Chemosphere 173 (2017) 572e579

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Chemosphere
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Metals in edible seaweed

C. Rubio a, *, G. Napoleone a, G. Luis-Gonza

lez a, A.J. Gutie

rrez a, D. Gonza

lez-Weller a, b,
a a
A. Hardisson , C. Revert
a
Area de Toxicologa, Universidad de La Laguna, 38071 La Laguna, Tenerife, Canary Islands, Spain
b
Health Inspection and Laboratory Service, Servicio Canario de Salud, 38006 S/C de Tenerife, Canary Islands, Spain

h i g h l i g h t s

Analysis of 20 metals was performed by ICP-OES.

Red seaweeds showed higher concentrations of trace and toxic metals.

Porphyra genera accumulated more metals than the other seaweed genera.

Seaweeds are a source of essential dietary elements, particularly Mg and Fe.

Seaweed consumption does not lead to signicant intake of toxic metals.

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

Article history: The concentration levels of 20 metals were analyzed by ICP-OES in edible seaweed (Chondrus, Eisenia,
Received 16 October 2016 Gelidium, Himanthalia, Laminaria, Palmaria, Porphyra, Undaria), from two origins (Asia vs EU) according
Received in revised form to their cultivation practices (conventional vs organic). Red seaweed showed higher concentrations of
11 January 2017
trace and toxic elements. Porphyra may be used as a potential bioindicator for metals. Signicant dif-
Accepted 11 January 2017
ferences were found between the Asian vs European mean contents. The mean Cd level from the con-
Available online 12 January 2017
ventional cultivation (0.28 mg/kg) was two points higher than the organic cultivation (0.13 mg/kg). A
Handling Editor: Petra Petra Krystek daily consumption of seaweed (4 g/day) contributes to the dietary intake of metals, mainly Mg and Cr.
The average intakes of Al, Cd and Pb were 0.064, 0.001 and 0.0003 mg/day, respectively. Based on ob-
Keywords: tained results, this study suggests that exposure to the toxic metals analyzed (Al, Cd and Pb) through
Food analysis seaweed consumption does not raise serious health concerns, but other toxic metals should be
Seaweed monitored.
Metals 2017 Published by Elsevier Ltd.
Inductively coupled plasma optical emission
spectrometry (ICP-OES)
Dietary intake

1. Introduction
Since ancient times, seaweed has been part of the diet (Jime
nez-
Escrig et al., 2011; Khan et al., 2015). Several edible varieties of
seaweed are known world-wide by names such as Kombu (Lami-
naria spp.), Wakame (Undaria pinnatda) and Nori (Porphyra spp.).
Seaweed has been used in pharmaceutical and cosmetic products,
as well as in the food industry and agriculture (Go
mez-Ordo

n~ ez

nez-Escrig et al., 2011; Khan et al., 2015).
et al., 2010; Jime
Nowadays, the direct consumption of seaweed is increasingdue
* Corresponding author.
E-mail address: crubio@ull.edu.es (C. Rubio).
to its nutritional value and health benets (Rupe
rez, 2002). Edible
marine algae are known for their richness in polysaccharides,
proteins, dietary ber, polyunsaturated fatty acids, vitamins B2 and
B12, as well as certain minerals, mainly magnesium, sodium and
iron (Bocanegra et al., 2009). Moreover, seaweeds used in food
technology for the acquisition of low-calorie food (Murata and
Nakazoe, 2001) and might be important in body weight control,
as well as in the prevention of gastrointestinal and cardio-vascular
diseases (Bocanegra et al., 2009; Li et al., 2011; Taboada et al., 2012).
Several studies show that safety hazards for seaweed may include
iodine, alpha-naphthoavones (ANFs), heavy metals, radioactive
isotopes, ammonium, dioxins, and pesticides (van der Spiegel et al.,
2013). The EFSA (European Food Safety Agency) Panel on Con-
taminants in the Food Chain (CONTAM PANEL) carries out risk

http://dx.doi.org/10.1016/j.chemosphere.2017.01.064
0045-6535/ 2017 Published by Elsevier Ltd.
 C. Rubio et al. / Chemosphere 173 (2017) 572e579
assessment on contaminants in food and feed. The task of the
CONTAM Panel is to assess whether or not exposure to a chemically
contaminated food is likely to be associated with adverse health
effects in the European population (Alexander et al., 2012). The
EFSA CONTAM PANEL believes that the exposure assessment of
seaweed, as a source for signicant levels of iodine, and possible
recommendations for the consumption of seaweed should be
conducted on a national (or even at the regional) level (EFSA, 2006).
The consumption of seaweed is subject to specic regulation
and the details of its chemical composition and variation among
species are required to obtain authorization for its use in human
nutrition. The European Commission Regulations (EC) N 629/2008
(EC, 2008) and (EC) N 488/2014 (EC, 2014) set maximum levels for
certain contaminants such as Cd and Pb in different foods but
maximum levels of toxic metals were not xed for seaweed.
However, France was the rst European country to establish a
specic regulation concerning the use of seaweed for human con-
sumption and French legislation has set a maximum level for Cd in
dehydrated seaweed of 0.5 mg/kg dry weight (Besada et al., 2009).
Seaweeds currently considered as a novel food and a novel dietary
habit in Spain but it is still regulated by a 1978 canned vegetables
group legislation (RD 2420/78). For the purposes of controlling the
maximum limit of contaminants and there are no specic regula-
tions for seaweed or its derived products probably because its
consumption is still limited in Spain.
Diet constitutes an important source of metals for humans
(Rubio et al., 2005, 2006, 2012; Gonza
lez Weller et al., 2013; Luis
et al., 2014, 2014b; Dorta et al., 2015; Luis Gonza
lez et al., 2015).
Several metals such as Mg, Cu and Fe are essential elements for
living organisms because of their important role as coenzymes but
other metals, such as Al, Cd and Pb, are non-essential, toxic ele-
ments of particular concern as food contaminants for their poten-
tial toxicity even at low concentrations.
The study of metal contents of seaweed is a valuable eld of
research, which is indispensable for both safety assessment as well
as knowledge of their nutritional value. Several authors have
mentioned that the capacity of seaweed to accumulate metals de-
pends on a variety of factors such as location, wave exposure,
temperature, salinity, light, pH, nitrogen availability, season, age of
the plant, metabolic processes and the afnity of the plant for each
element (Sa
nchez-Rodrguez et al., 2001; Almeda et al., 2006;
Smith et al., 2010; Akcali and Kucuksezgin, 2011; Brito et al.,
2012; Chakraborty et al., 2014; Astorga-Espan ~ a et al., 2015).
Graphite furnace atomic absorption spectrometry (GF-AAS)
(Almeda et al., 2002 and Almeda et al., 2006), ame atomic ab-
sorption spectrometry (FAAS) (Laib and Leghouchi, 2012), instru-
mental neutron activation analysis (INIA) (Sa
nchez-Rodrguez et al.,
2001), inductively coupled plasma optical emission spectrometry
(ICP-OES) (Moreda-Pin ~ eiro et al., 2007; Larrea-Marn et al., 2010;
Romars-Hortas et al., 2010) or inductively coupled plasma-mass
spectrometry (ICP-MS) (Li et al., 2011; Romars-Hortas et al.,
2012) have been used to determine metals in seaweed.
The objectives of this study were (1) to analyze the contents of
20 metals (Na, K, Ca, Mg, B, Ba, Co, Cr, Cu, Fe, Li, Mn, Mo,Ni, Sr, V, Zn,
Al, Cd and Pb) in 42 samples of 8 dehydrated red and brown edible
seaweed species (Chondrus, Eisenia, Gelidium, Himanthalia, Lami-
naria, Palmaria, Porphyra, Undaria) from two different production
origins (Asia vs European Union) but purchased in large Spanish
cities, (2) to compare the element contents according to their
cultivation practices (organic vs conventional) (3) to assess the
seaweed-derived intake of essential metals and their contribution
to the Recommended Dietary Intakes (RDIs), and (4) to evaluate the
intake of toxic metals and their contribution to the corresponding
Provisional Tolerable Weekly Intake (PTWI) and Tolerable Dairy
Intake (TDI).
573
2. Material and methods
2.1. Sampling
A total of 42 samples of 8 dehydrated edible seaweed species
were collected between January and June in 2014. The samples
were comprised of three groups: red seaweed (Chondrus n 2;
Eisenia n 6; Gelidium n 2; Palmaria n 4; Porphyra n 10),
brown seaweed: (Himanthalia n 6; Laminaria n 6; Undaria
n 4) and mixed (including red and brown seaweed) (n 2).
The sampling was focused on the most commonly consumed
seaweedsand two different cultivation practices (organic n 12
vs conventional n 30). The samples came from two different
production regions: Asia (mainly China, Japan and South Korea)
and the European Union which were purchased in large Spanish
cities.
2.2. Sample treatment and analysis
As published before by our research group (Rubio et al., 2012;
Luis et al., 2014, 2014b; Dorta et al., 2015; Luis Gonza
lez et al.,
2015), 3 g of each seaweed sample were weighed out and placed
into porcelain capsules before being desiccated in a thermo-
regulated vacuum oven (Nabertherm Inc, USA) at 70  C for 48 h.
Then, 5 mL of HNO3 65% was added very slowly and heating
continued at 120  C for 30 min. The samples were then subjected
to pyrolysis in a mufe furnace (Nabertherm Inc, USA) by gradu-
ally raising the temperature to 450  C, which was maintained for
48 h. The resulting white ash was dissolved in a solution of 1.5%
HNO3 (Merck, Darmstadt, Germany), which was completed to
25 mL. The minerals in the samples were determined by ICP-OES
using a Thermo Scientic iCAP 6000 series spectrometer (Wal-
tham, MA, USA) with the following settings: approximate RF po-
wer, 1.2 kW; gas ow (nebulizer ow; auxiliary ow), 0.5 L/min;
pump rate, 50 rpm; stabilization time 0s. All analyzes were per-
formed in duplicate. In order to prevent contamination, all the
laboratory material used was washed with a detergent solution
(Merck, Darmstadt, Germany) and conserved with 10% HNO3 (v/v)
for 24 h and then washed with milliQ water (Millipore, Bedford,
USA).
The quality controls used in this work were chosen by the
criterion of method accuracy. This was established by the average
recovery obtained with reference material measured under
reproducible conditions. SRM 1515 Apple leaves, SRM 1570a Trace
elements in spinach leaves and BCR 279 Sea lettucefrom the Na-
tional Institute of Standards and Technology (NIST) (Gaithersburg,
MD USA) were the reference materials used and the recovery rates
were over always 94.5% as shown in Table 1. Detection (LOD) and
quantication (LOQ) limits, were calculated with respectively
three and ten times the standard deviation (SD) resulting from
analysis of 15 targets of acid digest (IUPAC, 1995) and are shown in
Table 2.
2.3. Statistical analysis
The statistical analyses were performed using the data analysis
program SPSS Inc., version 19.0 (SPSS, IBM, Armonk, NY). Samples
were grouped for analysis according to the group (brown vs. red
seaweed), species, origin (Asia vs. European Union) and cultivation
method (organic vs. Conventional). In order to study the normality
of the obtained results, the Kolmogorov-Smirnov y Shapiro-Wilk test
(Xu et al., 2002) and the Levene test were applied to determine the
homogeneity of the variance (Pan, 2002). Given that the results did
follow a normal distribution, the nonparametric Kruskal-Wallis test
and Mann-Whitney U were used.
574 C. Rubio et al. / Chemosphere 173 (2017) 572e579

Table 1
Quality control of the method.

Reference material Element Certied valuea,b (mg/kg) Obtained valuea (mg/kg) Recovery (%)

SRM 1515 Apple leaves K 1.61 0.02c 1.62 0.01c 101

Ca 1.53 0.02c 1.51 0.01c 98.7
Mg 0.27 0.01c 0.26 0.05c 96.3
B 27 2 26.5 0.02 98.1
Ba 49 50 0.02 102
Cr 0.3d 0.29 0.01 96.7
Co 0.09c 0.09 0.01 100
Fe 80 0.0d 81.5 0.01 102
Mn 54 0.3 55.1 0.8 102
Mo 0.09 0.09 0.02 100
Ni 0.91 0.12 0.86 0.19 94.5
Al 286 285 0.3 99.7
SRM 1570a Trace elements in spinach leaves Na 1.82 0.04 1.81 0.06 99.4
Sr 55.6 0.8 54.1 0.4 97.3
V 0.57 0.03 0.6 0.01 105
BCR 279 Sea lettuce Cu 13.1 0.4 13.0 0.05 99.2
Zn 51.3 1.2 51.5 0.5 100
Cd 0.27 0.02 0.27 0.07 97.8
Pb 13.1 0.4 12.8 0.05 97.7
a
Mean standard deviation.
b
Condence interval: 95%.
c
Concentration in mass fraction (%).
d
Information values.

3. Results and discussion Fe > Zn > Mn > V > Ba > Li > Ni > Cu > Mo > Sr > Co > Cr. Statistical
analysis revealed no signicant differences between the two ori-
Table 3 shows the mean concentrations and standard deviations gins of seaweed for almost all of the studied trace elements except
for each of the 20 metals in the seaweeds according to their origin for the metals B, Cu, Fe, Ni and Zn (p < 0.05), respectively. In this
and cultivation method. K was found to be the quantitatively most study, 35.7% of the samples analyzed had V concentrations which
outstanding of the analyzed minerals with mean levels ranging were lower than the detection or quantication limits (0.0001 mg/L
between 6460 mg/kg in Asian seaweed and 7519 mg/kg in Euro- and 0.001 mg/L, respectively). However, only 11.9% of the samples
pean seaweed. The remaining macronutrients followed the con- analyzed presented Sr contents lower than the detection or quan-
centration sequence Na > Ca > Mg for both origins. Statistical tication limits (0.0002 mg/L and 0.0001 mg/L, respectively).
analysis revealed signicant differences between the mean con- With respect to toxic metals, the mean contents of Al in the
tents of Asian and European seaweed. It was detected that differ- analyzed seaweed samples ranged between 11.5 mg/kg in Asian
ences in K and Na levels between both seaweed origins were seaweed and 12.3 mg/kg in European seaweed followed by Cd with
signicant (p < 0.05). Furthermore, Fe was the most abundant trace concentrations ranging between 0.10 mg/kg in European seaweed
element in Asian seaweed (28.93 mg/kg) followed by the other and 0.44 mg/kg in Asian seaweed. The European Commission
microelements, ranked in descending order, Zn > B > Mn > Cu > Regulation (EC) N 629/2008 (EC, 2008) and European Commission
Ba > Sr > Li > V > Mo > Cr > Ni > Co. As regards European seaweed, Regulation (EC) N 488/2014 (EC, 2014) only set a maximum level
B (19.04 mg/kg) was the most abundant trace element followed by for Cd (3 mg/kg) in different food supplements consisting exclu-
sively or mainly of dried seaweed or of products derived from
seaweed. European legislation does not set a limit for Al and Pb in
Table 2 seaweed but the CEVA (Centre dEtude et de valorization des
Detection and quantication limits. Algues) in 2014 set the maximum levels for Cd (0.5 mg/kg dry
weight) and Pb (5 mg/kg dry weight) in authorized French edible
Element and wavelength Detection limit Quantication limit
(LOD) (mg/L) (LOQ) (mg/L) seaweed. Cd concentrations in this study did not exceed the legally
set limit in France (0.5 mg/kg dry weight) in any of the analyzed
Na (589.6 nm) 1.097 3.655
K (769.9 nm) 0.565 1.884
samples. Similar to Cd, mean levels of Pb in the analyzed seaweed
Ca (317.9 nm) 0.580 1.955 samples ranged between 0.04 mg/kg in Asian coast seaweed and
Mg (279.1 nm) 0.583 1.943 0.05 mg/kg in European seaweed; thus, Pb levels did not exceed the
B (249.7 nm) 0.003 0.012 legally set limit in French legislation (5 mg/kg dry weight) ac-
Ba (455.4 nm) 0.001 0.005
cording to CEVA (2014).
Co (228.6 nm) 0.0006 0.002
Cr (267.7 nm) 0.003 0.008 Despite the small sample sizes, the present study of metal
Cu (327.3 nm) 0.004 0.012 content according to the production method (organic vs. Conven-
Fe (259.9 nm) 0.003 0.009 tional) (Table 3) reveals that, for macroelements, the seaweed
Mn (257.6 nm) 0.002 0.008
produced by organic methods had the highest mean concentrations
Mo (202.0 nm) 0.0007 0.002
Li (670.8 nm) 0.005 0.013
of K (7541 mg/kg) and Na (4701 mg/kg) while the highest contents
Zn (206.2 nm) 0.002 0.007 of Ca (2662 mg/kg) and Mg (2887 mg/kg) were detected in the
Ni (231.6 nm) 0.0007 0.003 seaweed produced by the conventional method. Differences in K
Sr (407.7 nm) 0.0007 0.003 and Ca levels between both seaweed cultivation methods were
V (310.2 nm) 0.001 0.005
signicant (p < 0.05). Furthermore, Fe was the most abundant trace
Al (167.0 nm) 0.004 0.012
Cd (226.5 nm) 0.0003 0.001 element in the seaweed produced by the conventional method
Pb (220.3 nm) 0.0003 0.001 (58.8 mg/kg). The remaining trace elements followed the
 C. Rubio et al. / Chemosphere 173 (2017) 572e579 575

Table 3
Mean content standard deviation of metals in seaweed samples according to their origin and cultivation method (mg/kg dry weight).

Element Origin Cultivation method

Asian (n 14) European Union (n 18) Conventional cultivation (n 30) Organic cultivation (n 12)
a a
Na 2971 1386 5044 1760 4070 1802.58 4701 2076.78
K 6460 1095a 7519 2692a 6711 1920.23a 7541 3360.63a
Ca 2285 1329 2205 921 2662 1062.77a 1570 1047.66a
Mg 1753 543 2164 968 2887 532.20 1802 348.67
B 8.63 11.0a 19.0 11.1a 13.5 10.05 23.3 14.4
Ba 1.81 1.59 1.06 0.62 1.95 1.86 0.73 0.12
Co 0.03 0.01 0.09 0.09 0.08 0.12 0.08 0.08
Cr 0.16 0.15 0.08 0.05 0.17 0.26 0.12 0.06
Cu 2.00 0.93a 0.76 0.00a 1.63 1.10 0.83 0.19
Fe 28.9 20.1a 11.8 10.2a 58.8 27.47 18.9 13.79
Li 1.08 0.87 0.98 0.44 1.00 0.61 0.92 0.54
Mn 5.76 5.11 3.88 3.55 13.5 6.53 3.92 1.08
Mo 0.17 0.11 0.42 0.03 0.10 0.02 0.06 0.01
Ni 0.08 0.03a 0.79 0.02a 0.25 0.09a 1.13 0.53a
Sr 1.59 2.64 0.10 2.28 0.74 0.35 2.26 0.76
V 0.34 0.40 3.49 8.57 0.35 0.43 8.84 12.36
Zn 9.72 5.72a 4.59 2.34a 7.49 5.15 5.23 2.55
Al 11.5 6.08 12.3 9.82 16.2 3.42 14.9 3.81
Cd 0.44 0.34 0.10 0.10 0.28 0.05 0.13 0.03
Pb 0.04 0.00 0.05 0.03 0.08 0.13 0.05 0.03
a
Statistical signicance (p < 0.05).

concentration sequence B > Mn > Zn > Ba > Cu > Sr >
V > Ni > Cr > Li Mo > Co. As regards seaweed produced by the
organic cultivation method, B was found to be the quantitatively
most outstanding of the analyzed trace elements (23.3 mg/kg)
followed by the other microelements, ranked in descending order,
Fe > V > Zn > Mn > Sr > Ni > Li > Cu > Ba > Cr > Co > Mo. Several
authors (Besada et al., 2009; Astorga-Espan ~ a et al., 2015) have
suggested this is due to contamination during the procedure;
seaweed comes into physical contact with various tools and
equipment which are made of alloys of the mentioned metal. Sta-
tistical analysis revealed than Ni levels in seaweed produced by the
organic cultivation method were signicantly higher (p < 0.05)
than in seaweed produced by the conventional cultivation method.
With respect to toxic metals, seaweed produced by the con-
ventional cultivation method showed the highest toxic metal
concentrations, mainly Al (16.2 mg/kg for conventionally cultivated
seaweed and 14.9 mg/kg for organically cultivated seaweed) fol-
lowed by Cd and Pb (0.08 mg/kg for conventionally cultivated
seaweed and 0.05 mg/kg for organically cultivated seaweed). The
mean Cd level in seaweed produced by the conventional cultivation
method (0.28 mg/kg) was two points higher than seaweed pro-
duced by the organic cultivation method (0.13 mg/kg).
(p < 0.05). Moreover, differences in Cd contents between both
seaweed groups were signicant (p < 0.05). In general, red seaweed
showed a tendency to have higher concentrations of trace and toxic
elements than brown seaweed.
The metal content in seaweed is known to reect the mineral
composition of the taxonomic group. Several authors have reported
that the metal composition may vary with the characteristics of the
polysaccharides, mainly the amounts and types of polysaccharides,
present in the cell walls of such marine vegetables (Go
mez-
Ordo
n~ ez, 2012).
Table 5 show the mean concentrations and standard deviation
of the 20 metals determined in all species of seaweed studied.
Despite the small sample sizes per seaweed species, the analysis of
the different species of seaweed within each taxonomic group,
brown and red seaweed, showed that Chondrus had the highest
contents of metals, mainly Na (6799 mg/kg) and K (9901 mg/kg)
while the highest contents of Ca (3978 mg/kg) were detected in
Table 4
Mean metal contents standard deviations in seaweed samples by taxonomic group
(mg/kg dry weight).

The data presented in Table 4 show the mean concentrations Element Brown seaweeds (n 22) Red seaweeds (n 18)
and standard deviation of the 20 analyzed elements in seaweed Na 5118 1510a 2532 1001a
allocated to the taxonomic groups: brown seaweed and red K 7683 1742 6182 2398
seaweed, respectively. Brown seaweed had the highest contents of Ca 3082 625a 1349 153a
macroelements with the exception of the metal Mg. Differences in Mg 2485 478a 2586 4215a
B 17.9 7.28 11.6 14.0
Na, Ca and Mg levels between both taxonomic seaweed groups
Ba 1.33 0.38 2.19 2.61
were signicant (p < 0.05) in this study. As regards the trace ele- Co 0.07 0.09 0.09 0.15
ments, the higher mean levels of almost all metals were found in Cr 0.09 0.13a 0.26 0.31a
red seaweed with the exception of B, Fe and Mn, respectively. The Cu 0.94 0.37a 2.20 0.03a
detected Sr levels were below the quantication limit (0.001 mg/ Fe 7.88 0.00a 107 196a
Li 0.08 0.34a 1.29 0.77a
kg). Statistical analysis revealed no signicant differences between Mn 2.38 2.82a 23.4 0.00a
the two taxonomic groups of seaweed for almost all of the studied Mo 0.04 0.01a 0.16 0.11a
metals except for the metals Cr, Cu, Fe, Li, Mn, Mo, Sr, V and Zn Ni 0.16 0.15 0.46 0.10
(p < 0.05). Sr <0.001 0.00 3.09 0.00
V 0.39 0.55a 6.68 11.3a
With respect to toxic metals, mean contents of Al in the
Zn 4.29 1.93a 10.1 5.65a
analyzed seaweed samples ranged between 7.43 mg/kg in brown Al 7.43 5.26 27.1 22.6
seaweed and 27.1 mg/kg in red seaweed. After analyzing Al levels of Cd 0.10 0.06a 0.40 0.34a
the different taxonomic groups of seaweed, statistical analysis Pb 0.05 0.00 0.11 0.17
revealed signicant differences between both groups of seaweed a
Statistical signicance (p < 0.05).
576 C. Rubio et al. / Chemosphere 173 (2017) 572e579

Eisenia and Mg (3732 mg/kg) in Porphyra. With respect to trace
elements, Porphyra had the highest metal contents, mainly Ba
(3.19 mg/kg), Cr (0.33 mg/kg), Cu (2.99 mg/kg), Fe (156 mg/kg), Li
(1.41 mg/kg), Mn (36.5 mg/kg), Mo (0.22 mg/kg), and Zn (13.6 mg/
kg) followed by Chondrus with the metals B (43.3 mg/kg) and Ni
(5.08 mg/kg) and Palmaria with the highest levels of the metals Sr
(34.4 mg/kg) and V (25.5 mg/kg), respectively. In general, accu-
mulation of Fe was high in all the genera of seaweed. Chakraborty
et al. (2014) reported that this might be due to high rates of
photosynthesis in typical tropical climate coastal habitats. Statis-
tical analysis revealed signicant differences (p < 0.05) between
the eight genera of seaweed for almost all of the studied trace el-
ements except for B. So, the wide range of metal concentrations in
different seaweed genera reects the importance of biochemical
factors in affecting the relative tendency of different tissues to
accumulate metals (Jadeja and Batty, 2013).
As regards toxic metals, the highest levels of Al (32.0 mg/kg)
were detected in Palmaria while the lowest contents (4.46 mg/kg)
were observed in Eisenia. Accumulation of Al was highly variable in
the eight genera of seaweed. As for Cd and Pb, Himanthalia had the
highest Cd contents (0.82 mg/kg) while the highest contents of Pb
(0.15 mg/kg) were detected in Porphyra.
Table 6 presents a comparison of the mean levels of the essential
and toxic metals in the seaweed samples obtained in this study
with the results published by other authors. Metal contents in
seaweed vary widely between countries (Topcuoglu et al., 2003;
Runcie and Riddle, 2004; Pe
rez et al., 2007; Subba Rao et al.,
2007; Wallenstein et al., 2009; Larrea-Marn et al., 2010; Laib and
Leghouchi, 2012; Ruz-Navarro et al., 2013; Astorga-Espan ~ a et al.,
2015).
On the whole, as regards macroelements, India has reported the
highest contents in macroelements (Subba Rao et al., 2007). The Na
and Mg contents of the seaweed samples from the present study
were lower than the means or concentration ranges reported by
other authors. In the case of K and Ca, our data were similar to the
concentration ranges previously found in Spain by Ruz-Navarro
et al. (2013). As for trace elements, the highest metal contents in
general were detected by Topcuoglu et al. (2003) in Turkey and
Pe
rez et al. (2007) in the Antarctic. B, Ba and Co levels in the
analyzed seaweed samples were similar to the concentration
ranges in Spain found by Ruz-Navarro et al. (2013), although the
detected Sr and V contents were considerably higher and Li
contents were lower than the concentrations reported by other
authors (Pe
rez et al., 2007; Larrea-Marn et al., 2010; Ruz-Navarro
et al., 2013). As regards Mn, our results were similar to those re-
ported by Wallenstein et al. (2009) in the Azores islands. Our data
for Mo were similar to those reported by other authors (Subba Rao
et al., 2007; Ruz-Navarro et al., 2013). Cu and Fe contents varied
greatly with the results obtained in other countries. With respect to
toxic metals, the highest Al content was found by Larrea-Marn
et al. (2010) in Spain. Al levels in the different seaweed samples
considered in the present study were lower than those reported by
Ruz-Navarro et al. (2013). As for Cd and Pb, the Antarctic seaweed
presented the highest contents (Runcie and Riddle, 2004)
compared with those found for other countries. A comparison of
the results of the present study with those of other studies revealed
similar levels of Cd in seaweed studied in Algeria (Laib and
Leghouchi, 2012) and similar contents of Pb in seaweed from the
Azores (Wallenstein et al., 2009) and Spain (Ruz-Navarro et al.,
2013).
In order to assess the contribution of essential metals ingested
through seaweed consumption to the Recommended Dietary In-
takes (RDI) for the Spanish population (FESNAD, 2010), we used the
daily seaweed consumption (4 g/adult/day) known to be ingested
by the Japanese (Zava and Zava, 2011). As regards the macro-
minerals, brown seaweed provides greater intakes and nutritional
contributions to the recommended intakes than red seaweed
(Table 7). Mg was the macromineral in seaweed with the highest
contribution to the daily intake (3.43% in adult women and 2.94% in
adult men) followed by Na, Ca, and K. The above results conrm
that the consumption of seaweed in the population favours the
dietary intake of Mg and, therefore, contributes to its role in the
physiological process. There are discrepancies in the Na/K ratios of
seaweed. The Na/K ratio in brown seaweed was 0.67 while the Na/K
ratio in red seaweed was 0.41. Most authors found a range near or
lower than 1 (Rupe
rez, 2002; Taboada et al., 2012), while others
published values above 1 (Shams El-Din et al., 2012). The dietary
intake of high Na/K ratios has been correlated with a high incidence
of hypertension (Astorga-Espan ~ a et al., 2015).
With regard to trace elements, red seaweed provides greater
contributions to the recommended intakes than brown seaweed. Cr
in seaweed was found to be the trace element with the highest
contribution to the daily intake (2.56% in adult women and 1.83% in
adult men) followed by Fe (1.06%in adult women and 2.38% in adult

Table 5
Mean content standard deviation of elements in seaweed samples for different genera of seaweeds (mg/kg dry weight).

Genera Na K Ca Mg B Ba Co Cr Cu Fe

Brown Himalthalia (n 6) 5433 274 8092 874 2602 238 2461 119 12.2 0.98 0.96 0.06 0.20 0.06 0.04 0.03 0.84 0.22 3.99 0.92
Laminaria (n 6) 5809 1340 8968 1059 2906 66.2 2529 696 26.9 5.86 1.48 0.46 0.01 0.001 0.05 0.03 0.72 0.29 6.59 3.44
Undaria (n 4) 6621 441 8707 951 2721 216 3008 273 20.7 4.04 1.67 0.22 0.03 0.004 0.04 0.004 0.67 0.09 9.17 0.93
Red Chondrus (n 2) 6799 84.6 9901 270 2028 153 3134 45.7 43.3 6.60 0.35 0.08 0.13 0.01 0.15 0.00 0.79 0.21 22.3 3.79
Eisenia (n 6) 3109 6.57 5305 716 3978 248 2116 183 12.6 0.59 1.32 0.29 0.03 0.004 0.19 0.24 1.41 0.00 12.2 1.39
Gelidium (n 2) 1279 0.00 543 53.2 908 7.01 452 4.68 4.50 0.98 0.30 0.10 0.008 0.00 0.16 0.001 0.54 0.02 9.86 0.24
Palmaria (n 4) 3803 463 8044 0.00 459 0.00 787 87.6 31.5 6.45 0.62 0.28 0.03 0.01 0.15 0.02 1.03 0.09 34.7 8.10
Porphyra (n 10) 2274 675 6563 854 1793 1211 3732 5070 5.10 0.00 3.19 2.88 0.12 0.18 0.33 0.14 2.99 0.68 156 239
Mixed (n 2) 5893 23.1 2038 181 2570 192 2942 359 9.62 1.54 1.15 0.42 0.02 0.02 0.07 0.01 0.74 0.06 27.8 7.45

Li Mn Mo Ni Sr V Zn Al Cd Pb

Brown Himalthalia (n 6) 0.66 0.24 6.79 0.99 0.03 0.01 0.38 0.10 6.70 0.23 1.22 0.29 5.71 0.54 7.04 5.66 0.82 0.02 0.02 0.01
Laminaria (n 6) 0.68 0.40 0.62 0.23 0.03 0.004 0.07 0.02 e 0.49 2.12 1.78 0.27 7.97 6.44 0.07 0.03 0.07 0.05
Undaria (n 4) 1.20 0.24 0.69 0.23 0.03 0.004 0.11 0.02 e 0.04 0.06 3.21 0.22 11.7 5.19 0.06 0.02 0.07 0.03
Red Chondrus (n 2) 0.85 0.01 9.78 0.56 0.12 0.01 5.08 0.10 e 0.58 0.47 9.33 2.57 8.41 2.85 0.29 0.03 0.07 0.00
Eisenia (n 6) 0.66 0.22 0.85 0.27 0.06 0.003 0.08 0.03 e 0.13 0.09 6.08 0.61 4.46 1.07 0.19 0.04 0.03 0.01
Gelidium (n 2) 0.93 0.58 1.66 0.01 0.008 0.00 0.11 0.001 e e 2.21 0.25 8.21 0.61 0.008 0.00 0.05 0.01
Palmaria (n 4) 1.16 0.83 1.62 0.45 0.09 0.01 0.05 0.13 3.44 0.36 25.5 0.00 5.03 1.06 32.0 5.18 0.16 0.11 0.05 0.02
Porphyra (n 10) 1.41 0.00 36.5 56.9 0.22 0.09 0.50 0.87 2.22 2.92 0.48 0.41 13.6 3.72 28.9 27.3 0.58 0.30 0.15 0.21
Mixed (n 2) 0.91 0.002 2.43 0.63 0.03 0.01 0.09 0.00 e 0.05 0.32 6.84 0.32 26.1 0.00 0.33 0.06 0.08 0.02
 C. Rubio et al. / Chemosphere 173 (2017) 572e579 577

Table 6
Comparison of macro and trace elements in seaweeds from different countries (mg/100 g on a dry weight basis).

Metal Coast Black Sea Turkeya Antarcticb Gulf S. Jorge Argentinac Chiled Indiae Azoresf Algeriag Spainh Spaini This study

Na e e e 308e3880 5230 e e 2350e3720 425e431 128e680

K e e e 496e4770 2490 2670e4640 e 2650e7610 602e843 54.3e990
Ca e e e 180e1140 3350 217e855 e 580e1560 320e324 45.9e398
Mg e e e 381e1160 4950 449e650 e 580e1070 246e379 45.2e373
B e e e 0.04 e e e 2.63e4.94 0.45e4.33
Ba e e e e e e 0.2e1.14 0.16e0.38 0.03e0.32
Co Ndj-0.91 e e e e e e 0.007e0.01 0.001e0.02
Cr Ndj-0.12 0.06e1.31 0.08e0.11 e 0.18 e 0.07e0.09 e 0.02e0.03 0.004e0.33
Cu Ndj-2.01 0.13e4.9 0.17e0.38 e 0.83 0.33e0.75 e 1.45e2.18 0.20 0.05e0.30
Fe 13e499 e e e 137 5.33e32.3 e e 9.66e11.5 0.4e15.6
Li e e e e e e e e 0.19e0.28 0.07e0.14
Mn 0.67e36.5 0.28e15.4 0.81e5.14 0.14e1 7.09 1.15e3.07 e e 0.79e0.85 0.06e3.65
Mo e e e 5.54e366 0.03 e e e 0.01 0.001e0.02
Ni e 0.1e1.54 0.1e0.41 e 0.13 0.1e0.18 e e 0.18e0.30 0.005e0.51
Sr e e e 0.25e26.2 e e e 0.01e0.11 0.14e0.16 Ndj-0.67
V e e 0.22e0.56 e e e e e 0.11e0.20 Ndj-2.55
Zn 0.89e19.2 2.6e13.1 1.74e3.13 e 1.95 0.99e2.89 0.46e0.52 e 1.01e1.12 0.18e1.36
Al e e e e e e e 8.78e18.6 2.63e4.92 0.45e3.20
Cd Ndb-0.16 0.14e1.17 0.02e0.10 e 0.29 0.04e0.11 0.007e0.01 e 0.22e0.38 0.001e0.08
Pb Ndb-0.22 0.05e2.15 0.08e0.17 1.04e3.09 0.07 0.01e0.02 0.08e0.15 e 0.02 0.002e0.02
a
Topcuoglu et al., 2003.
b
rez et al., 2007.
Pe
c
Runcie and Riddle, 2004.
d
Astorga-Espan ~ a et al., 2015.
e
Subba Rao et al., 2007.
f
Wallenstein et al., 2009.
g
Laib and Leghouchi, 2012.
h
Larrea-Marn et al., 2010.
i
Ruz-Navarro et al., 2013.
j
Not detected (below quantication limit).

men), Mn (1.87% for both adults), Mo (0.8% for both adults), Cu
(0.51% for both adults) and Zn (0.43%in adult women and 0.32% in
adult men).
The estimated intake of B from a 4 g/day seaweed consumption
was 0.07 mg/kg for adults (B reference value is set in 0.16 mg/
kg bw/day by EFSA since 2004) which represents 0.68% of the EFSA
reference value for adult women (assuming a 60 kg body weight)
and 0.58% for adult men (assuming a 70 kg body weight).
The estimated intake of Ni was 0.002 mg/kg for adults. Based on
a Tolerable Daily Intake (TDI) of 8 mg Ni/kg bw/day as set by the
EFSA (EFSA, 2005), 4 g/day of seaweed consumption contributes
0.42%of the TDI of Ni for a 60 kg bw adult woman and 0.36% for a
70 kg bw adult man.
Estimated intakes of V, Sr, Ba, Li and Co were 0.011 mg/day,
0.007 mg/day, 0.006 mg/day, 0.004 mg/day and 0.0003 mg/day for
adults, respectively, from a 4 g/day seaweed consumption. There
are no intake reference values for these metals to compare with our
data.
Al was the metal that had the highest intakes, 0.064 mg/day for
adults (0.75% for a 60 kg bw woman and 0.64% for a 70 kg bw man,
respectively, of the 1 mg/kg bw/week reference value established
by the EFSA in 2011).
The estimated intake of Pb through seaweed consumption was,
based on the daily seaweed consumption of 4 g/adult/day,
0.0003 mg/day. In 2010, the EFSA set a TDI for Pb of 0.5 mg/kg bw/
day (EFSA, 2010). This 0.0003 mg Pb/day intake represents 0.93% of
the EFSA reference value for a 60 kg bw adult woman and 0.80% for
a 70 kg bw adult man.
Considering again a 4 g/adult/day seaweed consumption, the
average estimated intake of Cd was 0.001 mg/day for adults which

Table 7
Mean dietary intake (mg/day) of seaweed and contribution (%) to the daily requirements of macroelements and trace elements for adults in Spain.

Element Brown seaweed Red seaweed Total

Intake Contribution Intake Contribution Intake Contribution

Female Men Female Men Female Men

Macroelements
Na 20.5 1.37 1.37 10.1 0.67 0.67 17.0 1.13 1.13
K 30.7 0.99 0.99 24.7 0.80 0.80 27.8 0.90 0.90
Ca 12.3 1.23 1.23 5.40 0.54 0.54 9.40 0.94 0.94
Mg 9.94 3.31 2.84 10.3 3.43 2.94 10.3 3.43 2.94
Trace elements
Cra 0.004 16.0 11.4 0.001 4.00 2.86 0.006 2.56 1.83
Cu 0.004 0.36 0.36 0.009 0.82 0.82 0.006 0.51 0.51
Fe 0.03 0.17 0.38 0.43 2.39 5.38 0.19 1.06 2.38
Mn 0.01 0.43 0.43 0.09 3.91 3.91 0.043 1.87 1.87
Moa 0.0002 0.44 0.44 0.0006 1.33 1.33 0.0004 0.8 0.8
Zn 0.02 0.29 0.21 0.04 0.57 0.42 0.03 0.43 0.32
a
Intakes expressed in mg/day.
578 C. Rubio et al. / Chemosphere 173 (2017) 572e579
is 4.57% and 3.84%of the Cd reference value (2.5 mg/kg bw/week) set
by the EFSA in 2011 (EFSA, 2011a,b), respectively, for adult women
(assuming a 60 kg bw) and men (assuming a 70 kg bw).
4. Conclusions
Metals in seaweeds have been found in variable concentrations
among the different species. Red seaweeds showed higher con-
centrations of trace and toxic elements. Conventional cultivation
provides signicantly higher contents of metals compared to
organic cultivation and this fact supports the importance of the
cultivating techniques in the reduction of health risks. The present
study conrms that seaweeds are a source of essential dietary el-
ements, particularly Mg and Fe. Although the present study sug-
gests that exposure to Al, Cd and Pb through seaweed consumption
is low, and that there is negligible risk of their respective TDI/TWIs
being exceeded as a result of seaweed consumption, toxic metals
should be monitored in seaweeds.
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