InTechOpen uses cookies to offer you the best online experience. By continuing to use our site, you agree to our Privacy Policy.

Immunology and Microbiology » "Probiotics and Prebiotics in Human Nutrition and Health", book edited by Venketeshwer Rao and Leticia G. Rao, ISBN 978-953-51-2476-4, Print ISBN 978-953-51-2475-7, Published: July 13, 2016 under CC BY 3.0 license. © The Author(s).

Chapter 15

Pectic Oligosaccharides and Other Emerging Prebiotics

By Beatriz Míguez, Belén Gómez, Patricia Gullón, Beatriz Gullón and José Luis Alonso
DOI: 10.5772/62830

Article top

Pectic Oligosaccharides and Other Emerging Prebiotics

Beatriz Míguez1, 2, Belén Gómez1, 2, Patricia Gullón3, Beatriz Gullón4 and José Luis Alonso1, 2
Show details


A prebiotic is a selectively fermented ingredient that results in specific changes in the composition and/or activity of the gastrointestinal microbiota, thus conferring benefit(s) upon host health. The most widely accepted prebiotics are lactulose, inulin, fructooligosaccharides (FOS), galactooligosaccharides (GOS), and the human milk oligosaccharides (HMO). However, there is a growing list of potential prebiotics although the evidence for these, especially in humans, is not as well established as for FOS and GOS. Some of them are already commercialized but others such as polydextrose (PDX), pectic oligosaccharides (POS), bacterial exopolysaccharides (EPS), polysaccharides derived from algae and sugar alcohols are still in the early stages of development. This chapter summarizes the scientific literature regarding the manufacture and the evaluation of the properties of this group “emerging prebiotics”.

Keywords: emerging prebiotics, pectic oligosaccharides, polydextrose, algae-derived oligosaccharides, bacterial exopolysaccharides, sugar alcohols

1. Introduction

The consumption of prebiotics is being specially considered as a good health-improving strategy; they have been recently defined as “nondigestible compounds that through its metabolization by microorganisms in the gut, modulate the composition and/or the activity of the gut microbiota, thus conferring physiological benefit effects on the host health” [1].

The microbial communities that inhabit the human intestinal tract constitute a complex association, comprising more than 1000 species and around 1014 microorganisms, mainly anaerobic (>99.9%). Figure 1 shows the human gastrointestinal tract, indicating the different levels of microorganisms and the main bacterial groups. Along the jejunum, and particularly in the ileum, there is a gradual increase in the number and diversity of bacteria, and finally, the majority of gastrointestinal microbes are housed in the colon [2].


Figure 1.

The human gastrointestinal tract (CFU, colony-forming units).

However, scientific works on this field suggest that the gut microbiota is not only a simply collection of microorganisms, but also reflects an interrelationship between the different groups that might work together for the benefit of the host [2]. In addition, the microbiota also establishes a close symbiosis with the host: humans provide the nutrients and the appropriate conditions for its development, and it performs three essential primary functions: metabolic, trophic, and defensive [3]. In fact, there is a long list of pathologies which are linked to the alteration of the gut microbiota, including hepatic encephalopathy, diarrhea, diabetes, obesity, colon cancer, IBS, IBD, gastrointestinal infections, and necrotizing enterocolitis [4, 5].

The composition of the gut microbiota is influenced by a variety of factors that include: (i) the microbial species which are acquired at birth, (ii) host genetics, (iii) age [68], (iv) diseases and antibiotic usage [9, 10], (v) the stress [11], and (vi) the diet. In fact, the diet is probably the most important factor and several studies are focused on the modulation of the gut microbiota by the consumption of functional foods, such as prebiotics [1214].

For considering a food ingredient as a prebiotic, it must fulfill the following requirements [15]: (i) it cannot be hydrolyzed or absorbed in the upper gastrointestinal tract, (ii) it has to encourage the development of beneficial bacteria such as bifidobacteria and lactobacilli, and (iii) it must induce beneficial physiological effects on the host health, so that well-conducted human trials are required.

In addition to the generally identified as beneficial bacteria (bifidobacteria, lactobacilli, and even, eubacteria), a recent review by Hill et al. [16] indicates that the species Akkermansia muciniphila and Faecalibacterium prausnitzii, and others such as Roseburia spp. and Eubacterium hallii, which could be useful to alleviate gut inflammation, to induce and regulate of the immune system or to improve the intestinal barrier function.

The most widely accepted prebiotics are lactulose, inulin, fructooligosaccharides (FOS), galactooligosaccharides (GOS), and the human milk oligosaccharides (HMO). However, there is a growing list of potential prebiotics and some of them are already commercialized and others, like polydextrose (PDX), pectic oligosaccharides (POS), bacterial exopolysaccharides (EPS), polysaccharides derived from algae and sugar alcohols that are still in the early stages of study [15]. This chapter summarizes the scientific literature regarding the manufacture and evaluation of this group of emerging prebiotics.

2. Pectic oligosaccharides (POS)

POS have been recently classified as emerging prebiotics and their potential is currently being evaluated.

2.1. Raw materials for POS production

POS are oligosaccharides that can be obtained by partial hydrolysis of pectins, which are heteropolysaccharides with a highly complex structure.

Pectins are mainly made up by a backbone of galacturonic acid units (GalA) connected by α-(1,4) links that can be randomly acetylated at the O-2 and/or O-3 positions and methylated at C-6. This fraction is known as “smooth region,” and it is occasionally interrupted by the “hairy region,” where side chains, formed by a variety of neutral sugars, can be found. Figure 2 shows the major structural fragments of pectin:


Figure 2.

Simplified structure of pectin.

  1. Homogalacturonan (HG). HG is a linear polymer consisting of a chain with an estimated length of 72–100 GalA units that represent, approximately, 60% of the total pectin [17]. Acetylation and methylation degrees (DA and DM, respectively) vary according to the origin and the development stage of the plant [18].

  2. Xylogalacturonan (XG). XG is a chain of GalA residues partially substituted by D-xylose residues connected by β-(1,3) links at C-3 and/or C-2 positions.

  3. Rhamnogalacturonan I (RG-I). It represents up to 7–14% of the pectins [19] and contains alternating units of α-(1,4)-galacturonosyl and α-(1,2)-rhamnosyl. In many cases, rhamnose residues show side chains as substituents on the O-4 position, made up of arabinan and/ or arabinogalactan I and II, although lower concentrations of xylose or glucose can be also found [18].

  4. Rhamnogalacturonan II (RG-II). RGII is a region characterized by a length of 7–9 GalA units, where complex branches made up of 12 types of monosaccharides (as a maximum) can exist, including some minority monomers such as apiose, fucose, acetic acid, DHA, or KDO [20].

Pectin has a great number of applications including its use as ingredient for medicaments for treating gastrointestinal disorders, diabetes, high blood pressure, or hypercholesterolemia [2123].

Currently, citrus pulp and apple pomace are the major sources of pectin, but this polymer can also be found in other agro-products such as sugar beet pulp [24].

2.2. Manufacture and purification

Several methods have been used for POS production from both agro-industrial byproducts and purified pectins, including partial enzymatic hydrolysis, acid hydrolysis, hydrothermal treatments, dynamic high-pressure microfluidization, or photochemical reaction in media containing TiO2 [24].

Chemical methods include the acidic or basic hydrolysis of α and β-glucosidic links of the principal chains of HG, RG-I, and RG-II and their side chains. These methodologies include hydrothermal treatments and processes where external acids are added. In both cases, hydronium ions act as catalytic species [24]. A variety of raw materials such as orange albedo, apple pulp, or deesterified beet pulp have been treated to obtain POS, using acids such as HNO3, HCl, or TFA [24], although alkalis (KOH) can also be employed [25]. POS mixtures have been obtained from lemon and orange peel wastes [2628], dried apple pomace [29], sugar beet pulp [30], or alperujo [31] using stainless steel reactors, whereas Sato et al. [32] employed both a batch and a continuous tubular flow reactor to produce arabinooligosaccharides (AraOS) and feruloylated AraOS from beet fiber.

As an alternative, pectin-degrading enzymes constitute a group of enzymes that catalyze the degradation of the pectic polymers in plant cells. Although pectins have a complex structure, they can be modified by diverse enzymes, including hydrolases, lyases, and esterases [33].

Several raw materials with different characteristics have been enzymatically treated, such as bergamot peel [34], gum tragacanth [35, 36], ginseng pectin [37], orange peel wastes [38], lemon peel wastes [39], sugar beet [40, 41], apple pectin [42], or medicinal herbs [43].

Both mono-active and commercial mixtures can be used for pectin depolymerization; however, mono-active enzymes target only specific structures, causing the release of more defined oligosaccharides than when commercial enzyme mixtures or chemical treatments are employed [44]. Mixture of several preparations have been widely employed for POS production [38, 41, 4548]. A comparable yield respect to acidic treatments can be achieved using enzyme preparations [42].

In addition, enzymes can be also advantageous for the alteration of the methylation or acetylation degree of the polymer [44].

On the other hand, chemical and enzymatic hydrolysis have been combined to depolymerize pectin [49] or to obtain different pectin fractions, such as POS and neutral and acidic xylooligosaccharides [31]. Other technologies that have been combined are enzymatic and microwave-assisted alkaline extraction [48], hydrothermal and acid treatment for polygalacturonic acid hydrolysis [50], subcritical water and ultrasonic-assisted treatments [51].

Finally, physical technologies (for instance, the dynamic high-pressure microfluidization under acidic conditions) have been emerged as innovative [52].

After production, purification stages are usually needed to obtain a product suitable to be used as food ingredient. The most common purification technique is the membrane filtration. A process involving diafiltration followed by concentration was performed by Gómez et al. [26] to purify pectic oligosaccharides from autohydrolysis liquors obtained from lemon peel wastes, yielding a refined product with about 98 wt% of oligomers which contained oligogalacturonides (with DP in the range of 2–18) and AraOS (with DP in the range of 2–8). A similar approach was performed by Gómez et al. [27] achieving a refined final product containing 90% of the target product, where there were identified AraOS (DP 3–21), GalOS (DP 5–12), and OGalA (DP 2–12), with variable DM and also long-chain products.

Rubio-Senent et al. [53] isolated fractions (MW > 3 kDa) which were rich in pectic material from an alperujo aqueous hydrolysate by ultrafiltration thought 3 kDa regenerated cellulose.

Ultrafiltration and diafiltration (50 kDa cut-off) were employed by Sulek et al. [54] to isolate AraOS, which were further fractionated into a stirred membrane reactor equipped with a 1 kDa MWCO.

This methodology has also been employed to sequentially fractionate oligosaccharides by its molecular weight [55].

Other alternatives were also used in this field; Lama-Muñoz et al. [31] fractionated and purified neutral and POS by adsorption XAD chromatography (Amberlite XAD-16 resin), and the gel Sephadex G-75 was selected by Lee et al. [56] to purify POS from Korean Citrus Hallabong peels.

2.3. Prebiotic potential of POS

POS have been suggested as a new class of prebiotics, which are capable of exerting a number of health-promoting effects, including [24] stimulation of apoptosis in human colonic adenocarcinoma cells, potential for cardiovascular protection in vivo, reduction of damage by heavy metals, antiobesity effects, antitoxic, antiinfection, antibacterial, and antioxidant properties.

The main derived products from the intestinal bacterial fermentation of POS, as well as from other dietary fiber, are the SCFA (acetate, propionate, and butyrate). SCFA exert several beneficial effects including: (i) a key role in the prevention and treatment of the metabolic syndrome, bowel disorders, and cancer [5759]; (ii) protection against diet-induced obesity and regulation of the gut hormones [60]; or (iii) a positive effect on the treatment of ulcerative colitis, Crohn’s disease, and antibiotic-associated diarrhea and obesity [6163]. Particularly, butyrate is the major energy source for the colonocytes, propionate has a role in gluconeogenesis processes, and acetate is used for the lipogenesis [64].

The following paragraphs summarize the results derived from the recent in vitro and in vivo studies carried out employing POS as substrate:

a) In vitro assays

Citrus peel wastes and sugar beet pulp were subjected to hydrothermal treatment and the resulting liquors refined by membrane filtration. The final POS mixtures were then fermented by human fecal samples leading to an increase of the bacterial population of up to eight different groups. Specifically, POS from sugar beet pulp showed the highest bifidogenic potential and the maximum SCFA concentration. Meanwhile, the largest increase in Lactobacillus population was observed using POS from orange peel wastes as a carbon source, whereas the best results for other bacterial groups such as Eubacterium, Faecalibacterium, or Roseburia were observed for POS from lemon peels wastes [27, 65]. In the same way, POS derived from sugar beet (enriched in AraOS) were used as substrates in in vitro fermentation assays of POS leading to increases in bifidobacteria populations (which preferred low molecular weight fractions) without stimulating the growth of Clostridium [6668]. In a recent study with POS from sugar beet pulp containing GalOS, AraOS, and mixtures of acidic oligosaccharides (mainly made up of RG and HG oligosaccharides), no a clear bifidogenic effect was observed, whereas important increases of Faecalibacterium were reported. Moreover, the SCFA concentrations were found higher in experiments with POS than with FOS [69].

Regarding apple pectin, a variety of works were reported concluding that POS might be an interesting prebiotic candidate with slightly improved physiological properties if they are compared to commercial ones. In this context, Gulfi et al. [70] indicated that pectin hairy regions from ripe apples revealed to be a very readily fermentable substrate for human colonic bacteria, showing a substantial impact on pH and SCFA production. Suzuki et al. [71] found that AraOS from apple pectin, especially those that consist of more than three units, are more selectively utilized by Bifidobacterium adolescentis, B. longum, and Bacteroides vulgatus than FOS and XOS. Meanwhile, Chen et al. [52] reported the ability of apple-derived POS for promoting the bifidobacteria and lactobacilli growth and for decreasing numbers of bacteroides and clostridia, whereas the fermentation of refined POS mixture from apple pomace with human feces resulted in an increase in the populations of Bifidobacterium, Eubacterium rectale and Lactobacillus, but also of Clostridium and Bacteroides [72].

Some authors as Mandalari et al. [12] employed other types of pectin sources, demonstrating that almond seeds, which contain arabinose-rich pectin, exhibited potential for their use as a novel sources of prebiotics, increasing the populations of bifidobacteria and Eubacterium rectale with the subsequent increase in butyrate concentrations. Guevara-Arauza et al. [73] observed that POS from nopal act as prebiotics, reducing putrefactive ammonium production, increasing SCFA production, and sustaining bifidogenic effects over longer periods of time.

In addition, in order to elucidate structure–function relationships in POS, Onumpai et al. [74] compared the fermentation properties of pectin fractions and their parent pectins using a pH-controlled fecal fermentation system. All of the tested carbohydrates increased the populations of bacteroides, but just galactan- and arabinan-derived oligosaccharides increased the bifidobacteria counts. On the other hand, methylated oligogalacturonides, compared to the parent polysaccharide and to other pectic fractions, caused a significant increase in the Faecalibacterium prausnitzii populations [74].

b) In vivo assays

Despite the advances in in vitro models, the in vivo studies involving the use of animals and especially of humans provide the best models for studying the changes in the microbiota populations. However, they often require specialist facilities and are both expensive and time-consuming, limiting the number of this type of assays [75].

Jiao et al. [76] demonstrated that water-soluble oligosaccharides isolated from Panax ginseng significantly inhibited tumor growth in mice by enhancing their immune system. In this last year, native intact (TrPP) and modified, low molecular weight (MTrPP) forms of pectic polysaccharides isolated from turmeric were evaluated for ulcer-preventive potentials in in vivo rat models. MTrPP was rich in galacturonic acid (687 mg/g; TrPP-544 mg/g) and galactose (52.9%; TrPP-21.7%) from HG and RG-I containing galactan. The results suggested that MTrPP possess significantly improved ulcer-preventive properties than TrPP (inhibiting ulcer scores up to 85%), revealing that the fine structural features of pectin are crucial in delivering its therapeutic benefits against gastric ulcer [77].

Regarding the clinical assays, Fanaro et al. [78] observed increased counts of bifidobacteria and lactobacilli by the administration of POS as a component of infant formulae. Similarly, Magne et al. [79] detected increased proportions of bifidobacteria in the mixture GOS/FOS/POS respect to the mixture GOS/FOS, as well as the proportions of Bacteroides and Clostridium coccoides decreased. Moreover, the use of neutral and acidic oligosaccharides to preterm infants (mixtures of POS, GOS and FOS) showed a trend toward a lower incidence of serious endogenous infection and serious infectious episodes [80]. Finally, the intake of POS in a mixture with short-chain GOS and long-chain FOS by volunteers who were in the earlier stages of HIV-1 infection, resulted in the modulation of gut microbiota by increasing the bifidobacteria numbers and by decreasing the counts of pathogens [81].

3. Polydextrose (PDX)

3.1. Structure and manufacture

PDX is an artificial highly branched polysaccharide synthesized conventionally by random polycondensation of glucose with sorbitol and a food grade acid (e.g., citric acid) as catalyst, at a high temperature and under partial vacuum [82]. Recently, other methods have been explored as the synthesis by microwave irradiation [83]. PDX is composed of a mixture of glucose oligomers, with an average degree of polymerization (DP) of 12, ranging from DP 2–120 [84, 85] and contains all different combinations of α- and β-(1,2), (1,3), (1,4), and (1,6) glycosidic linkages, but α-( 1,6) linkages are predominant [85, 86]. PDX is regarded as a resistant polysaccharide [87] and it is widely used in the food industry as a low-energy bulking agent (1 kcal/g) and as a sugar or fat replacer [86].

3.2. Prebiotic effects

Due to its complex structure and to the nature of its glycosidic bonds, PDX is resistant to mammalian digestive enzymes in the upper gastrointestinal tract. For this reason, PDX reaches the colon intact where it is partially fermented by gut microbiota, stimulating selectively target bacterial groups [84, 85, 88]. These two characteristics, indigestibility and selective fermentability, support that the PDX has been identified as a source of prebiotic fiber with several health-promoting effects [89], including:

  • Improvement of the bowel function, by promoting the growth of beneficial bacteria (e.g., bifidobacteria and lactobacilli) while preventing the growth of harmful ones (such as clostridia and bacteroides), decrease of fecal pH and increase of the residual concentration of short chain fatty acids (SCFA) [88].

  • Reduction of the risk of colon cancer development [88, 90].

  • Modulation of the lipid metabolism, decreasing the total cholesterol and LDL cholesterol and increasing HDL cholesterol [84].

  • Prevention of the adhesion of opportunistic pathogens related with meningitis and sepsis in neonates [91].

  • Anti-inflammatory action [92] and positive effects on canine osteoarthritis [93].

  • Reduction of the symptoms of human atopic eczema [94].

  • Improvement of the absorption of magnesium, calcium and iron [9597]. The studies related to the biological and prebiotics effects of PDX (observed in vivo, in vitro and human intervention assays) are summarized in Table 1.

Biological and prebiotic effectsStudy typeReferences
Proliferation of Lactobacillus and Bifidobacterium species and decreases in Bacteroides species. Increases in concentrations of SCFA. Improvement of the bowel function and inhibition of the excessive glucose absorption in the small intestineC.I.[98]
Increases in Ruminococcus intestinalis and Clostridium clusters I, II, and IV that are butyrate-producing. Decreases in fecal water genotoxicityC.I.[88]
Reduction of LDL cholesterol and total cholesterolC.I.[99]
Infants fed with formulas with PDX had softer stools (similar to breastfed infants) in comparison with those who receive unsupplemented formulasC.I.[100]
Increases in bifidobacteria and stools weight. Decreased in fecal ammonia, phenol, indoles and BCFA (isobutyrate, isovalerate, and valerate)C.I.[101]
Reduction of the orofecal transit time, and improvement of stool consistency in persons suffering from constipationC.I.[102]
Increases in Faecalibacterium prausnitzii numbersC.I.[103]
Reduction in fecal pH and improvement of stool consistencyC.I.[104]
Supplementation with GOS–polydextrose and Lactobacillus rhamnosus GG in preterm infants reduces the risk of rhinovirus infections in infantsC.I.[105]
The intake of yogurt with polydextrose, B. lactis HN019, and L. acidophilus NCFM® improved constipationC.I.[106]
Reduction of the production of biogenic amines and BCFA in rats. Improvement of the immune functionA.S.[107]
Increases in defecation without diarrheaC.I.[108]
Increases in populations of bifidobacteria with a similar pattern with breastfed infantsC.I.[109]
Increases in the number of bifidobacteria and selective stimulation of Bifidobacterium infantis compared with other carbohydrates testedin vitro[110]
Increases in bifidobacteria and lactobacilli and SCFA productionin vitro [111]
Increases in the concentration of acetate and propionate and reduction of BCFA vitro
Increases in the production of fecal SCFA, especially acetate and propionate, and decreased fecal indoleA.S. (dogs)[113]
Reduction of the expression of mucosal COX-2 (closely related to the colorectal cancer)A.S. (pigs)[114]
Increases in the content of ileal lactobacilli and in the levels of propionic and lactic acid. Reduction of cytokine expressionA.S. (pigs)[89]
Reduction of chronic visceral hypersensitivity in rats exposed to early-life painful stimulusA.S. (rats)[115]
Improved calcium absorption in postmenopausal ratsA.S. (rats)[116]
Ability to inhibit adherence of C. sakazakii to gastrointestinal epithelial cellsin vitro[91]
Positive effect in canine osteoarthritisA.S. (dogs)[93]
Reduction of symptoms of allergen-induced dermatitisA.S.(mice)[94]
Stimulation of apoptosis in colon cancer cellsin vitro

Table 1.

Results obtained in studies carried out using polydextrose as substrate.

[i] - A.S., animal study; C.I., clinical intervention; C.M., colonic model.

4. Algae-derived oligosaccharides

4.1. Structure, sources, and production

Seaweeds are a source of bioactive compounds like sulphated polysaccharides, proteins, polyunsaturated fatty acids (PUFA), and polyphenols with potential beneficial health effects, such as antibacterial [115], anti-inflammatory [116, 117], antioxidant [118120], antitumoral [121, 122], anticoagulant [123] antiadhesive [116], and apoptotic activities [124, 125] among others. The major polysaccharides which can be found in seaweeds are alginates, laminarins, fucans and cellulose in brown seaweeds, ulvan in green seaweeds, and agars and carrageenans in red seaweeds. Several extraction methods of bioactive sulphated polysaccharides from seaweeds have been investigated in recent years, including: diluted acid extraction [126, 127], hydrothermal processing [128], microwave-assisted extraction [129131], ultrasound-assisted extraction [132], enzyme-assisted extraction [132, 133], or pressurized liquid extraction [134].

4.2. Prebiotic properties

In the last decade, seaweed polysaccharides have been considered as dietary fibers and have attracted much interest because of their potential use as prebiotics [135, 136]. In this sense, several studies have reported that seaweed polysaccharides resist the digestion in the upper of gastrointestinal tract, support the growth of lactic acid bacteria, reduce of harmful bacteria as well as modulate the intestinal metabolism through their effects on pH and SCFA concentration [137].

To date, several studies in vitro and in vivo were carried out to evaluate the potential prebiotic effects of seaweed polysaccharides. Table 2 summarizes the results obtained. No human trials have been conducted yet using this type of substrates.

Product or seaweedBiological and prebiotic effectsStudy typeReferences
Chondrus crispus and Sarcodiotheca gaudichaudiiIncreases in the numbers of Bif. longum and Streptococcus salivarius and reduction in the populations of C. perfringens. Increases in SCFAs concentration and i-butyric acid.A.S. (hens)[140]
LaminarinIncreases in the levels of SCFAs In vitro
LaminarinVariations of mucus composition in jejunum, ileum, cecum, and colonA.S. (rats)[137]
Ascophyllum nodosumReduction in populations of Escherichia coli In vitro
CarrageenansIncreases in cecal moisture and in concentrations of acetic and propionic acid. Reduction in the levels of triglycerides and total cholesterolA.S. (rats)[142]
Alginate oligosaccharidesIncreases in numbers of fecal bifidobacteria and lactobacilli and reduced counts of bacteroides respect to the
A.S. (rats)[143]
Alginate oligosaccharidesStimulation of the growth of Bifidobacterium bifidum ATCC 29521 and Bifidobacterium longum SMU 27001 In vitro [143]
Saccharina latissimaIncreases in the concentrations of acetic and propionic acidsA.S (rats)[144]
Laminarin and fucoidanReduction in the populations of Enterobacteria and increases in the populations of Lactobacilli A.S. (pigs)[145]
PorphyranIncreases in the content of propionic acid in the cecum. Decreases in the number of Clostridium coccoides.A.S. (mice)[146]
CarrageenanIncreases in the populations of Bif. breve and reduction in the populations of Clostridium septicum and Streptococcus neumoniae. Increases in the concentrations of SCFAs and immunoglobulin levelsA.S. (rats)[147]
Fucoidan and laminarinIncreases in the counts of Lactobacillus and Bifidobacterium in the ileumA.S. (piglet)[148]
Low MW polysaccharides from agar and alginateIncreases in the number of bifidobacteria. No effect on the populations of Lactobacilli, Bacteroides, Eubacterium rectale/C. coccoides, and C. histolyticum In vitro
FucoidanStimulation of apoptosis in HT-29 and HCT116 human colon cancer cells In vitro [150]
Himanthalia elongataIncreases in the acetic, propionic, and butyric acids concentrations. Improvement of the lipid profileA.S. (rats)[151]
FucoidanInhibition of the adhesion of Helicobacter pylori to the gastric mucous In vitro [152]
C. crispusEnhancement of the host immunity and reduction of the infection by Pseudomonas aeruginosa In vitro [153]

Table 2.

Results obtained in studies carried out using polysaccharides and oligosaccharides derived from algae as substrates.

[i] - A.S., animal study; C.I., clinical intervention; C.M., colonic model; HGM, human gut microbiota; PGM, pig gut microbiota.

5. Bacterial exopolisaccharides

5.1. Structure, sources, and production

Bacteria can produce polysaccharides that usually play a protective role against environment pressures. As these polymers are excreted into the extracellular surrounding, they are known as EPS. They can occur in two forms (capsules or biofilm) [150, 151] and are classified in two groups according to their composition:

  • homo-EPSs made up of a single type of monosaccharide such as fructans, α-D-glucans, β-D-glucans, dextran, curdlan, alternan, mutan, reuteran, or levan [152154].

  • hetero-EPSs composed of different types of monosaccharides, mainly d-glucose, d-galactose, l-rhamnose, and their derivatives, such as xanthan, gellan, alginate, hyaluronan, succinoglycan, kefiran, emulsan, galactoPol, or FucoPol [152154]. The heteropolysaccharides are the most abundant bacterial EPSs.

The critical factors for maximum EPSs production are carbon and nitrogen sources, mineral requirements, oxygen and aeration rate, temperature and pH [155], among others. Sugars are the most commonly carbon sources used for the production of bacterial EPSs. However, cheaper substrates, such as agro-food or industrial wastes and byproducts are suitable carbon sources for EPSs production [153]. EPSs synthesis is generally favored by the presence of the carbon source in excess, and the production of most bacterial EPSs occurs under aerobic conditions [153].

On the other hand, the methods for EPSs extraction have a crucial influence as their physicochemical properties could be affected by the isolation and purification techniques [154]. It can be carried out by two methods: (i) by solvent precipitation when they are in slim form and (ii) by alkaline extraction prior centrifugation and alcohol precipitation when they are in form of capsule. The recovery is performed by solvent precipitation [155].

5.2. Biological properties

The EPSs have been proved to have functional roles in human or animal health including immunomodulatory properties, antiviral, antioxidant, antimutagenecity, antihypertensive, antiulcer, and antitumor activities, and have also been used as food additives for texture improvement, as gelling agents or emulsifiers [152, 155, 156]. Moreover, EPSs may induce other positive physiological responses including lower cholesterol levels, reduced formation of pathogenic biofilms, modulation of adhesion to epithelial cells, and increased levels of bifidobacteria, showing a prebiotic potential [157].

The use of bacterial EPSs as prebiotic substrates has been scarcely investigated [151]. Table 3 shows the results from some in vitro and in vivo assays that have explored the prebiotic potential of this kind of substrates. Up to date, not human interventions with bacterial EPSs have been carried out.

EPS typeProducer strainBiological and prebiotic effectsStudy typeReferences
Levan Lactobacillus sanfranciscensis LTH1729, Lactobacillus sanfranciscensis LTH2590Bifidogenic effect; enhanced growth Eubacterium biforme In vitro (HGM)[162]
EPS (type not identified) Weissella cibaria A2, Weeissella confusa A9, Lactobacillus plantarum A3 and Pediococcus.pentosaceus 5S4 High resistance to gastric and intestinal digestions, enhancement of growth of Bifibacterium bifidum and some growth in case of B. longum, B. adolescentis,
and Lb. acidophilus
In vitro (pure cultures)[155]
EPS (type not identified) Weissella cibaria A2 Enhanced growth of Bifidobacterium and Lactobacillus
/Enteroccoccus groups, reduction of numbers of Clostrida. Increase in SCFA concentrations (acetate, propionate, butyrate)
In vitro (HGM)[155]
EPS (type not identified) B. animalis, B. pseudocatenultum, B. longum Increases in SCFA concentration and moderate bifidogenic effect In vitro (HGM)[163]
Fructan Lactobacillus sanfranciscensis TMW 1.392Metabolized by B. breve, B. bifidum, B. adolescentis,
and B. infantis
In vitro (pure cultures)[164]
Dextran Leuconostoc mesenteroides NRRL B-1426Low digestibility by simulated human gastric juice, high resistance to digestion by human a-amylases, stimulated the growth of B. animalis, B. infantis, Lb. acidophilus In vitro (pure cultures)[165]
Reuteran Lb. reuteri TMW 1.656Contribution to the prevention of enterotoxigenic E. coli adhesion to the intestinal mucosa In vivo (weanling piglets)[166]
EPS (type not identified) B. bifidum WBIN03Significant inhibition of enterobacteria, enterococci, and Bacteroides fragilis; significant enhancement of
the amount of Lactobacillus and total anaerobes
In vivo (mice)[167]

Table 3.

Results obtained in studies carried out using bacterial exopolysaccharides as substrates.

[i] - HGM, human gut microbiota.

6. Sugar alcohols

6.1. Definition and production

Sugar alcohols are low digestible carbohydrates that are hydrogenated, which means that there is an alcohol group (>CH–OH) in place of the carbonyl group (>C=O) in the aldose and ketose moieties of mono-, di-, oligo- and polysaccharides [162]. They can be classified into three groups: (i) hydrogenated monosaccharides (erythritol, xylitol, sorbitol, manitol); (ii) hydrogenated disaccharides (lactitol, isomalt, maltitol), and (iii) hydrogenated polysaccharides (hydrogenated starch hydrolysates (HSHs), polyglycitols) [163].

Sugar alcohols occur naturally in certain fruits and vegetables, and some of them are even generated by the human body. However, huge amounts of sugar alcohols are manufactured for the food industry (Table 4) where they are used as replacers in foodstuffs performing functions such as flavor enhancer, humectant, sweetener, anticaking agent, bulking agent, glazing agent, stabilizer, thickener, emulsifier, and sequestrant [166].

Sugar alcoholNatural sourceSynthesis
ErythritolVegetables, fruits (melons,
peaches, mushrooms, fermented foods (wine, beer, sake, soy sauce)
Fermentation of glucose using yeasts or lactic acid bacteria
XylitolFruits, vegetables, berries, oats, mushroomsMetal catalyzed hydrogenation of D-xylose
Biotechnological production from corn cobs, waste of sugarcane, and other fibers using yeasts
SorbitolApples, pears, apricots,
nectarines, prunes, dates, raisins
Catalytic hydrogenation of glucose or dextrose using Ni catalyst at high Tª. Electrochemical reduction of dextrose at pH>7
MannitolFruits, vegetables, brown seaweeds, wineFermentative process using lactic acid bacteria
IsomaltEnzymatic transglucosidation of sucrose into maltulose and further hydrogenation
LactitolCatalytic hydrogenation of lactose using Raney nickel as catalyst
MaltitolCatalytic hydrogenation of maltose or very high maltose glucose syrup
Partial hydrolysis of starch (from corn, potato or wheat) resulting in dextrins that undergoes subsequent hydrogenation

Table 4.

Natural sources and industrial synthesis of sugar alcohols [170, 171]

6.2. Biological properties

Sugar alcohols are characterized by their lower blood glucose response, and they can be metabolized without insulin [166]. Although they are structurally similar to sugars, their nutritional value is lower than them because they are only partially absorbed by the body, and the absorbed portions are either poorly metabolized (e.g., erythritol) or excreted via the urinary tract. The unabsorbed polyols are partially fermented in the colon, and they can modulate beneficially the gut microbiota acting as prebiotics [109, 162]. Table 5 lists the results obtained in several studies that have been carried out with sugar alcohols.

Sugar alcohol
Biological and prebiotic effectsStudy typeReferences
ErythritolNot change on bacterial population dynamics but significant increase in acetate In vitro (human gut microbiota)[113]
SorbitolFavors growth of autochthonous Lactobacillus species and increases colonic production of butyrate In vivo (in rat)[174]
MannitolModification of large intestine fermentation to produce more butyrate and propionate In vivo (in rat and pig model)[175]
Promotion of absorption and retention of Ca and Mg In vivo (in rat)[176]
Lowering effect on body fat accumulation and reduction of the level of serum triglycerides in vivo (in rat)[177]
IsomaltSignificant increase in bifidobacteria and increase in butyrate, acetate and
In vitro (human gut microbiota)[113]
LactitolAbility to reduce circulating levels of NH3 and toxic microbial substances, the clinical utility of which is the treatment of hepatic encephalopathyC.I.[178]
Reduction of levels of plasma endotoxin in chronic viral hepatitis through improving intestinal microbiotaC.I.[179]
Significant increases in counts of Bifidobacterium and both propionic and butyric acids and significant reduction of fecal pH with a consumption of 10 g/dC.I.[180]
Fermentation by pure cultures of Bifidobacterium lactis Bi-07, Lactobacillus acidophilus NCFM, Lactobacillis paracasei Lpc-37, Lactobacillus rhamnosus HN001 In vitro (pure cultures)[181]
Increase fecal numbers of L. acidophilus NCFM. No significant changes in SCFA and fecal concentrations of spermicine and PGE2C.I.[182]
Significant increase in bifidobacteria and increases in butyrate, acetate and
In vitro (human gut microbiota)[113]
MaltitolSignificant increase in bifidobacteria, minor increase in Lactobacillus/enterococci, and increases in major SCFA (acetate, propionate, and butyrate) In vitro (human gut microbiota)[113]
Significant increases in bifidobacteria, lactobacilli, clostridium histolyticum/perfringens populations, bacteroides, Fusobacterium prausnitzii, E. rectal, R. flavefaciens, Atopobium, R. bromii, and in major SCFA (acetate, propionate, and butyrate)C.I.[183]

Table 5.

Biological and prebiotic effects of sugar alcohols.

[i] - C.I., clinical intervention.


The authors acknowledge the financial support received from “Xunta de Galicia” (Project Ref. GRC2014/018 and “INBIOMED”) and from the Spanish “Ministry of Economy and Competitivity” (Project “Advanced processing technologies for biorefineries,” reference CTQ2014-53461-R). Both projects were partially funded by the FEDER Program of the European Union (“Unha maneira de facer Europa”).


1 - Bindels LB, Delzenne NM, Cani PD, Walter J. Towards a more comprehensive concept for prebiotics. Nature Reviews Gastroenterology & Hepatology 2015;12:303–10. doi:10.1038/nrgastro.2015.47.
2 - Binns N. Probiotics, prebiotics and the gut microbiota. ILSI Europe. Brussels, Belgium, 2013.
3 - Gotteland M. The role of the intestinal microbiota in the development of the obesity and the diabetes type-2. Chilean Journal of Endocrinology and Diabetes 2013; 6: 155-162.
4 - Guarner F. The colon as an organ: habitat of bacterial flora. Hospital Nutrition 2002; 17 Suppl 2: 7-10.
5 - Guarner F. Role of intestinal flora in health and disease. Hospital Nutrition 2007; 22 Suppl 2: 14-19.
6 - Woodmansey EJ. Intestinal bacteria and ageing. Journal of Applied Microbiology 2007;102:1178–86. doi:10.1111/j.1365-2672.2007.03400.x.
7 - O’Toole PW, Claesson MJ. Gut microbiota: Changes throughout the lifespan from infancy to elderly. International Dairy Journal 2010;20:281–91. doi:10.1016/j.idairyj.2009.11.010.
8 - Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012;488:178–84. doi:10.1038/nature11319.
9 - Ladirat SE. Galacto-oligosaccharides to counter the side effects of antibiotic treatments. Wageningen University. Wageningen, The Netherlands, 2014.
10 - Willing BP, Russell SL, Finlay BB. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nature Reviews Microbiology 2011;9:233–43. doi:10.1038/nrmicro2536.
11 - Prados-Bo A, Gómez-Martínez S, Nova E, Marcos A. Role of probiotics in obesity management. Nutrición Hospitalaria 2015;31 Suppl 1:10–8. doi:10.3305/nh.2015.31.sup1.8702.
12 - Mandalari G, Nueno-Palop C, Bisignano G, Wickham MSJ, Narbad A. Potential prebiotic properties of almond (Amygdalus communis L.) seeds. Applied and Environmental Microbiology 2008;74:4264–70. doi:10.1128/AEM.00739-08.
13 - Samanta AK, Senani S, Kolte AP, Sridhar M, Sampath KT, Jayapal N, et al. Production and in vitro evaluation of xylooligosaccharides generated from corn cobs. Food and Bioproducts Processing 2012;90:466–74. doi:10.1016/j.fbp.2011.11.001.
14 - Cruz-Guerrero A, Hernández-Sánchez H, Rodríguez-Serrano G, Gómez-Ruíz L, García-Garibay M, Figueroa-González I. Commercial probiotic bacteria and prebiotic carbohydrates: a fundamental study on prebiotics uptake, antimicrobials production and inhibition of pathogens. Journal of the Science of Food and Agriculture 2014;94:2246–52. doi:10.1002/jsfa.6549.
15 - Corzo N, Alonso JL, Azpiroz F, Calvo MAA, Cirici M, Leis R, et al. Prebiotics; concept, properties and beneficial effects. Hospital Nutrition 2015;31: 99–118. doi:10.3305/nh.2015.31.sup1.8715.
16 - Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology 2014;11:506–14. doi:10.1038/nrgastro.2014.66.
17 - Voragen AGJ, Coenen GJ, Verhoef RP, Schols H a. Pectin, a versatile polysaccharide present in plant cell walls. Structural Chemistry 2009;20:263–75. doi:10.1007/s11224-009-9442-z.
18 - Ele-Ekouna J-P, Pau-Roblot C, Courtois B, Courtois J. Chemical characterization of pectin from green tea (Camellia sinensis). Carbohydrate Polymers 2011;83:1232–9. doi:10.1016/j.carbpol.2010.09.028.
19 - Jackson CL, Dreaden TM, Theobald LK, Tran NM, Beal TL, Eid M, et al. Pectin induces apoptosis in human prostate cancer cells: correlation of apoptotic function with pectin structure. Glycobiology 2007;17:805–19. doi:10.1093/glycob/cwm054.
20 - Westphal Y. Analytical profiling of plant cell wall polysaccharides. Wageningen University. Wageningen, The Netherlands, 2010.
21 - Paulsen BS, Barsett H. Polysaccharides I. In: Heinze T, editor. Advances in Polymer Science, vol. 186, Berlin/Heidelberg: Springer-Verlag; 2005, pp. 69–101. doi:10.1007/b136812.
22 - Yamada H, Kiyohara H. Immunomodulating Activity of Plant Polysaccharide Structures. In: Kamerling JP, Boons GJ, Lee YC, Suzuki A, Taniguchi N, Voragen AGJ, editors. Comprehensive Glycoscience. Volume 4 Cell Glycobiology and Development Health and Disease in Glycomedicine. Oxford: Elsevier; 2007, p. 663–694. doi:10.1016/B978-044451967-2/00125-2.
23 - Matsumoto T, Moriya M, Sakurai MH, Kiyohara H, Tabuchi Y, Yamada H. Stimulatory effect of a pectic polysaccharide from a medicinal herb, the roots of Bupleurum falcatum L., on G-CSF secretion from intestinal epithelial cells. International Immunopharmacology 2008;8:581–8. doi:10.1016/j.intimp.2008.01.006.
24 - Gullón B, Gómez B, Martínez-Sabajanes M, Yáñez R, Parajó JC, Alonso JL. Pectic oligosaccharides: manufacture and functional properties. Trends in Food Science & Technology 2013;30:153–61. doi:10.1016/j.tifs.2013.01.006.
25 - Deng J, Shi ZJ, Li XZ, Liu HM. Soluble polysaccharides isolation and characterization from rabbiteye blueberry (Vaccinium ashei) fruits. BioResources 2013;8:405–19.
26 - Gómez B, Gullón B, Yáñez R, Parajó JC, Alonso JL. Pectic Oligosacharides from lemon peel wastes: production, purification, and chemical characterization. Journal of Agricultural and Food Chemistry 2013;61:10043–53. doi:10.1021/jf402559p.
27 - Gómez B, Gullón B, Remoroza C, Schols HA, Parajó JC, Alonso JL. Purification, characterization, and prebiotic properties of pectic oligosaccharides from orange peel wastes. Journal of Agricultural and Food Chemistry 2014;62:9769–82. doi:10.1021/jf503475b.
28 - Martínez-Sabajanes M, Yáñez R, Alonsó JL, Parajó JC. Chemical production of pectic oligosaccharides from orange peel wastes. Industrial and Engineering Chemistry Research 2010;49:8470–6. doi:10.1021/ie101066m.
29 - Wang X, Lü X. Characterization of pectic polysaccharides extracted from apple pomace by hot-compressed water. Carbohydrate Polymers 2014;102:174–84. doi:10.1016/j.carbpol.2013.11.012.
30 - Martínez-Sabajanes M, Gullón B, Schols HA, Alonso JL, Parajó JC. Assessment of the production of oligomeric compounds from sugar beet pulp. Industrial and Engineering Chemistry Research 2009;48:4681–7. doi:10.1021/ie8017753.
31 - Lama-Muñoz A, Rodríguez-Gutiérrez G, Rubio-Senent F, Fernández-Bolaños J. Production, characterization and isolation of neutral and pectic oligosaccharides with low molecular weights from olive by-products thermally treated. Food Hydrocolloids 2012;28:92–104. doi:10.1016/j.foodhyd.2011.11.008.
32 - Sato N, Takano Y, Mizuno M, Nozaki K, Umemura S, Matsuzawa T, et al. Production of feruloylated arabino-oligosaccharides (FA-AOs) from beet fiber by hydrothermal treatment. The Journal of Supercritical Fluids 2013;79:84–91. doi:10.1016/j.supflu.2013.01.012.
33 - Bonnin E, Garnier C, Ralet M-C. Pectin-modifying enzymes and pectin-derived materials: applications and impacts. Applied Microbiology and Biotechnology 2014;98:519–32. doi:10.1007/s00253-013-5388-6.
34 - Mandalari G, Nueno Palop C, Tuohy K, Gibson GR, Bennett RN, Waldron KW, et al. In vitro evaluation of the prebiotic activity of a pectic oligosaccharide-rich extract enzymatically derived from bergamot peel. Applied Microbiology and Biotechnology 2006;73:1173–9. doi:10.1007/s00253-006-0561-9.
35 - Coenen GJ, Kabel MA, Schols HA, Voragen AGJ. CE-MSn of complex pectin-derived oligomers. Electrophoresis 2008;29:2101–11. doi:10.1002/elps.200700465.
36 - Gavlighi HA, Meyer AS, Mikkelsen JD. Tragacanth gum: Functionality and prebiotic potential. Agro Food Industry Hi-Tech 2013;24:46–8.
37 - Yu L, Zhang X, Li S, Liu X, Sun L, Liu H, et al. Rhamnogalacturonan I domains from ginseng pectin. Carbohydrate Polymers 2010;79:811–7. doi:10.1016/j.carbpol.2009.08.028.
38 - Martínez-Sabajanes M, Yáñez R, Alonso JL, Parajó JC. Pectic oligosaccharides production from orange peel waste by enzymatic hydrolysis. International Journal of Food Science & Technology 2012;47:747–54. doi:10.1111/j.1365-2621.2011.02903.x.
39 - Gómez B, Yáñez R, Parajó JC, Alonso JL. Production of pectin-derived oligosaccharides from lemon peels by extraction, enzymatic hydrolysis and membrane filtration. Journal of Chemical Technology and Biotechnology 2016;91:234–247. doi:10.1002/jctb.4569.
40 - Concha J, Weinstein C, Zúñiga ME. Production of pectic extracts from sugar beet pulp with antiproliferative activity on a breast cancer cell line. Frontiers of Chemical Science and Engineering 2013;7:482–9. doi:10.1007/s11705-013-1342-5.
41 - Martínez-Sabajanes M, Gullón B, Yáñez R, Alonso JL, Parajó JC. Direct enzymatic production of oligosaccharide mixtures from sugar beet pulp: experimental evaluation and mathematical modeling. Journal of Agricultural and Food Chemistry 2009;57:5510–7. doi:10.1021/jf900654g.
42 - Wikiera A, Mika M, Starzyńska-Janiszewska A, Stodolak B. Application of Celluclast 1.5L in apple pectin extraction. Carbohydrate Polymers 2015;134:251–7. doi:10.1016/j.carbpol.2015.07.051.
43 - Sakurai MH, Matsumoto T, Kiyohara H, Yamada H. B-cell proliferation activity of pectic polysaccharide from a medicinal herb, the roots of Bupleurum falcatum L. and its structural requirement. Immunology 1999;97:540–7. doi:10.1046/j.1365-2567.1999.00774.x.
44 - Holck J, Hotchkiss AT, Meyer AS, Mikkelsen JD, Rastall RA. Production and bioactivity of pectic oligosaccharides from fruit and vegetable biomass. In: Moreno FJ, Sanz ML, editors. Food Oligosaccharides: Production, Analysis and Bioactivity, Chichester, UK: John Wiley & Sons, Ltd; 2014, p. 76–87. doi:10.1002/9781118817360.
45 - Concha Olmos J, Zúñiga Hansen ME. Enzymatic depolymerization of sugar beet pulp: Production and characterization of pectin and pectic-oligosaccharides as a potential source for functional carbohydrates. Chemical Engineering Journal 2012;192:29–36. doi:10.1016/j.cej.2012.03.085.
46 - Combo AMM, Aguedo M, Quiévy N, Danthine S, Goffin D, Jacquet N, et al. Characterization of sugar beet pectic-derived oligosaccharides obtained by enzymatic hydrolysis. International Journal of Biological Macromolecules 2013;52:148–56. doi:10.1016/j.ijbiomac.2012.09.006.
47 - Ravn HC, Bandsholm Sørensen O, Meyer AS. Time of harvest affects the yield of soluble polysaccharides extracted enzymatically from potato pulp. Food and Bioproducts Processing 2015;93:77–83. doi:10.1016/j.fbp.2013.11.006.
48 - Khodaei N, Karboune S. Enzymatic generation of galactose-rich oligosaccharides/oligomers from potato rhamnogalacturonan I pectic polysaccharides. Food Chemistry 2016;197:406–14. doi:10.1016/j.foodchem.2015.10.122.
49 - Wikiera A, Mika M, Starzyńska-Janiszewska A, Stodolak B. Development of complete hydrolysis of pectins from apple pomace. Food Chemistry 2015;172:675–80. doi:10.1016/j.foodchem.2014.09.132.
50 - Manderson K, Pinart M, Tuohy KM, Grace WE, Hotchkiss AT, Widmer W, et al. In vitro determination of prebiotic properties of oligosaccharides derived from an orange juice manufacturing by-product stream. Applied and Environmental Microbiology 2005;71:8383–9. doi:10.1128/AEM.71.12.8383-8389.2005.
51 - Chen H, Fu X, Luo Z. Properties and extraction of pectin-enriched materials from sugar beet pulp by ultrasonic-assisted treatment combined with subcritical water. Food Chemistry 2015;168:302–10. doi:10.1016/j.foodchem.2014.07.078.
52 - Chen J, Liang R, Liu W, Li T, Liu C, Wu S, et al. Pectic-oligosaccharides prepared by dynamic high-pressure microfluidization and their in vitro fermentation properties. Carbohydrate Polymers 2013;91:175–82. doi:10.1016/j.carbpol.2012.08.021.
53 - Rubio-Senent F, Rodríguez-Gutiérrez G, Lama-Muñoz A, Fernández-Bolaños J. Pectin extracted from thermally treated olive oil by-products: Characterization, physico-chemical properties, in vitro bile acid and glucose binding. Food Hydrocolloids 2015;43:311–21. doi:10.1016/j.foodhyd.2014.06.001.
54 - Sulek K, Vigsnaes LK, Schmidt LR, Holck J, Frandsen HL, Smedsgaard J, et al. A combined metabolomic and phylogenetic study reveals putatively prebiotic effects of high molecular weight arabino-oligosaccharides when assessed by in vitro fermentation in bacterial communities derived from humans. Anaerobe 2014;28:68–77. doi:10.1016/j.anaerobe.2014.05.007.
55 - Gavlighi HA, Michalak M, Meyer AS, Mikkelsen JD. Enzymatic depolymerization of gum tragacanth: bifidogenic potential of low molecular weight oligosaccharides. Journal of Agricultural and Food Chemistry 2013;61:1272–8. doi:10.1021/jf304795f.
56 - Lee EH, Park H-R, Shin M-S, Cho SY, Choi H-J, Shin K-S. Antitumor metastasis activity of pectic polysaccharide purified from the peels of Korean Citrus Hallabong. Carbohydrate Polymers 2014;111:72–9. doi:10.1016/j.carbpol.2014.04.073.
57 - Harig JM, Soergel KH, Komorowski RA, Wood CM. Treatment of diversion colitis with short-chain-fatty acid irrigation. New England Journal of Medicine 1989;320:23–8.
58 - Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metabolism 2011;13:517–26. doi:10.1016/j.cmet.2011.02.018.
59 - Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011;469:543–7. doi:10.1038/nature09646.
60 - Lin H V, Frassetto A, Kowalik EJ, Nawrocki AR, Lu MM, Kosinski JR, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. Plos One 2012;7:e35240. doi:10.1371/journal.pone.0035240.
61 - Di Sabatino A, Morera R, Ciccocioppo R, Cazzola P, Gotti S, Tinozzi FP, et al. Oral butyrate for mildly to moderately active Crohn’s disease. Alimentary Pharmacology & Therapeutics 2005;22:789–94. doi:10.1111/j.1365-2036.2005.02639.x.
62 - Binder HJ. Role of colonic short-chain fatty acid transport in diarrhea. Annual Review of Physiology 2010;72:297–313. doi:10.1146/annurev-physiol-021909-135817.
63 - Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SEK, et al. Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut 2015;64:1744–54. doi:10.1136/gutjnl-2014-307913.
64 - Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacological Research 2013;69:52–60. doi:10.1016/j.phrs.2012.10.020.
65 - Gómez B, Gullón B, Yáñez R, Schols H, Alonso JL. Prebiotic potential of pectins and pectic oligosaccharides derived from lemon peel wastes and sugar beet pulp: A comparative evaluation. Journal of Functional Foods 2016;20:108–21. doi:10.1016/j.jff.2015.10.029.
66 - Al-Tamimi MAHM, Palframan RJ, Cooper JM, Gibson GR, Rastall RA. In vitro fermentation of sugar beet arabinan and arabino-oligosaccharides by the human gut microflora. Journal of Applied Microbiology 2006;100:407–14. doi:10.1111/j.1365-2672.2005.02780.x.
67 - Holck J, Lorentzen A, Vigsnæs LK, Licht TR, Mikkelsen JD, Meyer AS. Feruloylated and nonferuloylated arabino-oligosaccharides from sugar beet pectin selectively stimulate the growth of Bifidobacterium spp. in human fecal in vitro fermentations. Journal of Agricultural and Food Chemistry 2011;59:6511–9. doi:10.1021/jf200996h.
68 - Gullón B, Martínez-Sabajanes M, Sanz Y, Alonso JL, Parajó JC. Pectic-oligosaccharides from sugar beet pulp: membrane purification and preliminary evaluation of its prebiotic potential. 6th International CIGR Technical Symposium—Towards a Sustainable Food Chain: Food Process, Bioprocessing and Food Quality Management, 2011.
69 - Leijdekkers AGM, Aguirre M, Venema K, Bosch G, Gruppen H, Schols HA. In vitro fermentability of sugar beet pulp derived oligosaccharides using human and pig fecal inocula. Journal of Agricultural and Food Chemistry 2014;62:1079–87. doi:10.1021/jf4049676.
70 - Gulfi M, Arrigoni E, Amadò R. In vitro fermentability of a pectin fraction rich in hairy regions. Carbohydrate Polymers 2007;67:410–6. doi:10.1016/j.carbpol.2006.06.018.
71 - Suzuki Y, Tanaka K, Amano T, Asakura T, Muramatsu N. Utilization by intestinal bacteria and digestibility of arabino-oligosaccharides in vitro. Journal of the Japanese Society for Horticultural Science 2004;73:574–9.
72 - Gullón B, Gullón P, Sanz Y, Alonso JL, Parajó JC. Prebiotic potential of a refined product containing pectic oligosaccharides. LWT—Food Science and Technology 2011;44:1687–96. doi:10.1016/j.lwt.2011.03.006.
73 - Guevara-Arauza JC, de Jesús Ornelas-Paz J, Pimentel-González DJ, Rosales Mendoza S, Soria Guerra RE, Paz Maldonado LMT. Prebiotic effect of mucilage and pectic-derived oligosaccharides from nopal (Opuntia ficus-indica). Food Science and Biotechnology 2012;21:997–1003. doi:10.1007/s10068-012-0130-1.
74 - Onumpai C, Kolida S, Bonnin E, Rastall RA. Microbial utilization and selectivity of pectin fractions with various structures. Applied and Environmental Microbiology 2011;77:5747–54. doi:10.1128/AEM.00179-11.
75 - Macfarlane GT, Macfarlane S. Models for intestinal fermentation: association between food components, delivery systems, bioavailability and functional interactions in the gut. Current Opinion in Biotechnology 2007;18:156–62. doi:10.1016/j.copbio.2007.01.011.
76 - Jiao L, Zhang X, Li B, Liu Z, Wang M, Liu S. Anti-tumour and immunomodulatory activities of oligosaccharides isolated from Panax ginseng C.A. Meyer. International Journal of Biological Macromolecules 2014;65:229–33. doi:10.1016/j.ijbiomac.2014.01.039.
77 - Harsha MR, Chandra Prakash S, Dharmesh SM. Modified pectic polysaccharide from turmeric (Curcuma longa): a potent dietary component against gastric ulcer. Carbohydrate Polymers 2016;138:143–55. doi:10.1016/j.carbpol.2015.11.043.
78 - Fanaro S, Jelinek J, Stahl B, Boehm G, Kock R, Vigi V. Acidic oligosaccharides from pectin hydrolysate as new component for infant formulae: effect on intestinal flora, stool characteristics, and pH. Journal of Pediatric Gastroenterology and Nutrition 2005;41:186–90. doi:10.1097/01.mpg.0000172747.64103.d7.
79 - Magne F, Hachelaf W, Suau A, Boudraa G, Bouziane-Nedjadi K, Rigottier-Gois L, et al. Effects on faecal microbiota of dietary and acidic oligosaccharides in children during partial formula feeding. Journal of Pediatric Gastroenterology and Nutrition 2008;46:580–8. doi:10.1097/MPG.0b013e318164d920.
80 - Westerbeek EA, van den Berg JP, Lafeber HN, Fetter WP, Boehm G, Twisk JW, et al. Neutral and acidic oligosaccharides in preterm infants: a randomized, double-blind, placebo-controlled trial. The American Journal of Clinical Nutrition 2010;91:679–86. doi:10.3945/ajcn.2009.28625.
81 - Gori A, Rizzardini G, van’t Land B, Amor KB, van Schaik J, Torti C, et al. Specific prebiotics modulate gut microbiota and immune activation in HAART-naive HIV-infected adults: results of the “COPA” pilot randomized trial. Mucosal Immunology 2011;4:554–63. doi:10.1038/mi.2011.15.
82 - Craig SAS, Holden JF, Troup JP, Auerbach MH, Frier HI. Polydextrose as soluble fiber: Physiological and analytical aspects. Cereal Foods World 1998;43:370–6.
83 - Wang H, Shi Y, Le G. Rapid microwave-assisted synthesis of polydextrose and identification of structure and function. Carbohydrate Polymers 2014;113:225–30. doi:10.1016/j.carbpol.2014.07.012.
84 - Putaala H. Polydextrose in Lipid Metabolism. In: Valenzuela R, editor. Lipid Metabolism. Croatia: InTechOpen; 2013, p. 233-261. doi:10.5772/51791
85 - Röytiö H, Ouwehand AC. The fermentation of polydextrose in the large intestine and its beneficial effects. Beneficial Microbes 2014;5:305–13. doi:10.3920/BM2013.0065.
86 - Lahtinen SJ, Knoblock K, Drakoularakou A, Jacob M, Stowell J, Gibson GR, et al. Effect of molecule branching and glycosidic linkage on the degradation of polydextrose by gut microbiota. Bioscience, Biotechnology, and Biochemistry 2010;74:2016–21. doi:10.1271/bbb.100251.
87 - Aidoo RP, Depypere F, Afoakwa EO, Dewettinck K. Industrial manufacture of sugar-free chocolates—applicability of alternative sweeteners and carbohydrate polymers as raw materials in product development. Trends in Food Science & Technology 2013;32:84–96. doi:10.1016/j.tifs.2013.05.008.
88 - Costabile A, Fava F, Röytiö H, Forssten SD, Olli K, Klievink J, et al. Impact of polydextrose on the faecal microbiota: a double-blind, crossover, placebo-controlled feeding study in healthy human subjects. The British Journal of Nutrition 2012;108:471–81. doi:10.1017/S0007114511005782.
89 - Herfel TM, Jacobi SK, Lin X, Fellner V, Walker DC, Jouni ZE, et al. Polydextrose enrichment of infant formula demonstrates prebiotic characteristics by altering intestinal microbiota, organic acid concentrations, and cytokine expression in suckling piglets. The Journal of Nutrition 2011;141:2139–45. doi:10.3945/jn.111.143727.
90 - Putaala H, Mäkivuokko H, Tiihonen K, Rautonen N. Simulated colon fiber metabolome regulates genes involved in cell cycle, apoptosis, and energy metabolism in human colon cancer cells. Molecular and Cellular Biochemistry 2011;357:235–45. doi:10.1007/s11010-011-0894-2.
91 - Quintero M, Maldonado M, Perez-Munoz M, Jimenez R, Fangman T, Rupnow J, et al. Adherence inhibition of Cronobacter sakazakii to intestinal epithelial cells by prebiotic oligosaccharides. Current Microbiology 2011;62:1448–54. doi:10.1007/s00284-011-9882-8.
92 - Witaicenis A, Fruet AC, Salem L, Di Stasi LC. Dietary polydextrose prevents inflammatory bowel disease in trinitrobenzenesulfonic acid model of rat colitis. Journal of Medicinal Food 2010;13:1391–6.
93 - Beynen AC, Saris DHJ, de Jong L, Staats M, Einerhand AWC. Impact of dietary polydextrose on clinical signs of canine osteoarthritis. American Journal of Animal and Veterinary Sciences 2011;6:93–9. doi:10.3844/ajavsp.2011.93.99.
94 - Weise C, Ernst D, van Tol EAF, Worm M. Dietary polyunsaturated fatty acids and non-digestible oligosaccharides reduce dermatitis in mice. Pediatric Allergy and Immunology 2013;24:361–7. doi:10.1111/pai.12073.
95 - Mineo H, Hara H, Kikuchi H, Sakurai H, Tomita F. Various indigestible saccharides enhance net calcium transport from the epithelium of the small and large intestine of rats in vitro. Journal of Nutrition 2001;131:3243–6.
96 - Freitas dos Santos E, Hitomi Tsuboi K, Araújo MR, Ouwehand AC, Adami Andreollo N, Kenji Miyasaka C. Dietary polydextrose increases calcium absorption in normal rats. ABCD Surgery Brazilian Archives of Digestive Surgery. 2009; 22: 201–205.
97 - Freitas dos Santos E, Hitomi Tsuboi K, Rachel Araujo M, Almeida Falconi M, Ouwehand AC. Ingestion of polydextrose increase the iron absorption in rats submitted to partial gastrectomy. Acta Cirurgica Brasileira 2010; 25: 518-524.
98 - Ashley C, Johnston WH, Harris CL, Stolz SI, Wampler JL, Berseth CL. Growth and tolerance of infants fed formula supplemented with polydextrose (PDX) and/or galactooligosaccharides (GOS): double-blind, randomized, controlled trial. Nutrition Journal 2012;11:38. doi:10.1186/1475-2891-11-38.
99 - Boler BMV, Serao MCR, Bauer LL, Staeger MA, Boileau TW, Swanson KS, et al. Digestive physiological outcomes related to polydextrose and soluble maize fibre consumption by healthy adult men. The British Journal of Nutrition 2011;106:1864–71. doi:10.1017/S0007114511002388.
100 - Hengst C, Ptok S, Roessler A, Fechner A, Jahreis G. Effects of polydextrose supplementation on different faecal parameters in healthy volunteers. International Journal of Food Sciences and Nutrition 2009;60 Suppl 5:96–105. doi:10.1080/09637480802526760.
101 - Hooda S, Boler BMV, Serao MCR, Brulc JM, Staeger MA, Boileau TW, et al. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. The Journal of Nutrition 2012;142:1259–65. doi:10.3945/jn.112.158766.
102 - Timm DA, Thomas W, Boileau TW, Williamson-Hughes PS, Slavin JL. Polydextrose and soluble corn fiber increase five-day fecal wet weight in healthy men and women. The Journal of Nutrition 2013;143:473–8. doi:10.3945/jn.112.170118.
103 - Luoto R, Ruuskanen O, Waris M, Kalliomäki M, Salminen S, Isolauri E. Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: a randomized, placebo-controlled trial. The Journal of Allergy and Clinical Immunology 2014;133:405–13. doi:10.1016/j.jaci.2013.08.020.
104 - Magro DO, de Oliveira LMR, Bernasconi I, Ruela Mde S, Credidio L, Barcelos IK, et al. Effect of yogurt containing polydextrose, Lactobacillus acidophilus NCFM and Bifidobacterium lactis HN019: a randomized, double-blind, controlled study in chronic constipation. Nutrition Journal 2014;13:75. doi:10.1186/1475-2891-13-75.
105 - Peuranen S, Tiihonen K, Apajalahti J, Kettunen A, Saarinen M, Rautonen N. Combination of polydextrose and lactitol affects microbial ecosystem and immune responses in rat gastrointestinal tract. The British Journal of Nutrition 2004;91:905–14. doi:10.1079/BJN20041114.
106 - Ribeiro TCM, Costa-Ribeiro H, Almeida PS, Pontes MV, Leite MEQ, Filadelfo LR, et al. Stool pattern changes in toddlers consuming a follow-on formula supplemented with polydextrose and galactooligosaccharides. Journal of Pediatric Gastroenterology and Nutrition 2012;54:288–90. doi:10.1097/MPG.0b013e31823a8a4c.
107 - Scalabrin DMF, Mitmesser SH, Welling GW, Harris CL, Marunycz JD, Walker DC, et al. New prebiotic blend of polydextrose and galacto-oligosaccharides has a bifidogenic effect in young infants. Journal of Pediatric Gastroenterology and Nutrition 2012;54:343–52. doi:10.1097/MPG.0b013e318237ed95.
108 - Probert HM, Apajalahti JHA, Rautonen N, Stowell J, Gibson GR. Polydextrose, lactitol, and fructo-oligosaccharide fermentation by colonic bacteria in a three-stage continuous culture system. Applied and Environmental Microbiology 2004;70:4505–11. doi:10.1128/AEM.70.8.4505-4511.2004.
109 - Beards E, Tuohy K, Gibson G. Bacterial, SCFA and gas profiles of a range of food ingredients following in vitro fermentation by human colonic microbiota. Anaerobe 2010;16:420–5. doi:10.1016/j.anaerobe.2010.05.006.
110 - Mäkeläinen HS, Mäkivuokko HA, Salminen SJ, Rautonen NE, Ouwehand AC. The effects of polydextrose and xylitol on microbial community and activity in a 4-stage colon simulator. Journal of Food Science 2007;72:M153–9. doi:10.1111/j.1750-3841.2007.00350.x.
111 - Beloshapka AN, Wolff AK, Swanson KS. Effects of feeding polydextrose on faecal characteristics, microbiota and fermentative end products in healthy adult dogs. The British Journal of Nutrition 2012;108:638–44. doi:10.1017/S0007114511005927.
112 - Fava F, Mäkivuokko H, Siljander-Rasi H, Putaala H, Tiihonen K, Stowell J, et al. Effect of polydextrose on intestinal microbes and immune functions in pigs. The British Journal of Nutrition 2007;98:123–33. doi:10.1017/S0007114507691818.
113 - Kannampalli P, Pochiraju S, Chichlowski M, Berg BM, Rudolph C, Bruckert M, et al. Probiotic Lactobacillus rhamnosus GG (LGG) and prebiotic prevent neonatal inflammation-induced visceral hypersensitivity in adult rats. Neurogastroenterology and Motility 2014;26:1694–704. doi:10.1111/nmo.12450.
114 - Legette LL, Lee W, Martin BR, Story JA, Campbell JK, Weaver CM. Prebiotics enhance magnesium absorption and inulin-based fibers exert chronic effects on calcium utilization in a postmenopausal rodent model. Journal of Food Science 2012;77:H88–94. doi:10.1111/j.1750-3841.2011.02612.x.
115 - [117] González del Val A, Platas G, Basilio A, Cabello A, Gorrochategui J, Suay I, et al. Screening of antimicrobial activities in red, green and brown macroalgae from Gran Canaria (Canary Islands, Spain). International Microbiology 2001;4:35–40. doi:10.1007/s101230100006.
116 - Cumashi A, Ushakova NA, Preobrazhenskaya ME, D’Incecco A, Piccoli A, Totani L, et al. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007;17:541–52. doi:10.1093/glycob/cwm014.
117 - Kang JY, Khan MNA, Park NH, Cho JY, Lee MC, Fujii H, et al. Antipyretic, analgesic, and anti-inflammatory activities of the seaweed Sargassum fulvellum and Sargassum thunbergii in mice. Journal of Ethnopharmacology 2008;116:187–90. doi:10.1016/j.jep.2007.10.032.
118 - Chandini SK, Ganesan P, Bhaskar N. In vitro antioxidant activities of three selected brown seaweeds of India. Food Chemistry 2008;107:707–13. doi:10.1016/j.foodchem.2007.08.081.
119 - Rupérez P, Ahrazem O, Leal JA. Potential antioxidant capacity of sulfated polysaccharides from the edible marine brown seaweed Fucus vesiculosus. Journal of Agricultural and Food Chemistry 2002;50:840–5. doi:10.1021/jf010908o.
120 - Balboa EM, Moure A, Domínguez H. Valorization of Sargassum muticum biomass according to the biorefinery concept. Marine Drugs 2015;13:3745–60. doi:10.3390/md13063745.
121 - Maruyama H, Tamauchi H, Hashimoto M, Nakano T. Antitumor activity and immune response of Mekabu fucoidan extracted from Sporophyll of Undaria pinnatifida. In Vivo 2003;17:245–9.
122 - Ye H, Wang K, Zhou C, Liu J, Zeng X. Purification, antitumor and antioxidant activities in vitro of polysaccharides from the brown seaweed Sargassum pallidum. Food Chemistry 2008;111:428–32. doi:10.1016/j.foodchem.2008.04.012.
123 - Pereira MG, Benevides NMB, Melo MRS, Valente AP, Melo FR, Mourão PAS. Structure and anticoagulant activity of a sulfated galactan from the red alga, Gelidium crinale. Is there a specific structural requirement for the anticoagulant action? Carbohydrate Research 2005;340:2015–23. doi:10.1016/j.carres.2005.05.018.
124 - Kwon M-J, Nam T-J. Porphyran induces apoptosis related signal pathway in AGS gastric cancer cell lines. Life Sciences 2006;79:1956–62. doi:10.1016/j.lfs.2006.06.031.
125 - Aisa Y, Miyakawa Y, Nakazato T, Shibata H, Saito K, Ikeda Y, et al. Fucoidan induces apoptosis of human HS-sultan cells accompanied by activation of caspase-3 and down-regulation of ERK pathways. American Journal of Hematology 2005;78:7–14. doi:10.1002/ajh.20182.
126 - Anastyuk SD, Imbs TI, Shevchenko NM, Dmitrenok PS, Zvyagintseva TN. ESIMS analysis of fucoidan preparations from Costaria costata, extracted from alga at different life-stages. Carbohydrate Polymers 2012;90:993–1002. doi:10.1016/j.carbpol.2012.06.033.
127 - Ale MT, Mikkelsen JD, Meyer AS. Designed optimization of a single-step extraction of fucose-containing sulfated polysaccharides from Sargassum sp. Journal of Applied Phycology 2012;24:715–23. doi:10.1007/s10811-011-9690-3.
128 - Balboa EM, Rivas S, Moure A, Domínguez H, Parajó JC. Simultaneous extraction and depolymerization of fucoidan from Sargassum muticum in aqueous media. Marine Drugs 2013;11:4612–27. doi:10.3390/md11114612.
129 - Rodriguez-Jasso RM, Mussatto SI, Pastrana L, Aguilar CN, Teixeira JA, Aguilar CN. Microwave-assisted extraction of sulfated polysaccharides (fucoidan) from brown seaweed. Carbohydrate Polymers 2011;86:1137–44. doi:sulfated polysaccharides.
130 - Lorbeer AJ, Lahnstein J, Fincher GB, Su P, Zhang W. Kinetics of conventional and microwave-assisted fucoidan extractions from the brown alga, Ecklonia radiata. Journal of Applied Phycology 2015;27:2079–87. doi:10.1007/s10811-014-0446-8.
131 - Yuan Y, Macquarrie D. Microwave assisted extraction of sulfated polysaccharides (fucoidan) from Ascophyllum nodosum and its antioxidant activity. Carbohydrate Polymers 2015;129:101–7. doi:10.1016/j.carbpol.2015.04.057.
132 - Rodrigues D, Sousa S, Silva A, Amorim M, Pereira L, Rocha-Santos TAP, et al. Impact of enzyme- and ultrasound-assisted extraction methods on biological properties of red, brown, and green seaweeds from the central west coast of Portugal. Journal of Agricultural and Food Chemistry 2015;63:3177–88. doi:10.1021/jf504220e.
133 - Athukorala Y, Jung W-K, Vasanthan T, Jeon Y-J. An anticoagulative polysaccharide from an enzymatic hydrolysate of Ecklonia cava. Carbohydrate Polymers 2006;66:184–91. doi:10.1016/j.carbpol.2006.03.002.
134 - Shang YF, Kim SM, Lee WJ, Um B-H. Pressurized liquid method for fucoxanthin extraction from Eisenia bicyclis (Kjellman) Setchell. Journal of Bioscience and Bioengineering 2011;111:237–41. doi:10.1016/j.jbiosc.2010.10.008.
135 - Devillé C, Gharbi M, Dandrifosse G, Peulen O. Study on the effects of laminarin, a polysaccharide from seaweed, on gut characteristics. Journal of the Science of Food and Agriculture 2007;87:1717–25. doi:10.1002/jsfa.2901.
136 - O’Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, et al. Prebiotics from marine macroalgae for human and animal health applications. Marine Drugs 2010;8:2038–64. doi:10.3390/md8072038.
137 - Gupta S, Abu-Ghannam N. Bioactive potential and possible health effects of edible brown seaweeds. Trends in Food Science & Technology 2011;22:315–26. doi:10.1016/j.tifs.2011.03.011.
138 - Gómez-Ordóñez E, Jiménez-Escrig A, Rupérez P. Effect of the red seaweed Mastocarpus stellatus intake on lipid metabolism and antioxidant status in healthy Wistar rats. Food Chemistry 2012;135:806–11. doi:10.1016/j.foodchem.2012.04.138.
139 - Wang Y, Han F, Hu B, Li J, Yu W. In vivo prebiotic properties of alginate oligosaccharides prepared through enzymatic hydrolysis of alginate. Nutrition Research 2006;26:597–603. doi:10.1016/j.nutres.2006.09.015.
140 - Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio MD, Rupérez P. Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. Journal of Applied Phycology 2012;25:503–12. doi:10.1007/s10811-012-9884-3.
141 - Lynch MB, Sweeney T, Callan JJ, O’Sullivan JT, 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. Journal of the Science of Food and Agriculture 2010;90:430–7. doi:10.1002/jsfa.3834.
142 - Kitano Y, Murazumi K, Duan J, Kurose K, Kobayashi S, Sugawara T, et al. Effect of dietary porphyran from the red alga, Porphyra yezoensis, on glucose metabolism in diabetic KK-Ay mice. Journal of Nutritional Science and Vitaminology 2012;58:14–9. doi:10.3177/jnsv.58.14.
143 - Liu J, Kandasamy S, Zhang J, Kirby CW, Karakach T, Hafting J, et al. 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 Complementary and Alternative Medicine 2015;15:279. doi:10.1186/s12906-015-0802-5.
144 - Murphya P, Dal Bello F, O’Doherty J, Arendt EK, 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. doi:10.1016/j.anaerobe.2013.03.002.
145 - Ramnani P, Chitarrari R, Tuohy K, Grant J, Hotchkiss S, Philp K, et al. In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds. Anaerobe 2012;18:1–6. doi:10.1016/j.anaerobe.2011.08.003.
146 - Kim EJ, Park SY, Lee J-Y, Park JHY. Fucoidan present in brown algae induces apoptosis of human colon cancer cells. BMC Gastroenterology 2010;10:96. doi:10.1186/1471-230X-10-96.
147 - Villanueva M-J, Morcillo M, Tenorio M-D, Mateos-Aparicio I, Andrés V, Redondo-Cuenca A. Health-promoting effects in the gut and influence on lipid metabolism of Himanthalia elongata and Gigartina pistillata in hypercholesterolaemic Wistar rats. European Food Research and Technology 2013;238:409–16. doi:10.1007/s00217-013-2116-5.
148 - Shibata H, Iimuro M, Uchiya N, Kawamori T, Nagaoka M, Ueyama S, et al. Preventive effects of Cladosiphon fucoidan against Helicobacter pylori infection in Mongolian gerbils. Helicobacter 2003;8:59–65. doi:10.1046/j.1523-5378.2003.00124.x.
149 - Liu J, Hafting J, Critchley AT, Banskota AH, Prithiviraj B. Components of the cultivated red seaweed Chondrus crispus enhance the immune response of Caenorhabditis elegans to Pseudomonas aeruginosa through the pmk-1, daf-2/daf-16, and skn-1 pathways. Applied and Environmental Microbiology 2013;79:7343–50. doi:10.1128/AEM.01927-13.
150 - Donot F, Fontana A, Baccou JC, Schorr-Galindo S. Microbial exopolysaccharides: Main examples of synthesis, excretion, genetics and extraction. Carbohydrate Polymers 2012;87:951–62. doi:10.1016/j.carbpol.2011.08.083.
151 - Hongpattarakere T, Cherntong N, Wichienchot S, Kolida S, Rastall RA. In vitro prebiotic evaluation of exopolysaccharides produced by marine isolated lactic acid bacteria. Carbohydrate Polymers 2012;87:846–52. doi:10.1016/j.carbpol.2011.08.085.
152 - Harutoshi T. Exopolysaccharides of Lactic Acid Bacteria for Food and Colon Health Applications. In: Kongo JM, editor. Lactic Acid Bacteria—R & D for Food, Health and Livestock Purposes, InTechOpen; 2013, p. 515–38. doi:10.5772/50839.
153 - Freitas F, Alves VD, Reis MAM. Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends in Biotechnology 2011;29:388–98. doi:10.1016/j.tibtech.2011.03.008.
154 - Mishra A, JHA B. Microbial exopolysaccharides, in the prokaryotes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. Applied Bacteriology and Biotechnology, Berlin, Heidelberg: Springer-Verlag; 2013, p. 179–92. doi:10.1007/978-3-642-31331-8_25.
155 - Kumar AS, Mody K, Jha B. Bacterial exopolysaccharides—a perception. Journal of Basic Microbiology 2007;47:103–17. doi:10.1002/jobm.200610203.
156 - Madhuri K, Prabhakar K. Microbial exopolysaccharides: biosynthesis and potential applications. Oriental Journal of Chemistry 2014;30:1401–10. doi:10.13005/ojc/300362.
157 - Patel A, Prajapat JB. Food and health applications of exopolysaccharides produced by lactic acid bacteria. Advances in Dairy Research 2013;01. doi:10.4172/2329-888X.1000107.
158 - Korakli M, Ganzle MG, Vogel RF. Metabolism by bifidobacteria and lactic acid bacteria of polysaccharides from wheat and rye, and exopolysaccharides produced by Lactobacillus sanfranciscensis. Journal of Applied Microbiology 2002;92:958–65. doi:10.1046/j.1365-2672.2002.01607.x.
159 - Kothari D, Tingirikari JMR, Goyal A. In vitro analysis of dextran from Leuconostoc mesenteroides NRRL B-1426 for functional food application. Bioactive Carbohydrates and Dietary Fibre 2015;6:55–61. doi:10.1016/j.bcdf.2015.08.001.
160 - Yang Y, Galle S, Le MHA, Zijlstra RT, Gänzle MG. Feed Fermentation with Reuteran- and Levan-producing Lactobacillus reuteri reduces colonization of weanling pigs by enterotoxigenic Escherichia coli. Applied and Environmental Microbiology 2015;81:5743–52. doi:10.1128/AEM.01525-15.
161 - Li S, Chen T, Xu F, Dong S, Xu H, Xiong Y, et al. The beneficial effect of exopolysaccharides from Bifidobacterium bifidum WBIN03 on microbial diversity in mouse intestine. Journal of the Science of Food and Agriculture 2014;94:256–64. doi:10.1002/jsfa.6244.
162 - Livesey G. Health potential of polyols as sugar replacers, with emphasis on low glycaemic properties. Nutrition Research Reviews 2003;16:163–91. doi:10.1079/NRR200371.
163 - Grabitske HA, Slavin JL. Gastrointestinal effects of low-digestible carbohydrates. Critical Reviews in Food Science and Nutrition 2009;49:327–60. doi:10.1080/10408390802067126.
164 - Sarmiento-Rubiano LA, Zúñiga M, Pérez-Martínez G, Yebra MJ. Dietary supplementation with sorbitol results in selective enrichment of lactobacilli in rat intestine. Research in Microbiology 2007;158:694–701. doi:10.1016/j.resmic.2007.07.007.
165 - Maekawa M, Ushida K, Hoshi S, Kashima N, Ajisaka K, Yajima T. Butyrate and propionate production from D-mannitol in the large intestine of pig and rat. Microbial Ecology in Health and Disease 2005;17:169–76. doi:10.1080/08910600500430730.
166 - Grembecka M. Sugar alcohols—their role in the modern world of sweeteners: a review. European Food Research and Technology 2015;241:1–14. doi:10.1007/s00217-015-2437-7.
167 - Xiao J, Li X, Min X, Sakaguchi E. Mannitol improves absorption and retention of calcium and magnesium in growing rats. Nutrition (Burbank, Los Angeles County, California) 2013;29:325–31. doi:10.1016/j.nut.2012.06.010.
168 - Nishiyama A, Nishioka S, Islam SM, Sakaguchi E. Mannitol lowers fat digestibility and body fat accumulation in both normal and cecectomized rats. Journal of Nutritional Science and Vitaminology 2009;55:242–51. doi:10.3177/jnsv.55.242.
169 - Blanc P, Daures JP, Rouillon JM, Peray P, Pierrugues R, Larrey D, et al. Lactitol or lactulose in the treatment of chronic hepatic encephalopathy: results of a meta-analysis. Hepatology 1992;15:222–8.
170 - Chen C, Li L, Wu Z, Chen H, Fu S. Effects of lactitol on intestinal microflora and plasma endotoxin in patients with chronic viral hepatitis. The Journal of Infection 2007;54:98–102. doi:10.1016/j.jinf.2005.11.013.
171 - Finney M, Smullen J, Foster HA, Brokx S, Storey DM. Effects of low doses of lactitol on faecal microflora, pH, short chain fatty acids and gastrointestinal symptomology. European Journal of Nutrition 2007;46:307–14. doi:10.1007/s00394-007-0666-7.
172 - Mäkeläinen H, Saarinen M, Stowell J, Rautonen N, Ouwehand AC. Xylo-oligosaccharides and lactitol promote the growth of Bifidobacterium lactis and Lactobacillus species in pure cultures. Beneficial Microbes 2010;1:139–48. doi:10.3920/BM2009.0029.
173 - Ouwehand AC, Tiihonen K, Saarinen M, Putaala H, Rautonen N. Influence of a combination of Lactobacillus acidophilus NCFM and lactitol on healthy elderly: intestinal and immune parameters. The British Journal of Nutrition 2009;101:367–75. doi:10.1017/S0007114508003097.
174 - Beards E, Tuohy K, Gibson G. A human volunteer study to assess the impact of confectionery sweeteners on the gut microbiota composition. The British Journal of Nutrition 2010;104:701–8. doi:10.1017/S0007114510001078.
175 - Jie Z, Bang-yao L, Ming-jie X, Hai-wei L, Zu-kang Z, Ting-song W, et al. Studies on the effects of polydextrose intake on physiologic functions in Chinese people. American Journal of Clinical Nutrition 2000;72:1503–9.
176 - Liu S, Tsai CE. Effects of biotechnically synthesized oligosaccharides and polydextrose on serum lipids in the human. Journal of the Chinese Nutrition Society 1995;20:1–12.
177 - Kulshreshtha G, Rathgeber B, Stratton G, Thomas N, Evans F, Critchley A, et al. Feed supplementation with red seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, affects performance, egg quality, and gut microbiota of layer hens. Poultry Science 2014;93:2991–3001. doi:10.3382/ps.2014-04200.
178 - Dierick N, Ovyn A, De Smet S. In vitro assessment of the effect of intact marine brown macro-algae Ascophyllum nodosum on the gut flora of piglets. Livestock Science 2010;133:154–6. doi:10.1016/j.livsci.2010.06.051.
179 - Bello FD, Walter J, Hertel C, Hammes WP. In vitro study of prebiotic properties of levan-type exopolysaccharides from Lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Systematic and Applied Microbiology 2001;24:232–7. doi:10.1078/0723-2020-00033.
180 - Salazar N, Gueimonde M, Hernández-Barranco AM, Ruas-Madiedo P, de los Reyes-Gavilán CG. Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria. Applied and Environmental Microbiology 2008;74:4737–45. doi:10.1128/AEM.00325-08.
181 - Patra F, Tomar SK, Arora S. Technological and functional applications of low-calorie sweeteners from lactic acid bacteria. Journal of Food Science 2009;74:R16–23. doi:10.1111/j.1750-3841.2008.01005.x.