Next Article in Journal
The Demography and Practice of Australians Caring for Native Wildlife and the Psychological, Physical and Financial Effects of Rescue, Rehabilitation and Release of Wildlife on the Welfare of Carers
Next Article in Special Issue
Effects of Activated Charcoal-Herb Extractum Complex on Antioxidant Status, Lipid Metabolites and Safety of Excess Supplementation in Weaned Piglets
Previous Article in Journal
The Meat Paradox, Omnivore’s Akrasia, and Animal Ethics
Previous Article in Special Issue
Nutritional Regulation of Gut Barrier Integrity in Weaning Piglets

Animals 2019, 9(12), 1126; https://doi.org/10.3390/ani9121126

Review
Seaweeds in Pig Nutrition
1
Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Via dell’Università 6, 26900 Lodi, Italy
2
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, Via Celoria 10, 20133 Milan, Italy
*
Author to whom correspondence should be addressed.
Received: 24 October 2019 / Accepted: 9 December 2019 / Published: 12 December 2019

Abstract

:

Simple Summary

In pig nutrition, alternative and safe supplements are needed to enhance the pigs’ health and welfare. Natural feed components, such as herbs and plant extracts, are of great importance in animal nutrition, and marine macroalgae can be considered as supplements positively influence animal health parameters. Seaweeds possess several bioactive molecules that are studied for their prebiotic, anti-microbial, antioxidant, anti-inflammatory and immunomodulatory effects. Seaweed benefits are related to their content of sulfated polysaccharides, phlorotannins, diterpenes, omega-3 polyunsaturated fatty acids, minerals and vitamins. This paper reviews the following biological functions of seaweeds and seaweed extracts in pig nutrition: prebiotics, anti-microbial, antioxidant, anti-inflammatory and immunomodulatory effects, promoting intestinal well-being and improving digestibility.

Abstract

Seaweeds are macroalgae, with different sizes, colors and composition. They consist of brown algae, red algae and green algae, which all have a different chemical composition and bioactive molecule content. The polysaccharides, laminarin and fucoidan are commonly present in brown seaweeds, ulvans are found in green seaweeds and, red algae contain a large amount of carrageenans. These bioactive compounds may have several positive effects on health in livestock. In order to reduce the antimicrobials used in livestock, research has recently focused on finding natural and sustainable molecules that boost animal performance and health. The present study thus summarizes research on the dietary integration of seaweeds in swine. In particular the influence on growth performance, nutrients digestibility, prebiotic, antioxidant, anti-inflammatory, and immunomodulatory activities were considered. The review highlights that brown seaweeds seem to be a promising dietary intervention in pigs in order to boost the immune system, antioxidant status and gut health. Data on the use of green seaweeds as a dietary supplementation seems to be lacking at present and merit further investigation.
Keywords:
seaweeds; dietary supplement; pig

1. Introduction

Marine-derived bioactive compounds are valuable as food and feed ingredients due to their biological activities [1]. The term “algae” includes photosynthetic organisms that are usually divided into microscopic unicellular organisms, identified as microalgae, and multicellular large-size organisms defined as macroalgae or seaweed.
Microalgae usually grow in seawater and freshwater environments and can be prokaryotic, similar to cyanobacteria (Chloroxybacteria), or eukaryotic, similar to green algae (Chlorophyta). Diatoms (Bacillariophyceae), green algae (Chlorophyceae) and golden algae (Chrysophyceae) are the most abundant but blue-green algae (Cyanophyceae) are also defined as microalgae [2]. The bioactive molecules of microalgae are used as food and feed supplements [3].
Seaweeds are marine organisms and comprise thousands of species, which are classified on the basis of their pigmentation: brown seaweeds (Phaeophyceae), red seaweeds (Rhodophyceae) and green seaweeds (Chlorophyceae).
There are around 1800 species of brown seaweeds include, only 1% of which are recognized from freshwater and the size range varies from 20 m to 30 cm long. The brown color of these algae is related to the main content of carotenoid fucoxanthin, which masks β-carotene, violaxanthin, diatoxanthin, and chlorophyll. The main polysaccharides are laminarin, fucoidans and alginates, and the cell walls are composed of cellulose and alginic acid [4].
Like brown seaweeds, red algae (about 6100 species) are marine, but are able to photosynthesize in deeper water. The size ranges from thin films to filamentous and membranous forms of 1 m. The color results from the presence of the pigments, phycoerythrin and phycocyanin which mask α, β carotene, lutein, zeaxanthin and chlorophyll [5,6]. The main reserves are typically floridean starch and floridoside, and the cells wall are made up of long-chain polysaccharide agars, carrageenans and cellulose [7].
There are around 2200 species of green seaweeds. They are of similar size to red seaweeds, only 10% are marine, and their color is related to the presence of chlorophyll. The reserves are composed of starch, and the cells wall are made up of polysaccharide ulvan [8].
In 2015, world production of algae amounted to 30.4 million tons, of which about 96% from aquaculture and only 1 million tons from harvesting of wild stock [9].
Due to their nutritional value and the content of bioactive molecules, seaweeds are often used as food, herbal medicines, dietary supplements, as a source of agar, alginate and carrageenan for several industrial applications, and as a fertilizer [10,11].

2. Chemical Composition

Several studies have been carried out in order to identify the nutritional composition and secondary metabolites of various seaweed species. In fact, it has been reported that seaweed contains several metabolites, such as the sulfated form of polysaccharides, omega 3 fatty acids, phlorotannins, diterpenes, vitamins and minerals, thus demonstrating positively health effects such as antibacterial, antioxidant, anti-inflammatory functions [12]. The chemical composition of seaweeds was found to vary in relation to their species and genera, harvesting period, and habitat condition (water temperature, light, salinity, nutrients) [13].
The chemical composition and mineral content of brown, red and green seaweeds are reported in Table 1. As shown, there is a different nutritional composition range for brown, red and green seaweed, although in the same genus, the values are comparable [14].
Of the brown seaweeds, common species such as Ascophyllum, Laminaria, Saccharina, Macrocystis, Fucus, and Sargassum was considered [15]. Brown seaweed shows a highly variable composition but presented a low protein (7.6–12.6% dry matter, DM) and fat content (0.8–6% DM). The Fucus species presents the highest protein content (12.9% DM), followed by Sargassum (10% DM), Laminaria (9.4% DM) and the Ascophillum nodosum (7.4% DM), as observed by Fleurence et al. [16]. The fat content of brown seaweeds is generally lower with an average value of 3.2% DM, and high values are observed in Fucus spp. and Ascophillum nodosum [17,18].
Red seaweeds contain a higher protein content (16.9% DM) and fat content (8.9% DM) than brown seaweeds [19].
The green seaweed Ulva lactuca has a protein content (16.2% DM) compared to red seaweeds and a comparable fat content (1.3% DM) with brown seaweeds [20]. The fat content of the studied seaweeds varies between 0.8 to 8.9% which is a similar range reported for other seaweeds species [13].
All seaweeds are characterized by a higher ash content (19.3–27.8% DM) than those observed in edible plants, in fact they are a considerable rich source of minerals for livestock nutrition [18,19].
Seaweeds are rich in potassium, sodium and calcium. Although there is a high variability, in general, the sodium and potassium contents in Ulva spp. are lower than those reported for red and brown seaweeds. A higher content of potassium has been observed in Palmaria palmata, Macrocystis pyrifera, and Laminaria spp. [19]. All seaweeds present higher levels of calcium than phosphorous, and thus may be a possible natural source of calcium in livestock. Seaweeds are also a source of essential trace elements such as iron, manganese, copper, zinc, cobalt, selenium and iodine. In particular, iron is abundant in all the species considered, and the iodine content is higher in brown than in red and green seaweeds (Laminaria spp., with a range 833–5100 mg/kg DM), and a higher zinc content has been observed in red and brown than in green seaweed.
The bioavailability of minerals is related to the fiber content of seaweeds. In addition, the interactions with several polysaccharides, such as alginates and agar or carrageenan, lead to the formation insoluble complexes with minerals, decreasing their bioavailability [21]. The mineral content in the insoluble indigestible fraction residues was higher in brown than in red seaweeds with a range of 150–260 g/kg [22]. Some studies in vitro and in rats have been performed on the bioavailability of minerals [21]. In an in vitro study of 13 seaweed species, only Palmaria palmata and Ulva lactuca showed higher Fe bioavailability than spinach, although six species had a higher Fe content. The apparent absorption values of Na and K were significantly higher in rats supplemented with Laminaria spp., while Mg absorption was not affected. It has also been reported that Laminaria spp. is rich in alginates, which probably hampers the bioavailability of Ca. The absorption of inorganic I, which is the predominant form in brown seaweeds, was observed to be moderate (20–70%). Therefore, the low bioavailability may be related to the iodine interaction with other compounds in the seaweed matrix.
The vitamin content showed that seaweeds are a source of water-soluble vitamins (B1, B2, B3 and C) and fat-soluble vitamins (E and provitamins carotenoids, with vitamin A activity). Seasonal effects have a great influence on vitamin content. Most of the red seaweeds, such as Palmaria palmata contained a considerable amount of provitamin A and vitamins B1 and B2. The brown seaweeds Laminaria spp., Ascophillum nodosum and Fucus spp. showed a high content of vitamins E and C [23].
The amino acid composition of different seaweeds species is reported in Table 2. Red seaweeds have a higher quality of protein than brown and green seaweeds [24], however there is a considerable difference in the amino acidic content among seaweeds, in relation to the different seasons. It has been reported that seaweeds have a low content of methionine and histidine [25,26]. Leucine was the most abundant amino acid, ranging from 2.43 g/kg DM to 6.63 g/kg DM for Palmaria palmata. and Ascophillum nodosum respectively, followed by lysine (1.42–7.60 g/kg DM), threonine (1.26–5.17 g/kg DM) and valine (2.25–5.87 g/kg DM). Glutamic and aspartic acids are the most common amino acids found in the non-essential fraction which are responsible for the flavor and taste of seaweeds [27].
The in vitro protein digestibility (IVPD) was mid-range (82–87%) for Saccharina latissima and Palmaria palmata, and lower (79%) for Ascophillum nodosum and Fucus spp. The Red seaweed IVPD of red seaweeds had an average value of 85%, while the brown seaweeds had a lower IVPD, with an average value of, 79.7%. A significant inverse correlation between the IVPD and total phenolic content was also observed [28].
Seaweeds also possess several biological activities due to the presence of several bioactive compounds, such as phenolic compounds, carotenoids, tocopherols, polysaccharides, and peptides. Seaweeds are rich in carboxylated and sulfated polysaccharides, such as alginates, ulvans and fucoidans: their composition and content depend on the algae species and of environmental factors such as the season and temperature. The total polysaccharide content (% DM) is 29–67% in green algae (Chlorophyta), 10–59% in red algae (Rhodophita) and 10–75% in brown algae (Phaecophyta). [29].
A major component of brown seaweed cell walls is a salt form of alginic acid, alginate with the content ranging from 140–400 g/kg DM [30]. Brown seaweed walls are also rich in fucoidans, which are saccharide units with different degrees of sulphation. Several species contained fucoidan with distinct structural characteristics, and thus the different types of functional components have various biological applications. The fucoidan content varies in relation to seaweed species and season, although the content ranges from 20 to 200 g/kg DM, with the highest value in Fucus vesiculosus [17,30,31]. Laminarin, composed of (1,3)-b-D-glucopyranose residues, is the main reserve carbohydrate of brown seaweeds with a content ranging from 0 to 300 g/kg DM. In Laminaria spp. and Saccharina latissima a high content of laminarin has been reported, while, Ascophyllum nodosum and, Fucus spp. presented a low laminarin content [17,30,31]. Laminarin presents prebiotic, immunomodulator and antioxidant activities [32].
The cell walls of red seaweeds are mainly composed of sulfated galactan such as carrageenans (content range: 220–770 g/kg DM) and agars (content range: 210–420 g/kg DM). Some red seaweed species contain xylan (in Palmaria palmata approximately 350 g/kg DM) and porphyran (average content 480 g/kg DM). The floridean starch is the main carbohydrate reserve with a content ranging from 250 to 420 g/kg DM [17,30,31].
Ulvan is one of the main sulfated polysaccharides from green seaweed cell walls with anticancer, antioxidant, antihyperlipidemic, and anticoagulant activities [33] and a content ranging from 400 to 500 g/kg DM [30].
For details and information on the monosaccharide composition of the different polysaccharides mentioned, some excellent reviews are available [34,35].
Considering their valuable source of bioactive molecules, seaweeds have been studied as feed supplements in livestock, particularly in pigs in order to boost growth performance and health [36]. Seaweeds exhibit prebiotics, anti-microbial, antioxidant, anti-inflammatory and immunostimulant properties and obviously effective absorption of dietary nutrients.

3. Influence on Growth Performance

Brown seaweeds have a generally positive effect on growth, as presented in Table 3. Some interactions between seaweeds bioactive molecules and dietary components should be probable, but considering the heterogeneity of seaweeds species, the effects on growth performances have to be firstly analyzed in relation to seaweed supplement, and bioactive molecules content. With dietary integration in sows at the end of gestation and during lactation, an increase in average daily gain (ADG) of suckling piglets has been observed (from +11.8 to +32.3% compared to the control group). Most of the studies we reviewed involve the dietary supplementation of brown seaweeds in weaned piglets. In weaned piglets, improvements of ADG are observed. The ADG of piglets fed brown seaweeds is higher than the ADG of piglets fed a control diet with an increase of between +4.6 and +40.8%.
Draper et al. [56] and Ruiz et al. [57] appear to be the only two authors to report the effects of long–term dietary supplementation with brown seaweed from weaning to slaughter on ADG. In this case, the influence on ADG was limited but statistically significant, and ranged from +1.2 to +3.3%. Bouwhuis et al. [58,59] evaluated the effects of brown seaweed supplementation on pigs’ growth performance after being challenged with Salmonella Typhimurium. When the challenge occurred in post–weaning, no significant effect was observed; in pigs with a live weight of 30 kg, the seaweed supplement led to a significant increase in growth (+16%). It is possible that the bioactive compounds of seaweeds are not able to positively modulate the immune system of the post–weaning piglet which is still immature.
Positive effects on growth are related to the improvement in digestibility and overall health conditions of piglets due to the prebiotic effects of seaweed polysaccharides, as described in the following sections. The effects of seaweed dietary supplementation on the improvement in antioxidant status and the decrease in inflammatory condition may contribute to reduce energy and amino acidic expenditure.

4. Influence on Digestibility

Many authors have evaluated the effects of algae supplementation on the digestibility of the diet in pigs, as presented in Table 4.
All digestibility trials were conducted in weaned piglets, except for the study by Gardiner et al. [72] which investigated male pigs with a 45 kg live weight. The Ascophyllum nodosum does not appear to have a significant influence on diet digestibility [42,72]. On the other hand, Laminaria digitata, Laminaria spp., Ecklonia cava and brown seaweed, titrated in alginates, showed positive effects on the digestibility of nitrogen (N), gross energy (GE), fiber (NDF) and ash in various experiments. Significant improvements from +5.1 and +8% in N digestibility are reported. Also for GE, dietary integration with seaweed improved the digestibility, with an increase of between +3.3 and +10%.
Some authors have also observed that introducing laminarin and fucoidans in the formula increases the digestibility of the fibrous fraction (NDF). The animals fed seaweed showed a higher digestibility of NDF (+39 to +73%) compared to the control group. Finally, ash digestibility presented values that in the seaweed group were 25.9–82.4% higher than in the control.
The improvement in nutrient digestibility is related to the influence of the seaweed constituents, in particular carbohydrates and antioxidants, on microbiota and on the villous architecture with an increase in absorptive capacity and nutrient transporters [73]. These effects are also related to the trophic effect on the intestinal mucosal cells of volatile fatty acid production (i.e., butyric acid).

5. Prebiotic Function

Seaweeds are rich in carboxylated and sulfated polysaccharides, such as alginates, ulvans and fucoidans which all act as prebiotics with positive effects on gut health. According to FAO [74] a prebiotic is a ‘non–viable food component that confers a health benefit on the host associated with the modulation of microbiota’. The health benefit is associated with the stimulated activity/growth of beneficial bacteria and the higher production of short chain fatty acids (SCFAs) with direct impact on gut health and also an immunomodulatory effect, as reported below.
Several papers have analyzed the prebiotic effects of algae [5,29,73,75,76,77,78,79]. In swine, 24 studies have been published in the last 10 years on the effects of supplementation with brown seaweeds, or their extracts, on gut health: Ascophyllum nodosum [42,60,72], Ecklonia cava [63], Laminaria digitata [64,80,81], Laminaria hyperborea [82,83], Laminaria digitata and Laminaria hyperborea association [84], Laminaria spp. [58,59,65,67,69,70,71,85,86,87,88,89,90]. Brown seaweeds titrated in alginic acid polysaccharides have also been studied [63]. Most of the studies were carried out on weaned piglets (14 trials), considering that the weaning phase is a critical period with a high incidence of enteric pathologies. Some studies were carried out on growing pigs ranging between 14 and 65 kg LW, and some others on gestating and lactating sows.
In general the compounds present in the brown seaweeds (in 20 trials the supplement was titrated in laminarin and/or fucoidans) stimulated the growth of Lactobacilli [61,64,65,70,71,72,81,82,83,84], and reduced the enterobacteria population or Escherichia coli [42,58,61,63,64,69,71,72,83,84,85,87]. Brown seaweed supplements supported the growth of Bifidobacteria species in the ileum in piglets [61,80,81]. Gut health is modulated by laminarin and/or fucoidans, with the microbial production of short–chain fatty acids (SCFAs), in particular butyrate [81,84,86]. Glucose are the main energy source for small intestinal epithelial cells, and SCFAs are the main energy source for caecum and colon cells, stimulating cell growth [91]. Several studies have reported that brown seaweeds have a positive influence on gut morphology [63,87,88,92]. Supplementation with Ecklonia cava (0.05 and 0.15% of dietary inclusion), linearly improved villi height in the ileum [63]. In weaning piglets, maternal dietary supplementation with laminarin and fucoidans (1 and 0.8 g/day) after 83 days of gestation and during lactation increased villi height in the jejunum and ileum (+43 and +88% respectively) [87]. According to Heim et al. [88], maternal dietary treatment with fucoidans (0.8 g/day) had no influence on the small intestine morphology, while laminarin increased the villus height in the ileum (+13%) at day 8 post–weaning. In vitro and in vivo experiments carried out by Dierick et al. [42] revealed that native seaweeds Ascophyllum nodosum suppressed in vitro the gut flora counts and metabolic activity (production of organic acids), while in vivo, a significant better lactobacilli/E. coli ratio was found in the small intestine. Michiels et al. [60] on the other hand observed no significant effects on gut health with the use of the same seaweed in weaned piglets, most probably due to the already high digestible basal diet, including lactose. To probiotic activity algae associate bacteriostatic and antibacterial activities recently reviewed by Perez et al. [93]. In particular potential applications in aquaculture [94] and in the pharmaceutical and food industry [95], have been evaluated.

6. Antibacterial Function

In addition to the probiotic action that positively modulates the intestinal microbiota, the seaweeds and their extracts show a specific anti-bacterial and / or bacteriostatic action [8,96,97]. Phlorotannins, fatty acids, peptides, terpenes, polysaccharides and sulphated polysaccharides, and several other bioactive compounds have been reported as bacterial inhibitors (Table 5). A very interesting action of seaweed extracts is the effectiveness against methicillin resistant Staphylococcus aureus and vancomycin–resistant Enterococcus faecium [98].
Antibacterial activity is expressed across multiple mechanisms: inhibition of oxidative phosphorylation and link with compounds in the bacterial cell wall and increased permeability of the cytoplasmic membrane causing cell lysis [97]. At the same time some seaweed compounds, in particular polysaccharides, contribute significantly to the health and well-being of the animals by enhancing the in vivo immune response.
The variability of bioactive compounds in seaweeds influences the lab techniques used to obtain antimicrobials ranging from traditional extraction techniques, solid–liquid extraction or liquid–liquid extraction, to the most modern process of supercritical fluid extraction using CO2 ultrasonically-assisted extraction [93]
The potential applications in aquaculture [94] and in the pharmaceutical and food industry [95], have been evaluated, while studies on food producing animals, and in pigs in particular, are limited. Berri et al. [112] evaluated the effect of marine-sulfated polysaccharide extract from the green macroalga Ulva armoricana against seven bacterial strains found in pigs (Table 6).

7. Influence on Antioxidant Function

Seaweeds have antioxidant properties due to the presence of phenols, carotenoid fucoxanthin, tannins and phlorotannins, polysaccharides (fucoidans and laminarans in brown seaweeds; ulvans in green seaweeds and carrageenans, porphyrin and agar in red seaweeds) [113]. The highest concentrations of phenols and phlorotannins have been observed in brown seaweed, up to 12–14% DM in Ascophhyllum nodosum, Fucus spp. and Sargassum spp. [114]. In green and red seaweeds concentrations lower than 1% have been reported [114,115,116].
The carotenoid fucoxanthin has only been detected in brown seaweeds with concentrations of up to 5.000 mg/kg [117,118,119]. Tocopherols are present in all seaweed, with variables concentrations. In brown seaweed higher values have been reported for Fucus spp. and Ascophyllum nodosum (up to 600 mg/kg DM) [120,121] than in Laminaria spp. [122]. Lower concentrations were observed in red seaweeds [122,123], and green seaweeds showed up to 1070 mg/kg DM in Ulva spp. [47].
The effects of dietary seaweeds are reported on serum and plasma antioxidant status, duodenum, jejunum and ileum antioxidant markers and Longissimus dorsi muscle oxidative stability (Table 7).
At the blood level, dietary supplementation with Laminaria spp. extract (laminarin 0.18 g/kg and fucoidans 0.33 g/kg) or brown seaweed (alginates 100 mg/kg) has a strong antioxidant effect in growing pigs [124] and weaned piglets [61,62]. The total antioxidant capacity (TAS), superoxide dismutase (SOD), glutathione (GSH) and catalase activities increased from +14 to +37% with respect to the control group. At the same time, there was a reduction in lipid oxidation with lower values of malondialdehyde (MDA) ranging from 10% to 26% than in the controls. Other authors reported the non-significant effects on serum MDA, using dietary Ascophyllum nodosum [60] and brown seaweeds [62].
Wan et al. [92] observed a significant reduction in the MDA concentration in duodenum, jejunum and ileum of between –35 and −40% and an increase in catalase activity. Finally, some studies have evaluated the oxidative stability of pork during storage time by evaluating thiobarbituric acid-reactive substances (TBARS). The reduction in TBARS concentration for long refrigerated storage times of 14 d, ranged between −21% and −60%. The administration of an extract of Laminaria digitata in liquid form instead of spray–dried appears to affect the antioxidant potential of the extract. The liquid form better exploits the antioxidant potential of the extract, with reductions in TBARS production of –47% compared to –29% with the spray-dried form [125].

8. Anti-inflammatory Function

Many studies have evaluated the anti–inflammatory activity of brown seaweeds, in particular Laminaria digitata, Laminaria hyperborea and Laminaria spp., usually titrated in laminarin and fucoidans [58,59,61,71,80,85,87,88,90,92]. In addition, non-specified brown seaweeds titrated in alginic acid have been evaluated by Wan et al. [61,92]. Of these authors, 8/10 showed anti-inflammatory effects. Walsh et al. [71] reported a lower expression of pro-inflammatory cytokines in the colon of piglets after dietary supplementation with laminarin, but not with fucoidans.
Dietary treatment of gestating and lactating sows with laminarin (1 g/d) and fucoidans (0.8 g/d) reduced the ileal gene expression of IL-6, IL-8, IL-10 of piglets at weaning [87]. Similarly, in piglets born from sows fed diets supplemented with laminarin from 109 d gestation and during lactation, a reduction on the colon IL-6 concentration at weaning and of ileal IL-8 concentration eight days post weaning were observed [88].
In a 28-day trial, Bouwhuis et al. [59] observed the effects of a diet supplemented with laminarin 0.18 g/kg and fucoidans 0.34 g/kg, in 30 kg LW female pigs. After an 11-day adaptation period, pigs were orally challenged with Salmonella Typhimurium. Dietary treatment reduced colon cytokine expression (IL-6, IL-18, IL-22 and TNF-α) 17 days post challenge, thus revealing an anti-inflammatory effect. In addition, in 18 kg LW pigs, laminarin from Laminaria digitata dietary supplementation (0.6 g/kg) significantly increased gut mucin gene expression (MUC2 and MUC4) from 20% to 33% with a protective effect on epithelial cells [127]. McDonnel et al. [90] observed an increase of 16% in mucin gene expression (MUC2) in the ileal in female pigs fed diets supplemented with Laminaria spp. (0.18 g of laminarin and 0.34 g of fucoidan per kg of feed). A study using an in vitro system of porcine intestinal epithelial cells showed that ulvans from Ulva armoricana, a green seaweed, upregulated the gene expression of cytokines such as IL1α, IL1β, L6, IL8, TNFα [112,128].

9. Immunomodulatory Function

Many studies have evaluated the immunomodulatory activity of seaweeds [61,63,85,129,130,131]. In addition to an anti-inflammatory action, laminarin also has an immunomodulatory function. Leonard et al. [85] reported that the dietary supplementation of sows from 109 days of gestation until weaning with Laminaria spp. extract (1 g laminarin and 0.8 g fucoidans/day) increased immunoglobulin G (IgG) and immunoglobulin A (IgA) in sow colostrum by 19% to 25%, respectively. Consequently, an increase in piglet serum IgG was observed (10%).
In another study, the effects were evaluated of sow supplementation with 30 g/day of an extract of Ascophyllum nodosum and Fucus from the 85th day of gestation until weaning on liver and lymphoid organs of piglets. The relative population of CD4 + CD8 + T cells was higher in piglets from treated sows in the thymus, spleen, mesenteric node, liver and in peripheral blood, thus suggesting an important effect of maternal diet on the immune status of 40-day-old piglets [130].
The immunomodulatory effect of green seaweed extract (Ulva armoricana) was evaluated in sows by Bussy et al. [131]. Different levels of inclusion were tested: 2, 8 and 16 g/day during two periods of three days: 34 days before farrowing, before the last vaccine booster against Bordetella bronchiseptica, and one week before farrowing. The higher dietary level increased anti-Bordetella IgG in sow’s blood and colostrum, while with the middle dietary integration, the authors observed an increase in milk IgA. Wan et al. [61] and Choi et al. [63] evaluated the immunomodulatory effects of seaweed fed to weaned piglets. Alginic acid oligosaccharides from brown seaweed increased IgG and IgA concentrations in piglet serum by 20% and 53 %, respectively after 21 days of treatment [61]. No immunomodulatory effect was observed in weaned piglets fed a diet supplemented with different Ecklonia cava concentrations [63]. According to the authors, the result may be the consequence of the low dosage and consequently the low content of fucoidan in the diets (0.056 – 0.112 – 0.168 g/kg, respectively).
In growing pigs (29 kg LW), 0.8% seaweed enhanced the immune function. Pigs were sensitized with the subcutaneous inoculum of sheep red blood cells at days 42 and 49. Seaweed increased the saliva IgA production five times more than the control after 56 days [129]. The concentration of antigen-specific IgG in peripheral blood was higher in the seaweed group, but not significantly due to the high standard deviation.

10. Potential Toxicity

The use of seaweed in swine nutrition may have the following limitations: mineral elements and potentially toxic mineral content. Generally, seaweeds are introduced in pig diets as ingredients/raw materials in a low percentage, thus there is no risk of potential toxicity in this case. In terms of microelements, the first limiting factor is the iodine content which, as reported in Table 1, can reach particularly high concentrations in brown seaweeds. According to NRC [132], tolerance levels in growing pigs and sows are 400 and 1500–2500 mg/kg DM for iodine from iodine salt, respectively. Of the potentially toxic minerals, the first limiting element is arsenic (As) which is found in high concentrations in brown seaweed (Table 8). However, a low content of the most toxic form of arsenic, inorganic arsenic, has been observed in seaweeds. The arsenic content of green seaweed is below the maximum level of 40 mg/kg feed (12% moisture content) set by European feed legislation (Commission Directive 2002/32/EC and amendments).

11. Conclusions

The biological activities of brown seaweeds could be used to improve the health and welfare of pigs. The prebiotic effects and the antimicrobial activities of laminarin and fucoidans may have beneficial effects in the prevention of gastrointestinal diseases and to enhance diet digestibility in post–weaning piglets. Laminarin also has an anti-inflammatory activity, which reduces the pro–inflammatory cytokine response. The seaweed content of antioxidant molecules enhances the antioxidant status and meat oxidative stability. Dietary supplementation with brown seaweed may positively affect the immune system, enhancing immunoglobulin production and modulating cytokine production. In conclusion, brown seaweeds seem to be a promising dietary intervention in pigs in order to enhance the immune system, antioxidant status and gut health. Data on the dietary supplementation with green seaweeds in pigs seem to be lacking at present and merit further investigations.

Author Contributions

C.C. and R.R. designed the study; C.C, R.R., S.C.M., A.D.G. and S.C. operated the investigation and wrote the manuscript; C.C. supervised the investigation and C.C, R.R. S.C.M., A.D.G. and S.C. reviewed and edited the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Rajauria, G.; Cornish, L.; Ometto, F.; Msuya, F.E.; Villa, R. Identification and selection of algae for food, feed, and fuel applications. In Seaweed Sustainability, Food and Non–Food Applications, 1st ed.; Academic Press: London, UK, 2015; pp. 315–345. [Google Scholar]
  2. Guedes, C.; Barbosa, A.; Amaro, C.R.; Pereira, H.M.; Malcata, X. Microalgal and cyanobacterial cell extracts for use as natural antibacterial additives against food pathogens. Int. J. Food Sci Technol. 2011, 46, 862–870. [Google Scholar] [CrossRef]
  3. García, J.L.; De Vicente, M.; Galán, B. Microalgae, old sustainable food and fashion nutraceuticals. Microb. Biotechnol. 2017, 10, 1017–1024. [Google Scholar] [CrossRef] [PubMed]
  4. Peng, J.; Yuan, J.P.; Wu, C.F.; Wang, J.H. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: Metabolism and bioactivities relevant to human health. Mar. Drugs 2011, 9, 1806–1828. [Google Scholar] [CrossRef] [PubMed]
  5. O’Sullivan, L.; Murphy, B.; McLoughlin, P.; Duggan, P.; Lawlor, P.G.; Hughes, H.; Gardiner, G.E. Prebiotics from marine macroalgae for human and animal health applications. Mar. Drugs 2010, 8, 2038–2064. [Google Scholar] [CrossRef]
  6. Koizumi, J.; Takatani, N.; Kobayashi, N.; Mikami, K.; Miyashita, K.; Yamano, Y.; Wada, A.; Maoka, T.; Hosokawa, M. Carotenoid Profiling of a Red Seaweed Pyropia yezoensis: Insights into Biosynthetic Pathways in the Order Bangiales. Mar. Drugs 2018, 16, 426. [Google Scholar] [CrossRef]
  7. Usov, A. Polysaccharides of the red algae. Adv. Carbohydr. Chem. Biochem. 2011, 65, 115–217. [Google Scholar]
  8. Kidgell, J.T.; Magnusson, M.; de Nys, R.; Glasson, C.R.K. Ulvan: A systematic review of extraction, composition and function. Algal Res. 2019, 39, 101422. [Google Scholar] [CrossRef]
  9. Food and Agriculture Organization of the United Nations (FAO). The Global State of Seaweed Production, Trade and Utilization; Globefish Research Program: Rome, Italy, 2018; p. 2. [Google Scholar]
  10. Lee, J.B.; Takeshita, A.; Hayashi, K.; Hayashi, T. Structures and antiviral activities of polysaccharides from Sargassum trichophyllum. Carbohydr. Polym. 2011, 86, 995–999. [Google Scholar] [CrossRef]
  11. Yaich, H.; Garna, H.; Besbes, S.; Paquot, M.; Blecker, C.; Attia, H. Chemical composition and functional properties of Ulva lactuca seaweed collected in Tunisia. Food Chem. 2011, 128, 895–901. [Google Scholar] [CrossRef]
  12. Ganesan, A.R.; Tiwari, U.; Rajauria, G. Seaweed nutraceuticals and their therapeutic role in disease prevention. Food Sci. Hum. Wellness 2019, 8, 252–263. [Google Scholar] [CrossRef]
  13. Marsham, S.; Scott, G.W.; Tobin, M.I. Comparison of nutritive chemistry of a range of temperate seaweeds. Food Chem. 2007, 100, 1331–1336. [Google Scholar] [CrossRef]
  14. Wong, K.H.; Cheung, P.C.K. Nutritional evaluation of some subtropical red and green seaweeds Part II. In vitro protein digestibility and amino acid profiles of protein concentrates. Food Chem. 2001, 72, 11–17. [Google Scholar] [CrossRef]
  15. Murty, U.S.; Banerjee, A.K. Seaweeds: The wealth of oceans. In Handbook of Marine Macroalgae: Biotechnology and Applied Phycology; Se-Kwon, K., Ed.; John Wiley & Sons: Hoboken, NJ, USA, 2012. [Google Scholar]
  16. Fleurence, J. Seaweed proteins: Biochemical, nutritional aspects and potential uses. Trends Food Sci. Technol. 1999, 10, 25–28. [Google Scholar] [CrossRef]
  17. Makkar, H.P.S.; Tran, G.; Heuze, V.; Giger-Reverdin, S.; Lessire, M.; Lebas, F.; Ankers, P. Seaweeds for livestock diets: A review. Anim. Feed Sci. Technol. 2016, 212, 1–17. [Google Scholar] [CrossRef]
  18. Lorenzo, J.M.; Agregán, R.; Munekata, P.E.S.; Franco, D.; Carballo, J.; Sahin, S.; Lacomba, R.; Barba, F.J. Proximate Composition and Nutritional Value of Three Macroalgae: Ascophyllum nodosum, Fucus vesiculosus and Bifurcaria bifurcate. Mar. Drugs 2017, 15, 360. [Google Scholar] [CrossRef]
  19. Cabrita, A.R.J.; Maia, M.R.G.; Oliveira, H.M.; Sousa-Pinto, I.; Almeida, A.A.; Pinto, E.; Fonseca, A.J.M. Tracing seaweeds as mineral sources for farm–animals. J. Appl. Phycol. 2016, 28, 3135–3150. [Google Scholar] [CrossRef]
  20. Burtin, P. Nutritional Value of Seaweeds. Electron. J. Environ. Agric. Food Chem. 2003, 2, 498–503. [Google Scholar]
  21. Circuncisão, A.R.; Catarino, M.D.; Cardoso, S.M.; Silva, A.M.S. Minerals from macroalgae origin: Health benefits and risks for consumers. Mar. Drugs 2018, 16, 11. [Google Scholar] [CrossRef]
  22. Ruperez, P.; Toledano, G. Indigestible fraction of edible marine seaweeds. J. Sci. Food Agric. 2003, 83, 1267–1272. [Google Scholar] [CrossRef]
  23. Dominguez, H. Functional Ingredients from Algae for Foods and Nutraceuticals; Woodhead Publishing Limited: Cambridge, UK, 2013; pp. 228–229. [Google Scholar]
  24. Angell, A.R.; Angell, S.F.; DeNys, R.; Paul, N.A. Seaweed as a protein source for mono–gastric livestock. Trends Food Sci. Technol. 2016, 54, 74–84. [Google Scholar] [CrossRef]
  25. Galland-Irmouli, A.V.; Fleurence, J.; Lamghari, R.; Lucon, M.; Rouxel, C.; Barbaroux, O.; Bronowicki, J.P.; Villaume, C.; Gueant, J.L. Nutritional value of proteins from edible seaweed Palmaria palmata (Dulse). J. Nutr. Biochem. 1999, 10, 353–359. [Google Scholar] [CrossRef]
  26. Biancarosa, I.; Espe, M.; Bruckner, C.G.; Heesch, S.; Liland, N.; Waagbø, R.; Torstensen, B.; Lock, E.J. Amino acid composition, protein content, and nitrogen–to protein conversion factors of 21 seaweed species from Norwegian waters. Appl. Phycol. 2017, 29, 1001–1009. [Google Scholar] [CrossRef]
  27. Saini, R.; Badole, S.L.; Zanwar, A.A. Bioactive Dietary Factors and Plant Extracts in Dermatology; Watson, R.R., Zibadi, S., Eds.; Humana Press: Totowa, NJ, USA, 2013; pp. 73–82. [Google Scholar]
  28. Tibbetts, S.M.; Milley, J.E.; Lall, S.P. Nutritional quality of some wild and cultivated seaweeds: Nutrient composition, total phenolic content and in vitro digestibility. J. Appl. Phycol. 2016, 28, 3575–3585. [Google Scholar] [CrossRef]
  29. Sardari, R.R.R.; Nordberg Karlsson, E. Marine Poly- and Oligosaccharides as Prebiotics. J. Agric. Food Chem. 2018, 66, 11544–11549. [Google Scholar] [CrossRef] [PubMed]
  30. Øverland, M.; Mydland, L.T.; Skrede, A. Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. J. Sci. Food Agric. 2019, 99, 13–24. [Google Scholar] [CrossRef]
  31. Tanna, B.; Mishra, A. Nutraceutical Potential of Seaweed Polysaccharides: Structure, Bioactivity, Safety, and Toxicity. Compr. Rev. Food Sci. Food Saf. 2019, 18, 817–831. [Google Scholar] [CrossRef]
  32. Balboa, E.M.; Conde, E.; Moure, A.; Falqué, E.; Domínguez, H. In vitro antioxidant properties of crude extracts and compounds from brown algae. Food Chem. 2013, 138, 1764–1785. [Google Scholar] [CrossRef]
  33. Pangestuti, R.; Kurnianto, D. Green Seaweeds–Derived Polysaccharides Ulvan: Occurrence, Medicinal Value and Potential Applications. In Seaweed Polysaccharides, Isolation, Biological and Biomedical Applications, 1st ed.; Jayachandran, V., Sukumaran, A., Se-Kwon, K., Eds.; Elsevier Science Publishing Co. Inc.: New York, NY, USA, 2017; pp. 205–221. [Google Scholar]
  34. Xu, S.-Y.; Huang, X.; Cheong, K.-L. Recent Advances in Marine Algae Polysaccharides: Isolation, Structure, and Activities. Mar. Drugs 2017, 15, 388. [Google Scholar] [CrossRef]
  35. Cherry, P.; Yadav, S.; Strain, C.R.; Allsopp, P.J.; McSorley, E.M.; Ross, R.P.; Stanton, C. Prebiotics from Seaweeds: An Ocean of Opportunity? Mar. Drugs 2019, 17, 327. [Google Scholar] [CrossRef]
  36. Maghin, F.; Ratti, S.; Corino, C. Biological functions and health promoting effects of brown seaweeds in swine nutrition. J. Dairy Vet. Anim. Res. 2014, 1, 14–16. [Google Scholar] [CrossRef]
  37. Chandini, S.K.; Ganesan, P.; Bhaskar, N. In vitro antioxidant activities of three selected brown seaweeds of India. Food Chem. 2008, 107, 707–713. [Google Scholar] [CrossRef]
  38. Schiener, P.; Black, K.D.; Stanley, M.S.; Green, D.H. The seasonal variation in the chemical composition of the kelp species Laminaria digitate, Laminaria hyperborean, Saccharina latissima and Alaria esculenta. J. Appl. Phycol. 2015, 27, 363–373. [Google Scholar] [CrossRef]
  39. Mæhre, H.K.; Malde, M.K.; Eilertsen, K.E.; Elvevoll, E.O. Characterization of protein, lipid and mineral contents in common Norwegian seaweeds and evaluation of their potential as food and feed. J. Sci. Food Agric. 2014, 94, 3281–3290. [Google Scholar] [CrossRef] [PubMed]
  40. Pomin, V.H. Seaweed: Ecology, Nutrient Composition and Medicinal Uses, 1st ed.; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2011; pp. 15–47. [Google Scholar]
  41. Kolb, N.; Vallorani, L.; Milanovi, N.; Stocchi, V. Evaluation of Marine Algae Wakame (Undaria pinnatifida) and Kombu (Laminaria digitata japonica) as Food Supplements. Food Technol. Biotechnol. 2004, 42, 57–61. [Google Scholar]
  42. Dierick, N.; Ovyn, A.; De Smet, S. Effect of feeding intact brown seaweed Ascophyllum nodosum on some digestive parameters and on iodine content in edible tissues in pigs. J. Sci. Food Agric. 2009, 89, 584–594. [Google Scholar] [CrossRef]
  43. Anderson, M.J.; Blanton, J.R.; Gleghorn, J.; Kim, S.W.; Johnson, J.W. Ascophyllum nodosum supplementation strategies that improve overall carcass merit of implanted English crossbred cattle. Asian Aust. J. Anim. Sci. 2006, 19, 1514–1518. [Google Scholar] [CrossRef]
  44. Park, Y.H.; Jang, D.S.; Kim, S.B. Utilization of Marine Products, 2nd ed.; Hyoungsul Press: Seoul, Korea, 1997; pp. 283–336. [Google Scholar]
  45. Marín, A.; Casas-Valdez, M.; Carrillo, S.; Hernández, H.; Monroy, A.; Sanginés, L.; Pérez-Gil, F. The marine algae Sargassum spp. (Sargassaceae) as feed for sheep in tropical and subtropical regions. Rev. Biol. Trop. 2009, 57, 1271–1281. [Google Scholar] [CrossRef]
  46. Sanz-Pintos, N.; Perez-Jimenez, J.; Buschmann, A.H.; Vergara-Salinas, J.R.; Perez-Correa, J.C.; Saura-Calixto, F. Macromolecular antioxidants and dietary fiber in edible seaweeds. J. Food Sci. 2017, 2, 289–295. [Google Scholar] [CrossRef]
  47. Ortiz, J.; Romero, N.; Robert, P.; Araya, J.; Lopez-Hernández, J.; Bozzo, C.; Navarrete, E.; Osorio, A.; Rios, A. Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem. 2006, 99, 98–104. [Google Scholar] [CrossRef]
  48. Cruz-Suárez, L.E.; Ricque-Marie, D.; Tapia-Salazar, M.; Guajardo-Barbosa, C. Uso de harina de kelp (Macrocystis pyrifera) en alimentos para camarón. In Avances en Nutrición Acuícola, V. Memorias del Quinto Simposium Internacional de Nutrición Acuícola; Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Olvera-Novoa, M.A., Cerecedo-Olvera, R., Eds.; Universidad Autónoma de Nuevo León: Monterrey, Nuevo León, México, 2000; pp. 227–266. [Google Scholar]
  49. Duis, K.; Inglis, V.; Beveridge, M.C.M.; Hammer, C. Leaching of four different antibacterials from oil- and alginate-coated fish-feed pellets. Aquac. Res. 1995, 26, 549–556. [Google Scholar] [CrossRef]
  50. Hagen Rødde, R.; Vårum, K.M.; Larsen, B.A.; Myklestad, S.M. Seasonal and geographical variation in the chemical composition of the red alga Palmaria palmata (L.) Kuntze. Bot. Mar. 2004, 47, 125–133. [Google Scholar]
  51. Wong, K.H.; Cheung, P.C.K. Nutritional evaluation of some subtropical red and green seaweeds: Part I—Proximate composition, amino acid profiles and some physico–chemical properties. Food Chem. 2000, 71, 475–482. [Google Scholar] [CrossRef]
  52. Gaillard, C.; Bhatti, H.S.; Novoa-Garrido, M.; Lind, V.; Roleda, M.Y.; Weisbjerg, M.R. Amino acid profiles of nine seaweed species and their in situ degradability in dairy cows. Anim. Feed Sci. Technol. 2018, 241, 210–222. [Google Scholar] [CrossRef]
  53. Catarino, M.D.; Silva, A.M.S.; Cardoso, S.M. Phycochemical Constituents and Biological Activities of Fucus spp. Mar. Drugs 2018, 16, 249. [Google Scholar] [CrossRef]
  54. Saravana, P.S.; Yin, S.; Choi, J.H.; Park, Y.B.; Woo, H.C.; Chun, B.S. Evaluation of the chemical composition of brown seaweed (Saccharina japonica) hydrolysate by pressurized hot water extraction. Algal Res. 2016, 13, 246–254. [Google Scholar] [CrossRef]
  55. Cruz-Suarez, L.E.; Tapia-Salazar, M.; Nieto-López, M.G.; Guajardo, C. Comparison of Ulva clathrata and the kelps Macrocystis pyrifera and Ascophyllum nodosum as ingredients in shrimp feeds. Aquac. Nutr. 2009, 15, 421–430. [Google Scholar] [CrossRef]
  56. Draper, J.; Walsh, A.M.; McDonnell, M.; O’Doherty, J.V. Maternally offered seaweed extracts improves the performance and health status of the post weaned pig. J. Anim. Sci. 2016, 94, 391–394. [Google Scholar] [CrossRef]
  57. Ruiz, Á.R.; Gadicke, P.; Andrades, S.M.; Cubillos, R. Supplementing nursery pig feed with seaweed extracts increases final body weight of pigs. Austral J. Vet. Sci. 2018, 50, 83–87. [Google Scholar] [CrossRef]
  58. Bouwhuis, M.A.; Sweeney, T.; Mukhopadhya, A.; McDonnell, M.J.; O’Doherty, J.V. Maternal laminarin supplementation decreases Salmonella Typhimurium shedding and improves intestinal health in piglets following an experimental challenge with S. Typhimurium post–weaning. Anim. Feed Sci. Technol. 2017, 223, 156–168. [Google Scholar] [CrossRef]
  59. Bouwhuis, M.A.; McDonnell, M.J.; Sweeney, T.; Mukhopadhya, A.; O’Shea, C.J.; O’Doherty, J.V. Seaweed extracts and galacto–oligosaccharides improve intestinal health in pigs following Salmonella Typhimurium challenge. Animal 2017, 11, 1488–1496. [Google Scholar] [CrossRef]
  60. Michiels, J.; Skrivanova, E.; Missotten, J.; Ovyn, A.; Mrazek, J.; De Smet, S.; Dierick, N. Intact brown seaweed (Ascophyllum nodosum) in diets of weaned piglets: Effects on performance, gut bacteria and morphology and plasma oxidative status. J. Anim. Physiol. Anim. Nutr. 2012, 96, 1101–1111. [Google Scholar] [CrossRef] [PubMed]
  61. Wan, J.; Jiang, F.; Xu, Q.S.; Chen, D.W.; He, J. Alginic acid oligosaccharide accelerates weaned pig growth through regulating antioxidant capacity, immunity and intestinal development. RSC Adv. 2016, 6, 87026–87035. [Google Scholar] [CrossRef]
  62. Wan, J.; Zhang, J.; Chen, D.W.; Yu, B.; He, J. Effects of alginate oligosaccharide on the growth performance, antioxidant capacity and intestinal digestion–absorption function in weaned pigs. Anim. Feed Sci. Technol. 2017, 234, 118–127. [Google Scholar] [CrossRef]
  63. Choi, Y.; Hosseindoust, A.; Goel, A.; Lee, S.; Jha, P.K.; Kwon, I.K.; Chae, B.J. Effects of Ecklonia cava as fucoidan–rich algae on growth performance, nutrient digestibility, intestinal morphology and caecal microflora in weanling pigs. Asian–Australas. J. Anim. Sci. 2017, 30, 64–70. [Google Scholar] [CrossRef]
  64. O’Doherty, J.V.; McDonnell, P.; Figat, S. The effect of dietary laminarin and fucoidan in the diet of the weanling piglet on performance and selected faecal microbial populations. Livest. Sci. 2010, 134, 208–210. [Google Scholar] [CrossRef]
  65. Dillon, S.; Sweeney, T.; Figat, S.; Callan, J.J.; O’Doherty, J.V. The effects of lactose inclusion and seaweed extract on performance, nutrient digestibility and microbial populations in newly weaned piglets. Livest. Sci. 2010, 134, 205–207. [Google Scholar] [CrossRef]
  66. Gahan, D.A.; Lynch, M.B.; Callan, J.J.; O’Sullivan, J.T.; O’Doherty, J.V. Performance of weanling piglets offered low–, medium– or high–lactose diets supplemented with a seaweed extract from Laminaria spp. Animal 2009, 3, 24–31. [Google Scholar] [CrossRef]
  67. Heim, G.; Sweeney, T.; O’Shea, C.J.; Doyle, D.N.; O’Doherty, J.V. Effect of maternal supplementation with seaweed extracts on growth performance and aspects of gastrointestinal health of newly weaned piglets after challenge with enterotoxigenic Escherichia coli K88. Br. J. Nutr. 2014, 112, 1955–1965. [Google Scholar] [CrossRef]
  68. McAlpine, P.; O’Shea, C.J.; Varley, P.F.; Flynn, B.; O’Doherty, J.V. The effect of seaweed extract as an alternative to zinc oxide diets on growth performance, nutrient digestibility, and fecal score of weaned piglets. J. Anim. Sci. 2012, 90, 224–226. [Google Scholar] [CrossRef]
  69. McDonnell, P.; Figat, S.; O’Doherty, J.V. The effect of dietary laminarin and fucoidan in the diet of the weanling piglet on performance, selected faecal microbial populations and volatile fatty acid concentrations. Animal 2010, 4, 579–585. [Google Scholar] [CrossRef]
  70. O’Shea, C.J.; McAlpine, P.; Sweeney, T.; Varley, P.F.; O’Doherty, J.V. Effect of the interaction of seaweed extracts containing laminarin and fucoidan with zinc oxide on the growth performance, digestibility and faecal characteristics of growing piglets. Br. J. Nutr. 2014, 111, 798–807. [Google Scholar] [CrossRef] [PubMed]
  71. Walsh, A.M.; Sweeney, T.; O’Shea, C.J.; Doyle, D.N.; O‘Doherty, J.V. Effect of supplementing varying inclusion levels of laminarin and fucoidan on growth performance, digestibility of diet components, selected faecal microbial populations and volatile fatty acid concentrations in weaned pigs. Anim. Feed Sci. Technol. 2013, 183, 151–159. [Google Scholar] [CrossRef]
  72. Gardiner, G.E.; Campbell, A.J.; O’Doherty, J.V.; Pierce, E.; Lynch, P.B.; Leonard, F.C.; Stanton, C.; Ross, R.P.; Lawlor, P.G. Effect of Ascophyllum nodosum extract on growth performance, digestibility, carcass characteristics and selected intestinal microflora populations of grower–finisher pigs. Anim. Feed Sci. Technol. 2008, 141, 259–273. [Google Scholar] [CrossRef]
  73. Sweeney, T.; O’Doherty, J.V. Marine macroalgal extracts to maintain gut homeostasis in the weaning piglet. Domest. Anim. Endocrinol. 2016, 56, S84–S89. [Google Scholar] [CrossRef] [PubMed]
  74. Food and Agriculture Organization of the United Nations (FAO). The State of World Fisheries and Aquaculture -2008 (SOFIA); FAO: Rome, Italy, 2009. [Google Scholar]
  75. Evans, F.D.; Critchley, A.T. Seaweeds for animal production use. J. Appl. Phycol. 2014, 26, 891–899. [Google Scholar] [CrossRef]
  76. Cian, R.E.; Drago, S.R.; Sánchez de Medina, F.; Martínez-Augustin, O. Proteins and carbohydrates from red seaweeds: Evidence for beneficial effects on gut function and microbiota. Mar. Drugs 2015, 13, 5358–5383. [Google Scholar] [CrossRef]
  77. De Jesus Raposo, M.F.; De Morais, A.M.M.B.; De Morais, R.M.S.C. Emergent Sources of Prebiotics: Seaweeds and Microalgae. Mar. Drugs 2016, 14, 27. [Google Scholar] [CrossRef]
  78. Okolie, C.L.; Rajendran, S.R.C.K.; Udenigwe, C.C.; Aryee, A.N.A.; Mason, B. Prospects of brown seaweed polysaccharides (BSP) as prebiotics and potential immunomodulators. J. Food Biochem. 2017, 41, e12392. [Google Scholar] [CrossRef]
  79. Chen, X.; Sun, Y.; Hu, L.; Yu, H.; Xing, R.; Li, R.; Wang, X.; Li, P. In vitro prebiotic effects of seaweed polysaccharides. J. Oceanol. Limnol. 2018, 36, 926–932. [Google Scholar] [CrossRef]
  80. Mukhopadhya, A.; O’Doherty, J.V.; Smith, A.; Bahar, B.; Sweeney, T. The microbiological and immunomodulatory effects of spray–dried versus wet dietary supplementation of seaweed extract in the pig gastrointestinal tract. J. Anim. Sci. 2012, 90, 28–30. [Google Scholar] [CrossRef]
  81. Murphy, P.; Dal Bello, F.; O’Doherty, J.; Arendt, E.K.; Sweeney, T.; Coffey, A. Analysis of bacterial community shifts in the gastrointestinal tract of pigs fed diets supplemented with b–glucan from Laminaria digitata, Laminaria hyperborea and Saccharomyces cerevisiae. Animal 2013, 7, 1079–1087. [Google Scholar] [CrossRef] [PubMed]
  82. Lynch, M.B.; Sweeney, T.; Callan, J.J.; O’Sullivan, J.T.; O’Doherty, J.V. The effect of dietary Laminaria derived laminarin and fucoidan on intestinal microflora and volatile fatty acid concentration in pigs. Livest. Sci. 2010, 133, 157–160. [Google Scholar] [CrossRef]
  83. Lynch, M.B.; Sweeney, T.; Callan, J.J.; O’Sullivan, J.T.; O’Doherty, J.V. The effect of dietary Laminaria derived laminarin and fucoidan on nutrient digestibility, nitrogen utilisation, intestinal microflora and volatile fatty acid concentration in pigs. J. Sci. Food Agric. 2010, 90, 430–437. [Google Scholar] [CrossRef]
  84. Reilly, P.; Sweeney, T.; Pierce, K.M.; Callan, J.J.; Julka, A.; O’Doherty, J.V. The effect of seaweed extract inclusion on gut health and immune status of the weaned pig. Animal 2008, 2, 1465–1473. [Google Scholar] [CrossRef] [PubMed]
  85. Leonard, S.G.; Sweeney, T.; Bahar, B.; O’Doherty, J.V. Effect of maternal seaweed extract supplementation on suckling piglet growth, humoral immunity, selected microflora, and immune response after an ex vivo lipopolysaccharide challenge. J. Anim. Sci. 2012, 90, 505–514. [Google Scholar] [CrossRef]
  86. Walsh, A.M.; Sweeney, T.; O’Shea, C.J.; Doyle, D.N.; O’Doherty, J.V. Effect of dietary laminarin and fucoidan on selected microbiota, intestinal morphology and immune status of the newly weaned pig. Br. J. Nutr. 2013, 110, 1630–1638. [Google Scholar] [CrossRef]
  87. Heim, G.; O’Doherty, J.V.; O’Shea, C.J.; Doyle, D.N.; Egan, A.M.; Thornton, K.; Sweeney, T. Maternal supplementation of seaweed–derived polysaccharides improves intestinal health and immune status of suckling piglets. J. Nutr. Sci. 2015, 4, e27. [Google Scholar] [CrossRef]
  88. Heim, G.; Sweeney, T.; O’shea, C.J.; Doyle, D.N.; O’doherty, J.V. Effect of maternal dietary supplementation of laminarin and fucoidan, independently or in combination, on pig growth performance and aspects of intestinal health. Anim. Feed Sci. Technol. 2015, 204, 28–41. [Google Scholar] [CrossRef]
  89. Bouwhuis, M.A.; Sweeney, T.; Mukhopadhya, A.; Thornton, K.; McAlpine, P.O.; O’Doherty, J.V. Zinc methionine and laminarin have growth–enhancing properties in newly weaned pigs influencing both intestinal health and diarrhoea occurrence. J. Anim. Physiol. Anim. Nutr. 2016, 101, 1273–1285. [Google Scholar] [CrossRef]
  90. McDonnell, M.; Bouwhuis, M.; Sweeney, T.; O’Shea, C.; O’Doherty, J. Effects of dietary supplementation of galactooligosaccharides and seaweed–derived polysaccharides on an experimental Salmonella Typhimurium challenge in pigs. J. Anim. Sci. 2016, 94, 153–156. [Google Scholar] [CrossRef]
  91. Rossi, R.; Pastorelli, G.; Cannata, S.; Corino, C. Recent advances in the use of fatty acids as supplements in pig diets: A review. Anim. Feed Sci. Technol. 2010, 162, 1–11. [Google Scholar] [CrossRef]
  92. Wan, J.; Zhang, J.; Chen, D.W.; Yu, B.; Huang, Z.; Mao, X.; Zheng, P.; Yu, J.; He, J. Alginate oligosaccharide enhances intestinal integrity of weaned pigs through altering intestinal inflammatory responses and antioxidant status. RSC Adv. 2018, 8, 13482–13492. [Google Scholar] [CrossRef]
  93. Pérez, M.J.; Falqué, E.; Domínguez, H. Antimicrobial Action of Compounds from Marine Seaweed. Mar. Drugs 2016, 14, 52. [Google Scholar] [CrossRef] [PubMed]
  94. Vatsos, I.N.; Rebours, C. Seaweed extracts as antimicrobial agents in aquaculture. J. Appl. Phycol. 2015, 27, 2017–2035. [Google Scholar] [CrossRef]
  95. Eom, S.H.; Kim, Y.M.; Kim, S.K. Antimicrobial effect of phlorotannins from marine brown algae. Food Chem. Toxicol. 2012, 50, 3251–3255. [Google Scholar] [CrossRef]
  96. Pina–Pérez, M.C.; Rivas, A.; Martínez, A.; Rodrigo, D. Antimicrobial potential of macro and microalgae against pathogenic and spoilage microorganisms in food. Food Chem. 2017, 235, 34–44. [Google Scholar] [CrossRef]
  97. Shannon, E.; Abu–Ghannam, N. Antibacterial derivatives of marine algae: An overview of pharmacological mechanisms and applications. Mar. Drugs 2016, 14, 81. [Google Scholar] [CrossRef]
  98. Lane, A.L.; Stout, E.P.; Lin, A.-S.; Prudhomme, J.; le Roch, K.; Fairchild, C.R.; Franzblau, S.G.; Hay, M.E.; Aalbersberg, W.; Kubanek, J. Antimalarial bromophycolides J–Q from the Fijian red alga Callophycus serratus. J. Org. Chem. 2009, 74, 2736–2742. [Google Scholar] [CrossRef]
  99. Castillo, S.; Heredia, N.; García, S. 2 (5H)–Furanone, epigallocatechin gallate, and a citric–based disinfectant disturb quorum–sensing activity and reduce motility and biofilm formation of Campylobacter jejuni. Folia Microbiol. 2015, 60, 89–95. [Google Scholar] [CrossRef]
  100. Kadam, S.U.; O’Donnell, C.P.; Rai, D.K.; Hossain, M.B.; Burgess, C.M.; Walsh, D.; Tiwari, B.K. Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: Ultrasound assisted extraction, characterization and bioactivity. Mar. Drugs 2015, 13, 4270–4280. [Google Scholar] [CrossRef]
  101. Rodrigues, D.; Alves, C.; Horta, A.; Pinteus, S.; Silva, J.; Culioli, G.; Thomas, O.P.; Pedrosa, R. Antitumor and antimicrobial potential of bromoditerpenes isolated from the red alga, Sphaerococcus coronopifolius. Mar. Drugs 2015, 13, 713–726. [Google Scholar] [CrossRef] [PubMed]
  102. Abou Zeid, A.H.; Aboutabl, E.A.; Sleem, A.A.; El-Rafie, H.M. Water soluble polysaccharides extracted from Pterocladia capillacea and Dictyopteris membranacea and their biological activities. Carbohydr. Polym. 2014, 113, 62–66. [Google Scholar] [CrossRef] [PubMed]
  103. Vijayabaskar, P.; Vaseela, N.; Thirumaran, G. Potential antibacterial and antioxidant properties of a sulfated polysaccharide from the brown marine algae Sargassum swartzii. Chin. J. Nat. Med. 2012, 10, 421–428. [Google Scholar] [CrossRef]
  104. Ren, D.; Bedzyk, L.A.; Ye, R.W.; Thomas, S.M.; Wood, T.K. Differential gene expression shows natural brominated furanones interfere with the autoinducer–2 bacterial signaling system of Escherichia coli. Biotechnol. Bioeng. 2004, 88, 630–642. [Google Scholar] [CrossRef] [PubMed]
  105. Holanda, M.L.; Melo, V.M.M.; Silva, L.M.C.M.; Amorim, R.C.N.; Pereira, M.G.; Benevides, N.M.B. Differential activity of a lectin from Solieria filiformis against human pathogenic bacteria. Braz. J. Med. Biol. Res. 2005, 38, 1769–1773. [Google Scholar] [CrossRef]
  106. Brameyer, S.; Heermann, R. Specificity of signal–binding via non–AHL LuxR–type receptors. PLoS ONE 2015, 10, e0124093. [Google Scholar] [CrossRef]
  107. Hentzer, M.; Givskov, M. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Investig. 2003, 112, 1300–1307. [Google Scholar] [CrossRef]
  108. Lee, J.-H.; Eom, S.-H.; Lee, E.-H.; Jung, Y.-J.; Kim, H.-J.; Jo, M.-R.; Son, K.-T.; Lee, H.-J.; Kim, J.H.; Lee, M.-S. In vitro antibacterial and synergistic effect of phlorotannins isolated from edible brown seaweed Eisenia bicyclis against acne–related bacteria. Algae 2014, 29, 47–55. [Google Scholar] [CrossRef]
  109. Lee, S.H.; Kim, S.K. Biological phlorotannins of Eisenia bicyclis. In Marine Algae Extracts: Processes, Products, and Applications; Kim, S.-K., Chojnacka, K., Eds.; Wiley: Oxford, UK, 2015; pp. 453–464. [Google Scholar]
  110. Eom, S.-H.; Lee, D.-S.; Jung, Y.-J.; Park, J.-H.; Choi, J.-I.; Yim, M.-J.; Jeon, J.-M.; Kim, H.-W.; Son, K.-T.; Je, J.-Y.; et al. The mechanism of antibacterial activity of phlorofucofuroeckol–A against methicillin–resistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 2014, 98, 9795–9804. [Google Scholar] [CrossRef]
  111. Beaulieu, L.; Bondu, S.; Doiron, K.; Rioux, L.-E.; Turgeon, S.L. Characterization of antibacterial activity from protein hydrolysates of the macroalga Saccharina longicruris and identification of peptides implied in bioactivity. J. Funct. Foods 2015, 17, 685–697. [Google Scholar] [CrossRef]
  112. Berri, M.; Olivier, S.C.; Olivier, M.; Helloin, E.; Jacques, I.; Salmon, H.; Demais, H.; Le Goff, M.; Nival Collen, P. Marine–sulfated polysaccharides extract of Ulva armoricana green algae exhibits an antimicrobial activity and stimulates cytokine expression by intestinal epithelial cells. J. Appl. Phycol. 2016, 28, 2999–3008. [Google Scholar]
  113. Jacobsen, C.; Sørensen, A.M.; Holdt, S.L.; Akoh, C.C.; Hermund, D.B. Source, Extraction, Characterization, and Applications of Novel Antioxidants from Seaweed. Annu. Rev. Food Sci. Technol. 2019, 10, 541–568. [Google Scholar] [CrossRef] [PubMed]
  114. Holdt, S.L.; Kraan, S. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 2011, 23, 543–549. [Google Scholar] [CrossRef]
  115. Rupérez, P.; Saura-Calixto, F. Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur. Food Res. Technol. 2001, 212, 349–354. [Google Scholar]
  116. Farvin, K.H.S.; Jacobsen, C. Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem. 2013, 138, 1670–1681. [Google Scholar] [CrossRef]
  117. Ramus, J.; Lemons, F.; Zimmerman, C. Adaptation of light–harvesting pigments to downwelling light and the consequent photosynthetic performance of the eulittoral rockweeds Ascophyllum nodosum and Fucus vesiculosus. Mar. Biol. 1977, 42, 293–303. [Google Scholar] [CrossRef]
  118. Noviendri, D.; Jaswir, I.; Salleh, M.H.; Taher, M.; Miyashita, K.; Ramli, N. Fucoxanthin extraction and fatty acid analysis of Sargassum binderi and S. duplicatum. J. Med. Plants Res. 2011, 5, 2405–2412. [Google Scholar]
  119. Narayani, S.S.; Saravanan, S.; Bharathiaraja, S.; Mahendran, S. Extraction, partially purification and study on antioxidant property of fucoxanthin from Sargassum cinereum J. Agardh. J. Chem. Pharm. Res. 2016, 8, 610–616. [Google Scholar]
  120. Jensen, A. Tocopherol content of seaweed and seaweed meal: II. Individual, diurnal and seasonal variations in some Fucaceae. J. Sci. Food Agric. 1969, 20, 454–458. [Google Scholar] [CrossRef]
  121. Jensen, A. Tocopherol content of seaweed and seaweed meal. 3. Influence of processing and storage on content of tocopherols, carotenoids and ascorbic acid in seaweed meal. J. Sci. Food Agric. 1969, 20, 622–626. [Google Scholar] [CrossRef]
  122. Wen, X.; Peng, C.; Zhou, H.; Lin, Z.; Lin, G.; Chen, S.; Li, P. Nutritional composition and assessment of Gracilaria lemaneiformis Bory. J. Integr. Plant Biol. 2006, 48, 1047–1053. [Google Scholar] [CrossRef]
  123. Naseri, A.; Holdt, S.L.; Jacobsen, C. Nutritional value added compounds in industrial red seaweed used in carrageenan production. J. Aquat. Food Prod. Technol. 2019, 28, 967–973. [Google Scholar] [CrossRef]
  124. Rajauria, G.; Draper, J.; McDonnel, M.; O’Doherty, J.V. Effect of dietary seaweed extracts, galactooligosaccharide and vitamin E supplementation on meat quality parameters in finisher pigs. Innov. Food Sci. Emerg. Technol. 2016, 37, 269–275. [Google Scholar] [CrossRef]
  125. Moroney, N.C.; O’Grady, M.N.; O’Doherty, J.V.; Kerry, J.P. Addition of seaweed (Laminaria digitata) extracts containing laminarin and fucoidan to porcine diets: Influence on the quality and shelf–life of fresh pork. Meat Sci. 2012, 92, 423–429. [Google Scholar] [CrossRef]
  126. Moroney, N.C.; O’Grady, M.N.; Robertson, R.C.; Stanton, C.; O’Doherty, J.V.; Kerry, J.P. Influence of level and duration of feeding polysaccharide (laminarin and fucoidan) extracts from brown seaweed (Laminaria digitata) on quality indices of fresh pork. Meat Sci. 2015, 99, 132–141. [Google Scholar] [CrossRef]
  127. Smith, A.G.; O’Doherty, J.V.; Reilly, P.; Ryan, M.T.; Bahar, B.; Sweeney, T. The effects of laminarin derived from Laminaria digitata on measurements of gut health: Selected bacterial populations, intestinal fermentation, mucin gene expression and cytokine gene expression in the pig. Br. J. Nutr. 2011, 105, 669–677. [Google Scholar] [CrossRef]
  128. Berri, M.; Olivier, M.; Holbert, S.; Dupont, J.; Demais, H.; Le Goff, M.; Collen, P.N. Ulvan from Ulva armoricana (Chlorophyta) activates the PI3K/Akt signalling pathway via TLR4 to induce intestinal cytokine production. Algal Res. 2017, 28, 39–47. [Google Scholar] [CrossRef]
  129. Katayama, M.; Fukuda, T.; Okamura, T.; Suzuki, E.; Tamura, K.; Shimizu, Y.; Suda, Y.; Suzuki, K. Effect of dietary addition of seaweed and licorice on the immune performance of pigs. Anim. Sci. J. 2011, 82, 274–281. [Google Scholar] [CrossRef]
  130. Azizi, A.F.N.; Miyazaki, R.; Yumito, T.; Ohashi, Y.; Uno, S.; Miyajima, U.; Kumamoto, M.; Uchiyama, S.; Yasuda, M. Effect of maternal supplementation with seaweed powder on immune status of liver and lymphoid organs of piglets. J. Vet. Med. Sci. 2018, 80, 8–12. [Google Scholar] [CrossRef]
  131. Bussy, F.; Le Goff, M.; Salmon, H.; Delaval, J.; Berri, M.; Pi, N.C. Immunomodulating effect of a seaweed extract from Ulva armoricana in pig: Specific IgG and total IgA in colostrum, milk, and blood. Vet. Anim. Sci. 2019, 7, 100051. [Google Scholar] [CrossRef]
  132. NRC, National Research Council. Nutrient Requirements of Swine, 7th Revised ed.; The National Academies Press: Washington, DC, USA, 2012. [Google Scholar]
  133. Duinker, A.; Roiha, I.S.; Amlund, H.; Dahl, L.; Lock, E.-J.; Kögel, T.; Måge, A.; Lunestad, B.T. Potential Risks Posed by Macroalgae for Application as Feed and Food—A Norwegian Perspective; National Institute of Nutrition and Seafood Research (NIFES): Trondheim, Norway, 2016; p. 23. [Google Scholar]
Table 1. Chemical composition of brown, red and green seaweeds (on DM basis) 1.
Table 1. Chemical composition of brown, red and green seaweeds (on DM basis) 1.
SeaweedsBROWNREDGREEN
Laminaria
spp. *
Ascophillum
nodosum
Sargassum
spp. ⁑
Fucus
spp. #
Saccharina
latissima
Macrocystis
pyrifera
Palmaria
palmata
Ulva
lactuca
Crude protein %9.4
(5.3–16.1)
7.4
(4.9–8.7)
10
(8.5–13.6)
12.6
(12.2–12.9)
7.6
(7.1–8.1)
8.3
(8–10)
21.9
(15.1–31.4)
16.2
(7.06–23.1)
Ether extract %1.1
(0.8–2.4)
5.3
(3.9–8.6)
0.8
(0.5–1.2)
6.1
(3.7–8.4)
5.51.8
(0.5–3.9)
8.9
(4.9–12.9)
1.3
(0.25–1.64)
Crude Fiber %11.6
(6.6–16.6)
5.5
(5.4–5.5)
18.2
(6.4–38)
10.7
(5.4–16)
23
(6.6–40)
33.4
(5.5–50)
1.5
(1.49–1.50)
9.6
(6.9–12.3)
Ash %27.8
(19.6–31.5)
24.8
(21.1–30.9)
27.6
(19.4–35.9)
21.6
(20.7–22.5)
22.5
(13.3–31.7)
25.8
(20–35)
19.3
(9–24.5)
25.7
(21.3–26.2)
Gross energy MJ/kg12.7
(12.5–13)
14.19.115.7
(15.5–16)
11.1916.915.2
(14.7–15.7)
Ca g/kg10
(8–12.55)
16.4
(9.8–20)
14.7
(3.8–27.2)
9.9
(8.9–12.8)
9.8
(9.6–10)
14.1
(11.6–16.6)
2.6
(1–4.2)
12.6
(6.1–29.2)
P g/kg2.2
(1.2–3)
11.7
(1–2.2)
1.9
(1.4–2.3)
2.7
(2.2–3.1)
2.9
(2.6–3.2)
4
(3–5)
2.1
(1.3–2.7)
K g/kg54
(48.6–59.5)
28.5
(20–37.7)
46.222.9
(0.4–36.1)
52.567.5
(44.8–112.3)
37.1
(27–47.2)
14.4
(1.5–22.1)
Na g/kg23.9
(22.5–25.3)
37.5
(25–45.7)
24.2
(0.2–45.8)
3336.9
(17.1-56.7)
7.2
(3.3–11)
13.9
(2.9–20.2)
Mg g/kg6.3(
5.5–7.2)
6.8
(1–8.6)
6.4
(4–7.7)
7.5
(7–8.33)
6.3
(5.1–7.4)
39
(16.2–61.8)
2.313
(1.9–20.5)
Mn, mg/kg7.1
(3.1–11)
17.8
(12–25)
88.3
(26.7–214)
104.7
(8.2–177.8)
8.2
(3.9–12.4)
1171.6
(11–168)
38.7
(10.1–122)
Zn mg/kg22.6
11–31.5)
116.8
(30.3–181)
79.3
(12–214)
118.1
(45.3–275.3)
35.4
(29.2–41.55)
1265.1
(23.6–143)
29
(16.1–45)
Cu mg/kg2.4
(1.2–5.9)
17.8
(4.2–28)
6.
(2.3–7)
9.3
(2–23.5)
4.5
(1.1–7.9)
211.1
(3.8–24)
8.5
(3.3–12)
Fe mg/kg107.3
(58–179)
157.8
(122–241)
2678
(307–7291)
351.9
(189–559)
529
(30–1028)
117202.5
(139–315)
462.2
(105–1481)
I mg/kg2991.7
(833–5100)
777399.5
(216–583)
376
(232–677)
1448.5
(957–1940)
27856.7
Se mg/kg0.6
(0.29–0.93)
0.51.2
(1.1–1.4)
0.8
(0.2–1.2)
1.1
(0.9–1.3)
0.11.2
(0.4–1.9)
Co mg/kg0.1
(0.08–0.11)
0.60.4
(0.36–0.47)
1.1
(0.8–1.4)
0.40.030.5
(0.3–0.6)
Vitamin E mg/kg672
(3–2000)
230
(80–500)
10164
(100–356)
1.692869.6
(22–152)
12.95
(2.8–35)
Vitamin A mg/kg **154.6
(22–299)
57
(35–80)
5117.8
(7–28.6)
0.4212.39142.9
(15.2–270)
3.5
(0.1–7)
Vitamin C mg/kg632
(355–910)
860
(81–1650)
560383
(141–770)
11.5
(3.5–18.8)
78.3
(0.7–156)
141.5
(42–241)
Vitamin B1 mg/kg7.45
(2.4–12.5)
14(1–27)40.20.72
(0.5–0.94)
18
(0.7–40)
40
Vitamin B2 mg/kg4.9
(1.4–8.5)
7.5
(5–10)
650.351.7
(1.4–2.1)
16
(4.3–19)
5.1
(5–5.3)
Vitamin B3 mg/kg314
(158–612)
152045
(10.1–83)
References[13,17,19,21,37,38,39,40,41][17,18,21,24,28,37,42,43,44,45][17,19,24,37,45][18,19,21,23,28,37,40][19,21,23,28,38][17,46,47,48,49][17,23,28,37,50][17,19,21,23,37,44,47,51]
1 data are reported as mean values and ranges. * values from Laminaria digitata and hyperarborea. ⁑ values from Sargassum Patens, hemifhyllum, henslowianum. # Values from Fucus vesciculosus, giuryi, serratus, spiralys. ** as provitamin carotenoids.
Table 2. Aminoacid profile of brown, red and green seaweeds (mg/g DM) 1.
Table 2. Aminoacid profile of brown, red and green seaweeds (mg/g DM) 1.
SeaweedsBROWNREDGREEN
Laminaria digitataAscophillum nodosumSargassum
spp. ⁑
Fucus
spp. #
Saccharina
latissima
Macrocystis pyriferaPalmaria
palmata
Ulva
lactuca
Lysine4.41
(4.1–4.8)
4.77
(4.3–5.4)
3.57
(2.8–4.3)
7.6
(6.7–8.2)
4.05
(4–4.1)
6.63
(5.2–7.5)
1.42
(1.2–1.65)
2.09
(0.5–1.9)
Histidine1.82
(1.3–2.4)
1.63
(1.4–1.9)
0.82
(0.6–1)
1.33
(0.4–2)
2.2
(1.2–3.2)
2.33
(2–2.9)
0.4
(0.3–0.5)
0.83
(0.1–2.0)
Isoleucine2.91
(2.6–3.2)
3.76
(3.1–4.3)
2.70
(1.9–3.5)
3.70
(0.9–6)
3.1
(3–3.1)
4.47
(3.2–5.6)
1.31
(0.7–1.9)
1.5
(0.4–5.2)
Leucine4.93
(4.4–5.4)
6.63
(5.3–7.5)
5.11
(4.4–5.8)
6.42
(1.6–10.5)
5.06
(4.2–5.9)
7.53
(5.5–9.2)
2.42
(1.3–3.6)
2.9
(0.7–6.6)
Arginine3.2
(2.9–3.4)
5.06
(4.2–6.0)
1.6
(1–3–1.9)
3.24
(1.1–4.6)
4.0
(3.9–4.1)
4.87
(3.5–6.1)
1.9
(1.2–2.6)
2.12
(0.5–1.3)
Methionine1.5
(1.4–1.5)
1.91
(1.3–2.5)
0.69
(0.68–0.7)
0.81
(0.2–1.8)
2
(1.9–2.1)
2.18
(1.6–2.6)
0.91
(0.5–2.3)
1.21
(0.2–1.8)
Phenylalanine3.24
(2.8–3.6)
4.23
(3.2–5.0)
2.98
(2.2–3.7)
3.56
(0.9–5.2)
3.82 5.42
(4.1–6.2)
1.7
(0.8–2.6)
2.4
(0.2–3.6)
Threonine3.68
(3.4–3.9)
4.6
(3.6–5.4)
3.9
(3.3–4.5)
3.09
(1.2–5.1)
4.3
(4.2–4.4)
5.17
(3.6–6.7)
1.26
(0.7–2.8)
2.17
(0.5–3.8)
Tryptophan1.74
(1.72–1.76)
1.22
(0.5–1.9)
0.4
(0.2–0.6)
0.51
(0.4–0.6)
Valine5.38
(4.7–6.0)
4.76
(4.1–5.5)
3.84
(2.9–4.8)
4.65
(1.1–8.0)
4.1
(3.7–4.5)
5.87
(4.3–7.1)
2.25
(1.1–3.4)
2.03
(0.9–4.4)
Tyrosine1.74
(1.7–1.8)
2.05
(0.9–3.2)
2.35
(1.8–2.9)
2.26
(1.9–2.6)
2.8
(2.1–3.5)
1.15
(0.6–1.7)
1.03
(0.5–1.4)
Alanine6.68
(4.5–8.8)
5.95
(5.4–6.5)
4.23
(3.3–5.1)
1.58
(1.5–1.6)
6.8
(5.0–8.5)
4.81
(4.5–5.0)
2.23
(1.1–3.3)
3.22
(0.7–5.9)
Glutamine7.3
(4.6–9.9)
14.5
(1.4–11.6)
19.5
(18.9–20.1)
20.1
(19.6–20.3)
10.5
(10.6–10.4)
14.1
(9.7–18.3)
16.6
(11.0–18.7)
13.2
(11.5–14.8)
Asparagine6
(3.9–8.1)
8.4
(8.3–8.5)
12
(11.5–12–5)
12.8
(10.9–16.7)
9.4
(8.8–9.8)
10.8
(8.3–13.3)
11.3
(9.9–14.3)
10.4
(7.9–12.2)
References[41,52][17,18][14][18,53][52,54][48,49,55][25,28][17,18,47]
1 data are reported as mean values. ⁑ values from Sargassum Patens and hemifhyllum. # Values from Fucus vesciculosus and serratus.
Table 3. Effect of seaweed supplement on average daily gain (ADG) in pigs.
Table 3. Effect of seaweed supplement on average daily gain (ADG) in pigs.
Algae SupplementDoseAnimalControlSupplementedDiff. %Ref.
A. nodosumDried seaweed 2.5–5–10 g/kgWeaning to 28 d0.2200.209−5.0[60]
0.198−10.0
0.213−3.18
A. nodosumDried seaweed 10–20 g/kgWeaning to 11 d0.0270.054+100[42]
0.040+48.14
Brown seaweedAlginic acid oligosaccharides
(50–100–200 mg/kg)
Weaning to 14 d0.2160.248 (50)+14.81[61]
0.304 * (100)+40.78
0.301 * (200)+39.35
Brown seaweedAlginates oligosaccharides (100 mg/kg) Weaning to 21 d0.4410.516+17.01[62]
Ecklonia cavaFUC = 0.05 – 0.10 – 0.156 g/kgWeaning to 28 d0.3440.347+0.87[63]
0.368 *+6.98
0.360 *+4.65
Laminaria digitataLAM + FUC (0.314 –0.250 g/kg) – lactose 15 or 25%)Weaning to 25 d0.275
0.287
0.293 (15% lact.)+6.55[64]
0.350 **
(25% lact.)
+21.95
Laminaria spp.LAM (1 g/day)—sows, 109 d until weaning at 20 d20 d lactation
Weaning to 26 d
Challenge Salmonella Typhimurium at 10 d post weaning
0.3400.450 **+32.35[58]
LAM (0.3 g/kg)—piglets0.4100.370−16.13
Laminaria spp.LAM + FUC
(0.18 + 0.34 g/kg)
30.9 kg pigs for 28 d
Challenge Salmonella Typhimurium at 10d
0.6200.720 ***+16.13[59]
Laminaria spp.LAM (0.112 g/kg) y
FUC (0.089 g/kg) z
Weaning to 25 d0.2810.322 **+14.59[65]
Laminaria spp.LAM + FUC
(1 g + 0.8 g day) − sows
LAM + FUC
(0.3 + 0.24 g/kg) − piglets
Weaning to 126 d0.7600.850 **(lactation effect)+11.84[56]
0.8000.810 (weaning effect)+1.23
Laminaria spp.Extract (1–2–4 g/kg) x
LAM = 0.11–0.22–0.44
FUC = 0.09–0.18–0.36
Weaning to 21 d0.2490.274 ***(1 g/kg)+10.04[66]
0.313 *** (2 g/kg)+25.70
0.303 ***(4 g/kg)+21.69
Laminaria spp.LAM (0.30 g/kg)Weaning to 32 d0.2800.353 *+26.07[67]
Laminaria spp.LAM + FUC
(0.30 + 0.24 g/kg)
Weaning to 40 d0.3560.374+5.06[68]
Laminaria spp.LAM (0.3 g/kg)
FUC (0.36 g/kg)
LAM + FUC
(0.3 + 0.36 g/kg)
Weaning to 21 d0.2880.319 * LAM 0.3+10.7[69]
0.302 FUC 0.36+4.86
0.328 LAM + FUC+13.89
Laminaria spp.LAM + FUC
(0.30 + 0.24 g/kg) k
Weaning to 21 d
21–40 d
0.2350.239+1.70[70]
0.4890.523+6.25
Laminaria spp.LAM (0.15–0.30 g/kg)
FUC (0.24 g/kg)
LAM + FUC (0.15 + 0.24
and 0.30 + 0.24 g/kg)
Weaning to 35 d0.3400.351 FUC 0.24+3.24[71]
0.334 LAM 0.15–1.76
0.347 FUC 0.24 LAM 0.15+2.06
0.390* LAM 300+14.71
0.358 FUC 0.24 LAM 0.3+5.29
OceanFeedSwineSeaweeed extract
(5 g/kg)
21 to 56 d0.4010.380−5.24[57]
56–160 d0.7980.824 *+3.26
Means marked with *, **, *** showed a significant effect of supplement for p < 0.05, p < 0.01 and p < 0.001 respectively; LAM, laminarin; FUC, fucoidan; y 990 g/kg Laminarin; z 720 g/kg Fucoidan; x 112 g/kg Laminarin, 89 g/kg Fucoidan and 799 g/kg ash; K 455 g/kg Laminarin and 360 g/kg Fucoidan.
Table 4. Influence of seaweed on digestibility in swine.
Table 4. Influence of seaweed on digestibility in swine.
Algae SupplementDose g/kgAnimalEffects on DigestibilityTreatment vs. Control, %Ref.
A. nodosumDried intact
(2.5 g/kg)
Male Pigs,
45 kg LW
NS[73]
A. nodosumDried intact (10–20 g/kg)Weaned piglets (35 d age)NS[42]
Brown seaweedAlginates olisaccharides
(100 mg/kg)
Weaned piglets, 6.2 kg LWImproved digestibility of [62]
N,
fat,
ash
GE
+6.7%
+10.8%
+25.9%
+4.0%
Ecklonia cavaSeaweed
(0.5–1—1.5 g/kg) s
Weaned piglets 7.8 kg LWImproved digestibility of GE+3.3% (1g/kg)[63]
Laminaria digitataLAM + FUC
(0.314–0.250 g/kg)
Weaned piglets,
7.2 kg LW
Improved digestibility of [64]
OM,
N,
NDF,
GE
+4.5%
+7.3%
+73.3%
+5.9%
Laminaria spp.Extract (1–2–4 g/kg) xWeaned piglets (24 d age)NS [66]
Laminaria spp.Seaweed extract
LAM (0.112 g/kg) y
FUC (0.089 g/kg) z
Weaned piglets, (24 d age)Improved digestibility of [65]
N,
GE
+6.7%
+5.2%
Laminaria spp.LAM + FUC (0.30 + 0.24 g/kg)Weaned piglets (22 d age)Improved digestibility of [68]
DM,
N,
NDF
+8.8%
+8.9%
+57.5%
Laminaria spp.LAM (0,15–0,30 g/kg)
FUC (0,24 g/kg)
LAM + FUC (0,15 + 0.24 and 0.30 + 0.24 g/kg)
Weaned piglets (24 d age)improved digestibility of [71]
DM, LAM and LAM + FUC
OM, LAM and LAM + FUC
N, LAM
NDF, LAM and LAM + FUC
GE, LAM and LAM + FUC
+7.0% – +4.5%
+5.9% – +3.5%
+5.1%
54.5% – 39.7%
+7.3% – +4.3%
Laminaria spp.LAM (0.30 g/kg)
FUC (0.24 g/kg)
LAM + FUC (0.30 + 0.24 g/kg)
Weaned piglets (24 d age)Improved digestibility of [67]
DM, LAM and LAM + FUC
N, LAM
Ash, LAM and LAM + FUC
GE, LAM and LAM + FUC
+7.9% – +4.5%
+6.6%
58.0% – 42.6%
+8.5% – +4.3%
Laminaria spp.Extract (0.66 g/kg) kWeaned piglets (24 d age)Improved digestibility of [70]
OM,
N,
Ash,
NDF,
GE
+8.8%
+8.9%
+82.4%
+57.5%
+10.9%
x 112 g/kg Laminarin, 89 g/kg Fucoidan and 799 g/kg ash.; k 455 g/kg Laminarin and 360 g/kg Fucoidan; s 112 g/kg Fucoidan; z 720 g/kg Fucoidan; y 990 g/kg Laminarin; FUC, Fucoidan; LAM, laminarin; LW, live weight; DM, dry matter; GE, gross energy; N, nitrogen; NDF neutral detergent fiber; OM, organic matter.
Table 5. Antibacterial activity of seaweeds.
Table 5. Antibacterial activity of seaweeds.
Strain SeaweedFunctional GroupSeaweedRef.
Campylobacter jejuniDelisea pulchraHalogenated furanoneRed[99]
Enterococcus faecium vancomycin-resistantCallophycus serratusDiterpene-benzoate Red[98]
Escherichia coliAscophyllum nodosum and Laminaria hyperboreaLaminarinBrown[100]
Sphaerococcus coronopifoliusSphaerane bromoditerpenes Red[101]
Pterocladia capillaceaWater-extracted polysaccharidesRed[102]
Sargassum swartziiSulphated polysaccharidesRed[103]
Delisea pulchraHalogenated furanoneRed[104]
Listeria monocytogenesAscophyllum nodosum and
Laminaria hyperborea
LaminarinBrown[100]
Pseudomonas aeruginosaSolieria filiformisLectin Red[105]
Sphaerococcus coronopifoliusSphaerane bromoditerpenes Red[101]
Delisea pulchraHalogenated furanoneRed[106,107]
PropionibacteriumEisenia bicyclisPhlorofucofuroeckol Brown[108,109]
Salmonella typhimuriumAscophyllum nodosum and Laminaria hyperboreaLaminarinBrown[100]
Staphylococcus aureusEisenia bicyclisPhlorofucofuroeckol Brown[110]
Ascophyllum nodosum and Laminaria hyperboreaLaminarinBrown[100]
Pterocladia capillaceaWater–extracted polysaccharidesRed[102]
Staphylococcus aureus
methicillin resistant
Saccharina longicrurisExtracted peptides (>10 kDa)Brown[111]
Sphaerococcus coronopifoliusSphaerane bromoditerpenes Red[101]
Callophycus serratusDiterpene-benzoateRed[98]
Table 6. Minimum inhibitory concentration (MIC) of marine–sulfated polysaccharides extract from Ulva armoricana [112].
Table 6. Minimum inhibitory concentration (MIC) of marine–sulfated polysaccharides extract from Ulva armoricana [112].
StrainMIC (mg/mL)
Pasteurella multocida1.56
Pasteurella multocida subsp. multocida3.125
Streptococcus suis6.25
Trueperella pyogenes50
Bordetella bronchiseptica50
Escherichia coli K85>50
Escherichia coli K88 (F4)>50
Table 7. Effects of seaweed on antioxidant capacity in pigs.
Table 7. Effects of seaweed on antioxidant capacity in pigs.
Algae SupplementDose
g/kg or g/day
AnimalAntioxidant EffectsTreatment
vs. Control, %
Ref.
A. nodosumDried seaweed 5–10 g/kgWeaned piglets,
6.59 kg LW
Plasma TBARS a, FRAP b, α-tocopherolNS[60]
Brown seaweedAlginic acid olisaccharides (100 mg/kg)Weaned piglets, 7.8 kg LWSerum [61]
T-AOC e
SOD f
CAT g
MDA h
+14%
+20%
+37%
−26%
Brown seaweedAlginates olisaccharides (100 mg/kg) Weaned piglets, 6.2 kg LWSerum [62]
T-AOC
CAT
GSHi
MDA
+21%
+28%
+28%
−10% NS
Brown seaweedAlginates olisaccharides (100 mg/kg) Weaned piglets, 6.2 kg LWDuodenum [92]
T-AOC+45%
MDA−40%
Jejunum
T-AOC+39%
CAT+22%
MDA−36%
Ileum
T-AOC+58%
CAT+72%
MDA–35%
Laminaria digitataWet (W) or spray dried (SD) seaweed
LAM + FUC
(0.5+0.4 g/kg)
Pigs, 14.5 kg LWPlasma TAS c
LD muscle TBARS
(refrig. storage 14 d)
NS
−29% SD
−47% W
[125]
Laminaria digitataLAM + FUC
(0.45 or 0.9 g/kg)
3 or 6 weeks pre slaughter
Pigs, 82 kg LWPlasma TAS
LD muscle TBARS (refrig. storage 14 d)
0.45 for 3 weeks
0.90 for 3 weeks
NS

−57%
−60%
[126]
Laminaria spp. LAM + FUC
(0.18 + 0.33 g/kg)
Pigs, 71 kg LWSerum
DPPH d
LD muscle TBARS
(refrig. storage 14 d)
+400%
−41%
[124]
LAM = Laminarin, FUC = Fucoidan; a TBARS, thiobarbituric acid-reactive substances; b FRAP, ferric reducing ability of plasma; c TAS, total antioxidant status; d DPPH, 2,2-diphenyl-1-picrylhydrazyl assay; e T-AOC, total antioxidant capacity; f SOD, superoxide dismutase; g CAT, catalase; h MDA, malondialdehyde; i GSH, glutathione.
Table 8. Potentially toxic trace element concentrations in seaweeds (mg/kg DM).
Table 8. Potentially toxic trace element concentrations in seaweeds (mg/kg DM).
Trace ElementBrown Seaweed 1Green Seaweed 2Red Seaweed 3Feed 4Feed Ingredient 4Ref.
Cadmium0.05–80.03–40.04–3.80.5 (1 *)1[19,21,39,133]
Mercury<0.005–0.160.005–0.07<0.005–0.030.1 (0.2 *)0.1[19,21,39,133]
Lead0.01–70.05–70.01–19510[19,21,133]
Arsenic8–1200.8–181–502 (10 *)40[19,21,39,133]
Inorganic arsenic0.03–7.70.2–0.40.03–0.6[21,133]
1Brown seaweed: Alaria esculenta, Ascophyllum nodosum, Fucus spiralis, Fucus vesicolosus, Himanthalia elongate, Laminaria digitata, Lamibaria hyperborea, Laminaria spp., Pelvetia canaliculata, Saccharina latissima Sargassum fusiformis, Undaria pinnatififda; 2 Green seaweed: Cladophora rupestris, Codium adhaerens, Codium vermilara, Enteromorpha intestinalis, Ulva lactuca, Ulva spp.; 3 Red seaweed: Chondrus crispus, Gigartina spp., Gracilaria vericulophylla, Gracilaria spp., Palmaria palmata, Polysiphonia lanosa, Porphyra spp.; 4 UE directive 2002/32/EC and amendments; * Fish feed.
Back to TopTop