1 s2.0 S0013935114003934 Main
1 s2.0 S0013935114003934 Main
1 s2.0 S0013935114003934 Main
Environmental Research
journal homepage: www.elsevier.com/locate/envres
Abbreviations: COPHES, COnsortium to Perform Human biomonitoring on a European Scale; CVD, Cardiovascular disease; DEMOCOPHES, DEMOnstration of a study to
COordinate and Perform Human biomonitoring on a European Scale; HBM, Human Biomonitoring; MeHg, methylmercury; PUFAs, polyunsaturated fatty acids
http://dx.doi.org/10.1016/j.envres.2014.10.029
0013-9351/& 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).
A. Castaño et al. / Environmental Research 141 (2015) 58–68 59
art ic l e i nf o a b s t r a c t
Article history: The toxicity of methylmercury (MeHg) in humans is well established and the main source of exposure is
Received 21 May 2014 via the consumption of large marine fish and mammals. Of particular concern are the potential neuro-
Received in revised form developmental effects of early life exposure to low-levels of MeHg. Therefore, it is important that pregnant
17 October 2014
women, children and women of childbearing age are, as far as possible, protected from MeHg exposure.
Accepted 20 October 2014
Within the European project DEMOCOPHES, we have analyzed mercury (Hg) in hair in 1799 mother–
Available online 7 February 2015
child pairs from 17 European countries using a strictly harmonized protocol for mercury analysis. Parallel,
Keywords: harmonized questionnaires on dietary habits provided information on consumption patterns of fish and
Human Biomonitoring marine products. After hierarchical cluster analysis of consumption habits of the mother–child pairs, the
Mercury in hair DEMOCOPHES cohort can be classified into two branches of approximately similar size: one with high fish
Sea fish
consumption (H) and another with low consumption (L). All countries have representatives in both
Shellfish
branches, but Belgium, Denmark, Spain, Portugal and Sweden have twice as many or more mother–child
Seafood products
pairs in H than in L. For Switzerland, Czech Republic, Hungary, Poland, Romania, Slovenia and Slovakia the
situation is the opposite, with more representatives in L than H.
There is a strong correlation (r¼ 0.72) in hair mercury concentration between the mother and child in
the same family, which indicates that they have a similar exposure situation. The clustering of mother–
child pairs on basis of their fish consumption revealed some interesting patterns. One is that for the same
sea fish consumption, other food items of marine origin, like seafood products or shellfish, contribute
significantly to the mercury levels in hair. We conclude that additional studies are needed to assess and
quantify exposure to mercury from seafood products, in particular. The cluster analysis also showed that
95% of mothers who consume once per week fish only, and no other marine products, have mercury levels
0.55 μg/g. Thus, the 95th percentile of the distribution in this group is only around half the US-EPA re-
commended threshold of 1 μg/g mercury in hair. Consumption of freshwater fish played a minor role in
contributing to mercury exposure in the studied cohort.
The DEMOCOPHES data shows that there are significant differences in MeHg exposure across the EU
and that exposure is highly correlated with consumption of fish and marine products. Fish and marine
products are key components of a healthy human diet and are important both traditionally and culturally
in many parts of Europe. Therefore, the communication of the potential risks of mercury exposure needs to
be carefully balanced to take into account traditional and cultural values as well as the potential health
benefits from fish consumption. European harmonized human biomonitoring programs provide an addi-
tional dimension to national HMB programs and can assist national authorities to tailor mitigation and
adaptation strategies (dietary advice, risk communication, etc.) to their country’s specific requirements.
& 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/3.0/).
n
Corresponding author.
E-mail address: castano@isciii.es (A. Castaño).
60 A. Castaño et al. / Environmental Research 141 (2015) 58–68
Fig. 2. Image of the harmonized DEMOCOPHES questionnaire on consumption habits of fish and marine products.
A. Castaño et al. / Environmental Research 141 (2015) 58–68 61
Fig. 3. Dendrogram of the hierarchical cluster analysis for fish and marine product consumption of participants in the European sample DEMOCOPHES with the two main
branches H (high consumption) and L (low consumption) and the secondary groups at the third level of dendrogram: H1, H2, H3 and L1, L2. Bar graph below each group,
showing percentages of pairs consuming SEA FISH more than weekly, SHELLFISH more than monthly, SEAFOOD PRODUCTS more than monthly and FRESHWATER FISH more than monthly.
A total of 59 pairs were excluded from the classification of fish total) and “low fish consumption” (L) branch with 990 pairs (55%
products consumption because of their incomplete questionnaires. of the total). All the top scoring pairs for any of the four questions
In Ireland, 19 pairs were excluded, because SEA FISH was consistently are in H. Moreover, considering a family habit of once per week as
reported, but there were missing answers for the rest of the items. a reference for SEA FISH (both members of the pair) and once per
The rest of the exclusions are scattered among eleven countries. month as a reference for SHELLFISH, FRESHWATER FISH and SEAFOOD, it was
Thus a final set of 1799 pairs was considered in the present ana- found that pairs reporting higher frequencies than the reference
lysis (Table 1). were all in H for SEA FISH (except three), they were ten times more
Mercury levels in the hair of participants showed large differ- abundant in H than in L for SHELLFISH and they were twice as many
ences, up to a factor of 40 in national medians, among the 17 in H than in L for SEAFOOD. Although FRESHWATER FISH presented just
participating countries. Analysis of the data clearly indicates that 1.4 more pairs above the reference in H, their consumption levels
differences in mercury levels for the European participants are were higher, even above one per week. Pairs with frequencies
associated with diet (Den Hond et al., 2015 and Tables S2 and S3 as above the reference for more than one question were mostly in H.
Supplementary material). All countries had participants in both branches, but it can be
pointed out that Belgium, Denmark, Spain, Portugal and Sweden
3.1. Cluster analysis of diet had twice as many or more pairs in H (high fish consumption)
than in L (the low fish consumption) groups, and vice versa for
Fish consumption reported in the DEMOCOPHES ques- Switzerland, Czech Republic, Hungary, Poland, Romania, Slovenia
tionnaires can be classified in two main branches and in secondary and Slovakia (Table S4).
groups. Fig. 3 and Fig. S2 show the dendrogram of the hierarchical There are no significant differences between the assignment of
cluster analysis considering the eight variables (questions B, C, D, pairs to H or L between the rural and urban locations of each
and E for each member of the pair). First, as a result of the clas- country (p 40.110), with the exceptions of Hungary (p ¼0.024) and
sification procedure, two broad branches were identified: “high Slovenia (p ¼0.005) where rural locations show lower consump-
fish consumption” (H) branch containing 809 pairs (45% of the tion levels.
Table 2
Recurrent diet patterns in pairs (both mother and child) of groups H3 and L2, according to the answers given to the DEMOCOPHES fish and marine product consumption
questionnaire. SHELLFISH and SEAFOOD PRODUCTS answers for both members of the pair are “almost never” in all six diet patterns. Mercury in hair median, 90th percentile and
percentage of subjects above the limit of quantification (LOQ) are also shown.
I II III IV V VI
Groupa L2 L2 L2 L2 H3 H3
N (pairs) 128 37 80 113 106 44
SEA FISH Mother/Child (Almost) never (Almost) never Once a month 2–3 Times per month Once a week Several times/week
FRESH WATER FISH Mother/Child (Almost) never Once a month (Almost) never (Almost) never (Almost) never (Almost) never
Hg in hair (lg/g) Mother P50 0.069 0.069 0.118 0.127 0.149 0.808
P90 0.243 0.345 0.387 0.479 0.550 2.391
4 LOQ % 53.5 49.5 59.8 74.3 75.0 84.9
Hg in hair (lg/g) Child P50 0.061 oLOQ 0.078 0.087 0.094 0.766
P90 0.168 0.178 0.285 0.472 0.473 1.918
4 LOQ % 52.3 49.4 38.0 68.0 73.5 74.5
Table 3 Likewise, the low fish consumption branch L was divided into a
Correlation (Kendall's tau-b) between mothers' and children's frequency of con- small group (L1, 72 pairs) and a mainstream group (L2, 918 pairs).
sumption of SEA FISH, SHELLFISH, SEAFOOD PRODUCTS and FRESHWATER FISH and mercury in hair
Within the L branch, the group L1 includes pairs with an in-
(μg/g). Correlation within each of the main groups according to cluster classification
represented in Fig. 2 (H1,H2, H3, L1 and L2). termediate range of SEA FISH consumption. None of the pairs an-
swered “almost never” to all B, C, D and E questions in L1. The
Group N SEA FISH SHELLFISH SEAFOOD PRODUCTS FRESHWATER FISH Hg in hair most prominent feature within the L groups is the difference in
n n n n consumption of SEAFOOD PRODUCTS: in L1, 21 pairs out of 72 (29%) had
H1 102 0.599 0.465 0.621 0.649 0.655n
H2 44 0.693n 0.445n 0.531n 0.048 0.592n consumption levels above the reference of once per month,
H3 663 0.667n 0.536n 0.509n 0.716n 0.535n whereas there were none in L2.
L1 72 0.283n 0.185n 0.010 0.427n 0.442n L2 grouped participants with the lowest consumption in the
L2 918 0.424n 0.589n 0.455n 0.699n 0.429n
whole European sample. Half the pairs in the group answered “2
Total 1858 0.678n 0.598n 0.610n 0.748n 0.545n
or 3 times per month” or less for SEA FISH AND “almost never” for
n
po 0.05. consumption of SHELLFISH, SEAFOOD PRODUCTS and FRESHWATER FISH.
Table 4
Results for mercury in hair (μg/g) for mothers and children in each of the groups, and selected subgroups utilized for comparisons. Groups were obtained from cluster
analysis of fish and marine products diet. Median (P50), 90th percentile (P90) and percentage of samples above the limit of quantification (LOQ).
Mothers Children
Group (N) Subgroup (N) P50 P90 Max 4LOQ % P50 95% CI P90 95%CI Max 4LOQ %
95% CI 95% CI
H1 (102) 0.630 2.770 8.90 97.0 0.370 1.560 6.60 93.1
0.442–0.877 2.000–3.400 0.280–0.494 1.164–2.764
H1a (88) 0.501 2.100 8.90 96.6 0.310 1.300 6.60 92.0
0.331–0.770 1.515–3.592 0.209–0.406 0.875–2.390
H1a1 (71) 0.400 1.671 4.50 95.7 0.232 0.898 2.80 90.0
0.233–0.683 1.305–2.094 0.168–0.345 0.702–1.791
H1b (14) 1.724 3.400 3.40 100 0.950 3.700 4.20 100
1.211–3.217 2.871–3.400 0.645–1.433 1.400–4.200
N ¼number of pairs, P50¼ 50th percentile, P90¼ 90th percentile, and CI ¼ confidence interval.
64 A. Castaño et al. / Environmental Research 141 (2015) 58–68
H3 group, representing the 37% of the studied population, consumption (almost everyone in H1b and almost nobody in H1a
consumed fish and/or marine products (B, C, D, E questions) on a having SEAFOOD PRODUCTS monthly) while the consumption frequency
weekly basis and its median mercury values are 0.4 μg/g. In fact of SEA FISH is the same, and 3 times more mercury in hair both in
except for the H2 group, the P50 values for the five main groups mothers and their children of H2 with regard to H3a1 or of H1b
were below 1 μg/g mercury in hair. with regard to H1a (Table 4).
Median as well as P90 values are higher for mothers than for Consumption of SHELLFISH also shows a certain influence on the
children. The correlation between mother and child mercury levels increase of Hg levels as was observed in a number of pair-wise
was a bit lower in low consumption groups than in higher con- group comparisons. To exemplify this, two subgroups of H3 (H3a1
sumption ones (Table 3). Correlation between mother and child in and H3b) were compared (Table 5B). When comparing H3a1 and
H3b SHELLFISH consumption is significantly different, and SEA FISH and
mercury shows wider variation by country (range 0.195–0.494)
FRESHWATER FISH are consumed at the same level. Mercury in hair was
than by diet group.
significantly higher in the subgroup with higher SHELLFISH con-
Mercury levels increased in relation to the frequency of SEA FISH
sumption (Table 5B).
consumption in study participants reporting no consumption of
Therefore consumption of SHELLFISH and SEAFOOD PRODUCTS need to
SHELLFISH and SEAFOOD PRODUCTS (Table 2). 90% of the women consuming
be further investigated, in addition to already established con-
only SEA FISH once per week (pattern V) (independently of the tribution of SEA FISH with respect to mercury exposure.
species or the size) had mercury levels of 0.55 μg/g and 50% of the There are also examples in the material of groups that, al-
mothers who consume SEA FISH several times per week (pattern VI) though having significant differences in SEA FISH and FRESHWATER FISH
had mercury levels of 0.80 μg/g. 89% of the mothers in the high consumption, showed no significant differences in mercury levels,
fish consumer group (pattern VI) are at the benchmark value set for example when comparing subgroups H1a1 and H3a1
up by JECFA/WHO 1.9 μg/g (EFSA, 2012) (Table 2). (Table 5C). In this case SEA FISH was consumed almost twice as fre-
All differences in mercury levels between pairs of the five main quently in H3a1 compared to H1a1, with no visible difference in
groups are significant (p o0.05) except for mothers in H3–L1 (the mercury level between the two groups. The consumption of
lowest high consumer group and the highest low consumer group) FRESHWATER FISH (98% more frequent) had no influence on mercury
(p ¼0.153). levels.
H1 and H2 have significantly different levels of mercury in hair The lack of association of FRESHWATER FISH consumption with the
despite having no significant differences in SEA FISH consumption levels of mercury was confirmed in H2 and H1b comparisons. In
and this was the driver to investigate the influence of other dietary this case, SEA FISH and SHELLFISH were equally frequent in the diets of
items on mercury levels. members of both subgroups but there was a significant difference
For that aim, some subgroups of the main five have been se- in the frequency of FRESHWATER FISH in the diet (92% more frequent in
lected from the lower branches of the dendrogram of our cluster H1b both in mothers and children), and no significant effect was
analysis (Table 4). These subgroups show either significantly dif- seen on mercury levels in hair for mothers neither for children
(p ¼0.131 and p ¼0.313, respectively) (Table 4).
ferent mercury levels although the same SEA FISH consumption fre-
quency, or the opposite way, there were significant differences in
SEA FISH consumption but with no differences in mercury in hair. The
4. Discussion
possible contribution of amalgam fillings, their occurrence and
their number, have been tested. Both have been found to be non- In this paper we have compared results both for dietary habits
significant with respect to the mercury levels measured in hair and mercury in hair for the first time in a harmonized way in
(Fisher exact test for the proportion of mothers with amalgam mother–child pairs in 17 European countries. Data are based on
fillings p 40.142, Wilcoxon–Mann–Whitney for their number European dietary habits and on fish marketed and consumed in
p 40.057). Europe. This was possible thanks to the use of a commonly de-
Significant differences in Hg levels although similar SEA FISH, veloped protocol (target population and questionnaires), a full
intake were observed in a number of group-pair comparisons. This training scheme for field work as well as stringent quality control
is exemplified when a subgroup of H3 (H3b) is compared with H2. programs for chemical and data analysis.
Both groups are described in Table 5A, in which the proportion of In the overview of results from the DEMOCOPHES project (Den
mothers and children having each of the food items more fre- Hond et al., 2015), we report that mercury levels in hair of parti-
quently than the reference (once per week for SEA FISH, once per cipants (mother–child pairs) varied with more than a factor of 50
month for SHELLFISH, SEAFOOD PRODUCTS and FRESHWATER FISH), are shown between the lowest (Hungary, geometric mean (GM) 0.02 μg/g
along with median values of mercury in hair. Incidence of amal- hair) and the highest (Portugal, GM 1.03 μg/g hair) with an overall
gam fillings is also shown for reference. The consumption of SEA FISH geometric mean in the DEMOCOPHES material of 0.14 μg/g, based
is high in both groups (50% of the members consume more than on values from the children. The mothers had higher mercury
levels than their children but followed the same pattern. Fish
once per week) with no significant differences between the two
consumption and social status were identified as important and
subgroups (p ¼0.201 for mothers and 0.137 for children). However,
independent determinants of mercury levels, both in mothers and
mercury in hair is more than twice in participants from H2 with
their children, which confirms results from other studies (Ma-
regard to those from H3b. The consumption frequency of SEAFOOD
haffey, 2004). Although France, Greece and Italy did not participate
PRODUCTS is what separates these groups and it seems that SEAFOOD
in the DEMOCOPHES project, recent biomonitoring studies on hair
PRODUCTS is the potential determinant for the increase in the mer-
levels of mercury in women from France (0.60 μg/g), Greece
cury levels. (1.12 μg/g) and Italy (0.77 μg/g) show that they fall well within the
Similar results have been observed in many other pairs of range of the DEMOCOPHES countries in which fish and other
groups, for example between groups H2, and H3a1 with a sig- marine products constitute an important part of the diet (Frery
nificantly (po 0.001) wide gap in their monthly SEAFOOD PRODUCTS et al., 2010; Miklavčič et al., 2013). The wide-spread difference in
consumption (almost everyone in H2 and almost nobody in H3a1 mercury exposure in the European population can be related to
having SEAFOOD PRODUCTS monthly), or between groups H1b and H1a dietary habits and in particular to consumption of fish and other
also with significantly (p o0.001) different SEAFOOD PRODUCTS products from the aquatic environment. With respect to mother–
66 A. Castaño et al. / Environmental Research 141 (2015) 58–68
child pairs, there is a strong correlation (r ¼0.72) in hair mercury product based on several fish species such as Alaska Pollock, Pa-
concentration between the mother and child (Den Hond et al., cific whiting, Tilapia and other species of less market value and it
2015) which shows that there is a common source of exposure in forms the bases for food items such as imitation crab meat, sat-
the studied families. Most likely this is the diet since mercury le- sumi-age/tenpura, hanpen, and fish sausage (Tina et al., 2010).
vels in hair reflect primarily exposure to MeHg from food sources Depending on the origin of surimi products, they may contribute
(Sherman et al., 2013). We also found that mercury from amalgam to the body burden of mercury. There could be a risk that they
fillings is of minor importance (Table 5) with respect to hair levels originate from environments with elevated mercury levels or that
as also reported by others (Sherman et al., 2013). some of the fish species used are top predators in the marine food
An important part of the study was the questionnaire data on chain. Eurostat data from 2011 and 2012 showed an increase of
the participants' consumption frequencies of fish and other pro- 69% in volumes of miscellaneous aquatic products imported from
ducts from the aquatic environment. The weakness of these types extra-EU countries, and it should be mentioned that no imports of
of questionnaires is that they are a retrospective survey in which seaweed and other algae were reported in 2011, but they totalled
the mothers have to remember what and when they ate the dif-
53.000 tonnes in 2012 (EUMOFA, 2014). Clearly, there is a need for
ferent items covered and to what extent their children ate them.
more extensive monitoring of these products to obtain a better
Probably the most certain reply is when the answer is “never” – in
picture of their role as potential sources of mercury exposure.
this case the respondents probably know for sure. Therefore, the
There were also groups of consumers that had lower mercury
questionnaire provided only approximate information on fish
levels than expected on basis of their consumption of SEA FISH and
consumption and was not a precise measure of the fish ingested by
SEAFOOD PRODUCTS. The species of fish consumed were not reported in
an individual. Despite this limitation, the material still allows for
the questionnaires and therefore it is difficult to make exact cor-
analysis of consumption patterns across the DEMOCOPHES coun-
relations. However, it is well known that type of fish, the size, age
tries and of items that may have an additional influence on the
levels of mercury measured in hair. and the position in the food chain are important with respect to
There is a clear pattern in consumption of fish and other mercury content. Top predators accumulate the highest levels
aquatic products across Europe, with relatively higher frequency in since mercury is concentrated along the food chain (NRC, 2000).
the Mediterranean and North European countries and a lower The metal is bioaccumulated over a lifetime and larger and older
frequency in Central European countries. Based on questionnaire specimens will have higher concentrations than younger and
answers we could separate mercury exposure due to SEA FISH con- smaller ones. Therefore active pelagic top predators like tuna,
sumption from FRESHWATER FISH consumption. In the results there was swordfish or long-lived species that such as sharks attain high
no evidence that consumption of FRESHWATER FISH contributes to mercury levels. The mercury values reported can be assumed to
mercury levels in mothers and their children. This finding is not represent exposure from fish landed in Europe by EU fishing fleets.
surprising since the market for FRESHWATER FISH is very limited in The majority of the fish marketed in Europe comes from North-
Europe with 5.3% of total sales of aquatic products while seawater East Atlantic (71.5%) and the Eastern Central Atlantic (13.4%)
fish represents 73.5% and the remaining 21.2% is other types of (EUROSTAT, 2014). According to the European Commission Reg-
aquatic products (EUMOFA, 2014). In some European countries ulation (EC) No. 78/2005 of January 19, 2005 the maximum al-
FRESHWATER FISH could be a significant source of mercury exposure. lowed level of mercury in the species anglerfish, swordfish and
Swedish FRESHWATER FISH (pike, Esox lucius, perch, Perca fluviatilis) tuna is 1 mg/kg. For other fishery products and fish muscle the
contain significant amounts of methylmercury, in the range of 0.5– maximum allowed level of mercury is 0.5 mg/kg.
1.0 mg/kg, because of historical mercury contamination (Åkerblom Individual susceptibility can also play a role in mercury accu-
and Johansson, 2008). This exposure was not reflected in the mulation. In fact, inter-individual variation in mercury biomarkers
Swedish data from the DEMOCOPHES study probably because may be partly explained by genetic variability. This may explain
consumption of FRESHWATER FISH is small and concentrated to local some of the exceptional cases that were identified in the present
populations, which were not captured in the DEMOCOPHES material. For example one mother in the L1 cluster reported that
sample. she “almost never” consumed fish or marine products. She re-
In the DEMOCOPHES material, the group H3, with 37% of the ported that she ate fish and shellfish “once per month or less” and
studied sample, reported consumption of fish and marine products “almost never” other SEAFOOD PRODUCTS. As mentioned, a “never” an-
once a week or more. The mercury levels in this group are below
swer in the questionnaire could be considered quite reliable. She
1.65 μg/g for 90% of the mothers. When analyzing the contribution
had 2.8 mg/g mercury in the hair which is the range of high SEA FISH
of the different food items, we found that 90% of those who ate
consumers. These exceptions in single cases could be associated
fish but no other marine products had mercury values below
with individual susceptibility or a genetic polymorphism (Basu
0.55 μg/g, and half of the group (P50) had values below 0.15 μg/g.
et al., 2014; Julvez and Grandjean, 2013).
Furthermore, 50% of the mothers consuming SEA FISH several times
Mercury contamination of the human food chain is a significant
per week had mercury values below 0.81 μg/g (Table 2). This
problem for human health and wellbeing. Fish and shellfish are
is valuable information for public health authorities when
important components in a healthy diet and have a high cultural
developing dietary recommendations. For example, the US-EPA
recommended level for women in childbearing age is 1 μg mercury and social value in many parts of Europe. They are central in-
per gram hair (US-EPA, 2001) which means that the whole group gredients in the so-called “Mediterranean diet”, which today is
studied here (eating only SEA FISH once per week independently of recommended to mitigate obesity and cardio-vascular disease.
the species and size) and half of the group of frequent consumers Unfortunately these products can be a significant source of mer-
would be on the “safe side”. Furthermore, if we consider the JECFA/ cury exposure. There is a risk that people stop eating fish and
WHO recommended levels of 1.9 μg/g, 89% of the higher con- shellfish because of the perceived health risks of mercury, which
sumers (eating only SEA FISH) fall below this limit (Table 2). would be highly undesirable from a public health point of view.
A very clear, additional pattern comes out from the analysis. The first recommendation is to focus the advice on the vulnerable
SEAFOOD PRODUCTS, and to a lesser extent SHELLFISH, contributes sig- groups, which in the case of mercury, is pregnant women. Well-
nificantly to the mercury exposure, both in mothers and their designed communications strategies are therefore important in
children. The SEAFOOD PRODUCTS group includes algae, seaweed and order to correctly communicate both the risks and benefits to
surimi that are quite common in “modern diets”. Surimi is a food human health. An example of this comes from the Bermuda
A. Castaño et al. / Environmental Research 141 (2015) 58–68 67
Åkerblom, S., Johansson, K., 2008. Kvicksilver i svensk insjö fisk – variationer i tid
och rum. Report 2008/8. Swedish Agricultural University, Institute for En-
5. Conclusions vironmental Analysis (in Swedish).
Basu, N., Goodrich, J.M., Head, J., 2014. Ecogenetics of mercury: From genetic
polymorphisms and epigenetics to risk assessment and decision-making. En-
There is a widespread difference in mercury exposure in the
viron. Toxicol. Chem. 33, 1248–1258.
European population and the difference is very likely related to Becker, K., Seiwert, M., Casteleyn, L., Joas, R., Joas, A., Biot, P., Aerts, D., Castaño, A.,
dietary habits and in particular to consumption of fish and other Esteban, M., Angerer, J., Koch, H.M., Schoeters, G., Hond, E.D., Sepai, O., Exley, K.,
Knudsen, L.E., Horvat, M., Bloemen, L., Kolossa-Gehring, M., 2014. A systematic
products from the marine environment. The frequency of fish and
approach for designing a HBM pilot study for Europe. Int. J. Hyg. Environ.
aquatic products consumption shows a clear pattern across Europe Health 217, 312–322.
with a relatively higher frequency in the Mediterranean and North Casteleyn, L., Dumez, B., Becker, K., Kolossa-Gehring, M., Den Hond, E., Schoeters, G.,
Castaño, A., Koch, H.M., Angerer, J., Esteban, M., Exley, K., Sepai, O., Bloemen, L.,
European countries and a lower frequency in Central European Horvat, M., Knudsen, L.E., Joas, A., Joas, R., Biot, P., Koppen, G., Dewolf, M.-C.,
countries. The hair mercury levels also show the same general Katsonouri, A., Hadjipanayis, A., Cerna, M., Krskova, A., Schwedler, G., Fiddicke,
pattern. The mercury levels in the mothers and their children are U., Nielsen, J.K.S., Jensen, J.F., Rudnai, P., Kozepesy, S., Mulcahy, M., Mannion, R.,
Gutleb, A.C., Fischer, M.E., Ligocka, D., Jakubowski, M., Reis, M.F., Namorado, S.,
strongly correlated indicating a common source of exposure, most Lupsa, I.-R., Gurzau, A.E., Halzlova, K., Jajcaj, M., Mazej, D., Tratnik Snoj, J., Po-
likely the diet. There was no significant contribution from dental sada, M., Lopez, E., Berglund, M., Larsson, K., Lehmann, A., Crettaz, P., Aerts, D.,
amalgams to hair mercury levels. The mercury exposure is related 2015. A pilot study on the feasibility of European harmonized human biomo-
nitoring: challenges and opportunities. Environ. Res. 141, 2–13.
to consumption of marine fish and seafood and the contribution Choi, A.L., Mogensen, U.B., Bjerve, K.S., Debes, F., Weihe, P., Grandjean, P., Budtz-
from freshwater fish was minor in the studied sample. The ma- Jørgensen, E., 2014. Negative confounding by essential fatty acids in methyl-
jority (a 95%) of those consuming fish once a week or more have mercury neurotoxicity associations. Neurotoxicol. Teratol. 42, 85–92.
Den Hond, E., Govarts, E., Willems, H., Smolders, R., Casteleyn, L., Kolossa-Gehring,
mercury levels (0.55 mg/g hair) well below the health based M., Schwedler, G., Seiwert, M., Fiddicke, U., Castaño, A., Esteban, M., Angerer, J.,
limit values recommended by US-EPA (1 mg/g hair) and by WHO Koch, H.M., Schindler, B.K., Sepai, O., Exley, K., Bloemen, L., Horvat, M., Knudsen,
(1.9 mg/g hair) for the most vulnerable population group. Seafood L.B., Joas, A., Joas, R., Biot, P., Aerts, D., Koppen, G., Katsonouri, A., Hadjipanayis,
A., Krskova, A., Maly, M., Mørck, T.A., Rudnai, P., Kozepesy, S., Mulcahy, M.,
products and shellfish were found to significantly contribute to Mannion, R., Gutleb, A.C., Fischer, M.E., Ligocka, D., Jakubowski, M., Reis, M.F.,
mercury exposure and this potential exposure source should be Namorado, S., Gurzau, A.E., Lupsa, I.R., Halzlova, K., Jajcaj, M., Mazej, D., Tratnik,
further monitored. As mercury will be present in the environment J.S., López, A., López, E., Berglund, M., Larsson, K., Lehmann, A., Crettaz, P.,
Schoeters, G., 2015. First steps toward harmonised human biomonitoring in
for many years to come, human biomonitoring programs, like Europe: demonstration project to perform human biomonitoring on a Eur-
DEMOCOPHES, are important tools in assessing current population opean scale. Environ. Health Perspect 123, 255–263.
exposure and in discovering trends and patterns related to mer- Dewailly, E., Rouja, P., Forde, M., Peek-Ball, C., Côté, S., Smith, E., Drescher, O., Ro-
bertson, L., 2012. Evaluation of a public health intervention to lower mercury
cury mitigation policies (Minamata convention), life style and food exposure from fish consumption in Bermuda. PLoS ONE 7, e47388.
consumption. This information is essential for assessing the ef- Esteban, M., Schindler, B.K., Jiménez-Guerrero, J.A., Koch, H.M., Angerer, J., Rivas, T.
C., Rosado, M., Gómez, S., Casteleyn, L., Kolossa-Gehring, M., Becker, K., Scho-
fectiveness of policies and for advisory authorities in developing
eters, G., Den Hond, E., Bloemen, L., Sepai, O., Exley, K., Knudsen, L.E., Horvat,
relevant consumer recommendations with respect to products M., Joas, A., Joas, R., Aerts, D., Biot, P., Borošová, D., Davidson, F., Dumitrascu, I.,
from the aquatic environment. Fischer, M.E., Grander, M., Janasik, B., Jones, K., Kašparová, L., Larssen, T., Naray,
M., Nielsen, F., Hohenblum, P., Pinto, R., Pirard, C., Plateel, G., Tratnik, J.S.,
Wittsiepe, J., 2015. EQUAS reference laboratories, In: Castaño A. Mercury ana-
lysis in hair: Comparability and quality assessment within the transnational
COPHES/ DEMOCOPHES project. Environ. Res. 141, 23–29.
Funding EUMOFA database. 〈http://ec.europa.eu/fisheries/market-observatory/home〉 (ac
cessed 10.07.14).
The DEMOCOPHES Project (LIFE09 ENV/BE/000410) is jointly EUROSTAT. 2014. Fishery statistics. 〈http://epp.eurostat.ec.europa.eu/statistics_ex
plained/index.php/Fishery_statistics〉 (accessed 14.03.14).
funded by the European Commission programme LIFE þ (50%), EFSA, 2012. Scientific opinion on the risk for public health related to the presence of
with the remaining 50% being provided by the participating mercury and methylmercury in food. EFSA J 10, 2985–3136.
countries (see the national implementation websites accessible via Fiddicke, U., Becker, K., Schwedler, G., Seiwert, S., Joas, R., Joas, A., Biot, P., Aerts, D.,
Casteleyn, L., Castaño, A., Esteban, M., Angerer, J., Koch, H.M., Schoeters, G., Den
http://www.eu-hbm.info/democophes/project-partners). The CO- Hond, E., Sepai, O., Exley, K., Knudsen, L.E., Horvat, M., Bloemen, L., Katsonouri,
PHES Project that provided the operational and scientific frame- A., Hadjipanayis, A., Cerna, M., Krskova, A., Mørck, T.A., Rudnai, P., Kozepesy, S.,
work was funded by the European Commission Seventh Frame- Mulcahy, M., Mannion, R., Gutleb, A.C., Fischer, M., Ligocka, D., Jakubowski, M.,
Namorado, S., Reis, M.F., Lupsa, I.R., Gurzau, A.E., Halzlova, K., Jajcaj, M., Mazej,
work Programme-DG Research (Grant agreement no. 244237- D., Tratnikj, J.S., Rivas, T.S., Gómez, S., Berglund, M., Larsson, K., Lehmann, A.,
www.eu-hbm.info). This work would not have been possible Crettaz, P., Kolossa-Gehring, M., 2015. Lessons learnt on recruitment and
without the additional funding from the Spanish Ministry of fieldwork from a pilot European human biomonitoring survey. Environ. Res.
141, 14–22.
Agriculture, Food and Environment (MAGRAMA) and The Institute Frery, N., Saoudi, A., Garnier, R., Zeghnoun, A., Falq, G., Guldner, L., 2010. Exposure
of Health Carlos III (ISCIII) Agreement, SEG 1112/10. of the French Population to Environmental Pollutants – Environmental
68 A. Castaño et al. / Environmental Research 141 (2015) 58–68
Components of the French National Survey on Nutrition and Health – Initial Miklavčič, A., Casetta, A., Snoj Tratnik, J., Mazej, D., Krsnik, M., Mariuz, M., Sofianou,
Results. French Institute for Public Health Surveillance, Saint-Maurice (Fra). K., Spirić, Z., Barbone, F., Horvat, M., 2013. Mercury, arsenic and selenium ex-
Harkins, D., Susten, A.S., 2003. Hair analysis: exploring the state of the science. posure levels in relation to fish consumption in the Mediterranean area. En-
Environ. Health. Perspect. 111, 576–578. viron. Res. 120, 7–17.
Joas, R., Casteleyn, L., Biot, P., Kolossa-Gehring, M., Castano, A., Angerer, J., Schoeters, Myers, G.J., Davidson, P.W., Cox, C., Shamlaye, C., Palumbo, D., Cernichiari, E.,
G., Sepai, O., Knudsen, L.E., Joas, A., Horvat, M., Bloemen, L., 2012. Harmonised Sloane-Reeves, J., Wilding, G.E., Kost, J., Haung, Li-S., Clarkson, T.W., 2003.
human biomonitoring in Europe: activities towards an EU HBM framework. Int. Prenatal methylmercury exposure from ocean fish consumption in the Sey-
J. Hyg. Environ. Health. 215, 172–175. chelles child development study. Lancet 361, 1686–1692.
Johnson, R.A., Wichern, D.W., 1988. Applied Multivariate Statistical Analysis, Second NRC (National Research Council), 2000. Toxicological Effects of Methylmercury.
Edition Prentice Hall International Inc., New Jersey, USA. National Academy Press, Washington, DC.
Julshamn, K., Andersen., A., Ringdal, O., Mørkøre, J., 1987. Trace elements intake in Schoeman, K., Bend, J.R., Hill, J., Nash, K., Koren, G., 2009. Defining a lowest ob-
the Faroe Islands. I. Element levels in edible parts of pilot whales (Globicephalus servable adverse effect hair concentrations of mercury for neurodevelopmental
meleanus). Sci. Total Environ. 65, 53–62. effects of prenatal methylmercury exposure through maternal fish consump-
Julvez, J., Grandjean, P., 2013. Genetic susceptibility to methylmercury develop- tion: a systematic review. Ther. Drug Monit. 31, 670–682.
mental neurotoxicity matters. Front. Genet. 4, 278. Selin, N.E., 2009. Global biogeochemical cycling of mercury: a review. Annu. Rev.
Karagas, M.R., Choi, A.L., Oken, E., Horvat, M., Schoeny, R., Kamai, E., Cowell, W., Environ. Resour. 34, 43–63.
Grandjean, P., Korrick, S., 2012. Evidence on the human health effects of low- Sherman, L.S., Blum, J.D., Franzblau, A., Basu, N., 2013. New insight into biomarkers
level methylmercury exposure. Environ. Health Perspect. 120, 799–806. of human mercury exposure using naturally occurring mercury stable isotopes.
Kjellstrom, T., Kennedy, P., Wallis, S., Mantell, C., 1986. Physical and mental devel- Environ. Sci. Technol. 47, 3403–3409.
opment of children with prenatal exposure to mercury from fish. Stage 1 pre- Tina, N., Nurul, H., Ruzita, A., 2010. Surimi-like material: challenges and prospects.
liminary tests at age 4, Solna, National Swedish Environmental Board. (Report Int. Food Res. J. 17, 509–517.
number 3080). US EPA, 2001. Water Quality Criterion for the Protection of Human Health: Me-
Kurland, L.T., Faro, S.N., Siedler, H., 1960. Minamata disease. The outbreak of a thylmercury. US Environmental Protection Agency.
neurologic disorder in Minamata, Japan, and its relationship to the ingestion of Valent, F., Mariuz, M., Bin, M., Little, D., Mazej, D., Tognin, V., Tratnik, J., McAfee, A.J.,
seafood contaminated by mercuric compounds. World Neurol. 1, 370–395. Mulhern, M.S., Parpinel, M., Carrozzi, M., Horvat, M., Tamburlini, G., Barbone, F.,
Lamborg, C.H., Hammerschmidt, C.R., Bowman, K.L., Swarr, G.J., Munson, K.M., 2013. Associations of prenatal mercury exposure from maternal fish con-
Ohnemus, D.C., Lam, P.J., Heimbürger, L.E., Rijkenberg, M.J.A., Saito, M.A., 2014. sumption and polyunsaturated fatty acids with child neurodevelopment: a
A global ocean inventory of anthropogenic mercury based on water column prospective cohort study in Italy. J. Epidemiol. 23, 360–370.
measurements. Nature 512, 65–68. WHO, 1996. Biological Monitoring of Chemical Exposure in the Workplace, vol. 1.
Mahaffey, K.R., 2004. Fish and shellfish as dietary sources of methylmercury and World Health Organization.
the omega-3 fatty acids, eicosahexaenoic acid and docosahexaenoic acid: risks Yorifuji, T., Tsuda, Toshihide, Harada, M., 2013. Minamata disease: a challenge for
and benefits. Environ. Res. 95, 414–428. democracy and justice, Late Lessons from Early Warnings: Science, Precaution,
Mason, R.P., Choi, A.L., Fitzgerald, W.F., Hammerschmidt, C.R., Lamborg, C.H., Soer- Innovation. European Environment Agency, Copenhagen, Denmark p. 92,
ensen, A.L., Sunderland, E.M., 2012. Mercury biogeochemical cycling in the http://www.eea.europa.eu/publications/late-lessons-2 (accessed 12.03.14).
ocean and policy implication. Environ. Res. 119, 101–107.