Open access peer-reviewed chapter

Pectic Oligosaccharides and Other Emerging Prebiotics

By Beatriz Míguez, Belén Gómez, Patricia Gullón, Beatriz Gullón and José Luis Alonso

Submitted: November 4th 2015Reviewed: March 3rd 2016Published: July 13th 2016

DOI: 10.5772/62830

Downloaded: 1907

Abstract

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 concentration.in vitro
(C.M.)
[112]
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
(C.M.)
[90]

Table 1.

Results obtained in studies carried out using polydextrose as substrate.

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 SCFAsIn vitro
(HGM)
[137]
LaminarinVariations of mucus composition in jejunum, ileum, cecum, and colonA.S. (rats)[137]
Ascophyllum nodosumReduction in populations of Escherichia coliIn vitro
(PGM)
[141]
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
FOS
A.S. (rats)[143]
Alginate oligosaccharidesStimulation of the growth of Bifidobacterium bifidum ATCC 29521 and Bifidobacterium longum SMU 27001In 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 LactobacilliA.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. histolyticumIn vitro
(HGM)
[149]
FucoidanStimulation of apoptosis in HT-29 and HCT116 human colon cancer cellsIn 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 mucousIn vitro[152]
C. crispusEnhancement of the host immunity and reduction of the infection by Pseudomonas aeruginosaIn vitro[153]

Table 2.

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

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, mainlyd-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
LevanLactobacillus sanfranciscensis LTH1729, Lactobacillus sanfranciscensis LTH2590Bifidogenic effect; enhanced growth Eubacterium biformeIn vitro (HGM)[162]
EPS (type not identified)Weissella cibaria A2, Weeissella confusa A9, Lactobacillus plantarum A3 and Pediococcus.pentosaceus 5S4High 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 A2Enhanced 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. longumIncreases in SCFA concentration and moderate bifidogenic effectIn vitro (HGM)[163]
FructanLactobacillus sanfranciscensis TMW 1.392Metabolized by B. breve, B. bifidum, B. adolescentis,
and B. infantis
In vitro (pure cultures)[164]
DextranLeuconostoc 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. acidophilusIn vitro (pure cultures)[165]
ReuteranLb. reuteri TMW 1.656Contribution to the prevention of enterotoxigenic E. coli adhesion to the intestinal mucosaIn 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.

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
Polyglycitols/
HSHs
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 acetateIn vitro (human gut microbiota)[113]
SorbitolFavors growth of autochthonous Lactobacillus species and increases colonic production of butyrateIn vivo (in rat)[174]
MannitolModification of large intestine fermentation to produce more butyrate and propionateIn vivo (in rat and pig model)[175]
Promotion of absorption and retention of Ca and MgIn vivo (in rat)[176]
Lowering effect on body fat accumulation and reduction of the level of serum triglyceridesin vivo (in rat)[177]
IsomaltSignificant increase in bifidobacteria and increase in butyrate, acetate and
propionate
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 HN001In 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
propionate
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.

C.I., clinical intervention.


Acknowledgments

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”).

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Beatriz Míguez, Belén Gómez, Patricia Gullón, Beatriz Gullón and José Luis Alonso (July 13th 2016). Pectic Oligosaccharides and Other Emerging Prebiotics, Probiotics and Prebiotics in Human Nutrition and Health, Venketeshwer Rao and Leticia G. Rao, IntechOpen, DOI: 10.5772/62830. Available from:

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