Seaweed Minerals as Nutraceuticals

Ladislava Misurcova,*'1 Ludmila Machu,t and Jana Orsavovâ*

Contents I. Introduction 372

II. Functions of Iodine, Iron, Zinc, and Manganese in the Human Body 372

A. Iodine 372

C. Zinc 374

D. Manganese 374

III. Requirements of Minerals by Humans 375

IV. Content of Minerals in Seaweed 376

A. Contribution of seaweed minerals to daily requirements 377

B. Factors influencing mineral contents in seaweed 383

V. Bioavailability of Seaweed Minerals by Humans 385

VI. Conclusion 386 References 386

Abstract Seaweed is known as an abundant source of minerals. Mineral com position of seaweed is very changeable because of many exogenous and endogenous factors and differs also within the same species.

* Department of Food Technology and Microbiology, Faculty of Technology, Tomas Bata University in Zlin, Zlin, Czech Republic

{ Department of Food Analysis and Chemistry, Faculty of Technology, Tomas Bata University in Zlin, Zlin, Czech Republic

{ Jana Orsavova is not employed in academic institution but contributed to this chapter. 1 Corresponding author: Ladislava Misurcova, E-mail address: [email protected]

Advances in Food and Nutrition Research, Volume 64 © 2011 Elsevier Inc.

ISSN 1043-4526, DOI: 10.1016/B978-0-12-387669-0.00029-6 All rights reserved.

Principally, seaweed is an excellent source of some essential elements. Mainly, iron and iodine are in high concentration. Seaweeds could be prospective as functional foods and also producers of mineral nutraceuticals.

I. INTRODUCTION

Seaweeds are well-known source of many different bioactive compounds with many health benefit activities. Thus, seaweeds are categorized into the group of functional foods. Because of abundant amounts of many minerals, seaweeds could be utilized as nutraceuticals. The most abundant elements in seaweed tissue are iron (Fe) and iodine (I). Mineral composition of seaweeds is very changeable according to many exogenous and endogenous factors, and it is obviously corresponding with the concentration of minerals in the seawater or a growth medium.

Minerals are structural components and significantly important elements that perform many necessary functions in the living body, including the cell transport and wide range of metabolic processes serving as various catalytic metalloenzymes cofactors. This chapter is focused on some trace elements that are abundantly contained in seaweed. Common feature of all trace elements is their important participation in the formation of binding site of metalloenzymes, where each element plays specific roles in living systems and many of them have a lot of beneficial functions.

II. FUNCTIONS OF IODINE, IRON, ZINC, AND MANGANESE IN THE HUMAN BODY

A. Iodine

Dietary iodine is essential for the production of thyroid hormones, thy-roxine and triiodothyronine, which regulate many important physiological processes in humans (Haldimann et al., 2005). More than 1.9 billion individuals are estimated to have inadequate iodine nutrition; the lowest iodine deficiency is in America and the highest in Europe (de Benoist et al., 2003).

Iodine deficiency has effects on growth and development because of inadequate production of thyroid hormones. Health consequences of iodine deficiency are goiter, increased occurrence of hypothyroidism in moderate-to-severe iodine deficiency or decreased occurrence of hypo-thyroidism in mild iodine deficiency, and increased susceptibility of the thyroid gland to nuclear radiation. Abortion, stillbirth, congenital anomalies, perinatal and infant mortality, or endemic cretinism may occur in neonates. Iodine deficiency during child and adolescent age could cause delay of physical development and impairment of mental function or iodine-induced hyperthyroidism in adults as well (Zimmermann and Crill, 2010). In severe iodine deficiency, hypothyroidism and developmental brain damage are the dominating disorders (Laurberg et al., 2010).

Excess iodine could lead to thyrotoxicosis and may be connected with hyperthyroidism, euthyroidism, hypothyroidism, or autoimmune thyroid disease (Biirgi, 2010; Laurberg et al., 2010). However, thyroid possesses the adaptation mechanisms regulating thyroid hormones synthesis and secretion and protecting from thyrotoxicosis (Wolff, 1989).

Iron is an essential element for humans because of its participation in fundamental cell functions. Iron is the most abundant transition metal in the body, which takes part in the utilization of oxygen, and as a component of numerous enzymes, it affects many vitally important metabolic processes, including oxygen transport, DNA synthesis, and electron transport (Lieu et al., 2001; Puntarulo, 2005). The main part, 60-70% of Fe is bound to hemoglobin in circulating erythrocytes, 10% of Fe is present in the form of myoglobins, cytochromes, and iron-containing enzymes, and 20-30% of surplus Fe is stored as ferritins and hemosiderins (Lieu et al., 2001). Iron is stored in the liver, spleen, and bone marrow in specific proteins (Puntarulo, 2005).

Iron deficiency is considered as the most common nutritional disorder worldwide, which results mainly from excessive bleeding (Deegan et al., 2005; Puntarulo, 2005), but partly can be induced also by plant-based diets of vegans, which contains less bioavailable Fe (Martinez-Navarrete et al., 2002). Iron deficiency adversely affects the cognitive performance, behavior, physical growth, the immune status, and morbidity from infections of all age groups. Iron-deficient humans have impaired gastrointestinal functions and altered patterns of hormone production and metabolism (Walker, 1998; WHO, 2001).

Homeostatic mechanisms are very important for the prevention of accumulation of excess Fe that is believed to generate oxidative stress by catalysis of variety of chemical reactions involving free radicals, which could result in cell damage (Pietrangelo, 2002; Puntarulo, 2005). Excess Fe accumulation may promote cancer and increase the cardiovascular risk (Martinez-Navarrete et al., 2002). Iron overload can be observed in some cases including an excessive dietary iron intake, inherited diseases, for example, idiopathic hemochromatosis, congenital atransferrinemia, or the medical treatment of thalassemia (Fontecave and Pierre, 1993).

C. Zinc

Zinc (Zn) is one of the most important essential elements that occurs in hundreds of zinc metalloenzymes and in thousands of protein domains as zinc-fingers (Maret and Sandstead, 2006; McCall et al., 2000; Tapiero and Tew, 2003). Zinc is necessary for growth and development; it is a structural ion of biological membranes; it has roles in gene expression and endocrine function, DNA synthesis, RNA synthesis, and cell division (O'Dell, 2000; Salgueiro et al., 2002). Zinc is an antioxidant, regulates immune response, and has a role in vitamin A metabolism (Rink and Haase, 2007; Salgueiro et al., 2000). Zinc interacts with important hormones involved in bone growth and enhances the effects of vitamin D on bone metabolism (Salgueiro et al., 2002). The majority (85%) of Zn in the whole body is deposited in muscles and bones, 11% is in skin and liver, and the remaining amount is in other tissues. High level of Zn is present in the brain (Tapiero and Tew, 2003). Disturbances of Zn homeostasis have been associated with several diseases including diabetes mellitus, and the alteration of Zn homeostasis in the brain may be associated with the manifestation of epileptic seizures (Chausmer, 1998; Takeda, 2000).

Zinc deficiency occurs in populations whose diets contain high concentration of phytate, a powerful chelator, and low protein (Tapiero and Tew, 2003). Zinc deficiency negatively affects the epidermal, central nervous, immune, gastrointestinal, skeletal, and reproductive systems (Salgueiro et al., 2000,2002; Tapiero and Tew, 2003; Verstraeten et al, 2004).

The exposure to elevated levels of Zn and zinc-containing compounds may cause many adverse effects in the gastrointestinal, hematological, and respiratory systems together with the alterations in the cardiovascular and neurological systems of humans (Nriagu, 2011). An excessive Zn intake leads to acute adverse effects like diarrhea, vomiting, and headache. Zinc chronic toxicity is reflecting in the effects like functional impairment in immunological response, reduced copper status, altered Fe function, or cholesterol metabolism (Scherz and Kirchhoff, 2006).

D. Manganese

Manganese (Mn) is an essential trace element required for a variety of biological processes. The highest Mn levels are concentrated in tissues with high-energy demand, such as brain, and in retina and dark skin with the high content of pigment. Further, bone, liver, pancreas, and kidney contain obviously high Mn concentration, too (Aschner and Aschner, 2005).

Mn is involved in the metabolism of protein, lipid, and carbohydrate, and performs as various enzymes cofactors. Mn is needed for normal immune function, regulation of blood sugar and cellular energy, reproduction, digestion, bone growth, aids in defense mechanisms against free radicals, and together with vitamin K, it supports blood clotting and hemostasis and finally, it is essential for the development and function of the brain (Aschner and Aschner, 2005; Takeda, 2003).

A large portion of Mn is bound to manganese metalloproteins. Approximately 3-5% of ingested Mn is absorbed and it is cleared from the blood by the liver and excreted in bile (Mergler, 1999). Manganese absorption is influenced by the presence of other trace elements, phytate, and ascorbic acid (Aschner and Aschner, 2005).

Manganese deficiency can lead to several diseases including osteoporosis, epilepsy, impaired growth, poor bone formation and skeletal defects, abnormal glucose tolerance, and altered lipid and carbohydrate metabolism (Aschner and Aschner, 2005; Nkwenkeu et al., 2002).

Manganese toxicity is associated with damaged ganglia structures and leads to neuropsychiatric symptoms and behavioral dysfunction reminiscent of Parkinson's disease, which is the most common form of parkinsonism and is caused by neurodegenerative disease, drugs, toxicants, and infections (Cersosimo and Koller, 2006; Nkwenkeu et al., 2002; Ordofnez-Librado et al., 2010). High liver Mn content has been reported in alcoholic liver disease and it may affect hepatic fibrogenesis (Rodriguez-Moreno et al., 1997).

III. REQUIREMENTS OF MINERALS BY HUMANS

An adequate intake of minerals is essential for a high nutritional quality of the diet and contributes to the prevention of chronic nutrition-related diseases and degenerative diseases including cancer, cardiovascular disease, Alzheimer's disease, and premature aging (Fenech and Ferguson, 2001; Kersting et al., 2001). However, too high intakes of trace elements could cause toxicity and too low intakes of trace elements may result in nutritional deficiencies (Goldhaber, 2003).

Dietary Reference Intakes (DRIs) are used quite a lot and refer to a set of four nutrient-based reference values that represent the approach to provide quantitative estimates of nutrient intakes. The DRIs replace and expand on the Recommended Dietary Allowances (RDAs) for the United States and the Recommended Nutrient Intakes (RNIs) for Canada. The DRIs consist of the RDAs, the Tolerable Upper Intake Level (UL), the Estimated Average Requirement (EAR), and the Adequate Intake (AI). Generally, each of these values represents average daily nutrient intake of individuals in the diet (Goldhaber, 2003; Murphy and Poos, 2002; Parr et al., 2006; Trumbo et al., 2001; Yates et al., 1998). In addition, dietary intake data for minerals could be assessed within the context of the bioavailability and other factors affecting the utilization of elements by the human body, such as age, sex, and health aspects (Dokkum, 1995).

Table 29.1 shows the recommended daily intakes (RDIs) for the selected trace elements. Data vary according to various countries and their values are adequate of diverse dietary pattern and different levels of these elements in the population of these countries.

In light of the essentiality of trace elements in adequate dietary intakes on one side and the toxicity of trace elements in high-level intakes on the other side, there should be a set of rules for physiological benefit and safe intakes of trace elements. Table 29.2 shows the UL for selected elements suggested for the United States and Australia.

IV. CONTENT OF MINERALS IN SEAWEED

Seaweeds are a well-known source of minerals and their levels depend on different seaweed genera. Formerly, brown seaweed was used for the production of soda and potash and it has also been a source for iodine

TABLE 29.1 RDIs of selected macroelements and microelements in various countries

EU (mg/day) USA (mg/day) Australia (mg/day) Asia (mg/day)

Macroelements

TABLE 29.1 RDIs of selected macroelements and microelements in various countries

EU (mg/day) USA (mg/day) Australia (mg/day) Asia (mg/day)

Macroelements

Calcium

800a

1000b

1000c

700d

Chloride

800a

2300e

Magnesium

375a

400f

400c

230d

Phosphorus

700a

700f

1000c

Potassium

2000a

4700e

Sodium

1500e

Microelements

Chromium

0.04a

0.035g

Copper

1a

0.9g

Fluoride

3.5a

4f

Iodine

0.15a

0.15g

0.15c

0.15d

Iron

14a

8g

8c

15d

Manganese

2a

2.3g

Molybdenum

0.05a

0.045g

0.045c

0.34d

Selenium

0.055a

0.055h

0.07c

Zinc

10a

11g

14c

6.5d

a European Commission (2008). b Institute of Medicine (2011).

c National Health and Medical Research Council (2006). d International Life Sciences Institute—Southeast Asia Region (2005). e Institute of Medicine (2005). f Institute of Medicine (1997). g Institute of Medicine (2001). h Institute of Medicine (2000).

a European Commission (2008). b Institute of Medicine (2011).

c National Health and Medical Research Council (2006). d International Life Sciences Institute—Southeast Asia Region (2005). e Institute of Medicine (2005). f Institute of Medicine (1997). g Institute of Medicine (2001). h Institute of Medicine (2000).

TABLE 29.2 ULs of selected macroelements and microelements in various countries

Australia (mg/day)

Macroelements

Calcium

Chloride

Magnesium

Phosphorus

Sodium

Microelements

Copper

Fluoride

Iodine

Iron

Manganese

Molybdenum

Selenium

Zinc

Boron

Nickel

Vanadium

2500a

3600c

350d

4000

2300

1.1e

11e 2e

0.4f

40e 20e 1e

2500b

350b

4000b

2300b

10b 10b 1.1b 45b

0.4b 40b a Institute of Medicine (2011).

b National Health and Medical Research Council (2006). c Institute of Medicine (2005). d Institute of Medicine (l997). e Institute of Medicine (2001). f Institute of Medicine (2000).

production for many years (Chapman, 1980). Nowadays, seaweeds are considered as a potential material for the production of different nutraceu-ticals and food supplements (Martinez-Navarrete etal., 2002; Shahidi, 2009).

Mineral content of widely used seaweeds is documented and has been very changeable in different genera across all groups of brown, red, and green seaweeds. Generally, macroelements in seaweeds have been determined in relatively low concentrations, but levels of trace elements have frequently reached the high values which exceeded RDIs. Some of the seaweeds are excellent contributors, especially of iodine and iron.

A. Contribution of seaweed minerals to daily requirements

Seaweeds could be excellent contributors of some microelements to RDIs, as it is documented in Tables 29.3 and 29.4. The contents of I and Fe, Mn, and Zn have been mentioned in mg/8 g of dry matter of particular

TABLE 29.3 Iodine content (mg/8 g) in seaweeds and its contribution to RDI (%)

% RDI

% RDI

% RDI

EU, USA,

EU, USA,

EU, USA,

Brown algae

mg/

Australia, Asia

Red algae

mg/

Australia, Asia Green algae

mg/

Australia, Asia

RDI—I (mg/day)

8 g

0.15

RDI—I (mg/day)

8 g

0.15

RDI—I (mg/day)

8 g

0.15

Sargassum

47.51

31,675

Gracilaria lemaneiformisb

34.09

22,725

Enteromorpha spp.c

60.30

40,200

vachellianum"

S. henslowianum"

41.57

27,717

Gracilaria fergusonid

31.92

21,280

Ulva spp.c

1.30

867

Laminaria digitatac

34.00

22,667

Gracilaria fergusonid

16.87

11,248

Codium fragilea

1.23

821

Ecklonia radiatae

31.92

21,280

Palmaria palmatac

5.10

3400

Ulva fasciatad

1.03

688

Ecklonia radiatae

29.76

19,837

Rhodomela confervoidesa

3.45

2300

Enteromorpha intestinalisa

0.92

612

Laminaria japónica"

24.32

16,213

Gracilara confervoides"

2.82

1883

Ulva rigidaf

0.52

350

Laminaria japonicab

24.32

16,213

Corynomorpha prismaticad

2.38

1584

Monostroma fragile

0.51

339

S. parvifoliuma

17.26

11,504

Polysiphonia urceolatea

2.34

1562

Ulva lactucaa

0.43

287

Macrocystis pyriferae

16.93

11,284

Chondrus crispusc

1.90

1267

Ulva pertusaa

0.27

177

Undaria pinnatifidaa

12.57

8379

Laurencia okamurai"

1.80

1199

Ulva stenophyllae

0.22

144

Hormosira banksiie

8.33

5552

Gelidium amansila

1.63

1087

Ascophyllum

5.80

3867

Gracilaria corticatad

1.49

992

nodosumc

Sargasso NIES-09f

4.20

2801

Sarcodia ceylanicad

1.43

955

Undaria pinnatifidac

3.20

2133

Corallina piluliferaa

1.29

860

Himanthalia elongatac

2.80

1867

Cheilosporum spectabiled

1.25

832

Sargassum thunbergiia

2.69

1794

Leathesia difformesa

1.04

693

Undaria pinnatifidaf

2.44

1630

Porphyra umbilicalisc

0.94

627

1252

1086

" HouandYan (1998). h Wen et al (2006). c MacArtain et al. (2007). d Mageswaran et al. (1985). f Smith etal (2010). f Romaris-Hortas et al. (2011).

Durvillaea antarctica

2.33

Sargassum

2.18

kjellmamanum"

Puncyaria

1.88

plantaginea"

Sargassum

1.63

kjellmamanum"

Chnoospora fastigiatad

1.46

Spyridia aculeatad

0.90

597

Myelophycus simplex"

0.76

509

Dictyopteris divaricate"

0.75

498

Gloeosiphonia capillaris"

0.65

433

Palmaria palmati/

0.62

412

Ceramium boydenoo"

0.57

379

TABLE 29.4 Content of iron, zinc, and manganese (mg/8 g) in seaweed and their contribution to RDIs (%)

Brown algae 8 g EU USA Australia Asia Red algae 8 g EU USA Australia Asia Green algae 8 g EU USA Australia Asia

(mg/day) Colpomenia 41.8

sinuosa" Puncyaria 31.2

plantaginea" Sargassum 23.8

thunbergii" Laminaria digitatac 22.1 Scytosiphon 17.9

lomentariusa Sargassum 14.6

kjellmanianum"

Undaria 5.05 pinnatifidaf

Padina 2.46

h gymnospora

Hijikia fusiformef 2.00

298 522 522 279

223 390 390 208

170 297 297 158

158 276 276 147

128 223 223 119

104 182 182 97

51 46 36 78

25 22 18 38

20 18 14 31

Myelophycus 49.7

simplex"

Polysiphonia 43.4

urceolate"

Dictyopteris 25.3

divaricate'

Corallina piluliferaa 24.7

Leathesia difformesa 22.0

Gelidium amansila 20.3

Rhodomela 18.0

confervoidesa

Porphyra tenerae 14.7

Chondrus ocellatusg 2.27

Spyridia clavatah 1.20

Acanthophora 0.82 spiciferah

355 621 621 331

310 543 543 289

181 317 317 169

176 309 309 165

157 275 275 146

145 254 254 135

129 226 226 120

105 184 184 98

23 21 16 35

12 11 9 18

Codium fragilea 75.4

Ulva pertusaa 46.3

Ulva clathratab 33.4

Ulva rigidad 22.6

Monostroma 19.0

fragile"

Ulva lactucaa 16.3

Ulva clathratab 1.51 Caulerpa racemosai 0.55 Ulva stenophyllaj 0.49

539 943 943 503

331 579 579 309

238 417 417 223

162 283 283 151

136 238 238 127

116 203 203 108

15 14 11 23

Laminaria japonicak 1.07 11 10 8

16 Gracilaria sp.h

Sargassum 0.86 9 8 6

stenophyUum'1 Mn

Laminaria japonicak 2.55 128 111

Puncyaria 1.43 72 62

plantaginea'1

S. hensloiinanunf 1.33 67 58

Sargassum 0.99 50 43 vaclielliamwf

13 Palmaria palmatae

(mg/day) Porphyra teñerae Ceramium boydenoo'1 Rhodomela confervoides'1 Gloeosiphonia capillaris'1 Polysiphonia urceolate'1

1 Peña-Rodríguez et ai. (2011). c MacAxtain et ai. (2007). d Taboada et ai. (2010). f Misurcová et ai. (2009).

Kikunaga et al. (1999). s McDermid and Stuercke (2003). h Karez et al. (1994). ' Kumar et al. (2011). i Smith et al. (2010). 1 Wen et al. (2006).

2.88 144 125

2.34 117 102

0.93 47 40

0.82 41 36

0.82 41 36

12 Caulerpa 0.43

veravelensis'

Codiumfragüé1 2.22 111 97

Ulva stenophyiy 1.54 77 67

Ulm pertusa" 0.82 41 36

seaweed genera from groups of brown, red, and green together with their percentage participation on the RDIs of the minerals mentioned above. According to reported data about the seaweed consumption in Asian countries, the amount of 8 g of seaweed dry matter was considered as an average daily intake (MacArtain et al., 2007; Miyake et al., 2006). The seaweed participation on RDI was calculated for EU countries, the United States, Australia, and Asia. The conversion factor of 8 g was used as a daily intake for all countries though daily seaweed consumptions are lower in EU countries, the United States, and Australia. Unfortunately, data about them were not available. The participation values of particular seaweed genera on RDI were evaluated from data from several studies (Hou and Yan, 1998; Karez et al., 1994; Kikunaga et al., 1999; Kumar et al., 2011; MacArtain et al., 2007; Mageswaran et al., 1985; McDermid and Stuercke, 2003; Misurcova et al., 2009; Pern-Rodriguez et al., 2011; Romaris-Hortas et al., 2011; Smith et al., 2010; Taboada et al., 2010; Wen et al., 2006).

Due to high iodine concentration in seaweeds, many of them could be utilized as natural sources for the production of iodine nutraceuticals; brown seaweed of genera Sargassum, Laminaria, Ecklonia, Macrocystis, Undaria, Ascophylum, and Durvillaea; red seaweed of genera Gracilaria, Palmaria, Chondrus, Laurencia, and Gelidium; and even green seaweed of genera Enteromorpha, Ulva, Codium, and Monostroma. Besides the well-known seaweed genera, some other seaweed genera which are used in a lesser extent—Himalanthia and Chnoospora from brown seaweed, further Corynomorpha, Polysiphonia, Sarcodia, Coralina, Cheilosporum, Leathesia, Spiridia, and Myelophycus from red seaweed genera—could be considered as an abundant source of iodine. However, the extent of utilization of these seaweeds for iodine production should be considered because of their expanse occurrence. Table 29.3 shows the participation of selected seaweeds from all seaweed groups on the RDI whose iodine value is equal for the EU, the United States, Australia, and Asia. Seaweeds with the highest content of iodine, that is, Gracilaria lemaneiformis—red macro-alga, Sargassum vachellianum—brown macroalga, and Enteromorpha spp.— green alga, exceed the RDI up to 200, 300, and 400 times, respectively (Hou and Yan, 1998; MacArtain et al., 2007; Wen et al., 2006). Finally, great differences were observed not only between various seaweed genera but also within the same genus.

Further, this review is focused on the concentrations of Fe, Zn, and Mn in 8 g of dry matter of different seaweed genera and their participation on the RDIs as it is shown in the Table 29.4. Seaweeds from all groups of green, brown, and red are the excellent contributors of Fe. The highest participation on RDI was observed in green seaweed Codium fragile, red seaweed Myelophycus simplex, and brown seaweed Colpomelia sinuosa as their iron contents exceeded RDIs in a range from 3 to 10 times (Hou and

Yan, 1998). The other seaweed genera such as green Ulva and Monostroma, red Polysiphonia, Dictyopteris, Corallina, Leathesia, Gelidium, Rhodomela, and Porphyra, and finally brown seaweed genera Puncyaria, Sargassum, Laminaria, and Scytosiphon contain high amount of Fe. Considering Zn and Mn, their amounts across all seaweed groups do not reach the RDIs. Their participation on RDIs was mostly in the units and tens of percents except from Laminaria japonica, Porphyra tenera, Ceramium boydenoo, and C. fragile, whose concentrations of Mn exceeded 100% of RDI (Hou and Yan, 1998; Misurcova et al., 2009; Wen et al., 2006).

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