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Impact of gums on the growth of probiotics BERNICE D. KARLTON-SENAYE*, SALAM. A. IBRAHIM *Corresponding Author North Carolina Agricultural and Technical State University, Bernice D. Food Microbiology and Biotechnology laboratory, Karlton-Senaye Greensboro, NC 27411-1011, USA

KEYWORDS: gums; ; probiotics; prebiotics

ABSTRACT: Gums are polysaccharides used as stabilizers in food that could also enhance growth and viability of probiotics. Thus, the aim of this review was to provide general information about common gums used in different food applications and to introduce a new application of gums as possible functional ingredients to promote the viability of probiotics in food products.

INTRODUCTION Molecular structure, chemical composition and functionality of gums Gums are complex polysaccharides extracted from sources Gums are chemically closely related with , such as endosperm of seeds, plant exudates, sea but are comprised of , , , oxidation weeds, , and animal sources (1, 2). Gums are products of these materials, acids, salts of carbon, , with hydrophilic ability due to the presence of and oxygen (12). Gums also contain , , a hydroxyl bond. The composition and structure of gums potassium and sometimes nitrogen (12). Gums can be enable gums to imbibe large amount of water forming a gel, obtained commercially by tapping from certain trees which makes gums useful in the food industry. Gums are used and shrubs, by extracting from marine , by milling as stabilizers improving viscosity and texture by preventing or extracting from some seeds, by thermal treatment of

Probiotics “wheying off” (3). Gums have also found usefulness in other starches from kernels or crops, by chemical processing industries, namely pharmaceutical, cosmetic, paint, ink, of cellulose from tree trunks and the cotton plant, as well paper, color, and adhesive industries (4). as by separating animal by-products and by purifi cation A number of polysaccharides are used as prebiotics processes (12). Gums also differ in their chemical to promote growth and viability of lactic acid bacteria composition as shown in table 1 (13). (LAB) in dairy products (5) already exist with inulin and (FOS) being the most recognized (6- 9). A is defi ned as a “non-digestible food ingredient that benefi cially affects the host by selectively stimulating the growth and/or activity of one or a limited number of bacteria in the colon, and thus improves host health” (6). These health benefi ts include reinforcement of gut mucosal vol 24(4) - July/August 2013 - immunity, decreased risk associated with mutagenicity and carcinogenicity, alleviation of intolerance, acceleration of intestinal mobility, hypocholesterolemic effect, reduced duration of , prevention of infl ammatory bowel disease, prevention of colon cancer, inhibition of Helicobacter pylori and intestinal pathogens, and treatment and prevention of allergy (10). Though gums are known to improve texture of food, limited studies have been conducted using gums to enhance growth and

Agro FOOD Industry Hi Tech viability of probiotics. Thus, the aim of this review was to provide information about common gums used in the food industry and introduce a recent study related to the impact of gums on the growth of Lactobacillus species.

SOURCES OF GUMS

Gums are classifi ed according to their source of extraction, chemical structure, and physical characteristics. Gums are extractable from land plants (e.g. locust bean, guar, , tara) or marine plants (e.g. carrageenan, alginate, furcelluran), from microorganisms (e.g. xanthan, gellan, pullulan) or animal source (e.g. ). Due to the presence of the hydroxyl group and their hydrophilic nature, Table 1. Main chemical composition of algal, plant, and exudates gums are able to impact viscosity or gelling properties to gums. *Williams and Phillips, 2000, Piotr Tomasik, 2004 their media (11).

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Agro FOOD Industry Hi Tech - vol 24(4) - July/August 2013 Probiotics 11 ), which is ), which is Chemically described , and soluble solids, which vary , and soluble solids, 2+ the Aspergillus family. -carrageenan is soluble and forms a hard -carrageenan is soluble and forms a hard Chondrus crispus. Of major importance to food are k -Carrageenan, on the other hand, is soluble at lower -Carrageenan, on the other hand, is soluble at lower ratio is 1.6:1. Its fl our is used in the production of noodles, of noodles, the production is used in our fl is 1.6:1. Its ratio It has a (16). er and thickener texture modifi and as a jellies, swells 2,000,000 Da. Konjac weight of 200,000 to molecular the and heat increase but shear at room temperature er, a pseudoplastic viscosifi rate. It is considered hydration at pH 3 gels that are stable thermally irreversible and yields (15). set with alkali or heat to 9 when Pectin the cell walls of plants. Pectin consists Pectin is obtained from galacturonic acid units joined of chains of 300 to 1,000 cation of esterifi linearly with 1α→4 linkages. The degree of pectin. The neutral side- affects the gelling properties molecule form weak non-covalent chains in the pectin formation. The structure of pectin has bonds and hinder gel to every two carboxyl groups; hence three methyl ester join cation called a DE-60 pectin. of esterifi it is has a 60% degree uenced are complex and are mostly infl Pectin gel formations Ca by factors such as pH, made up of about 25% sulfate ester groups and about 34% made up of about 25% sulfate ester groups and about 34% anhydro-; iota (ι) constitutes about 32% sulfate ester groups and about 30% anhydro-galactose; and lambda (λ) which comprises 35% sulphate ester groups and no anhydo-galactose (18). According to Bixler (19), these chemical differences confer varying functionality as well. K brittle gel that is converted by heat at low temperature. I temperature and forms sof, elastic gels. λ-carrageenan is non-gelling and soluble in cold water (19). These three types of carrageenan are extracted traditionally from Irish moss, and λ-carrageenan (19). in their in their effect on gelling process of different pectin in their in their effect in jellies, and types. Pectin is used in fruit preservationand jams preparations. Inulin obtainedInulin is a natural plant-derived mostly from the Compositae family including , dahlia, produced byand Jerusalem (17). Inulin is also and fungimicroorganisms including Streptococcus mutans, belonging to (n-1)-D- as α-D-glucopyranosyl-[β-D-fructofuranosyl] consistingfructofuranoside, inulin is a of chain lengthof linear carbon chains. Generally, inulin has species. It haswith 2-200 attached subject to the from 10,000much larger degree of polymerization ranging non-toxic, andto 100,000 (17). Biochemically, inulin is inert, aresoluble in water. Inulin and in dogenic activity the best studied prebiotics for their bifi bonds thatthe intestine (6) . Inulin has β (2-1) glycosidic by certainmakes it indigestible by humans but digestible inulinase activitymicroorganisms living in the gut that have of inulin in theincluding lactobacilli. The non-digestible nature enhances growthdigestive system makes it a prebiotics which which ora that in turn produces bioproducts of a healthy gut fl suppress colon cancer development. Inulin also has several food and pharmaceutical applications (17). Algal and microbial gums Carrageenan Carrageenan is a group of polysaccharides extracted from seaweeds (Rhodophyta). Carrageenan is made of polysaccharides which are linear sulfated galactose polymers with a size of 400-600 kilodaltons. Like other gums, varieties of carrageenan are grouped according to their composition and functionality. There are three commonly known types of carrageenan, namely: kappa (k Cyamopsis Cyamopsis Amorphophallus ). It consists mainly of . Tara gum is structurally characterized . It is a straight chain galactomannan with chain galactomannan . It is a straight β-(1→6) glucosyl units(3). The mannan:galactose . It has a konjac. Konjac has been cultivated for centuries in Japan. It is a β-(1→4) linked polysaccharide composed of a D-lucosyl and D-mannosyl backbone lightly branched, possibly through Konjac Konjac is extracted from the tubers of as a galactomannan, and is similar to guar and locust bean gums, two other galactomannans. It consists of a linear chain of (1→4)-β-D-manna units with α-D-galacto- pyranose units attached by (1→6) linkages with a ratio of to galactose being 3:1(14). Tara gum possesses some unique properties, making it ideal for use in stabilizer cheese, cream desserts, as frozen such dairy foods blends for and cultured products (15). Tara gum Tara gum is obtained by grinding the endosperm of seeds of Caesalpinia spinosa high molecular weight (~ 200,000-300,000) polysaccharides high molecular weight (~ 200,000-300,000) composed of galactomannans. The mannose:galactose in but ratio is about 5:1. Cassia gum is insoluble disperses well in cold water and forms colloidal solutions. rm viscoelastic gel with xanthan at 40 ºC Cassia forms a fi and with sodium borate at the pH of 9 and above (fao.org). It is used as a thickening agent in dry soups and seasoning, water retention agent in baked products, and texture improvement in meat and poultry products. Cassia is also er, foam stabilizer, and texturizing agent. used as an emulsifi Cassia plants Cassia is produced from the seeds of leguminous (Cassia tora and Cassia obtusifolia Locust bean gum a Locust bean gum, also galactomannan, is extracted from carob seed, Cerotonia siliqua molecular weight of 400,000 to 1,000,000 and it is comprised of long chains of galactose and mannose. with attached It consists of a D-mannopyranosyl backbone rise to synergistic D-galactopyranosyl units in 4:1 ratio giving gum is similar to activities with carrageenan. Locust bean chain distribution guar gum in structure but the uneven side forming a weaker makes it less soluble and less viscous, thus temperature, gel. Though locust bean gum swells at room (60 to its solubility is enhanced with higher temperature binding property, 90°C). Locust bean gum contributes water desserts, speeds smoothness, body and chewiness to frozen a binder in up curd formation in cheeses, and acts as sausages, salami, and bologna (13). galactose on every other mannose unit. Guar gum contains unit. Guar gum on every other mannose galactose with every second unit units 1-4-β-D-mannopyranosyl a molecular unit and with 1-6-α-D-galactopyrasyl bearing a cold hydrates rapidly in 220,000 (13). It weight of about changes in pH, neutral in solution, and water. It is resistant to most foods. Guar gum stops synergism it is compatible with body and chewiness in cheeses, and in cheeses, contributes cream. Guar also increases shelf resists heat shock in ice reduces hygroscopy in icing, and life in baked products, dressings and sauces. increases viscosity in Plant gums Plant gum Guar seed of is obtained from the Guar gum tetragonolobus Alginate Curdlan Alginates are extracted from different seaweeds (Macrocystis Curdlan is produced by pure culture fermentation pyrifera, L. digitata, or L. saccharina). They are composed of from a nonpathogenic and nontoxicogenic strain of chains of β-D-mannuronic and α-L-guluronic acids attached Agrobacterium biobar (identifi ed as Alcaligenes faecalis with 1→4 linkages (20). Though insoluble in water, alginates var. myxogenes) or Agrobacterium radiobacter. It is a high are able to readily absorb water. Alginates are useful as molecular weight polymer of glucose, β-(1→3)-. This gelling and thickening agents. The sodium salt of alginic water-insoluble polysaccharide has an unusual property acid, sodium alginate, is used in the food industry to increase of forming an elastic gel when its aqueous suspension viscosity and as an emulsifi er. Alginate is used in combination is exposed to heat (25). The linear structure of curdlan with carrageenan, locust bean, or xanthan and gellan gum makes it resistant to heat and pH between 2 and 10. in microencapsulation to enhance the viability of probiotics. Curdlan forms a retortable, freezable gel at both relatively Alginates are used in food products such as ice cream, high and low temperatures. At temperatures above 80 °C, mousse, and in slimming aids where they serve as appetite this gel is irreversible; however, at temperatures below 60 °C, suppressants. Alginates have a wide range of applications the gel is reversible. Curdlan powder can be stored for in food, drug delivery, tissue engineering, cell encapsulation, a long period, and, nutritionally, it is an inert dietary and transplantation (20). fiber (25).

Xanthan Plan exudate gums Xanthan is produced through fermentation by Gum arabic microorganisms, Xanthonmonas campestris (21), found on Gum arabic, the oldest and best known cruciferous vegetables such as cabbage and caulifl ower. of all natural gums, originates from Xanthan is made up of a β-D-glucose backbone with every exudate of trees of Acacia senegal. second glucose unit attached to a consisting Gum arabic is made up of of mannose, glucuronic acid, and mannose. The mannose and galactose in a 1:1 closest to the backbone has an acetic acid ester on ratio. It is a branched, neutral carbon 6, and the mannose at the end of the trisaccharide or slightly acidic, complex is linked through carbons 6 and 4 to the second. Xanthan polysaccharide obtained as gum is used extensively in the food industry because it a mixed calcium, magnesium, is soluble in cold and hot water, highly viscous at low and potassium salt (26). The concentrations,, thermally stable, and provides good backbone consists of 1,3-linked freeze-thaw stability (21). The negatively charged carboxyl β-D-galactopyranosyl units. The

Probiotics groups on the side chains cause the molecules to form very side chains are composed of two to viscous fl uids when mixed with water. is used fi ve 1,3-linked β-D-galactopyranosyl units, as an emulsifi er, a thickener for sauces, prevents ice crystal joined to the main chain by 1,6-linkages. Both the main and formation in ice cream, and a fat replacer in food (22). the side chains contain units of α-l-arabinofuranosyl, α-l- rhamnopyranosyl, β-D-glucuronopyranosyl, and 4-O-methyl- Agar b-d-glucuronopyranosyl, the latter two mostly as end-units. Agar gum is a water-soluble, gel-forming polysaccharide It also contains glycoprotein as a minor component (26). extract from agarophyte members of the Rhodophyta, Gum arabic is used as a stabilizer, thickener, and binder in composed of repeating agarobiose units alternating the making of confectionaries, soft drinks, food fl avorings, between 3-linked β- D-galactopyranosyl and 4-linked food sweeteners, and drugs (26). 3,6- anhydro-α-L- galactopyranosyl units (23). This disaccharidey may be marked or modifi ed in a number Gum tragacanth vol 24(4) - July/August 2013 - of ways by substitution of hydroxyl groups with sulfate Gum tragacanth is an exudate extracted from leguminous hemiesters and methyl ethers in various combination, and shrubs of the genus Astragalus. The main chain is formed more rarely with a cyclic pyruvate ketal as 4,6-O-[(R)-1- by 1,4-linked d-galactose residues with side chains of carboxyethylidene] acetal and sometimes by additional d- units attached to the main chain by 1,3 linkages. (23). The water-soluble tragacanthin is a neutral, highly branched arabinogalactan with a spherical molecular Gellan shape. Its structure probably consists of a core composed Gellan gum is a polysaccharide with a high molecular of 1,6- and 1,3-linked d-galactose with attached chains weight produced as a fermentation product by a pure of 1,2-, 1,3- and 1,5-linked l-arabinose in a molar ratio

Agro FOOD Industry Hi Tech culture of the microbe Sphingomonas elodea which of 3: 52: 29: 6: 5: 5 (27). Gum tragacanth is less brittle is then recovered with isopropyl alcohol (USDA.gov). and has a binding strength 8 to 10 times greater than Its structure consists of four linked monosaccharides, that of gum arabic. It is slightly acidic and composed of including one molecule of , one molecule of tragacanthin, bassorin, , and cellulose (28). Gum glucuronic acid, and two molecules of glucose (USDA. tragacanth has a large molecular weight of 840,000 gov). The molecular formula of gellan gum varies and forms strong gel at a lower concentration than gum depending on different factors. Gellan gum is a water arabic (29). Gum tragacanth solutions become thin at soluble, off-white powder with molecular weight greater high temperatures but regain viscosity upon coolint. This than 70,000 Da. It forms gels when positively charged ions characteristic indicates the non-degradable nature of the are added. Gellan gum is highly temperature resistant. gum. Solutions of gum tragacanth have longer shelf lives Its thickening property can be manipulated to give than other gums (28). impact on texture by adding potassium, magnesium, calcium, and/or sodium salts. Gellan gum has numerous uses in dairy products, bakery fi llings, confections, dessert HEALTH BENEFITS OF GUMS gels, frostings, icings and glazes, jams and jellies, low- fat spreads, microwavable foods, puddings, sauces, The application of gums in the food industry as stabilizing structured foods, and toppings (24). and thickening agents is well known. Some gums also serve

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Agro FOOD Industry Hi Tech - vol 24(4) - July/August 2013 Probiotics 13

6 The high fiber level level The high fiber cfu ⁄ g was maintained. Inulin being a cfu ⁄ g was maintained. Inulin being a 7 –10 6 in the presence of Figure 1. Growth of Lactobacillus reuteri in the presence of different gums during incubation at 37ºC for 16 hours. recently studied in our laboratory. In this study,Bbatches of recently studied in our laboratory. In this study,Bbatches of CFU/ml of probiotic cultures in food daily (33). Gums, like other (33). Gums, like other CFU/ml of probiotic cultures in food daily food ingredients that polysaccharides, contain the necessary in food and subsequently could support the survival of probiotics and impacting in the gut creating gastrointestinal balance, Several studies intestinal and other health benefits (33-35). viability of probiotics. use other polysaccharides toyenhance not been a study to However, to our knowledge, there has of probiotics in determine the impact of gums on viability et al. showed dairy foods. A study conducted by Ghasempour although minimum that zedo gum did not improve viability therapeutic level of 10 To create the required microbial balance that promotes health, that promotes health, To create the required microbial balance a minimum amount of 10 there is a need to ingest and maintain IMPACT OF GUMS ON PROBIOTICS as prebiotics (inulin and fructooligosaccharides), which impact impact which and fructooligosaccharides), (inulin as prebiotics have and pectin Guar for consumers. benefits health numerous in lower blood cholesterol by many studies to been found when their hypercholesterolemia with mild to moderate individuals gums (30). with these diet was supplemented ingredient in made it an important guar gum has also (80–85%) of reducing plasma foods capable of of functional the development lowering the risk of and subsequently and glucose levels cholesterol and diabetics, respectively (31). Diets cardiovascular disease gum arabic also showed elevated fecal supplemented with in decreased urea nitrogen concentration nitrogen excretion and renal failure (31). A study conducted among patients with chronic failure fed on diet supplement with gum rats with acute renal also improvement in renal function (31). Inulin arabic has shown an of a glucagon-like peptide (GLP)-1 hormone, induces production inulin and suppresses appetite. Dietary stimulates secretion, of colon cances in animal models. Dietary inhibits development effect shown to have an immunomodulatory inulin has also been secretory immunoglobulin (Ig) A and on the gut, increasing and decreasing the oxidative burst interleukin-10 production, activity of blood neutrophils (32). Lactobacillus reuteri The impact of different gums on the growth of Lactobacillus reuteri was modified M17 broth were prepared with 0.5 % (w/v) of one of the following gums: carrageenan, guar, carrageenan-maltodextrie, locust bean, pectin-dextrose, alginate, pectin, pectin- carrageenan, and inulin, sterilized at 121°C for 15 minutes and PRELIMINARY RESULTS recognized prebiotic was reported in several studies to enhance studies to enhance recognized prebiotic was reported in several (5, 7). growth and viability of probiotic bacteria allowed to cool to 42°C. Sterilized samples were inoculated with Lactobacillus reuteri strains at a final inoculum level of 3 log CFU/ml, incubated at 37°C for 16 h, serially diluted, and plated on MRS agar to obtain final bacterial counts. Our results showed higher bacterial counts in samples with gums compared to control (without gum). Bacterial population in the control sample increased from initial counts of 2.78 log CFU/ml to 7.16 log CFU/ml whereas samples with pectin increased from 3.3 log CFU/ml to 9.0 log CFU/ml (Figure 1). The bacterial population in samples with carrageenan- also increased from 3.1 log CFU/ml to 8.9 log CFU/ml. This study therefore indicates that pectin and carrageenan-maltodextrin could enhance the growth of Lactobacillus reuteri and subsequently improve the quality of functional food.

CONCLUSION

Gums have been used in diverse ways in the food industry as stabilizing and texture enhancing agents while improving the organoleptic quality of food. These properties of gums have been the main focus of research over the years. Gums have also been found to comprise cellulose, starches, sugars, oxidation products of these materials, salts, minerals, and sometimes protein. In addition, gums can bind with water forming a gel, a structure that supports the stability and activities of probiotic microorganisms. These properties could make gums a good candidate as growth enhancer for probiotics.wWe studied the impact of different gums 11. R. Whistler, T. Hymowitiz, Guar agronomy, production,

Probiotics on the growth of probiotics and found that pectin and carrageenan-maltodextrin could be added to different industrial use and , 1–96 (1979). food application to enhance the growth of Lactobacillus 12. C.L. Mantell, Economic , 3(1), 3–31 (1949). 13. P. Tomasik, Chemical and functional properties of food reuteri. However, with further research, gums could be saccharides (2004). used as prebiotics to promote the quality of functional 14. Anonymous, Dairy Foods, 98(12), 42– (1997). food through maintenance of viability and functionality of 15. L.A. Kuntz, Special Effects With Gums. Food Product Design. probiotics in food products. 1999. 16. I. Ratcliffe, P.A. Williams et al., Biomacromolecules, 6(4), 1977–86 (2005). ACKNOWLEDGEMENTS 17. T. Barclay, M. Ginic-Markovic et al., J. of Excipients and Food Chem, 1(3), 27–50. (2010). This work was supported by the USDA National Institute of 18. D. Goff, Dairy Ind. Int., 69(2), 31–3 (2004). vol 24(4) - July/August 2013

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