Seaweed Polysaccharides in Pigs
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This entry is adapted from the peer-reviewed paper 10.3390/ani11061573

The polysaccharides contained in brown, red, and green seaweeds present different bioactive molecules such as fucoidan, laminarin, alginate, ulvan, and carrageenan.

pig polysaccharides prebiotics seaweed

1. Overview

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. 

2. Background

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.

3. 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.
Table 1. Polysaccharides and monosaccharides constituent of brown, green, and red seaweeds.
Table
Chemical Constituent Brown Seaweed Green Seaweed Red Seaweed
Polysaccharides alginate, laminarin, fucoidan (sulphated), cellulose,
mannitol		 ulvan (sulphated), mannan, galactans (sulphated), xylans, starch, cellulose, lignin carrageenans (sulphated), agar (sulphated), glucans (floridean starch), cellulose, lignin, funoran
Monosaccharides glucose, galactose, fucose, xylose, uronic acid, mannuronic acid, guluronic acid, glucuronic acid glucose, mannose, rhamnose, xylose, uronic acid, glucuronic acid glucose, galactose, agarose
References [12][13] [12][13] [12][13]
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 2. Polysaccharides composition of brown, red, and green seaweed (g kg−1 DM) 1.
Table
Seaweed Polysaccharides, % Alginates Carragenan Fucoidan Laminarin Ulvan References
Brown              
Ascophillum nodosus 62
(42–70)		 285
(240–330)		 - 75
(11–120)		 118
(12–120)		 - [8][18][22][23][24][25]
Laminaria hyperborea 39.9
(14.4–65.5)		 215
(22–408)		 - 30
(20–40)		 125
(0–320)		 - [8][18][26][27][28]
Laminaria digitata 57.3
(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 pinnafitica 40
(35–45)		 425
(340–510)		 - 219
(30–690)		 30 - [8][18][29][40]
Red   - - - - -  
Chondrus crispus 60.5
(55–66)		 - 439.5
(338–510)		 - - - [18][34][41]
Kappaphycus alvarezii 58
(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].

4. 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].

5. Seaweed Polysaccharides as Prebiotics in Sows

The effects of algae polysaccharides as prebiotics in sows have been evaluated by several authors.

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 [55]. 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.

6. 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 [56]. 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 [57].
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 [56]. After weaning, structural and functional alterations of the small intestine have also been observed with negative effects on the absorptive capacity [58].
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 [59].
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 [60].
Several studies have evaluated the effects of seaweed polysaccharides as prebiotics in post weaning piglets.
The dietary inclusion of Ascophillum nodosum in the piglets’ diet can reduce the Escherichia Coli content in the small intestine of weaned piglets [61]. 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. 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 [62][63]. An improvement in Lactobacillus count has also been detected [62][64][65][66][67].
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 [68].
Fucoidan also supports Lactobacillus growth with a positive effect on feed digestibility [69][68].
The increase in butyric acid reported in several studies, is usually related to carbohydrate fermentation which has a positive effect.

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.
  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.
  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.
  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.
  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.
  6. Corino, C.; Modina, S.C.; Di Giancamillo, A.; Chiapparini, S.; Rossi, R. Seaweeds in Pig Nutrition. Animals 2019, 9, 1126.
  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.
  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.
  9. Sweeney, T.; O’Doherty, J. Marine macroalgal extracts to maintain gut homeostasis in the weaning piglet. Domest. Anim. Endocrinol. 2016, 56, S84–S89.
  10. Lean, Q.Y.; Eri, R.; Fitton, J.H.; Patel, R.P.; Gueven, N. Fucoidan Extracts Ameliorate Acute Colitis. PLoS ONE 2015, 10, e0128453.
  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.
  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.
  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.
  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.
  15. Sardari, R.R.R.; Karlsson, E.N. Marine Poly- and Oligosaccharides as Prebiotics. J. Agric. Food Chem. 2018, 66, 11544–11549.
  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.
  17. Lahaye, M. Developments on gelling algal galactans, their structure and physico-chemistry. Environ. Boil. Fishes 2001, 13, 173–184.
  18. Holdt, S.L.; Kraan, S. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 2011, 23, 543–597.
  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.
  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.
  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.
  22. Moen, E.; Horn, S.; Østgaard, K. Biological degradation of Ascophyllum nodosum. Environ. Boil. Fishes 1997, 9, 347–357.
  23. Rioux, L.-E.; Turgeon, S.; Beaulieu, M. Characterization of polysaccharides extracted from brown seaweeds. Carbohydr. Polym. 2007, 69, 530–537.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  37. Catarino, M.D.; Silva, A.M.S.; Cardoso, S.M. Fucaceae: A Source of Bioactive Phlorotannins. Int. J. Mol. Sci. 2017, 18, 1327.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  55. 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.
  56. 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.
  57. 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.
  58. Campbell, J.M.; Crenshaw, J.D.; Polo, J. The biological stress of early weaned piglets. J. Anim. Sci. Biotechnol. 2013, 4, 19.
  59. Trevisi, P.; Luise, D.; Correa, F.; Bosi, P. Timely Control of Gastrointestinal Eubiosis: A Strategic Pillar of Pig Health. Microorganisms 2021, 9, 313.
  60. 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.
  61. 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.
  62. 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.
  63. 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.
  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.
  65. 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.
  66. 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.
  67. 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.
  68. 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.
  69. 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.
  70. 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.
  71. 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.
  72. 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.
  73. 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.
  74. 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.
  75. 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.
  76. 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.
  77. 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.
  78. 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.
  79. 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.
  80. 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.
  81. 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.
  82. 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.
  83. 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.
  84. 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.
  85. 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.
  86. 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.
  87. 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.
  88. Kogan, G.; Kocher, A. Role of yeast cell wall polysaccharides in pig nutrition and health protection. Livest. Sci. 2007, 109, 161–165.
  89. 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.
  90. Ouwehand, A.C.; Salminen, S.; Isolauri, E. Probiotics: An overview of beneficial effects. Antonie van Leeuwenhoek 2002, 82, 279–289.
  91. 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.
  92. 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.
  93. 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.
  94. Lostroh, C.P.; Lee, C.A. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 2001, 3, 1281–1291.
  95. 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.
  96. 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.
  97. 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.
  98. 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.
  99. 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.
  100. 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.
  101. 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.
  102. 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.
  103. 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.
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Subjects: Agriculture, Dairy & Animal Science
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Raffaella Rossi
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Carlo Corino
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