea, J.G., 2005. Breast-milk mercury concentrations and amal-
gam surface in mothers from Brasilia, Brazil. Biol. Trace Elem. Res. 106 (2), 145–151.
https://doi.org/10.1385/BTER:106:2:145.
Drasch, G., Aigner, S., Roider, G., Staiger, F., Lipowsky, G., 1998. Mercury in human colos-
trum and early breast milk. Its dependence on dental amalgam and other factors.
J. Trace Elem. Med. Bio. 12 (1), 23–27.
Eggesbø, M., Stigum, H., Longnecker, M.P., Polder, A., Aldrin, M., Basso, O., Thomsen, C.,
Skaare, J.U., Becher, G., Magnus, P., 2009. Levels of hexachlorobenzene (HCB) in breast
milk in relation to birth weight in a Norwegian cohort. Environ. Res. 109 (5),
559–566. https://doi.org/10.1016/j.envres.2009.04.001.
Eggesbø, M., Moen, B., Peddada, S., Baird, D., Rugtveit, J., Midtvedt, T., Bushel, P.R., Sekelja,
M., Rudi, K., 2011. Development of gut microbiota in infants not exposed to medical
interventions. Acta Pathol. Microbiol. Immunol. Scand. 119 (1), 17–35. https://doi.
org/10.1111/j.1600-0463.2010.02688.x.
 M. Vollset et al. / Science of the Total Environment 677 (2019) 466–473
Ettinger, A.S., Téllez-Rojo, M.M., Amarasiriwardena, C., Peterson, K.E., Schwartz, J., Aro, A.,
Hu, H., Hernández-Avila, M., 2006. Influence of maternal bone lead burden and cal-
cium intake on levels of lead in breast milk over the course of lactation. Am.
J. Epidemiol. 163 (1), 48–56. https://doi.org/10.1093/aje/kwj010.
European Food Safety Authority, 2014. Scientific opinion on health benefits of seafood
(fish and shellfish) consumption in relation to health risks associated with exposure
to methylmercury. EFSA J. 12 (7), 3761. https://doi.org/10.2903/j.efsa.2014.3761
2014.
Fleisch, A.F., Burns, J.S., Williams, P.L., Lee, M.M., Sergeyev, O., Korrick, S.A., Hauser, R.,
2013. Blood lead levels and serum insulin-like growth factor 1 concentrations in
peripubertal boys. Environ. Health Perspect. 121, 854–858. https://doi.org/10.1289/
ehp.1206105.
García-Esquinas, E., Pérez-Gómez, B., Fernández, M.A., Pérez-Meixeira, A.M., Gil, E., de Paz,
C., Iriso, A., Sanz, J.C., Astray, J., Cisneros, M., de Santos, A., Asensio, A., García-Sagredo,
J.M., García, J.F., Vioque, J., Pollán, M., López-Abente, G., González, M.J., Martínez, M.,
Bohigas, P.A., Pastor, R., Aragonés, N., 2011. Mercury, lead and cadmium in human
milk in relation to diet, lifestyle habits and sociodemographic variables in Madrid
(Spain). Chemosphere 85 (2), 268–276. https://doi.org/10.1016/j.
chemosphere.2011.05.029.
Goudarzi, M., Parsaei, P., Nayebpour, F., Rahimi, E., 2013. Determination of mercury, cad-
mium and lead in human milk in Iran. Toxicol. Ind. Health 29 (9), 820–823. https://
doi.org/10.1177/0748233712445047.
Grandjean, P., Jørgensen, P.J., Weihe, P., 1994. Human milk as a source of methylmercury
exposure in infants. Environ. Health Perspect. 102 (1), 74–77. https://doi.org/
10.1289/ehp.9410274.
Grandjean, P., Weihe, P., Needham, L.L., Burse, V.W., Patterson, D.G., Sampson, E.J.,
Jorgensen, P.J., Vahter, M., 1995. Relation of a seafood diet to mercury, selenium, ar-
senic, and polychlorinated biphenyl and other organochlorine concentrations in
human milk. Environ. Res. 71 (1), 29–38. https://doi.org/10.1006/enrs.1995.1064.
Gundacker, C., Pietschnig, B., Wittmann, K.J., Lischka, A., Salzer, H., Hohenauer, L.,
Schuster, E., 2002. Lead and mercury in breast milk. Pediatrics 110 (5), 873–878.
Gundacker, C., Pietschnig, B., Wittmann, K.J., Salzer, H., Stöger, H., Reimann-Dorninger, G.,
Schuster, E., Lischka, A., 2007. Smoking, cereal consumption, and supplementation af-
fect cadmium content in breast milk. J. Expo. Sci. Env. Epid. 17 (1), 39–46. https://doi.
org/10.1038/sj.jes.7500518.
Guzzi, G., La Porta, C.A., 2008. Molecular mechanisms triggered by mercury. Toxicology
244 (1), 1–12. https://doi.org/10.1016/j.tox.2007.11.002.
Hallén, I.P., Jorhem, L., Lagerkvist, B.J., Oskarsson, A., 1995. Lead and cadmium levels in
human milk and blood. Sci. Total Environ. 166 (1), 149–155.
Holmes, P., James, K., Levy, L., 2009. Is low-level environmental mercury exposure of con-
cern to human health? Sci. Total Environ. 408 (2), 171–182. https://doi.org/10.1016/j.
scitotenv.2009.09.043.
Järup, L., 2003. Hazards of heavy metal contamination. Br. Med. Bull. 68 (1), 167–182.
Jenssen, M., Brantsæter, A., Haugen, M., Meltzer, H., Larssen, T., Kvalem, H., Birgisdottir, B.,
Thomassen, Y., Ellingsen, D., Alexander, J., Knutsen, H.K., 2012. Dietary mercury expo-
sure in a population with a wide range of fish consumption—self-capture of fish and
regional differences are important determinants of mercury in blood. Sci. Total Envi-
ron. 439, 220–229. https://doi.org/10.1016/j.scitotenv.2012.09.024.
Jo, S., Woo, H.D., Kwon, H.-J., Oh, S.-Y., Park, J.-D., Hong, Y.-S., Pyo, H., Park, K.S., Ha, M.,
Kim, H., Sohn, S.J., Kim, Y.M., Lim, J.A., Lee, S.A., Eom, S.Y., Kim, B.G., Lee, K.M., Lee,
J.H., Hwang, M.S., Kim, J., 2015. Estimation of the biological half-life of methylmercury
using a population Toxicokinetic model. Int. J. Environ. Res. Public Health 12,
9054–9067. https://doi.org/10.3390/ijerph120809054.
Joossens, L., Raw, M., 2006. The tobacco control scale: a new scale to measure country ac-
tivity. Tob. Control. 15 (3), 247–253. https://doi.org/10.1136/tc.2005.015347.
Julshamn, K., Lundebye, A.-K., Heggstad, K., Berntssen, G., Boe, B., 2004. Norwegian mon-
itoring programme on the inorganic and organic contaminants in fish caught in the
Barents Sea, Norwegian Sea and North Sea, 1994–2001. Food Addit. Contam. 21,
365–376. https://doi.org/10.1080/02652030310001639512.
Julshamn, K., Duinker, A., Frantzen, S., Torkildsen, L., Maage, A., 2008. Organ distribution
and food safety aspects of cadmium and Lead in great scallops, Pecten maximus L.,
and horse mussels, Modiolus modiolus L., from Norwegian waters. Bull. Environ.
Contam. Toxicol. 80 (4), 385–389.
Karagas, M.R., Choi, A.L., Oken, E., Horvat, M., Schoney, R., Kamai, E., Cowell, W.,
Grandjean, P., Korrick, S., 2012. Evidence on the human health effects of low-level
methylmercury exposure. Environ. Health Perspect. 120 (6), 799–806. https://doi.
org/10.1289/ehp.1104494.
Lanphear, B.P., Hornung, R., Khoury, J., Yolton, K., Baghurst, P., Bellinger, D.C., Canfield, R.L.,
Dietrich, K.N., Bornschein, R., Greene, T., Rothenberg, S.J., Needleman, H.L., Schnaas, L.,
Wasserman, G., Graziano, J., Roberts, R., 2005. Low-level environmental lead expo-
sure and children's intellectual function: an international pooled analysis. Environ.
Health Perspect. 113 (7), 894–899. https://doi.org/10.1289/ehp.7688.
Leotsinidis, M., Alexopoulos, A., Kostopoulou-Farri, E., 2005. Toxic and essential trace ele-
ments in human milk from Greek lactating women: association with dietary habits
and other factors. Chemosphere 61 (2), 238–247. https://doi.org/10.1016/j.
chemosphere.2005.01.084.
Llobet, J., Falco, G., Casas, C., Teixido, A., Domingo, J., 2003. Concentrations of arsenic, cad-
mium, mercury, and lead in common foods and estimated daily intake by children,
adolescents, adults, and seniors of Catalonia, Spain. J. Agric. Food Chem. 51 (3),
838–842. https://doi.org/10.1021/jf020734q.
Lund, I., Lund, K.E., 2014. Lifetime smoking habits among Norwegian men and women
born between 1890 and 1994: a cohort analysis using cross-sectional data. BMJ
Open 4 (10). https://doi.org/10.1136/bmjopen-2014-005539.
Meltzer, H.M., Dahl, H., Brantsæter, A.L., Birgisdottir, B.E., Knutsen, H.K., Bernhoft, A.,
Oftedal, B., Lande, U.S., Alexander, J., Haugen, M., Ydersbond, T.A., 2013. Consumption
473
of lead-shot cervid meat and blood lead concentrations in a group of adult Norwe-
gians. Environ. Res. 127, 29–39. https://doi.org/10.1016/j.envres.2013.08.007.
Miklavčič, A., Casetta, A., Tratnik, J.S., Mazej, D., Krsnik, M., Mariuz, M., Sofianou, K., Špirić,
Z., Barbone, F., Horvat, M., 2013. Mercury, arsenic and selenium exposure levels in re-
lation to fish consumption in the Mediterranean area. Environ. Res. 120, 7–17.
https://doi.org/10.1016/j.envres.2012.08.010.
Morel, F.M.M., Kraepiel, A.M.L., Amyot, M., 1998. The chemical cycle and bioaccumulation
of mercury. Annu. Rev. Ecol. Evol. Syst. 29 (1), 543–566. https://doi.org/10.1146/
annurev.ecolsys.29.1.543.
National Research Council, 1993. Measuring Lead Exposure in Infants, Children, and Other
Sensitive Populations. The National Academies Press, Washington, DC (356 pp).
Norwegian Directorate of Health, 2019. Råd til spesielle grupper - Ammende.
Matportalen.no. Norwegian Directorate of Health, Norway http://www.
matportalen.no/rad_til_spesielle_grupper/tema/ammende/#tabs-1-2-anchor,
Accessed date: 11 April 2019.
Norwegian Food Safety Authority, 2015. Ferskvannsfisk og kvikksølvforurensning.
Matportalen.no. The Norwegian Food Safety Authority http://www.matportalen.no/
matvaregrupper/tema/fisk_og_skalldyr/ferskvannsfisk_og_kvikksolvforurensing,
Accessed date: 11 April 2019.
Örün, E., Yalçın, S.S., Aykut, O., Orhan, G., Morgil, G.K., Yurdakök, K., Uzun, R., 2011. Breast
milk lead and cadmium levels from suburban areas of Ankara. Sci. Total Environ. 409
(13), 2467–2472. https://doi.org/10.1016/j.scitotenv.2011.02.035.
Oskarsson, A., Schütz, A., Skerfving, S., Hallén, I.P., Ohlin, B., Lagerkvist, B.J., 1996. Total and
inorganic mercury in breast milk and blood in relation to fish consumption and amal-
gam fillings in lactating women. Arch. Environ. Health 51 (3), 234–241. https://doi.
org/10.1080/00039896.1996.9936021.
Pappas, R.S., Stanfill, S.B., Watson, C.H., Ashley, D.L., 2008. Analysis of toxic metals in com-
mercial moist snuff and Alaskan iqmik. J. Anal. Toxicol. 32 (4), 281–291.
Park, J.-D., Zheng, W., 2012. Human exposure and health effects of inorganic and elemen-
tal mercury. J. Prev. Med. Public Health 45 (6), 344–352. https://doi.org/10.3961/
jpmph.2012.45.6.344.
Polder, A., Skaare, J.U., Skjerve, E., Løken, K.B., Eggesbø, M., 2009. Levels of chlorinated pes-
ticides and polychlorinated biphenyls in Norwegian breast milk (2002-2006), and
factors that may predict the level of contamination. Sci. Total Environ. 407 (16),
4584–4590. https://doi.org/10.1016/j.scitotenv.2009.04.032.
Poulin, J., Gibb, H., 2008. In: Prüss-Üstün, A. (Ed.), Mercury: Assessing the Environmental
Burden of Disease at National and Local Levels. WHO Environmantal Burden of Dis-
ease World Health Organization, Geneva, Switzerland.
Rathore, M., Singh, A., Pant, V.A., 2012. The dental amalgam toxicity fear: a myth or actu-
ality. Toxicol. Int. 19 (2), 81–88. https://doi.org/10.4103/0971-6580.97191.
Rebelo, F.M., Caldas, E.D., 2016. Arsenic, lead, mercury and cadmium: toxicity, levels in
breast milk and the risks for breastfed infants. Environ. Res. 151, 671–688. https://
doi.org/10.1016/j.envres.2016.08.027.
Schoeters, G., Den Hond, E., Zuurbier, M., Naginiene, R., van den Hazel, P., Stilianakis, N.,
Ronchetti, R., Koppe, J.G., 2006. Cadmium and children: exposure and health effects.
Acta Paediatr. Suppl. 95 (453), 50–54. https://doi.org/10.1080/08035320600886232.
Sharma, B.M., Sáňka, O., Kalina, J., Scheringer, M., 2019. An overview of worldwide and re-
gional time trends in total mercury levels in human blood and breast milk from 1966
to 2015 and their associations with health effects. Environ. Int. 125, 300–319. https://
doi.org/10.1016/j.envint.2018.12.016.
Skjelvik, J.M., 2012. Review of Norwegian Experiences with the Phase-out of Dental Amal-
gam Use. Vista Analysis, Norway. https://www.vista-analyse.no/en/publications/re-
view-of-norwegian-experiences-with-the-phase-out-of-dental-amalgam-use/
(accessed 11 April 2019). ISBN 978-82-8126-042-9.
SSB, 2017. Smoking habits, 2016. Division for Helath Statistics, Statistics Norway.
Steinnes, E., Berg, T., Uggerud, H.T., 2011. Three decades of atmospheric metal deposition
in Norway as evident from analysis of moss samples. Sci. Total Environ. 412-413,
351–358. https://doi.org/10.1016/j.scitotenv.2011.09.086.
Textor, J., Hardt, J., Knuppel, S., 2011. DAGitty: a graphical tool for analyzing causal dia-
grams. Epidemiology 22 (5), 745. https://doi.org/10.1097/EDE.0b013e318225c2be.
Thomsen, C., Stigum, H., Frøshaug, M., Broadwell, S.L., Becher, G., Eggesbø, M., 2010. De-
terminants of brominated flame retardants in breast milk from a large scale Norwe-
gian study. Environ. Int. 36 (1), 68–74. https://doi.org/10.1016/j.envint.2009.10.002.
Ursinyova, M., Masanova, V., 2005. Cadmium, lead and mercury in human milk from
Slovakia. Food Addit. Contam. 22 (6), 579–589. https://doi.org/10.1080/
02652030500135201.
Vahidinia, A., Samiee, F., Faradmal, J., Rahmani, A., Javad, M.T., Leili, M., 2019. Mercury,
lead, cadmium, and barium levels in human breast milk and factors affecting their
concentrations in Hamadan, Iran. Biol. Trace Elem. Res. 187, 32. https://doi.org/
10.1007/s12011-018-1355-5 (2019).
Vahter, M., Berglund, M., Åkesson, A., Lidén, C., 2002. Metals and women's health. Environ.
Res. 88 (3), 145–155.
Vimy, M., Hooper, D., King, W., Lorscheider, F., 1997. Mercury from maternal “silver” tooth
fillings in sheep and human breast milk. Biol. Trace Elem. Res. 56 (2), 143–152.
WHO, 2007. Fourth WHO-Coordinated Survey of Human Milk for Persistent Organic Pol-
lutants in Cooperation with UNEP - Guidelines for Developing a National Protocol.
World Health Organisation, Geneva, Switzerland.
WHO, 2010. Exposure to Lead: A Major Public Health Concern. World Health Organiza-
tion, Geneva, Switzerland (6pp).
Yalçın, S.S., Yurdakök, K., Yalçın, S., Engür-Karasimav, D., Cokun, T., 2010. Maternal and
environmental determinants of breast-milk mercury concentrations. Turk. J. Pediatr.
52 (1), 1–9.