Effect of Food Composition on Probiotic Bacteria Viability

Chapter 17

Effect of Food Composition on Probiotic Bacteria Viability E. Sendra, M.E. Sayas-Barberá, J. Fernández-López and J.A. Pérez-Alvarez Departamento de Tecnología Agroalimentaria, Universidad Miguel Hernández de Elche, Orihuela Alicante, Spain

1 INTRODUCTION This chapter is a revised and updated version of a chapter from the first edition of this book by the same authors (Sendra et al., 2010). Intensive research is being run in the fields of probiotics and prebiotics, however, main topics regarding food formulation effects are quite similar and broader and more detailed data is available, with little changes on its fundamentals. Fermented milks flavored with juice is the most common presentation of probiotics. Other foods used to deliver probiotics are ice cream, cheese, candy, chocolate, chewing gum, oat or soy-enriched milk or directly oat- or soy-based products, infant formula, and fermented meats (Pennachia et al., 2006; Sendra, 2008). The only health claims for lactic acid bacteria (LAB) cultures endorsed by EFSA under article 13 of R1924/2006 are for traditional yogurt cultures and their ability to improve tolerance to lactose (EFSA, 2010). EFSA considers there is not enough scientific evidence to this date to substantiate the claims of probiotics. Consequently, there is an urgent need to provide consumers and authorities with the information on: (1) identification of the genus, species, and strain of the probiotic present in the product; (2) citations of published human studies on the effectiveness of the probiotic strain; and (3) assurance that the product contains the effective level of the probiotic through the end of shelf life as determined in the published studies (Douglas and Sanders, 2008). Regarding the probiotics bacteria used (Table 17.1), they are mainly bifidobacteria and lactobacilli. The main technological properties of probiotics (given that they should fulfill the desired biological effect and have no toxicity) are: l l l l l l l l

Oxygen tolerance Acid tolerance Bile tolerance Heat tolerance Ability to grow in milk Ability to metabolize prebiotics Not adversely affect product quality or sensory characteristics Stable to commercial conditions.

Many reviews provide comprehensive views on probiotics and prebiotics (Douglas and Sanders, 2008). The most commonly used prebiotics are fructans and resistant starches. The group of prebiotic ingredients will continue to expand as ingredient technology develops. Dosage of prebiotics ranges from 2.5 to 20 g resistant starch/day, 3-8 g fructans/day (Douglas and Sanders, 2008; Ananta et al., 2004); however substrate specificity may be important in considering prebiotic products and dose level. The International Scientific Association for Probiotics and Prebiotics (ISAPP, 2014) has settled on “Prebiotics target the microbiota already present within the ecosystem acting as a ‘food’ for the target microbes seen as beneficial.” A good prebiotic should: l l

be safe have good sensory properties

Probiotics, Prebiotics, and Synbiotics. http://dx.doi.org/10.1016/B978-0-12-802189-7.00017-4 © 2016 Elsevier Inc. All rights reserved.

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TABLE 17.1  Potentially Probiotic Cultures Used in Probiotic Foods or Probiotic Food Supplements Genera

Species

Lactobacillus

acidophilus/johnsonii/gasseri brevis delbrueckii subsp. bulgaricusa casei crispatus lactis paracasei fermentum plantarum rhamnosus reuteri salivarius

Bifidobacterium

adolescentis animalis/lactis bifidum breve essensis infantis longum

Bacillus

subtilisb clausiib

Enterococcus

faecalis faecium

Escherichia

coli strain Nissle

Pediococcus

acidilacti

Propionibacterium

freudenreichii

Saccharomyces

boulardii

Streptococcus

thermophilusa

a

Yogurt starter cultures. Spores.

b

l l l l l l l

be stable under heat and when dried withstand storage at room temperature resist degradation by stomach acid, mammalian enzymes, or hydrolysis be fermented by intestinal microbes selectively stimulate the growth and/or activity of positive microorganisms of the gut have proven health effects by clinical studies in humans be administered in adequate dose (5-8 g/day for fructans).

Today, only bifidogenic, nondigestible oligosaccharides (particularly inulin) and their hydrolysis product (oligofructose) and trans-galactooligosaccharides, fulfill all the criteria for prebiotic classification (Table 17.2). They are dietary fibers with a well-established positive impact on the intestinal microflora. Some prebiotics occur naturally in foods, but to exert prebiotic effects, it would be necessary to intake large amounts of these foods, so it is more popular to fortify foodstuffs with defined amounts of prebiotics. As most common prebiotics are water soluble and clear in water, they are easily incorporated in most foods and almost undetectable. This chapter reviews the impact of food formulation and food processing on the survival, growth, and activity of probiotics and prebiotics as well as food quality and stability.

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TABLE 17.2  Substances with Proven Prebiotic Properties Carbohydrate

Nondigestible

Fermentable

Selectively used

Inulin

Yes

Yes

Yes

Oligofructose

Yes

Yes

Yes

Transgalacto-oligosaccharides

Yes

Yes

Yes

Lactulose

Yes

Yes

Yes

Tagatosea

Yes

Yes

Yes

Isomalto-oligosacharides

Partially

Yes

Probably

Lactosacarose

NP

Yes

Probably

Xylo-oligosaccharides

NP

Yes

Probably

Soy oligosaccharides

Yes

Yes

NP

Resistant starchb

Yes

Yes

NP

NP not yet proven. a

Koh et al. (2013).

Depending on crystallinity of the polymorph (Lesmes et al., 2008). Adapted from Gibson et al. (2004).

b

2  EFFECT OF FOOD PROCESSING ON PROBIOTIC BACTERIA AND PREBIOTIC INGREDIENTS 2.1  Effect of Food Processing on Probiotic Bacteria Probiotic cultures are commonly included in fermented milk and it is widely accepted that there is the need to develop foods containing probiotic bacteria in sufficient numbers (over 7 log CFU/g). Such counts may be present till the end of shelf life; however, foods pose hurdles for the survival of probiotics such as acidity, oxygen stress, competition with other microorganism of the product, storage temperature, and moisture content (Stanton et al., 2003). There is a considerable strain variability for acid, bile, and oxygen tolerance. For some strains and manufacturing conditions, it is possible to use only the probiotic strain as an acid-producing strain, but it is more usually used in combination with supporter cultures. In non-dairy products, probiotics do not usually multiply, and so its stability is critical. Interactions of probiotics with starter bacteria should be evaluated prior to product development, especially metabolites released by starters: lactic acid, hydrogen peroxide, and bacteriocins (Mattila-Sandholm et al., 2002). A first step in the manufacture of probiotic foods is the availability of commercial starter cultures. The preparation of bulk cultures is difficult and may be reviewed in another chapter of this book; the most common presentations are freezedried powders, frozen concentrates, and spray-dried powder. The main challenges associated with the development of dried probiotic cultures are (Stanton et al., 2003): l

l

Freeze-drying: the loss of viability in this process is linked to temperature changes, phase changes, and drying as all tend to damage cell membranes and proteins. The use of cryoprotectants may reduce its impact on cell viability. Spray-drying: its cost is lower than that of freeze-drying; some species of lactobacilli and bifidobacteria undergo successful spray-drying. But many strains do not survive the spray-drying process well: present low survival rates, low stability under storage, or difficulties during rehydration. Controlled stress to stimulate cross-protection mechanisms and encapsulation may be applied to enhance bacterial survival to spray-drying stress.

Encapsulation of probiotics is a common practice in order to improve their performance under heat, spray-drying, and gastric acid exposure. Several techniques of encapsulation have been reported: spray-drying, extrusion, emulsion, and phases separation. Some possibilities are the encapsulation in calcium alginate beds, starch, or mixtures as gum acacia combined with gelatin and soluble starch. In any case the coating may be suited to the food application of the probiotics, and their protective effect against acidity, bile salts and heat has to be tested (Ananta et al., 2004; Stanton et al., 2003;

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Mattila-Sandholm et al., 2002; Champagne and Gardner, 2005). Hexopolysaccharide-producing strains of bifidobacteria may be naturally protected (Ding and Shah, 2007). The EU Commission financed a project on the processing effects on the nutritional advancement of probiotics and prebiotics (Ananta et al., 2004): cell viability, storage stability, and probiotic properties (acid/bile tolerance) could be influenced by fermentation technology and downstream processing. “Viability” is the percentage of viable cultures at the end of the shelf life of a food product and “vitality” is its ability to resist external stress conditions occurring in a food product during its shelf life, resulting in a higher survival rate during passage in the GI tract (Ananta et al., 2004). Both characteristics are relevant for the successful inclusion of probiotics in foods. We will focus on the conclusions of that study related to food product development. Critical environmental factors for probiotic survival in fermented foods are: oxygen stress, acidity, osmotic pressure, storage temperature, and co-culture competition. A high strain dependency has been reported in the response to such factors. l

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Oxygen stress: As probiotics are anaerobic, the use of impermeable containers and the presence of S. thermophilus, which acts as an oxygen scavenger, enhance probiotics' survival (Lourens-Hatting and Viljoen, 2001). Oxygen has a direct toxicity to probiotic cells, probably due to the intracellular production of hydrogen peroxides of certain cultures, particularly Lactobacillus delbrueckii ssp. bulgaricus (L. bulgaricus), which justifies the removal of this species from the starter cultures in order to enhance the survival of probiotic bacteria (Champagne and Gardner, 2005). The elimination of peroxide-producing strains and the addition of anti-oxidants (such as ascorbic acid) may be used in order to prevent oxygen derived toxicity. It has been reported that Propionibacterium freudenreichii produces extracellular growth stimulator(s) for bifidobacteria that effectively suppress the production of peroxide under anaerobic conditions (Mori et al., 1997). The effects of packaging materials on the survival of probiotics have been evaluated (da Cruz et al., 2007): the lower the level of oxygen the more favorable the survival of probiotics. The use of glass containers enhances the survival of probiotics due to their low oxygen permeability; however, the high costs and hazards of handling make it an inappropriate packaging for dairy products. The development of multilayer packaging with selective permeability and the inclusion of oxygen scavengers in the packaging material have potential application for probiotics foods. Acidity: Over-acidification in fermented milks is mainly due to strains of L. bulgaricus, which is the reason why this strain is sometimes reduced or suppressed from starter cultures (Lourens-Hatting and Viljoen, 2001; Champagne and Gardner, 2005). Probiotic lactobacilli are more acid tolerant than bifidobacteria although acid tolerance is straindependent (Lourens-Hatting and Viljoen, 2001; Champagne and Gardner, 2005; Donkor et al., 2006). For practical application, final pH must be maintained above 4.6 to prevent the decline in bifidobacteria populations (Lourens-Hatting and Viljoen, 2001). It has been suggested that over-acidification may be prevented by (i) heat shock (58 °C for 5 min) to yogurt before the addition of probiotic cultures, (ii) lowering storage temperature to less than 3-4 °C, (iii) adding whey proteins (Ananta et al., 2004) to improve buffering capacity of yogurt, as well as the proper selection of acid tolerant strains together with the reduction or even elimination of L. bulgaricus. Cheeses with higher pH than fermented milks may be better vehicles for probiotics (Sharp et al., 2008). When aged cheeses are to be used as carriers, it must be taken into consideration that high numbers of probiotic bacteria will be alive at the time of consumption, so either the strains are capable of growing during cheese ripening or they are inoculated at high levels during cheese manufacturing and survive all the ripening period. It seems that some adaptation mechanisms to acidity occur. It was observed that L. acidophilus suffered greater viability losses during storage of refrigerated yogurt when the probiotic was added to the yogurt prior to storage rather than added at the beginning of fermentation (Hull et al., 1984). Starter cultures: When mixing probiotics with starter cultures, every single strain needs to be tested together with the starter to evaluate competitive growth as well as stability during storage. Microbial metabolism releases to the medium bacteriocins which may reduce the growth of unwanted microorganisms (Galtz, 1992), as well as hydrogen peroxide and organic acids, all of which may decrease probiotic populations; but metabolism also releases vitamins, free amino acids, and may cause oxygen depletion (S. thermophilus) in which case probiotics survival is enhanced (LourensHatting and Viljoen, 2001). The addition of LAB together with probiotics slows down the growth of the probiotics (Champagne and Gardner, 2005) due to the fast growth of the LAB and the liberation of bacteriocins and other inhibitors. However, It seems that bifidobacteria perform better when it is inoculated separately from the starter cultures, whereas L. acidophilus performs better when it is added together with the traditional starter cultures (Lourens-Hatting and Viljoen, 2001). To enhance probiotic survival, several strategies may be used (Champagne and Gardner, 2005): (i) reduction of the inoculate starter with the risk of liberation of inhibitors from the probiotic bacteria that may inhibit the starters, or inhibit the probiotics between themselves; (ii) the use of starters with proteolytic or oxygen scavenging properties which may enhance bifidobacteria growth; (iii) the addition of soy-based substrates which enhances the

Effect of Food Composition  Chapter | 17  261

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growth of probiotic lactobacilli; (iv) promote sequenced growth, as for propionibacteria following the lactic fermentation, so they may use the lactate; sometimes associations between probiotic cultures may be beneficial; (v) interactions between probiotic yeasts and starters may be of interest and need to be explored. It is usual to avoid the inoculation of probiotics together with lactic cultures; addition of probiotics after fermentation, just before packaging, is the most common industrial practice in fermented milks (Stanton et al., 2003). Bacteriophages are not yet a big concern for probiotics, but the problem may arise if a given strain is extensively used. Preventive strategies may be (i) strain rotation, making sure the same biological effect on health of the new strain, which is rather difficult; (ii) adding the probiotic at the very end of the manufacturing process, which is costly. Inoculation practice also affects probiotic survival: higher inoculation of conventional starter cultures will lead them to dominate the fermentation and result in lower populations of probiotics in the final product, and high numbers of inoculation (up to 10-20%) favor the growth of probiotic bacteria (Lourens-Hatting and Viljoen, 2001). However, although counts of probiotic bacteria are desired to be high, low sensory scores have been reported for yogurts with excessive inoculation of L. acidophilus (2.33 g/100 g) as well as increased syneresis and higher a* and b* values (Olson and Aryana, 2008). Incubation temperature of 43 °C favors starter cultures whereas lower temperatures (37-40°) will favor the growth rate and survival of probiotic bacteria (Lourens-Hatting and Viljoen, 2001). Osmotic pressure effects are strain specific, most studies are in the usual range of probiotic foods formulation (from 0% to 10% sucrose addition) (Ananta et al., 2004). Salt tolerance needs to be tested when aged cheeses or fermented sausages are intended to be used as probiotic carriers. Heating effect: Heating under 45 °C is not detrimental to probiotics, but over 45 °C will destroy at least a fraction of the population (Champagne and Gardner, 2005). L. acidophilus is quite sensitive to heating, and in general, heat treatments over 65 °C are quite detrimental to probiotics. Microencapsulation or probiotic addition prior to aseptic packaging may be good options to protect against heat damage. The possibility of pre-adapting the probiotic cells with NaCl, bile salts, heating, and hydrogen peroxide has been suggested (Stanton et al., 2003). The previous heat treatment of the milk may affect the growth of probiotics: milk heated at 85-95 °C seems appropriate for the subsequent growth of probiotics. High-pressure homogeneization: An interesting finding is that milk treated by high-pressure homogenization when used for the manufacture of probiotic Crescenza cheese enhanced the viability of L. acidophilus and L. paracasei (Burns et al., 2008). Storage temperature: It seems that the ability to survive during processing and storage are not linked: Freezing does not seem to affect the ability to assimilate cholesterol, but this characteristic can be reduced in L. acidophilus following storage in unfermented milk at 5 °C for 21 days (Champagne and Gardner, 2005). The effect of refrigerated storage temperature (at 2, 5, and 8 °C) on the viability of probiotics (L. acidophilus, Bifidobacterium animalis subsp. lactis BB-12) in yogurt has been studied (Mortazavian et al., 2007). After 20 days, storage at 2 °C resulted in the highest viability of L. acidophilus, whereas for B. lactis, the highest viability was obtained when yogurt was stored at 8 °C. However, although bifidobacteria are less tolerant to low temperatures than lactobacilli, low storage temperatures favor the survival of probiotics as L. bulgaricus growth and post-acidification are restricted (Lourens-Hatting and Viljoen, 2001). Although tolerance to frozen stress is strain-dependent, most lactobacilli survive well in frozen storage. Ice cream, which is subject to freezing and has high pH, seems a good product for the delivery of probiotics. The survival of two probiotics (L. acidophilus La-5 and B animalis subsp. lactis Bb-12) inoculated at 4% dose in ice creams (4% fat) and stored at −25 °C for 60 days was studied (Magariños et al., 2007). Both probiotics had final counts over 6 log CFU/g. Frozen yogurts have more difficulties as low pH, freezing injuries, high temperatures of treatment, oxygen toxicity, or moisture content may reduce probiotic survival. Stanton et al. (2003) suggested several solutions: the addition of substances with cryoprotective properties which are usually present in ice-cream formulation (including casein, sucrose, fat, and glycerol), or even the use of microencapsulation technologies to aid in pH protection (encapsulation in gelatin and vegetable gums). Regular ice creams, nonfermented, have the advantage of having moderate pH. Type of substrate: Champagne and Gardner (2005) pointed out that milk type may influence probiotics survival. Probiotic cultures generally grow faster on synthetic media than in pure milk; that may be due to the low proteolytic activity of milk. Mixing nonproteolytic strains with a high proteolytic LAB may seem helpful, but the growth of LAB may overwhelm the probiotics and so milk is sometimes supplemented with yeast extract, a combination of substances (amino acids, minerals, ribonucleotides) or casein hydrolisates. This strategy works better for lactobacilli than for bifidobacteria where other factors such as redox conditions have greater impact. Regarding yeasts, although many types of yeast are unable to grow in milk, some yeasts have the ability to become established in dairy products and act as starters (i.e., Kefir starters). The potential use of yeasts as probiotics is of great interest due to their ability

262  PART | II  Probiotics in Food

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to grow at low pH, low water activities, low temperature, and high salt concentration. Stanton et al. (2003) pointed out that type and quantities of available carbohydrates and the degree of hydrolysis of milk proteins and lipids are essential variables for the propagation of microorganisms in milk and milk products. Dry-cured meat products have the advantage of not suffering heat treatment and having a moderate high pH which is beneficial for the growth and survival of probiotics. Growth promoting factors: Several bifidogenic factors have been reported: fructo-oligosaccharides (FOS), galactooligosaccharides, protein hydrolysates, and the co-culture of proteolytic species. Stanton et al. (2003) studied the inclusion of casein hydrolysates, yeast extracts, amino sugars, and peptides to improve the growth of bifidobacteria. As some strains do not grow well in milk, in such cases the presence of plant-based ingredients may improve the growth of probiotic cultures in milk (Stanton et al., 2003; Champagne and Gardner, 2005), the effect of the following plant ingredients on probiotic cultures growth has been evaluated: tomato juice, peanut milk, soy milk, buffalo whey/soy milk, rice, carrot, and cabbage juice, as well as casein peptone, whey protein, sucrose, papaya pulp, manganese, and magnesium ions, simple fermentation sugars or combinations of various. Lourens-hatting and Viljoen (2001) reported that growthpromoting factors in probiotic fermented milks that do stimulate L. acidophilus are: (1) combination of casitone, casein hydrolysate, and fructose; (2) whey protein concentrate, tomato juice, and papaya (due to simple sugars and minerals); (3) acetate. And to stimulate bifidobacteria: (i) cysteine, acid hydrolysates, tryptone; (ii) peptides and amino acids; (iii) Vitamins, dextrins, and maltose; (iv) 0.01% baker's yeast. And for both Lactobacilli and bifidobacteria: microencapsulation combined with the addition of oligosaccharides.

Evidence of the beneficial prebiotic-probiotic interaction in finished foods has been reported (Ananta et al., 2004). Inulin, oligofructose, and galacto-oligosaccharides were supplemented in the milk-based media for bifidobacteria. A 5% of oligofructose was the best growth promoter of bifidobacteria and also enhanced viability of bifidobacteria during the refrigerated storage of yogurts. In in vitro studies, it has been reported that the presence of up to 3% oligofructose improves the survival of probiotics during gastrointestinal transit but this effect was only found when yogurts were stored for four or more weeks. Lactitol and various types of FOS and other potential prebiotic carbohydrates were tested for feeding rats with probiotics and to evaluate the production of their short-chain fatty acids as estimators of the capability to improve colonic health and reduce the prevalence of colonic diseases. FOS performed better than lactitol as FOS metabolisms increased the release of propionic and butyric acid, whereas lactitol caused high proportions of acetic acid. The degree of polymerization and the crystallinity of the carbohydrates are of great importance for the total fermentability, as well as the short fatty acid pattern. However, the combination of the carbohydrates with certain probiotic strains may modify the fatty acid pattern.

2.2  Effect of Food Processing on Prebiotics Regarding modification of prebiotics due to food processing, Huebner et al. (2008) studied the effect of processing conditions (low pH, heating at low pH, and Maillard reaction conditions) on some commercial prebiotics (two types of FOS and two types of inulins). Prebiotic activity was stable at low pH and Maillard reaction conditions, but heating at low pH caused some hydrolysis of the prebiotics resulting in formation of sucrose, glucose, and fructose, and so no longer offering selective stimulation. This is a relevant finding for acidic foods such as yogurt, cultured dairy products, salad dressings, crackers, and others. Champagne and Gardner (2005) suggested that some changes in food processing steps may enhance probiotic survival: changes in incubation temperature, addition of enzymes (β-galactosidase) to enhance prebiotic use by probiotics, modifying the redox conditions (mainly by addition of l-cysteine or ascorbic acid), microencapsulation of probiotics, and others.

3  SENSORY ASPECTS OF PROBIOTIC, PREBIOTIC, AND SYMBIOTIC FOODS Most of the studies reflect that little or no effect on sensory properties is reported when probiotic bacteria are less than 10% of the total microbial population (Champagne and Gardner, 2005), as stated previously, an excess inoculation of L. acidophilus impairs yogurt sensory properties (Olson and Aryana, 2008). In the case of soy-based probiotic foods, fermentation with probiotics improves flavor due to the ability of probiotics to reduce pentanal and n-hexanal, which are responsible for the beany taste of soya. Most studies related to sensory impact of the inclusion of probiotics in dairy foods have been successful: in Minas cheese (Souza and Saad, 2009); inulin and oligofructose addition to ice cream together with L. acidophilus La-5 and B. animalis Bb-12 (Akalin and Erişir, 2008). Inulin yielded best results regarding rheological properties, whereas

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oligofructose was needed to ensure counts of bifidobacteria over 6 log CFU/g. A symbiotic ice cream containing 1% of resistant starch, encapsulated L. casei (Lc-01), and B. animalis subsp lactis (Bb-12) ensured increased survival rate of probiotic bacteria in ice cream over an extended shelf life (Homayouni et al., 2008). Chocolate products have been also tested as probiotic carriers: Chocolate mousse with L. paracasei and inulin maintained viability and sensory acceptability (Aragon-Alegro et al., 2007). Nebesny et al. (2007) reported that liophilized probiotics added to dark chocolate masses did not affect sensory attributes of chocolates. In tomato juice, King et al. (2007) reported that calcium alginate immobilized L. acidophilus enhanced cell viability and sensory quality of the juice.

4  FOOD FORMULATION EFFECTS ON PROBIOTIC VIABILITY Most of the literature regarding the effect of food formulation on probiotic survival is centered on dairy products, given that fermented milks are the most common vehicle for probiotics. Regular yogurts are fortified in milk non-fat solids; if they contain fruits they have additional carbohydrates in the form of sucrose, glucose, and fructose. Hussain et al. (2009) reported that it is commercial practice that probiotic yogurt contain higher fat, non-fat solids, and have higher pH than regular yogurt. The sugar used to sweeten yogurt does not affect the health benefits associated with the probiotics contained in the yogurt (Douglas and Sanders, 2008). Regarding dairy ingredients, total solids of milk and milk-whey mixture affected the viability of L. delbrueckii subsp. bulgaricus and L. acidophilus (Almeida et al., 2009). Champagne and Gardner (2005) reported that fat content does not affect probiotic stability during storage. Some ingredients may influence growth of the probiotic bacteria such as salts, sweeteners, aroma compounds, and preservatives.

4.1  Effects of Food Ingredients on Probiotic Viability 4.1.1  Carbohydrates: Prebiotics and Others The metabolic capacity to form acid from dietary sugars differed significantly between probiotic strains (Hedberg et al., 2008). Regarding the addition of carbohydrates to fermented yogurts and milks, Aryana and McGrew (2007) reported that the effect of chain length of inulins short (P95), medium (GR), and long (HP) chain lengths) on the characteristics of fatfree plain yogurt manufactured with L. casei has been studied. Flavor scores and yogurt syneresis decreased with increased chain length, although body and texture improved. de Souza Oliveira et al. (2009) reported that co-culture together with prebiotics addition is highly beneficial: Inulin (4%) has been used as a prebiotic to improve the quality and consistency of skim milk fermented by co-cultures and pure cultures of L. acidophilus, L. rhamnosus, L. bulgaricus, and B. lactis with S. thermophilus. It was reported that inulin addition to the milk increased co-cultures acidification rate, favored post-acidification, exerted a bifidogenic effect, and preserved almost intact cell viability during storage. In addition, S. thermophilus was shown to stimulate the metabolism of the other lactic bacteria. Contrary to co-cultures, most of the effects in pure cultures were not statistically significant. The same behavior was observed for lactulose (De Souza Oliveira et al., 2011). Tagatose, a low calorie monosaccharide epimer of fructose, has proven to enhance the growth of L. casei 01 and L. rhamnosus CG and to enhance their probiotic activity (Koh et al., 2013). The simultaneous effects of different binary co-cultures of L. acidophilus, L. bulgaricus, L. rhamnosus, and B. lactis with S. thermophilus and of different prebiotics (4% (w/w) maltodextrin, oligofructose, and polydextrose) on the production of fermented milk was studied (Oliveira et al., 2009). Fermented milk quality was strongly influenced by both the co-culture composition and the selected prebiotic. Polydextrose addition led to the highest post-acidification. Probiotic counts were stimulated by oligofructose and polydextrose, and among these B. lactis always exhibited the highest counts in all supplemented milk samples. However, other studies (de Castro et al., 2009) reported that oligofructose did not show any significant influence on fermentation time, acidity, syneresis, and probiotics survival of fermented milks. The addition of prebiotics to cream cheeses has been successful. Cardarelli et al. (2008) reported that the addition of inulin, oligofructose, and oligosaccharides from honey to probiotic petit-suisse containing B. animalis subsp. lactis and L. acidophilus yielded high probiotic counts for all formulations, but best sensory scores for the combination of inulin and oligofructose. Inulin has been successfully inoculated in a probiotic fresh cream cheese (L. paracasei) obtaining good sensory scores (Buriti et al., 2008). Sugar and aloe vera, sugar and chocolate, and sugar and jam have been tested on probiotic sweet whey cheeses (Madureira et al., 2008). All combinations yielded high survival rates. Recently, Varga et al. (2014) reported that the addition of honey (5%) to camel milk enhanced the viability of B. animalis ssp. lactis during cold storage in co-cultured fermented milk.

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4.1.2 Proteins The effect of the addition (1-2%) of a protein-based fat replacer on the growth and metabolic activities of yogurt starters (S. thermophilus and L. delbrueckii ssp. bulgaricus) and probiotics (L. casei, L. acidophilus, and B. longum) has been tested by Ramchandran and Shah (2008). The addition of the fat replacer resulted in significantly improved growth of S. thermophilus and B. longum but inhibited that of L. casei, L. acidophilus, and L. delbrueckii ssp. bulgaricus. Supplementation with whey protein concentrate (1.5%) in reduced fat yogurt increased the viable counts of S. thermophilus, L. delbrueckii subs. bulgaricus, and B. animalis by 1 log cycle in the first week of storage when compared to control sample. Similar improvement in the growth of both yogurt bacteria and B. animalis was also obtained in the fullfat yogurt containing 3% milk fat and no supplement (Akalin et al., 2007).

4.1.3  Yeast Extracts Yeat extracts have been successful in increasing probiotic survival: L. reuteri RC-14 and L. rhamnosus GR-1 survival was tested on low fat yogurt (1% fat) enriched with: 0.33% yeast extract (T1); 0.4% inulin (T2); 0.33% yeast extract and 0.4% inulin (T3); and one with no additives (T4) (Hekmat et al., 2009). L. rhamnosus GR-1 survived better than L. reuteri RC-14 and that survival was highest in media including 0.33% yeast extract (T1 and T3).

4.1.4  Addition of Fruit and Plant Products Several fruit ingredients seem to enhance probiotic survival. The authors (Sendra et al., 2008) reported that the addition of citrus fiber to probiotic fermented milks stimulated the growth and survival of L. casei and L. acidophilus, whereas bifidobacteria was unevenly affected. The co-culture with conventional starters favored the survival of probiotics. A probiotic coconut flan, with high counts of probiotics (B.animalis subsp lactis, L. paracasei, and B. lactis + L. paracasei) and high sensory scores was successfully developed (Corrêa et al., 2008). In 2011, Espirito-Santo et al. reviewed the influence of fruit matrices on probiotic viability. Both dairy and non-dairy (mainly fruit) products were reviewed, as well as viability in both conditions: the food and the gastrointestinal tract. Most of the studies on fruit additions into dairy products showed that fruits (mango, berries, banana, strawberry, passion fruit, lemon … among others) either maintained or enhanced the viability of probiotics in the dairy food. Only studies when fruits promoted a high release of lactic and acetic acids were the viability of some probiotics reduced. Green tea and other plant extracts rich in phenolic compounds have also been added to probiotic milks. Such extracts affect probiotic viability (Najgebauer-Lejko, 2014) depending on the extract (phenolic composition), the strain, the presence of co-cultures (acidification rate and phenolics metabolism), and the concentration of plant extract on the final product.

4.1.5  Soy and Pulse Ingredients Soy-based foods and soy ingredients are increasingly demanded by consumers due to their healthy image: they target preand post-menopausal women, milk allergies, or intolerants. Many studies report interactions among soy components and probiotic bacteria. Pham and Shah (2008a) reported that the addition of skim milk powder for the manufacture of fermented soymilk (SM) supplemented with probiotic bacteria (L. acidophilus 4461, L. acidophilus 4962, L. casei 290, and L. casei 2607) increased microbial counts of probiotics and enhanced the biotransformation level of isoflavone glycosides (IG) to isoflavone aglycones (IA). The same authors (Pham and Shah, 2008b) reported that L. acidophilus 4461, L. acidophilus 4962, L. casei 290, and L. casei 2607 presented higher activity to hydrolyze IG to biologically active forms—IA—in SM when 0.5% (w/v) of lactulose was added. Probiotic counts were also increased. The reverse option, the supplementation of skim milk with soy protein isolate together with six probiotic organisms (L. acidophilus 4461, L. acidophilus 4962, L. casei 290, L. casei 2607, B. animalis subsp. lactis bb12, and B. longum 20099), enhanced lactose utilization acetic acid production but slightly reduced the lactic acid production and the growth of probiotic microorganisms (Pham and Shah, 2008c). The same effect was observed for B. animalis A and B (Pham and Shah, 2007). Three probiotics: L. acidophilus LAFTI® L10, B. lactis LAFTI® B94, and L. casei LAFTI® L26 were evaluated by Donkor and Shah (2008) for the manufacture of fermented SM and production of β-glucosidase for hydrolysis of isoflavone to aglycones and observed that all of them produced β-glucosidase. Fermenting calcium-fortified SM with L. acidophilus ATCC 4962, ATCC33200, ATCC 4356, ATCC 4461, L. casei ASCC 290, L. plantarum ASCC 276, and Lactobacillus fermentum VRI-003 can potentially enhance the calcium bioavailability of calcium-fortified SM due to increased calcium solubility and bioactive IA enrichment (Tang et al., 2007). Soy and cows' milk yogurts prepared including a yogurt starter in conjunction with either the probiotic bacteria L. johnsonii NCC533 (La-1), L. rhamnosus ATCC 53103 (GG) or human-derived bifidobacteria have been studied (Farnworth et al., 2007). The presence of the probiotic bacteria did not affect the growth of the yogurt strains. The probiotic

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bacteria and the bifidobacteria were using different sugars to support their growth, depending on whether the bacteria were growing in cows' milk or soy beverages. Zare et al. (2012) studied the effect of pulse ingredients addition on the acidification rate of several probiotics and yogurt starters. Lentil and soy flour enhanced acidification rates, pea protein, chickpea flour, and pea fiber also favored acidification by probiotic bacteria. Starter cultures were only slightly favored by pulse enrichment.

4.1.6  Non-Dairy Products Several non-dairy products may be good carriers of probiotic bacteria such as fermented vegetable drinks, fermented sausages, cereal-based fermented drinks, as well as pharmaceutical preparations containing probiotic bacteria. Non-dairy probiotics are a growing field; there is a great demand especially from those allergic to milk, as well as those populations that are not used to dairy products but have a wide variety of fermented cereal, starchy, and starch/cereal fermentations such as Africans (Franz et al., 2014). Several commercial probiotic strains (L acidophilus, L. casei, and B. animalis ssp. lactis) have proven amylolytic activity, however in order to achieve acidification rate and yogurt-like characteristics, their association with amylolytic L. fermentum and L. plantarum was needed (Espirito-Santo et al., 2014). Traditional African fermented foods can be classified by raw material in the following groups (Olasupo et al., 2010): (a) non-alcoholic cereals, (b) starchy root crops, (c) animal proteins (milk and fish), and (d) vegetable proteins. Main potential probiotics associated with fermented African foods are L. plantarum and L. fermentum (Franz et al., 2014). Probiotic viability in the presence of fruit juices is proven to be strain-dependent (Espırito-Santo et al., 2011): Natural fruit juices may inhibit some strains while enhancing others. Juices from tomato, beetroot, carrots, and other horticultural products are good vehicles for probiotics, probably related to their carotenoid content. Kedia et al. (2007), in a cereal-based fermented beverage, reported the presence of yeast enhanced the growth of probiotic LAB. Other food grade formulas may also include probiotics: fruit coatings have been successfully formulated to be carriers of probiotic bacteria (Tapia et al., 2007) like edible coatings for apple and papaya cuts containing B. animalis ssp. lactis Bb-12 based on alginate- (2% w/v) or gellan (0.5%). Cereal-based foods are a group of fermented foods of special interest regarding formulation. The effects of the addition of β-glucan from cereals (oat and barley) on growth and metabolic activity of B. animalis ssp. lactis (Bb-12™) compared to unsupplemented and inulin supplemented controls have been investigated by Vasiljevic et al. (2007). Oat β-glucan addition resulted in improved probiotic viability and stability comparable to that of inulin. It also enhanced lactic and propionic acid production. The barley β-glucan addition suppressed proteolytic activity more than that from oats. These improvements were hindered by greater syneresis likely caused by thermodynamic incompatibility. The addition of β-glucan may be possible at or below 0.24 w/w% to avoid phase separation. Kedia et al. (2008) tested oat-bran, whole, and white oat flour as substrates for L. plantarum for the production of a probiotic beverage. The highest probiotic cell concentration was observed in white flour (9.16 log CFU/mL) and the lowest in the bran sample (8.17 log CFU/mL). Saarela et al. (2006) evaluated some fibers (oat flour, apple fiber, wheat dextrin, polydextrose, and inulin) as carriers for probiotic bacteria L. rhamnosus and evaluated the stability of probiotics during freeze-drying and further use in apple juice and chocolate-coated breakfast cereals. The best storage stability was obtained with wheat dextrin and polydextrose. In the probiotic apple juice, which is an acidic food, oat flour with 20% β-glucan had a protective effect on fresh L. rhamnosus, this effect was not observed for freeze-dried bacteria. In chocolate-coated cereals, a low water activity food, polydextrose, and wheat dextrin provided the best probiotic protection, for 7 and 3 months, respectively. It is possible to use fibers to maintain the viability and stability of probiotics, although this function seems to be application dependent (pH, food composition, water activity…) and species dependent as in a study by Guergoletto et al. (2010) on L. casei adhesion to inulin, oat-bran, unripe banana, and apple fiber, oat-bran was shown to be the carrier that promoted greatest viability during cold storage. Chestnut extracts have proven to enhance acid tolerance of probiotic strains in the form of a dried ingredient and also to carry and maintain the viability of L. rhamnosus in a dried powder formula for the preparation of a chestnut mousse (Romano et al., 2014).

4.2  Effects of Food Formulation on Probiotic Activity Probiotic foods should meet international standards and should contain appropriate microorganisms in shelf stable formulations that have been shown in well-designed clinical studies to confer defined health benefits on the consumer (Reid, 2008); so, it is crucial to prove the effect of the ingredients in the activity of probiotics and prebiotics. Prebiotic compounds may also contribute to the immunomodulatory properties of probiotic bacteria: in a study using L. rhamnosus GG and B. lactis, Bb-12 plus 10 g of inulin enriched with oligofrutose in colon cancer patients, several colorectal cancer biomarkers were

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altered favorably by symbiotic intervention (Roller et al., 2007; Rafter et al., 2007). There have been reported beneficial effects of probiotics in which fermentation of mannitol, FOS, and inulin promoted the production of formic, lactic, and butyric acids, respectively, and correlated with cholesterol removal (Liong and Shah, 2005a,b,c). The administration of certain prebiotics together with the probiotics seems to be important in modulating gut microbiota and abdominal organ health: in animal studies, Le Leu et al. (2003) observed that the administration of resistant starch (which escapes small intestinal digestion by microbes), in the form of high amylase corn starch, decreased intestinal pH, increased short-chain fatty acids formation, and induced an apoptotic response to a genotoxic carcinogen. However, several studies report no enhancement of the beneficial effect by administration of symbiotics (Larkin et al, 2007; Smith et al., 2008). A symbiotic with L. fermentum and FOS was investigated to alleviate mucositis in rats. L. fermentum BR11 consumption reduced inflammation of the upper small intestine. However, Smith et al. (2008) reported that its combination with FOS did not confer any further therapeutic benefit for the alleviation of mucositis. Larkin et al. (2007) reported that the consumption of probiotic yogurt or resistant starch (as prebiotic) in combination with high soy intake had no effect on isoflavone bioavailability, probably indicating the gut microflora were not modified in a manner that significantly affected isoflavone bioavailability or metabolism.

5  CONCLUSIONS AND FUTURE PROSPECT The consumption of designed healthy foods is included in the trend toward long-term prevention of illness. It is in this scenario where probiotic, prebiotic, and symbiotic foods fit. Probiotics need to have clinically proven health benefits and be able to withstand large-scale cultivation, concentration, incorporation and food manufacturing, and storage. Prebiotics, as well as probiotics doses and types, need to be established to ensure that health benefits are accomplished, so reliable clinical data is needed to determine if the probiotic counts and prebiotic doses used are sufficient for health benefits. The influence of the carrier must be examined, having in mind the main constraints for the survival of probiotics: low oxygen tolerance and low acidity tolerance; and the convenience of the inclusion of prebiotics or growth promoting factors in the formulation of probiotic foods. In the near future, genomics will provide details on the physiological performance of health-promoting strains in a variety of environments that may lead to novel solutions for current and future challenges on probiotic foods development. A potential major problem of probiotics was the misuse of the term, as the term “probiotic” should be only applied to strains fulfilling the outlines of the guidelines of the World Health Organization (FAO/WHO, 2002). Recently, the ISAPP launched recommendations on the use of the term probiotic (Hill et al., 2014) which may be expected to clarify this situation.

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Liong, M.T., Shah, N.P., 2005a. Production of organic acids from fermentation of mannitol, fructooligosaccharide and inulin by a cholesterol removing Lactobacillus acidophilus strain. J. Appl. Microbiol. 99 (4), 783–793. Liong, M.T., Shah, N.P., 2005b. Optimization of cholesterol removal, growth and fermentation patterns of Lactobacillus acidophilus ATCC 4962 in the presence of mannitol, fructo-oligosaccharide and inulin: a response surface methodology approach. J. Appl. Microbiol. 98 (5), 1115–1126. Liong, M.T., Shah, N.P., 2005c. Optimization of cholesterol removal by probiotics in the presence of prebiotics by using a response surface method. Appl. Environ. Microbiol. 71 (4), 1745–1753. Lourens-Hatting, A., Viljoen, B.C., 2001. Yogurt as probiotic carrier food. Int. Dairy J. 11, 1–17. Madureira, A.R., Soares, J.C., Pintado, M.E., Gomes, A.M.P., Freitas, A.C., Malcata, F.X., 2008. Sweet whey cheese matrices inoculated with the probiotic strain Lactobacillus paracasei LAFTI® L26. 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