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Review

Prebiotic Effects of Seaweed Polysaccharides in Pigs

by
Carlo Corino
,
Alessia Di Giancamillo
,
Silvia Clotilde Modina
and
Raffaella Rossi
*
Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Via dell’Università 6, 26900 Lodi, Italy
*
Author to whom correspondence should be addressed.
Animals 2021, 11(6), 1573; https://doi.org/10.3390/ani11061573
Submission received: 29 March 2021 / Revised: 22 May 2021 / Accepted: 24 May 2021 / Published: 27 May 2021
(This article belongs to the Special Issue Feeding Strategies to Minimize the Use of Antimicrobials and Zinc Oxide in Pig Production)
Versions Notes

Abstract

:

Simple Summary

In recent decades, the ban of antibiotic growth promoters together with the reduction in the feed of trace minerals with antimicrobial properties such as zinc and copper, has increased the demand to identify organic alternatives with antimicrobial properties that may improve the production efficiency and sustainability in an antibiotic-free system. The sustainability of pig production can be enhanced, by increasing the feed efficiency, modulating the microbiota, and reducing the impact of different diseases through the use of natural substances. Considerable research has focused on the gut environment and microbiota modulation as key to boosting pig health. Sustainable dietary interventions that positively modulate the gut environment and microbiota in pigs are required to enhance pig health and welfare. In the field of natural substances, seaweed and their bioactive compounds have assumed particular importance as feed ingredients for pigs. In fact, seaweeds include numerous bioactive substances with prebiotic, anti-microbial, antioxidant, anti-inflammatory, and immunomodulatory activities. The present paper reviews the prebiotic effects of seaweed polysaccharides in pigs.

Abstract

To ensure environmental sustainability, according to the European Green Deal and to boost the One Health concept, it is essential to improve animals’ health and adopt sustainable and natural feed ingredients. Over the past decade, prebiotics have been used as an alternative approach in order to reduce the use of antimicrobials, by positively affecting the gut microbiota and decreasing the onset of several enteric diseases in pig. However, dietary supplementation with seaweed polysaccharides as prebiotics has gained attention in recent years. Seaweeds or marine macroalgae contain several polysaccharides: laminarin, fucoidan, and alginates are found in brown seaweeds, carrageenan in red seaweeds, and ulvan in green seaweeds. The present review focuses on studies evaluating dietary seaweed polysaccharide supplementation in pig used as prebiotics to positively modulate gut health and microbiota composition.

1. Introduction

Gut health, which is described as a generalized condition of homeostasis in the gastrointestinal tract [1], has been recognized as playing a key role in maintaining pig health. In fact, the gut plays an important role in efficient feed digestion and absorption, for the protection of the gut barrier, the microbiota composition, and the improvement in the immune status [2]. In fact, commensal bacteria such as Lactobacilli and Bifidobacteria are necessary to sustain the host immune system, protecting against the colonization of opportunistic pathogens [3].
Since the ban on in-feed antibiotics, reliable dietary interventions are needed that are capable of sustaining pig performance and improving gut health, by minimizing the use of antimicrobials. A large amount of evidence has reported the beneficial effects of some feed ingredients or additives in modulating gut health and microbiota in pig.
The review by Xiong et al. [2] focused on the effects of several feed ingredients or additives such as functional amino acids, natural extracts, and short-chain fatty acids and prebiotics on gut health in weaned pigs.
Over the past few decades, prebiotics have been used as an alternative approach aimed at reducing the use of antimicrobials, by positively affecting the gut microbiota and decreasing the onset of several enteric diseases in pig [4]. However, dietary supplementation with seaweed polysaccharides as prebiotics, has also gained attention in recent years. In fact, natural bioactive compounds have been considered as attractive dietary interventions in pig in order to ensure environmental sustainability, in line with the European Green Deal plan and to improve animal health according to the One Health approach.
Marine macroalgae, or seaweeds, are classified as brown algae (Phaeophyceae), red algae (Rhodophyta), and green algae (Chlorophyta) and include thousands of species. The chemical composition and the bioactive metabolite content of several species have been extensively studied, along with the variations related to species and genera, harvesting season, environmental conditions, and geographical location [5,6]. Seaweeds also contain large amounts of carboxylated and sulfated polysaccharides, with important functions for the macroalgal cells including structural and energy storage [7]. Seaweed polysaccharides are safe, environmental-friendly, and economical natural polymers. Seaweed polysaccharides, such as fucoidan, laminarin, ulvan, carrageenan, and alginates, show several biological activities in vitro and in vivo studies [8,9]. In fact, polysaccharides and oligosaccharides originating from seaweeds have been shown to regulate intestinal metabolism and fermentation and reduce the adhesion of pathogenic bacteria [10]. Several seaweed polysaccharides have also shown anti-inflammatory, antiviral, and antioxidant activities [11]. Considering the above mentioned properties, the present paper reviews the prebiotic effects of seaweed polysaccharides in pig nutrition.

2. Seaweed Polysaccharides

The polysaccharides contained in brown, red, and green seaweeds present different bioactive molecules such as fucoidan, laminarin, alginate, ulvan, and carrageenan, which are reported in Table 1.
The yield of seaweed polysaccharides varies in relation to the species-growing conditions, extraction method, such as solvent concentration and extraction time [14]. The polysaccharide content of brown, red, and green seaweeds is reported in Table 2. The total polysaccharide content in seaweeds is highly variable, fluctuating from 4 to 80% of dry matter (DM), according to the data of Lafarga et al. [12].
In green seaweeds, the content ranges from 15 to 65% of DM with the highest value for Ulva spp., in red seaweeds from 53 to 66% of DM with the highest value in Chondrus crispus, and in brown seaweeds from 10 to 66% DM with the highest amount in Ascophyllum nodosum and Saccharina spp. [15].
Carrageenans and agars are the two main polysaccharides in red seaweeds, but porphyran and xylan have also been observed [16]. Carrageenans are sulfated polysaccharides, composed of d-galactose units, with a structural role, similar to cellulose in plants, and are present in some red algae, such as Chondrus, Gigartina, and Hypnea [17], with the highest amount in Chondrus and Kappaphycus spp. [18]. Agar is largely observed in the Gelidium and Gracilaria spp. and is composed of agarose and agaropectin [19]. Fucoidans, alginates, and laminarin are the main polysaccharides in brown seaweeds.
Alginates are the main cell wall polysaccharides in brown algae, such as Laminaria spp., Fucus spp., Ascophyllum nodosum, and Macrocystis pyrifera [20]. Besides alginates, fucoidans are cell wall water-soluble polysaccharides in brown seaweeds, containing L-fucose and sulfate groups, in addition to monosaccharides such as mannose, glucose, xylose, and glucuronic acid [21].
Table
Table 2. Polysaccharides composition of brown, red, and green seaweed (g kg−1 DM) 1.
Table 2. Polysaccharides composition of brown, red, and green seaweed (g kg−1 DM) 1.
SeaweedPolysaccharides, %AlginatesCarragenanFucoidanLaminarinUlvanReferences
Brown
Ascophillum nodosus62
(42–70)		285
(240–330)		-75
(11–120)		118
(12–120)		-[8,18,22,23,24,25]
Laminaria hyperborea39.9
(14.4–65.5)		215
(22–408)		-30
(20–40)		125
(0–320)		-[8,18,26,27,28]
Laminaria digitata57.3
(44–70.7)		435
(350–520)		-49.5
(22–112)		120
(0–350)		-[8,18,26,27,29,30,31]
Laminaria sp. *45
(13–77)		309
(225–343)		-147.5
(22–550)		153
(62.4–340)		-[8,26,29,32,33,34,35]
Fucus sp. #57
(34.5–66)		162-105
(11–200)		2.3
(0.4–3.8)		-[18,23,24,27,34,36,37,38]
Sargassum sp. ⁑36 (4–68)296
(93–499)		-38
(31–45)		3
(0–6)		-[18,34,36]
Saccharina sp. **69
(58–80)		242.5
(200–285)		-33
(13–80)		97.5
(0–330)		-[5,8,18,23,27,29,39]
Undaria pinnafitica40
(35–45)		425
(340–510)		-219
(30–690)		30-[8,18,29,40]
Red -----
Chondrus crispus60.5
(55–66)		-439.5
(338–510)		---[18,34,41]
Kappaphycus alvarezii58
(53.5–64)		-448.5
(187–756)		---[32,41,42,43]
Green -
Ulva sp. §42
(15–65)		----176
(11–400)		[18,34,44,45,46,47,48]
1 Data are reported as mean values and range (minimum-maximum). * Values from Laminaria claustonii and japonica. # values from Fucus vesciculosus, serratus, spiralys. ⁑ Values from Sargassum patens, hemifhyllum, henslowianum. ** Values from Saccharina longicruris, latissima, cichorioides, japonica, longissimi. § Values from Ulva armoricana, lactuca, intestinalis, meridionalis, pertusa. - Polysaccharides not present in the considered seaweed.
Laminarin, also called laminaran, is a storage polysaccharide in brown seaweeds which is composed of (1–3)-β-d-glucan. The laminarin structure differs in the degree of branching and polymerization. The highest laminarin content is found in Laminaria spp. and Saccharina spp. (32% DM), however it is also present in small amounts in Ascophyllum, Fucus, and Undaria spp. [18]. Ulvan is the constituent of the cell wall of green seaweeds and is constituted by β-(1–4)-xyloglucan, glucuronan, and cellulose in a linear arrangement [49]. The ulvan content varies from 2.7% DM in Ulva flexuosa to 40% DM in Ulva Armoricana [48].

3. Seaweed Polysaccharides as Prebiotic

Carbohydrates, which are indigestible to hydrolytic enzymes and are fermentable, are considered as prebiotics. They must not be digested or adsorbed in the first tract of the gut, however they should be fermented in the colon by Lactobacillus and Bifidobacterium, enhancing their growth and decreasing the concentration of other invading pathogens in the large intestine [50]. Digestion can affect the seaweed polysaccharide activity as prebiotics. The first step is to verify the resistance to hydrolysis by acids and enzymes in in vitro conditions.
Laminarins from different seaweeds vary in terms of the structural characteristics such as the degree of polymerization and the presence of inter-chain hydrogen bonds. These complex structures are resistant to hydrolysis in the first tract of the gut and are studied as dietary fibers [51]. In brown seaweed, polysaccharide laminarins were indigestible in an in vitro model with hydrochloric acid and enzymes [52]. In addition, laminarin from Laminaria saccharina and digitata were fermented, producing short-chain fatty acids (SCFA) [53]. Another study reported that SCFA that are produced from the fermentation of Laminaria digitata and Undaria pinnatifida are not metabolized well compared to the sugar beet fibers [54].
In a simulated digestion model, Ascophyllum nodusum was fermentable, thus producing SCFA and reducing the concentration of total anaerobe bacteria such as Escherichia coli and Streptococcus in batch systems inoculated with porcine cecal suspensions [55]. The same result was obtained in the Porphyra spp., a red seaweed with galactoside, which was not digested by salivary, gastric, pancreatic, or intestinal enzymes and was fermentable by Bifidobacterium [56].
Alginate, agarose, and carrageenan, from brown and red seaweeds are not digested but fermented by the gut bacteria [57]. Oligosaccharides enzymatically hydrolyzed from alginate, agarose, and carrageenan have shown prebiotic activities, stimulating Bifidobacteria and Lactobacilli growth and producing SCFA [58,59]. A recent in vitro study evaluated the fermentability of the three aforementioned oligosaccharides using pig fecal microbiota. The data reported that all the oligosaccharides considered were able to enhance SCFA concentration, in particular butyric acid. A positive shift in gut microbiota was also observed for alginate and agarose oligosaccharides with a decrease in pathogenic bacteria [60].
Ulvan, the main sulphated polysaccharide in green seaweeds, is a water-soluble dietary fiber resistant to digestive tract enzymes, however it is poorly fermented by colonic bacteria and thus in its form, it is not studied as a prebiotic, but could be hydrolyzed to bioactive oligosaccharides [61]. Low molecular weight Ulva armoricana aqueous extract, whose main component is ulvan, has shown antibacterial activity against several Gram-positive and Gram-negative bacterial strains [62].
Several in vivo studies in rats, highlighted the prebiotic activity of seaweed polysaccharides, as reviewed by O’Sullivan et al. [63]. In fact, it is reported that in rats, dietary supplementation with alginate oligosaccharides or agarose hydrolysate increased the cecum Bifidobacterium and Lactobacillus count. Another study on rats reported that dietary supplementation with Chondrus crispus increased the SCFA concentration and reduced the Clostridium and Streptococcus concentration [64]. In mice fed Laminaria japonica, a higher production of SCFA and butyric acid was observed, together with a decrease in Clostridium, Escherichia coli, and Enterobacter [65]. Considering the data on in vitro studies and laboratory animals, several studies on dietary supplementation with seaweed polysaccharides have been conducted in pigs to improve microbiota composition, and reduce the onset of several diseases and the subsequent antibiotic treatment.

4. Seaweed Polysaccharides as Prebiotics in Sows

The effects of algae polysaccharides as prebiotics in sows have been evaluated by several authors as presented in Table 3.
The effects of polysaccharides in the gut are usually assessed by evaluating the SCFA content and the intestinal microbiota composition and/or the presence of beneficial bacteria [72]. The effects of dietary supplementation with seaweeds in sows can modulate the productive performances and health of lactating piglets, making them more resistant to pathogens.
Dietary brown seaweeds were evaluated as a prebiotic in field conditions. In the study by Leonard et al. [66] an antimicrobial effect of seaweeds was observed. In fact, the establishment of neonatal gut microbiota was mediated by the fecal microflora of sows or by the colostrum and milk composition. This early gut colonization is fundamental for the development of healthy microbiota and for modulation of the immune system [73].
In piglets after 9 days of weaning, a decrease in Escherichia Coli was observed, however the same trend was also detected for Bifidobacteria and Lactobacillus. Moreover, a positive effect on the intestinal morphology was observed in the treated piglets. Similar result on the modulation of the microbiota was observed in a subsequent study from the same authors [67]. A reduction in fecal Escherichia coli in sows may positively affect piglet’s microbiota with a lower Enterobacteriaceae count which influences the onset of enteric pathologies [74]. In fact, although the Enterobacteriaceae count was higher in sows receiving dietary laminarin and fucoidan, the diarrhea score was lower in piglets from treated dams [68]. A positive impact on the ileum morphology of piglets from treated sows has also been observed, with an increase in villi height at weaning. In the study by Bouwhuis et al. [70] a lower expression was observed of heat-labile enterotoxin and enteroaggregative heat-stable enterotoxin, which are responsible for the intestinal colonization of enterotoxigenic Escherichia coli and represent the most frequent cause of diarrhea. It has been reported that laminarin, which is a source of β-glucans, lowered intestinal Enterobacteriaceae and reduced Escherichia coli numbers in feces. This could be ascribed to the potential agglutination activity, as earlier observed for yeast β-glucans which prevent bacterial adhesion and the colonization of the epithelial mucosa [75,76].
An antibacterial activity of fucoidan has also been reported [77]. An increase in Lactobacilli count was also observed which was also shown to be helpful for gut health with a positive modulation of the immune system [78,79].
In the considered studies the effects of laminarin and fucoidan from Laminaria spp. on Lactobacilli population were inconsistent.

5. Seaweed Polysaccharides as Prebiotics in Post Weaning Piglets

Weaning is a critical phase in pig production, often characterized by high antibiotic and microelement use. In fact, at weaning the gastrointestinal tract and immune system of piglets are not yet fully developed and the social, environmental, and physiological challenges, predispose the piglets to dysbiosis [80]. These challenges lead to a lower feed intake and growth rate and a high incidence of post-weaning diarrhea (PWD) due to the presence of enteric pathogenic bacteria [81].
In fact, at weaning, a lower Lactobacilli count has been observed, with a high growth of facultative anaerobes bacteria such as Enterobacteriaceae, Proteobacteriaceae, Clostridiaceae, and Prevotellaceae [80]. After weaning, structural and functional alterations of the small intestine have also been observed with negative effects on the absorptive capacity [82].
Feeding strategies in the post-weaning phase can reestablish the gut eubiosis that was lost at weaning, aimed at restoring the Lactobacillus count, promoting the growth of beneficial bacteria that boost the mucosal immune system and lowering the pathogenic bacteria proliferation [83].
The role of diet in the post weaning health status is widely recognized, in fact feed ingredients and additives can exert selective pressure on the gut microbiota. It has also been reported that dietary fermentable carbohydrates play a key role in positively affecting the intestinal microbiota of post-weaning piglets [84].
Several studies have evaluated the effects of seaweed polysaccharides as prebiotics in post weaning piglets, as reported in Table 4.
The dietary inclusion of Ascophillum nodosum in the piglets’ diet can reduce the Escherichia Coli content in the small intestine of weaned piglets [85]. The Lactobacillus/Escherichia coli ratio in the small intestine was shown to increase in the piglets receiving dietary seaweeds suggesting a helpful microbial modification. A reduction in the Enterobacteriaceae count was also observed. These are opportunistic pathogens such as Salmonella Typhimurium and enterotoxigenic Escherichia coli (ETEC) that induce PWD in piglets [85]. No effects of dietary Ascophillum nodosum on the small intestinal morphology were observed but an increase in total SCFA and butyric acid content were reported [85,86]. Similar data on gut health improvement have been observed with dietary supplementation with Laminaria spp.
Laminarin and fucoidan, as sources of seaweed polysaccharides with prebiotic effects, are able to decrease fecal Escherichia coli counts in the feces, thus improving post-weaning piglet health with a positive effect on growth performance and gain to feed ratio [88,90]. An improvement in Lactobacillus count has also been detected [88,89,91,92,93].
It has been also reported that laminarin, modifying the resident microbiota, may indirectly enhance mucin synthesis and secretion, as adherence of beneficial bacteria to mucosal epithelia up-regulates the mucin production. An enhancement of cytokine gene expression was also observed after a lipopolysaccharide (LPS) challenge [101].
Fucoidan also supports Lactobacillus growth with a positive effect on feed digestibility [87,101].
The increase in butyric acid reported in several studies, is usually related to carbohydrate fermentation which has a positive effect on gut health [87,91,92,97]. However, in the study by Sweety et al. [91], after a Salmonella typhimurium challenge, proliferation of Salmonella shedding was observed after dietary supplementation with laminarin and fucoidan. This is probably related to the decreased content of propionic acid and increased content of acetic acid which can modulate the gene activation in Salmonella pathogenicity Island 1 (SPI−1) [102].
A recent study showed that the alginic acid oligosaccharide from seaweed, which contains 96% α-L-guluronic acid and 4% β-D-mannuronic acid, has antibacterial and anti-biofilm activities. These oligosaccharides can modulate mucosal cytokine expression and antibody production and promote the growth of Lactobacillus [103]. As recently reported, dietary seaweed alginic acid oligosaccharides in weaned piglets can boost the intestinal barrier integrity, upregulating occludin mRNA expression in the caecal mucosa and claudin—1 mRNA expression in the caecal and colonic mucosa [98].
A recent study in piglets also showed that supplementing a seaweed product in drinking water (Algo-Bio®) decreased the Enterobacteria resistance rate to tetracycline [104]. In addition, in piglets treated with a seaweed supplement, the antibiotic susceptibility test showed a high sensitivity of Escherichia coli to imipenem, amikacin, and netilmicin with low chloramphenicol resistance. In fact, in agreement with the data of Berri et al. [105], the use of seaweed in pig nutrition to overcome antibiotic resistance is promising.

6. Seaweed Polysaccharides as Prebiotics in Growing-Finishing Pigs

Table 5 reports the effects of seaweed carbohydrates as prebiotics in growing-finishing pigs. The antimicrobial properties of seaweed polysaccharides in growing-finishing pigs could be effective in reducing pre-slaughter enteric pathogens.
In fact, several studies have reported a lower enteric Escherichia coli count in growing-finishing pigs fed Ascophillum nodosus or Laminaria spp. [101,106,107]. Dietary seaweed polysaccharides reduced intestinal and fecal Salmonella Typhimurium and lowered the colonic gene expression of pro-inflammatory cytokines in growing-finishing pigs after an experimental Salmonella Typhimurium challenge [108,109].
The effects of Laminaria digitata extract in wet, spray-dried, and freeze-dried forms have also been evaluated [110,111]. The laminarin and fucoidan from L. digitata in wet form showed a prebiotic effect in pig, enhancing the Bifidobacterium sp. count in the ileum. In fact, several technological processes, such as spray drying techniques, have been shown to reduce the functionality of some bioactive compounds [112]. An increase in the colon and cecum SCFA was also detected following dietary supplementation with laminarin [101] and fucoidan [113].
In the growing finishing phase, the decline in enteric Escherichia coli and Salmonella Typhimurium count and the improvement in beneficial bacteria, such as Bifidobacterium and Lactobacillus, suggest that brown seaweed polysaccharides are a sustainable dietary strategy to improve gut health, by modulating microbiota and reducing pre-slaughter pathogens.
Table
Table 5. Prebiotic effects of seaweed in growing finishing swine.
Table 5. Prebiotic effects of seaweed in growing finishing swine.
Seaweed SupplementDoseAnimalPrebiotic EffectEffect vs. Control %Reference
Ascophyllum nodosumDried intact x
(3–6–9 g kg−1)		Pig,
48.7 kg LW		Ileum:
Coliform
Lattobacillus
Adherent Lactob.
Biphydobacteria
−19%
NS
NS
NS		[106]
L. digitataWet (W) or
spray dried (SD)
seaweed		Pig
14.5 kg LW		Ileum:
Bifidobacterium
Lactobacillus
Enterobacteriaceae
+18% wet
NS
NS		[110]
L. digitataWet (W) or
spray dried (SD)
seaweed
LAM + FUC
(0.50–0.42 g kg−1)		Pig,
14.5 kg LW		Ileum: Bifidobacterium

Lactobacilli spp.
+45% SD
+66% W
+31% SD
+47% W		[111]
L. digitataSeaweed extract y
LAM
(0.3–0.6 g kg−1)		Pigs,
18 kg LW		Colon:
Enterobacteriaceae
Caecum:

SCFA
−29% LAM 0.3
−22% LAM 0.6

+9% LAM 0.3
+12% LAM 0.6		[101]
L. hyperboreaSeaweed extract
LAM (0.30 g g kg−1)
FUC (0.36 g kg−1)
LAM + FUC
(0.3 + 0.36 g kg−1)		Boars,
65 kg LW		Proximal colon:
Enterobacterium spp.
Lactobacilli spp.
SCFA
Distal colon:
Enterobacterium spp.
Lactobacilli spp.
SCFA
+14% LAM + FUC
+16% FUC
+16% FUC

+30% LAM + FUC
+43% FUC
+36% FUC		[113]
L. hyperboreaSeaweed extract z
(0.7–1.4–2.8–5.6 g kg−1)
LAM = 0.08–0.16–0.32–0.64 g kg−1
FUC = 0.06–0.12–0.24–0.48 g kg−1		Boars,
76 kg LW		Caecum:
Bifidobacterium spp.
Enterobacterium spp.
Colon:
Entorobacteria
Bifidobacterium spp.
Lactobacilli spp.
−3, +5, +2, +3%
+3,− 4, −7, −4%

−3, −9, −7, −2%
+3, +5, +2, −3%
0, −1, −2, −3%		[107]
Laminaria spp.Seaweed extract
LAM + FUC
(0.18 + 0.34 g kg−1)		Female pigs, 30.9 kg LW
Challenge Salmonella Typhimurium 11 d		Caecum:
S. Typhimurium
Lactobacillus spp.
Colon
S. Typhimurium
Lactobacillus spp.
−16%
+3%

−24%
+1%		[108]
Laminaria spp.Seaweed extract
in diet
LAM + FUC (0.18 + 0.34 g kg−1)		Female pigs,
30.9 kg
Challenge Salmonella Typhimurium
at 11 d		Salmonella Typhimurium
Caecum
Colon
−16%
−24%		[109]
LAM: laminarin; FUC: fucoidan; SCFA: short-chain fatty acids. x The Ascophillum Nodosum seaweed extract (Kerry Enhancer, Kerry Algae, Curraheen, Tralee Co., Kerry, Ireland). y Purified laminarin (990 g/kg) laminarin was sourced from Bioatlantis Limited, Tralee, County Kerry, Republic of Ireland. z The seaweed extract contained laminarin (112 g kg−1), fucoidan (89 g kg−1).

7. Conclusions

Overall, the present data demonstrate that the prebiotic activity of seaweed polysaccharides could be used to improve pig health in several production phases, thus reducing the use of antimicrobials. The gut health enhancement and reduction in pathogenic bacteria in lactating and post weaning piglets are fundamental in modulating productive performance and health, by reducing gastrointestinal diseases and enhancing feed digestibility. In the growing-fattening phase, a modulation of microbiota and a reduction in pre-slaughter enteric pathogens have also been observed.
In conclusion, dietary supplementation with brown seaweed polysaccharides seems to be a valid strategy to modulate microbiota, making pigs more resistant to pathogens and thus reducing antimicrobial use. Considering that prebiotic and antibacterial activities have also been observed for red and green seaweed polysaccharides, further studies are needed to evaluate their effects on pig health.

Author Contributions

Conceptualization, C.C. and R.R.; methodology, C.C. and R.R.; writing—original draft preparation, C.C., R.R., A.D.G. and S.C.M. writing—review and editing, C.C., R.R., S.C.M. and A.D.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Pluske, J.R.; Turpin, D.L.; Kim, J.C. Gastrointestinal tract (gut) health in the young pig. Anim. Nutr. 2018, 4, 187–196. [Google Scholar] [CrossRef] [PubMed]
  2. Xiong, X.; Tan, B.; Song, M.; Ji, P.; Kim, K.; Yin, Y.; Liu, Y. Nutritional Intervention for the Intestinal Development and Health of Weaned Pigs. Front. Vet. Sci. 2019, 6, 46. [Google Scholar] [CrossRef] [Green Version]
  3. Knecht, D.; Cholewińska, P.; Jankowska-Mąkosa, A.; Czyż, K. Development of Swine’s Digestive Tract Microbiota and Its Relation to Production Indices—A Review. Anim. 2020, 10, 527. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Liu, Y.; Espinosa, C.D.; Abelilla, J.J.; Casas, G.A.; Lagos, L.V.; Lee, S.A.; Kwon, W.B.; Mathai, J.K.; Navarro, D.M.; Jaworski, N.W. Non-antibiotic feed additives in diets for pigs: A review. Anim. Nutr. 2018, 4, 113–125. [Google Scholar] [CrossRef] [PubMed]
  5. Renaud, S.M.; Luong-Van, J.T. Seasonal Variation in the Chemical Composition of Tropical Australian Marine Macroalgae. J. Appl. Phycol. 2006, 18, 381–387. [Google Scholar] [CrossRef]
  6. Corino, C.; Modina, S.C.; Di Giancamillo, A.; Chiapparini, S.; Rossi, R. Seaweeds in Pig Nutrition. Animals 2019, 9, 1126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Garcia-Vaquero, M.; Rajauria, G.; O’Doherty, J.; Sweeney, T. Polysaccharides from macroalgae: Recent advances, innovative technologies and challenges in extraction and purification. Food Res. Int. 2017, 99, 1011–1020. [Google Scholar] [CrossRef] [Green Version]
  8. Kadam, S.U.; Tiwari, B.K.; O’Donnell, C. Extraction, structure and biofunctional activities of laminarin from brown algae. Int. J. Food Sci. Technol. 2014, 50, 24–31. [Google Scholar] [CrossRef]
  9. Sweeney, T.; O’Doherty, J. Marine macroalgal extracts to maintain gut homeostasis in the weaning piglet. Domest. Anim. Endocrinol. 2016, 56, S84–S89. [Google Scholar] [CrossRef]
  10. Lean, Q.Y.; Eri, R.; Fitton, J.H.; Patel, R.P.; Gueven, N. Fucoidan Extracts Ameliorate Acute Colitis. PLoS ONE 2015, 10, e0128453. [Google Scholar] [CrossRef] [Green Version]
  11. Lopez-Santamarina, A.; Miranda, J.M.; Mondragon, A.D.C.; Lamas, A.; Cardelle-Cobas, A.; Franco, C.M.; Cepeda, A. Potential Use of Marine Seaweeds as Prebiotics: A Review. Molecules 2020, 25, 1004. [Google Scholar] [CrossRef] [Green Version]
  12. Lafarga, T.; Acién-Fernández, F.G.; Garcia-Vaquero, M. Bioactive peptides and carbohydrates from seaweed for food applications: Natural occurrence, isolation, purification, and identification. Algal Res. 2020, 48, 101909. [Google Scholar] [CrossRef]
  13. Stiger-Pouvreau, V.; Bourgougnon, N.; Deslandes, E. Carbohydrates From Seaweeds. In Seaweed in Health and Disease Prevention; Elsevier BV: Amsterdam, The Netherlands, 2016; pp. 223–274. [Google Scholar]
  14. Bilan, M.I.; Grachev, A.A.; Shashkov, A.S.; Nifantiev, N.E.; Usov, A.I. Structure of a fucoidan from the brown seaweed Fucus serratus L. Carbohydr. Res. 2006, 341, 238–245. [Google Scholar] [CrossRef]
  15. Sardari, R.R.R.; Karlsson, E.N. Marine Poly- and Oligosaccharides as Prebiotics. J. Agric. Food Chem. 2018, 66, 11544–11549. [Google Scholar] [CrossRef]
  16. Kraan, S. Algal Polysaccharides, Novel Applications and Outlook. In Carbohydrates—Comprehensive Studies on Glycobiology and Glycotechnology; Chang, C.-F., Ed.; IntechOpen: London, UK, 2012; pp. 489–532. [Google Scholar]
  17. Lahaye, M. Developments on gelling algal galactans, their structure and physico-chemistry. Environ. Boil. Fishes 2001, 13, 173–184. [Google Scholar] [CrossRef]
  18. Holdt, S.L.; Kraan, S. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 2011, 23, 543–597. [Google Scholar] [CrossRef]
  19. Armisen, R.; Galatas, F. Production, Properties and Uses of Agar. In Production and Utilization of Products from Commercial Seaweeds; McHugh, D.J., Ed.; FAO Fisheries Technical Paper; The Food and Agriculture Organization (FAO): Rome, Italy, 1987; pp. 1–57. [Google Scholar]
  20. Lorbeer, A.J.; Charoensiddhi, S.; Lahnstein, J.; Lars, C.; Franco, C.M.; Bulone, V.; Zhang, W. Sequential extraction and char-acterization of fucoidans and alginates from Ecklonia radiata, Macrocystis pyrifera, Durvillaea potatorum, and Seirococcus axillaris. J. Appl. Phycol. 2017, 29, 1515–1526. [Google Scholar] [CrossRef]
  21. Wu, L.; Sun, J.; Su, X.; Yu, Q.; Yu, Q.; Zhang, P. A review about the development of fucoidan in antitumor activity: Progress and challenges. Carbohydr. Polym. 2016, 154, 96–111. [Google Scholar] [CrossRef]
  22. Moen, E.; Horn, S.; Østgaard, K. Biological degradation of Ascophyllum nodosum. Environ. Boil. Fishes 1997, 9, 347–357. [Google Scholar] [CrossRef]
  23. Rioux, L.-E.; Turgeon, S.; Beaulieu, M. Characterization of polysaccharides extracted from brown seaweeds. Carbohydr. Polym. 2007, 69, 530–537. [Google Scholar] [CrossRef]
  24. Fletcher, H.; Biller, P.; Ross, A.; Adams, J. The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res. 2017, 22, 79–86. [Google Scholar] [CrossRef] [Green Version]
  25. Agregán, R.; Franco, D.; Carballo, J.; Tomasevic, I.; Barba, F.J.; Gómez, B.; Muchenje, V.; Lorenzo, J.M. Shelf life study of healthy pork liver pâté with added seaweed extracts from Ascophyllum nodosum, Fucus vesiculosus and Bifurcaria bifurcata. Food Res. Int. 2018, 112, 400–411. [Google Scholar] [CrossRef]
  26. Schiener, P.; Black, K.D.; Stanley, M.S.; Green, D. The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. Environ. Boil. Fishes 2015, 27, 363–373. [Google Scholar] [CrossRef]
  27. Graiff, A.; Wolfgang, R.; Udo, K.; Ulf, K. Chemical characterization and quantification of the brown algal storage compound laminarin—A new methodological approach. J. Appl. Phycol. 2016, 28, 533–543. [Google Scholar] [CrossRef]
  28. Rajauria, G.; Ravindran, R.; Garcia-Vaquero, M.; Rai, D.K.; Sweeney, T.; O’Doherty, J. Molecular characteristics and antioxidant activity of laminarin extracted from the seaweed species Laminaria hyperborea, using hydrothermal-assisted extraction and a multi-step purification procedure. Food Hydrocoll. 2021, 112, 106332. [Google Scholar] [CrossRef]
  29. Bruhn, A.; Janicek, T.; Manns, D.; Nielsen, M.M.; Balsby, T.J.S.; Meyer, A.S.; Rasmussen, M.B.; Hou, X.; Saake, B.; Göke, C.; et al. Crude fucoidan content in two North Atlantic kelp species, Saccharina latissima and Laminaria digitata—seasonal variation and impact of environmental factors. Environ. Boil. Fishes 2017, 29, 3121–3137. [Google Scholar] [CrossRef] [Green Version]
  30. Fertah, M.; Belfkira, A.; Dahmane, E.M.; Taourirte, M.; Brouillette, F. Extraction and characterization of sodium alginate from Moroccan Laminaria digitata brown seaweed. Arab. J. Chem. 2017, 10, S3707–S3714. [Google Scholar] [CrossRef] [Green Version]
  31. Allahgholi, L.; Sardari, R.R.R.; Hakvåg, S.; Ara, K.Z.G.; Kristjansdottir, T.; Aasen, I.M.; Fridjonsson, O.H.; Brautaset, T.; Hreggvidsson, G.O.; Karlsson, E.N. Composition analysis and minimal treatments to solubilize polysaccharides from the brown seaweed Laminaria digitata for microbial growth of thermophiles. Environ. Boil. Fishes 2020, 32, 1933–1947. [Google Scholar] [CrossRef] [Green Version]
  32. Istini, S.; Ohno, M.; Kusunose, H. Methods of analysis for Agar, Carrageenan and Alginate in Seaweed. Bull. Mar. Sci. Fish Kochi Univ. 1994, 14, 49–55. [Google Scholar]
  33. Lu, J.; You, L.; Lin, Z.; Zhao, M.; Cui, C. The antioxidant capacity of polysaccharide from Laminaria japonica by citric acid extraction. Int. J. Food Sci. Technol. 2013, 48, 1352–1358. [Google Scholar] [CrossRef]
  34. Jacobsen, C.; Sørensen, A.-D.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]
  35. Li, X.-Y.; Chen, H.-R.; Zha, X.-Q.; Chen, S.; Pan, L.-H.; Li, Q.-M.; Luo, J.-P. Prevention and possible mechanism of a purified Laminaria japonica polysaccharide on adriamycin-induced acute kidney injury in mice. Int. J. Biol. Macromol. 2020, 148, 591–600. [Google Scholar] [CrossRef] [PubMed]
  36. Ale, M.T.; Mikkelsen, J.D.; Meyer, A.S. Important Determinants for Fucoidan Bioactivity: A Critical Review of Structure-Function Relations and Extraction Methods for Fucose-Containing Sulfated Polysaccharides from Brown Seaweeds. Mar. Drugs 2011, 9, 2106–2130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Catarino, M.D.; Silva, A.M.S.; Cardoso, S.M. Fucaceae: A Source of Bioactive Phlorotannins. Int. J. Mol. Sci. 2017, 18, 1327. [Google Scholar] [CrossRef] [Green Version]
  38. Agregán, R.; Munekata, P.E.; Domínguez, R.; Carballo, J.; Franco, D.; Lorenzo, J.M. Proximate composition, phenolic content and in vitro antioxidant activity of aqueous extracts of the seaweeds Ascophyllum nodosum, Bifurcaria bifurcata and Fucus vesiculosus. Effect of addition of the extracts on the oxidative stability of canola oil under accelerated storage conditions. Food Res. Int. 2017, 99, 986–994. [Google Scholar] [CrossRef]
  39. Jiménez-Escrig, A.; Gómez-Ordóñez, E.; Rupérez, P. Infrared characterisation, monosaccharide profile and antioxidant activity of chemical fractionated polysaccharides from the edible seaweed sugar Kombu (Saccharina latissima). Int. J. Food Sci. Technol. 2014, 50, 340–346. [Google Scholar] [CrossRef] [Green Version]
  40. Skriptsova, A.; Khomenko, V.; Isakov, V. Seasonal changes in growth rate, morphology and alginate content in Undaria pinnatifida at the northern limit in the Sea of Japan (Russia). Environ. Boil. Fishes 2004, 16, 17–21. [Google Scholar] [CrossRef]
  41. Pereira, L. A review of the nutrient composition of selected edible seaweeds. In Seaweed: Ecology, Nutrient Composition and Medicinal Use, 1st ed.; Pomin, V.H., Ed.; Nova Science Publishers: Coimbra, Portugal, 2011; Chapter 2; ISBN 978-1-61470-878-0. [Google Scholar]
  42. Hayashi, L.; Edison, P.; Fungyi, C. Growth rate and carrageenan analyses in four strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales) farmed in the subtropical Waters. J. Appl. Phycol. 2007, 19, 393–399. [Google Scholar] [CrossRef]
  43. Khalil, H.A.; Lai, T.K.; Tye, Y.Y.; Rizal, S.; Chong, E.W.N.; Yap, S.W.; Hamzah, A.A.; Fazita, M.R.N.; Paridah, M.T. A review of extractions of seaweed hydrocolloids: Properties and applications. Express Polym. Lett. 2018, 12, 296–317. [Google Scholar] [CrossRef]
  44. Alves, A.; Sousa, R.A.; Reis, R.L. A practical perspective on ulvan extracted from green algae. Environ. Boil. Fishes 2012, 25, 407–424. [Google Scholar] [CrossRef] [Green Version]
  45. Castelar, B.; Reis, R.P.; Calheiros, A.C.D.S. Ulva lactuca and U. flexuosa (Chlorophyta, Ulvophyceae) cultivation in Brazilian tropical waters: Recruitment, growth, and ulvan yield. Environ. Boil. Fishes 2014, 26, 1989–1999. [Google Scholar] [CrossRef]
  46. Shao, P.; Qin, M.; Han, L.; Sun, P. Rheology and characteristics of sulfated polysaccharides from chlorophytan seaweeds Ulva fasciata. Carbohydr. Polym. 2014, 113, 365–372. [Google Scholar] [CrossRef]
  47. Rahimi, F.; Tabarsa, M.; Rezaei, M. Ulvan from green algae Ulva intestinalis: Optimization of ultrasound-assisted extraction and antioxidant activity. Environ. Boil. Fishes 2016, 28, 2979–2990. [Google Scholar] [CrossRef]
  48. Kidgell, J.T.; Magnusson, M.; de Nys, R.; Glasson, C.R. Ulvan: A systematic review of extraction, composition and function. Algal Res. 2019, 39, 101422. [Google Scholar] [CrossRef]
  49. Jaulneau, V.; Lafitte, C.; Jacquet, C.; Fournier, S.; Salamagne, S.; Briand, X.; Esquerré-Tugayé, M.-T.; Dumas, B. Ulvan, a Sulfated Polysaccharide from Green Algae, Activates Plant Immunity through the Jasmonic Acid Signaling Pathway. J. Biomed. Biotechnol. 2010, 2010, 1–11. [Google Scholar] [CrossRef] [Green Version]
  50. Sridevi, K.; Dhevendaran, K. Genetic analysis of antibiotic production and other phenotypic traits from Streptomyces associated with seaweeds. Afr. J. Biotechnol. 2014, 13, 2648–2660. [Google Scholar] [CrossRef] [Green Version]
  51. Neyrinck, A.M.; Mouson, A.; Delzenne, N. Dietary supplementation with laminarin, a fermentable marine β (1–3) glucan, protects against hepatotoxicity induced by LPS in rat by modulating immune response in the hepatic tissue. Int. Immunopharmacol. 2007, 7, 1497–1506. [Google Scholar] [CrossRef]
  52. Deville, C.; Damas, J.; Forget, P.; Dandrifosse, G.; Peulen, O. Laminarin in the dietary fiber concept. J. Sci. Food Agric. 2004, 84, 1030–1038. [Google Scholar] [CrossRef]
  53. Deville, C.; Gharbi, M.; Dandrifosse, G.; Peulen, O. Study on the effects of laminarin, a polysaccharide from seaweed, on gut characteristics. J. Sci. Food Agric. 2007, 87, 1717–1725. [Google Scholar] [CrossRef]
  54. Michel, C.; Macfarlane, G. Digestive fates of soluble polysaccharides from marine macroalgae: Involvement of the colonic microflora and physiological consequences for the host. J. Appl. Bacteriol. 1996, 80, 349–369. [Google Scholar] [CrossRef]
  55. Dierick, N.; Ovyn, A.; De Smet, S. Effect of feeding intact brown seaweedAscophyllum nodosumon some digestive parameters and on iodine content in edible tissues in pigs. J. Sci. Food Agric. 2009, 89, 584–594. [Google Scholar] [CrossRef]
  56. Muraoka, T.; Ishihara, K.; Oyamada, C.; Kunitake, H.; Hirayama, I.; Kimura, T. Fermentation Properties of Low-Quality Red Alga SusabinoriPorphyra yezoensisby Intestinal Bacteria. Biosci. Biotechnol. Biochem. 2008, 72, 1731–1739. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Shang, Q.; Jiang, H.; Cai, C.; Hao, J.; Li, G.; Yu, G. Gut microbiota fermentation of marine polysaccharides and its effects on intestinal ecology: An overview. Carbohydr. Polym. 2018, 179, 173–185. [Google Scholar] [CrossRef] [PubMed]
  58. Wang, Y.; Han, F.; Hu, B.; Li, J.; Yu, W. In vivo prebiotic properties of alginate oligosaccharides prepared through enzymatic hydrolysis of alginate. Nutr. Res. 2006, 26, 597–603. [Google Scholar] [CrossRef]
  59. Hu, B.; Gong, Q.; Wang, Y.; Ma, Y.; Li, J.; Yu, W. Prebiotic effects of neoagaro-oligosaccharides prepared by enzymatic hydrolysis of agarose. Anaerobe 2006, 12, 260–266. [Google Scholar] [CrossRef]
  60. Han, Z.-L.; Yang, M.; Fu, X.-D.; Chen, M.; Su, Q.; Zhao, Y.-H.; Mou, H.-J. Evaluation of Prebiotic Potential of Three Marine Algae Oligosaccharides from Enzymatic Hydrolysis. Mar. Drugs 2019, 17, 173. [Google Scholar] [CrossRef] [Green Version]
  61. Andrieux, C.; Hibert, A.; Houari, A.M.; Bensaada, M.; Popot, F.; Szylit, O. Ulva lactuca is poorly fermented but alters bacterial metabolism in rats inoculated with human fecal flora from methane and non-methane producers. J. Sci. Food Agric. 1998, 77, 25–30. [Google Scholar] [CrossRef]
  62. Berri, M.; Slugocki, C.; Olivier, M.; Helloin, E.; Jacques, I.; Salmon, H.; Demais, H.; Le Goff, M.; Collen, P.N. Marine-sulfated polysaccharides extract of Ulva armoricana green algae exhibits an antimicrobial activity and stimulates cytokine expression by intestinal epithelial cells. Environ. Boil. Fishes 2016, 28, 2999–3008. [Google Scholar] [CrossRef]
  63. 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] [Green Version]
  64. Liu, J.; Kandasamy, S.; Zhang, J.; Kirby, C.W.; Karakach, T.K.; Hafting, J.; Critchley, A.T.; Evans, F.; Prithiviraj, B. Prebiotic effects of diet supplemented with the cultivated red seaweed Chondrus crispus or with fructo-oligo-saccharide on host immunity, colonic microbiota and gut microbial metabolites. BMC Complement. Altern. Med. 2015, 15, 1–12. [Google Scholar] [CrossRef]
  65. Kim, J.; Yu, D.; Kim, J.; Choi, E.; Lee, C.; Hong, Y.; Kim, C.; Lee, S.; Choi, I.; Cho, K. Effects of Undaria linnatifida and Laminaria japonica on rat’s intestinal microbiota and metabolite. J. Nutr. Food Sci. 2016, 6, 1000502. [Google Scholar] [CrossRef]
  66. Leonard, S.G.; Sweeney, T.; Bahar, B.; Lynch, B.P.; O’Doherty, J.V. Effect of dietary seaweed extracts and fish oil supplementation in sows on performance, intestinal microflora, intestinal morphology, volatile fatty acid concentrations and immune status of weaned pigs. Br. J. Nutr. 2010, 105, 549–560. [Google Scholar] [CrossRef] [Green Version]
  67. 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 challenge1. J. Anim. Sci. 2012, 90, 505–514. [Google Scholar] [CrossRef]
  68. 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] [Green Version]
  69. Heim, G.; Sweeney, T.; O’Shea, C.; Doyle, D.; O’Doherty, J. 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]
  70. 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]
  71. Bouwhuis, M.; Sweeney, T.; Mukhopadhya, A.; McDonnell, M.; O’Doherty, J. 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]
  72. Chater, P.I.; Wilcox, M.; Cherry, P.; Herford, A.; Mustar, S.; Wheater, H.; Brownlee, I.; Seal, C.; Pearson, J. Inhibitory activity of extracts of Hebridean brown seaweeds on lipase activity. Environ. Boil. Fishes 2016, 28, 1303–1313. [Google Scholar] [CrossRef] [Green Version]
  73. Yao, K.; Sun, Z.; Liu, Z.; Li, Z.; Yin, Y. Development of the gastrointestinal tract in pigs. In Nutritional and Physiological Functions of Amino Acids in Pigs; Blachier, F., Wu, G., Yin, Y., Eds.; Springer Verlag: Vienna, Austria, 2013; pp. 3–18. ISBN 978-3-7091-1328-8. [Google Scholar]
  74. Melin, L.; Mattsson, S.; Katouli, M.; Wallgren, P. Development of Post-weaning Diarrhoea in Piglets. Relation to Presence of Escherichia coli Strains and Rotavirus. J. Vet. Med. Ser. B 2004, 51, 12–22. [Google Scholar] [CrossRef]
  75. Mirelman, D.; Altmann, G.; Eshdat, Y. Screening of bacterial isolates for mannose-specific lectin activity by agglutination of yeasts. J. Clin. Microbiol. 1980, 11, 328–331. [Google Scholar] [CrossRef] [Green Version]
  76. Kogan, G.; Kocher, A. Role of yeast cell wall polysaccharides in pig nutrition and health protection. Livest. Sci. 2007, 109, 161–165. [Google Scholar] [CrossRef]
  77. Shibata, H.; Iimuro, M.; Uchiya, N.; Kawamori, T.; Nagaoka, M.; Ueyama, S.; Hashimoto, S.; Yokokura, T.; Sugimura, T.; Wakabayashi, K. Preventive Effects of Cladosiphon Fucoidan Against Helicobacter pylori Infection in Mongolian gerbils. Helicobacter 2003, 8, 59–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Ouwehand, A.C.; Salminen, S.; Isolauri, E. Probiotics: An overview of beneficial effects. Antonie van Leeuwenhoek 2002, 82, 279–289. [Google Scholar] [CrossRef] [PubMed]
  79. Pierce, K.; Sweeney, T.; Brophy, P.; Callan, J.; McCarthy, P.; O’Doherty, J. Dietary manipulation post weaning to improve piglet performance and gastro-intestinal health. Anim. Sci. 2005, 81, 347–356. [Google Scholar] [CrossRef]
  80. Gresse, R.; Chaucheyras-Durand, F.; Fleury, M.A.; Van de Wiele, T.; Forano, E.; Blanquet-Diot, S. Gut Microbiota Dysbiosis in Postweaning Piglets: Understanding the Keys to Health. Trends Microbiol. 2017, 25, 851–873. [Google Scholar] [CrossRef]
  81. Estrada, A.; Drew, M.D.; Van Kessel, A. Effect of the dietary supplementation of fructooligosaccharides and Bifidobacterium longum to early-weaned pigs on performance and fecal bacterial populations. Can. J. Anim. Sci. 2001, 81, 141–148. [Google Scholar] [CrossRef] [Green Version]
  82. Campbell, J.M.; Crenshaw, J.D.; Polo, J. The biological stress of early weaned piglets. J. Anim. Sci. Biotechnol. 2013, 4, 19. [Google Scholar] [CrossRef] [Green Version]
  83. Trevisi, P.; Luise, D.; Correa, F.; Bosi, P. Timely Control of Gastrointestinal Eubiosis: A Strategic Pillar of Pig Health. Microorganisms 2021, 9, 313. [Google Scholar] [CrossRef]
  84. Williams, B.A.; Mikkelsen, D.; Flanagan, B.M.; Gidley, M.J. “Dietary fibre”: Moving beyond the “soluble/insoluble” classification for monogastric nutrition, with an emphasis on humans and pigs. J. Anim. Sci. Biotechnol. 2019, 10, 45. [Google Scholar] [CrossRef] [Green Version]
  85. 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. 2011, 96, 1101–1111. [Google Scholar] [CrossRef]
  86. Rattigan, R.; Sweeney, T.; Maher, S.; Thornton, K.; Rajauria, G.; O’Doherty, J. Laminarin rich extract improves growth per-formance, small intestinal morphology, gene expression of nutrient transporters, and the large intestinal microbial composition of piglets during the critical post-weaning period. Br. J. Nutr. 2019, 123, 1–23. [Google Scholar] [CrossRef]
  87. Reilly, P.; O’Doherty, J.; Pierce, K.; Callan, J.; O’Sullivan, J.; Sweeney, T. The effects of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient digestibility, volatile fatty acid concentrations and the immune status of the weaned pig. Animal 2008, 2, 1465–1473. [Google Scholar] [CrossRef] [Green Version]
  88. Dillon, S.; Sweeney, T.; Figat, S.; Callan, J.; O’Doherty, J. 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]
  89. 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]
  90. 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] [Green Version]
  91. Sweeney, T.; Dillon, S.; Fanning, J.; Egan, J.; O’Shea, C.; Figat, S.; Gutierrez, J.; Mannion, C.; Leonard, F.; O’Doherty, J. Evaluation of seaweed-derived polysaccharides on indices of gastrointestinal fermentation and selected populations of microbiota in newly weaned pigs challenged with Salmonella Typhimurium. Anim. Feed. Sci. Technol. 2011, 165, 85–94. [Google Scholar] [CrossRef]
  92. 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] [Green Version]
  93. Walsh, A.; Sweeney, T.; O’Shea, C.; Doyle, D.; O ’Doherty, J. 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]
  94. 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] [Green Version]
  95. 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. 2013, 111, 798–807. [Google Scholar] [CrossRef] [Green Version]
  96. Rattigan, R.; Sweeney, T.; Maher, S.; Ryan, M.T.; Thornton, K.; O’Doherty, J.V. Effects of reducing dietary crude protein concentration and supplementation with either laminarin or zinc oxide on the growth performance and intestinal health of newly weaned pigs. Anim. Feed Sci. Technol. 2020, 270, 114693. [Google Scholar] [CrossRef]
  97. Vigors, S.; O’Doherty, J.V.; Rattigan, R.; McDonnell, M.J.; Rajauria, G.; Sweeney, T. Effect of a Laminarin Rich Macroalgal Extract on the Caecal and Colonic Microbiota in the Post-Weaned Pig. Mar. Drugs 2020, 18, 157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. Wan, J.; Jiang, F.; Xu, Q.; Chen, D.; 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]
  99. Wan, J.; Zhang, J.; Chen, D.; Yu, B.; Huang, Z.; Mao, X.; Zheng, P.; Yu, J.; He, J. Alterations in intestinal microbiota by alginate oligosaccharide improve intestinal barrier integrity in weaned pigs. J. Funct. Foods 2020, 71, 104040. [Google Scholar] [CrossRef]
  100. 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. 2016, 30, 64–70. [Google Scholar] [CrossRef] [Green Version]
  101. Smith, A.G.; O’Doherty, J.V.; Reilly, P.; Ryan, M.; 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] [Green Version]
  102. Lostroh, C.P.; Lee, C.A. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 2001, 3, 1281–1291. [Google Scholar] [CrossRef]
  103. Xing, M.; Cao, Q.; Wang, Y.; Xiao, H.; Zhao, J.; Zhang, Q.; Ji, A.; Song, S. Advances in Research on the Bioactivity of Alginate Oligosaccharides. Mar. Drugs 2020, 18, 144. [Google Scholar] [CrossRef] [Green Version]
  104. Kone, A.N.T.; Ouattara, B.M.; Tiekoura, B.; Konan, F.K.; Koffi, E.; Kouadio, I.K.; Dadie, A.; Guessennd, N.K. Bio-activities of Tetracycline and Algae Food Supplement Algo-Bio® on Escherichia coli Antimicrobial Resistance Isolated from Piglet’s Intestinal Flora. Microbiol. Res. J. Int. 2019, 29, 1–8. [Google Scholar] [CrossRef]
  105. Berri, M.; Slugocki, M.; Olivier, M.; Holbert, S.; Helloin, E.; Jacques, I.; Salmon, H.; Collen, P.N.; Le Goff, M.; Demais, H. L’activité antibactérienne et immuno modulatrice d’un extrait d’algue verte riche en polysaccharides sulfatés. J. Rech. Porc. 2015, 47, 309–310. [Google Scholar]
  106. Gardiner, G.; Campbell, A.; O’Doherty, J.; Pierce, E.; Lynch, P.; Leonard, F.; Stanton, C.; Ross, R.; Lawlor, P. 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]
  107. 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. 2009, 90, 430–437. [Google Scholar] [CrossRef]
  108. 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] [Green Version]
  109. Bouwhuis, M.; McDonnell, M.; Sweeney, T.; Mukhopadhya, A.; O’Shea, C.; O’Doherty, J. Seaweed extracts and galacto-oligosaccharides improve intestinal health in pigs following Salmonella Typhimurium challenge. Animal 2017, 11, 1488–1496. [Google Scholar] [CrossRef]
  110. 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]
  111. Murphya, P.; Bello, F.D.; O’Doherty, J.; Arendt, E.K.; Sweeney, T.; Coffey, A. The effects of liquid versus spray-dried Laminaria digitata extract on selected bacterial groups in the piglet gastrointestinal tract (GIT) microbiota. Anaerobe 2013, 21, 1–8. [Google Scholar] [CrossRef]
  112. Lopez-Rubio, A.; Gavara, R.; Lagaron, J.M. Bioactive packaging: Turning foods into healthier foods through biomaterials. Trends Food Sci. Technol. 2006, 17, 567–575. [Google Scholar] [CrossRef]
  113. Lynch, M.; Sweeney, T.; Callan, J.; O’Sullivan, J.; O’Doherty, J. 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]
Table
Table 1. Polysaccharides and monosaccharides constituent of brown, green, and red seaweeds.
Table 1. Polysaccharides and monosaccharides constituent of brown, green, and red seaweeds.
Chemical ConstituentBrown SeaweedGreen SeaweedRed Seaweed
Polysaccharidesalginate, laminarin, fucoidan (sulphated), cellulose,
mannitol		ulvan (sulphated), mannan, galactans (sulphated), xylans, starch, cellulose, lignincarrageenans (sulphated), agar (sulphated), glucans (floridean starch), cellulose, lignin, funoran
Monosaccharidesglucose, galactose, fucose, xylose, uronic acid, mannuronic acid, guluronic acid, glucuronic acidglucose, mannose, rhamnose, xylose, uronic acid, glucuronic acidglucose, galactose, agarose
References[12,13][12,13][12,13]
Table
Table 3. Prebiotic effects of brown seaweed in sow.
Table 3. Prebiotic effects of brown seaweed in sow.
Seaweed SupplementDoseAnimalPrebiotic EffectEffect vs. Control, %Reference
Laminaria spp. xLAM + FUC
(1 + 0.8 g/day)		Sow
lactation		Piglets
(9 days after weaning):
Villous height ileum
Crypt depth duodenum
Colon:
Bifidobacteria spp.
Lactobacilli spp.
E. coli

+8%
−5%

−4%
−2% (p < 0.10)
−16% (p < 0.10)		[66]
Laminaria spp. xLAM + FUC
(1 + 0.8 g/day)		Sow
107 d gestation
and lactation		Piglets Colon:
E. coli
Lactobacillus spp.
SCFA
−21%
NS
NS		[67]
Laminaria spp. xLAM + FUC
(1 + 0.8 g/day)		Sow
83 d gestation
and lactation		Sow:
Enterobacteriaceae
Piglets:
Enterobacteriaceae
−9.2%

NS		[68]
Laminaria spp. xLAM (1 g/day)
FUC (0.8 g/day)
LAM + FUC

(1 + 0.8 g/day)
Sow 109 d gestation and lactationSow:
Lactobacillus spp.
Enterobacteriaceae
Piglets:
Lactobacillus spp.
−9% FUC
+4.7% LAM + FUC

+5.8% LAM		[69]
Laminaria spp. xSow
LAM + FUC
(1 and 0.8 g/day)
Piglets
LAM + FUC (0.30 + 0.24 g kg−1)		Sow 107 d gestation and lactation
Weaned piglets,
5.9 kg LW		Weaned piglets:
heat-labile enterotoxin (caecum)
enteroaggregative heat- stable enterotoxin (colon)		−14%
−10%		[70]
Laminaria spp. xSows
LAM (1 g/day)
Piglets
LAM (0.3 g kg−1)		Sow 109 d g
Gestation and lactation (LT)
Weaned piglets,
5.6 kg LW (PW)
Challenge Salmonella Typhimurium
10 d post weaning		Sow: Lactobacillus
colon
rectum
LT + PW
E. coli in rectum
LT stimulated VFA production
LT × PW
SCFA and
butyric acid
+4%
+7%

−13%
+29%

+24%
+8.1%		[71]
FUC: fucoidan; LAM: laminarin; LT: lactation diet; LW: live weight; PW, post weaning diet; SCFA: short-chain fatty acid. x Extract from Laminaria spp. from BioAtlantis Ltd. (Clash Industrial Estate, Tralee, Co. Kerry, Ireland).
Table
Table 4. Prebiotic effects of seaweed in weaned piglets.
Table 4. Prebiotic effects of seaweed in weaned piglets.
Seaweed SupplementDoseAnimalPrebiotic EffectEffect vs. Control, %Reference
Ascophyllum nodosumaDried intact
(10–20 g kg−1)		Weaned piglets, 9 kg LW10 g kg−1 E. coli:
stomach
small intestine
−42%
−27%		[55]
Ascophyllum nodosum aDried seaweed
(5–10 g kg−1)		Weaned piglets,
6.59 kg LW		Proximal, distal small intestine and caecum
NS		[85]
Ascophyllum nodosumFucoidan rich extract
(0.250 mg kg−1 FUC) n		Weaned piglets,
8.5 kg LW		Small Intestinal
Morphology
Caecum:
Bacteroides
Clostridia
Colon:
SCFA
NS

+ +
-

+19%		[86]
L. digitataL. hyperboreaL. digitata extract (Ld)
In diet LAM + FUC
(0.170–0.136 g kg−1)
L. hyperborean extract (Lh)
In diet LAM + FUC
(0.170–0.131 g kg−1)
In diet Ld + Lh extracts
(0.170–0.134 g kg−1)		Weaned piglets,
6.5 kg LW		Caecum
Lactobacillus


Enterobatteriaceae

SCFA
−13% Lh
−14% Ld
−17% Lh + Ld
−74% Ld
−65% Lh + Ld
+26% Ld		[87]
Laminaria spp.Seaweed extract
LAM + FUC c
(0.300–0.236 kg−1)		Weaned piglets,
6.4 kg LW		Faecal
Lactobacilli spp.
E. coli		+2% (15% lactose)
+5% (25% lactose)
−8% (15% lactose)
−29% (25% lactose)		[88]
Laminaria spp.Seaweed extract
LAM (0.300 g kg−1) y
FUC (0.236 g kg−1) z
LAM (0.3 g kg−1) + FUC (236 g kg−1)		Weaned piglets,
24 d age		Faecal
Lactobacillus spp.
E. coli
+5%
−8% LAM		[89]
Laminaria spp.Seaweed extract
LAM (0.3 g kg−1)
FUC (0.36 g kg−1)
LAM + FUC
(0.3 + 0.36 g kg−1)		Weaned piglets,
6.4 kg		Faecal
E. coli		−8% LAM
−12% LAM + FUC		[90]
Laminaria spp.Seaweed extract
LAM (0.30 g kg−1) y
FUC (0.24 g kg−1) z		Weaned piglets,
7.9 kg LW Challenge with Salmonella typhimurium		Caecum
Lactobacillus spp.
Acetic acid
Propionic acid
Butyric acid

Colon:
Lactobacillus spp.
Acetic acid
Propionic acid
Butyric acid
+208% FUC
+11% LAM FUC
−15% LAM
−22% FUC
+23% FUC

NS
+10% FUC
−24% FUC
+31% FUC		[91]
Laminaria spp.Seaweed extract
LAM (0.30 g kg−1)
FUC (0.24 g kg−1)
LAM + FUC
(0.30 + 0.24 g kg−1)		Weaned piglets,
6.8 kg LW		Colon prox:
Enterobacteriaceae
Escherichia coli
Caecum SCFA		−15% FUC
−15% LAM
+15% LAM
+8% FUC		[92]
Laminaria spp.Seaweed extract
LAM (0.15–0.30 g kg−1)
FUC (0.24 g kg−1)
LAM + FUC (0.15 + 0.24 and
0.30 + 0.24 g kg−1)		Weaned piglets,
6.8 kg LW		Faecal
Lactobacillus spp.
Bifidobacterium spp.
E. coli
+8.6% FUC
NS
NS		[93]
Laminaria spp.Seaweed extract
LAM (0.30 g kg−1)		Weaned piglets,
6.9 kg LW		Faecal
E. coli,
Lactobacillus spp.,
Bifidobacterium
SCFA
NS
NS
NS
NS		[94]
Laminaria spp.Seaweed extract
In diet LAM + FUC
(0.30 + 0.24 g kg−1) k		Weaned piglets,
6.5 kg LW		Faecal
Lactobacillus spp.
E. coli
−11%
NS		[95]
Laminaria spp.21% CP + LAM 0.30 g kg−1
18% CP + LAM 0.30 g kg−1		Weaned piglets,
6.5 kg		Colon
Enterobacteriaceae
Lattobacillaceae
NS
NS		[96]
Laminaria spp.Seaweed extract
(0.30 g kg−1) r		Weaned piglets,
8.4 kg LW		Caecum
Enterobatteciaceae
Prevotella
Colon
SCFA
Acetic acid
Butirric acid
-
+ +

+21%
+12%
+53%		[97]
Brown seaweedAlginic acid
olisaccharides
(ALGO) m		Weaned piglets,
7.8 kg LW		Ileum
Bifidobacterium
Lactobacillus
E. coli
Caecum
Bifidobacterium
Lactobacillus
E. coli
Colon
Bifidobacterium
Lactobacillus
E. coli
+13%
+20%
NS

NS
NS
−13%

NS
NS
−13%		[98]
Brown seaweedAlginates oligosaccharides
from brown seaweed
(100 mg kg−1)		Weaned piglets,
6.2 kg LW		Caecum
Acetic acid
Propionic acid
Butyric acid
Colon
Acetic acid
Propionic acid
Butyric acid
+13%
+66%
+12%

NS
NS
+20%		[99]
Ecklonia cavaSeaweed (0.5–11.5 g kg−1) s
FUC = 0.056–0.112–0.168 g kg−1		Weaned piglets,
7.8 kg LW		Lactobacillus spp.
Enterobacterium spp.		+3%
−4%		[100]
LAM: laminarin; FUC: fucoidan; SCFA: short-chain fatty acids. a Sum of non-starch polysaccharidemonomers and lignin = 503 g kg−1. c Laminaria extract with a content of 112 g kg−1 Laminarin and 89 g kg−1 Fucoidan. y Laminaria extract with a content of 990 g kg−1 Laminarin. z Laminaria extract with a content of 720 g kg−1 Fucoidan. k Laminaria extract with a content of 455 g kg−1 Laminarin and 360 g kg−1 Fucoidan. s Ecklonia cava with a content of 112 g kg−1 Fucoidan. r 653.2 g kg−1 Laminarin, 190 g kg−1 Fucoidan. m Alginic acid oligosaccharide (ALGO) is the lyase–lysate of alginic acid, which is a naturally occurring anionic polysaccharide isolated from the cell walls of seaweed polysaccharide isolated from the cell walls of seaweed. n 441 g kg−1 fucoidan, 25.9 g kg−1 laminarin, 135 g kg−1 alginates, 43.8 g kg−1 mannitol, 34.8 g kg−1 phlorotannins, 319.5 g kg−1 ash.
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Corino, C.; Di Giancamillo, A.; Modina, S.C.; Rossi, R. Prebiotic Effects of Seaweed Polysaccharides in Pigs. Animals 2021, 11, 1573. https://doi.org/10.3390/ani11061573

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Corino C, Di Giancamillo A, Modina SC, Rossi R. Prebiotic Effects of Seaweed Polysaccharides in Pigs. Animals. 2021; 11(6):1573. https://doi.org/10.3390/ani11061573

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Corino, Carlo, Alessia Di Giancamillo, Silvia Clotilde Modina, and Raffaella Rossi. 2021. "Prebiotic Effects of Seaweed Polysaccharides in Pigs" Animals 11, no. 6: 1573. https://doi.org/10.3390/ani11061573

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