Critical Reviews in Food Science and Nutrition

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Fermented Milks and Milk Products as Functional Foods—A Review

V. K. Shiby & H. N. Mishra

To cite this article: V. K. Shiby & H. N. Mishra (2013) Fermented Milks and Milk Products as Functional Foods—A Review, Critical Reviews in Food Science and Nutrition, 53:5, 482-496, DOI: 10.1080/10408398.2010.547398 To link to this article: https://doi.org/10.1080/10408398.2010.547398

Accepted author version posted online: 01 Aug 2012. Published online: 01 Aug 2012.

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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=bfsn20 Critical Reviews in Food Science and Nutrition, 53:482–496 (2013) Copyright C Taylor and Francis Group, LLC ISSN: 1040-8398 / 1549-7852 online DOI: 10.1080/10408398.2010.547398

Fermented Milks and Milk Products as Functional Foods—A Review

V. K. SHIBY1 andH.N.MISHRA2 1Freeze Drying and Animal Products Technology Discipline, Defence Food Research Laboratory, Siddharthanagar, Mysore, India 570011 2Department of Agricultural and Food Engineering, Post Harvest Technology Centre, Indian institute of Technology, Kharagpur, India

Fermented foods and beverages possess various nutritional and therapeutic properties. Lactic acid bacteria (LAB) play a major role in determining the positive health effects of fermented milks and related products. The L. acidophilus and Bifidobacteria spp are known for their use in probiotic dairy foods. Cultured products sold with any claim of health benefits should meet the criteria of suggested minimum number of more than 106 cfu/g at the time of consumption. Yoghurt is redefined as a probiotic carrier food. Several food powders like yoghurt powder and curd (dahi) powder are manufactured taking into consideration the number of organisms surviving in the product after drying. Such foods, beverages and powders are highly acceptable to consumers because of their flavor and aroma and high nutritive value. Antitumor activity is associated with the cell wall of starter bacteria and so the activity remains even after drying. Other health benefits of fermented milks include prevention of gastrointestinal infections, reduction of serum cholesterol levels and antimutagenic activity. The fermented products are recommended for consumption by lactose intolerant individuals and patients suffering from atherosclerosis. The formulation of fermented dietetic preparations and special products is an expanding research area. The health benefits, the technology of production of fermented milks and the kinetics of lactic acid fermentation in dairy products are reviewed here.

Keywords Fermented milks, L. acidophilus, bifidobacteria, probiotics, lactic acid bacteria

INTRODUCTION promoting entity. Alternatively, concentration of adverse com- ponents may be reduced or there may be a partial interchange Healthiness is one of the most frequently mentioned reasons between toxic and beneficial ingredients. Functional food may behind food choices in EU countries (Lappalainen et al., 1998). be considered as a therapeutic aid without prescription. The Individuals are considered responsible for their own state of term nutraceutical was coined by Stephen De Felice, founder of health. Diseases are seen more and more as consequences of the Foundation for Innovation in Medicine, in 1989. He defined consumer’s own behavior rather than the result of environment a nutraceutical as a food, dietary supplement or medical food (Ogden, 1998). Diet may strongly influence an individual’s risk that has a medical or health benefit including the prevention or of obesity; cardiovascular diseases, cancer, and other life style treatment of disease. Today the term nutraceutical is often used related diseases. Traditionally, the healthfulness has been as- interchangeably with functional food. An official definition for sociated with nutritional factors such as fat, fiber, salt, and vi- the term functional foods is lacking in USA and Europe. Ac- tamin contents of food. In addition to traditional healthiness cording to EU concerted action “a food can be considered as food may contain single components that may have a positive functional if it has been satisfactorily demonstrated to affect impact on our well-being. Products that are claimed to have beneficially one or more target functions in the body beyond special beneficial physiological effects in the body are usually adequate nutritional effects in a way that is relevant to either called functional foods (Bellisle et al., 1998; Roberfroid, 1999; an improved state of health and well-being and/or a reduction Hardy, 2000; Kwak and Jukes, 2001). A particular food may be of risk of disease.” These functional foods may also be used as made more functional by increasing or adding a potential health conventional foods (Diplock et al., 1999). There are several methods of manufacturing functional foods, based either on the method used to produce them or on their Address correspondence to Prof. H. N. Mishra, Department of Agricultural purpose. Functional foods may be processed by modification and Food Engineering, Post Harvest Technology Centre, Indian Institute of Technology, Kharagpur-721302, India. E-mail: [email protected] or they may be fortified with different substances and the

482 FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODS—A REVIEW 483 functionality of a product can be targeted to a special disease or face Methodology has been successfully used in modeling of just to improve overall well being (Roberfroid, 1999). Informa- acidification rate and growth of starter bacteria as a function tion relating health effects and the ways of communicating such of parameters such as fermentation temperature, fat and solid information are the key factors because the health effect cannot content, inoculum size, and cocci/rods ratio on the fermenta- be perceived from the product itself (Urala et al., 2003). Since tion process of yoghurt (Torriani et al., 1996). The pH mea- 1989, the nutraceutical or functional food industry has evolved surement method described by Spinnler and Corrieu (1989) is into a market worth $20.2 billion in 2002. Functional beverages widely used in the determination of acidification kinetics during reached $ 10.35 billion sales in 2002, up 10.7% and are projected gel formation. Several research workers have tried to optimize to reach $15.9 billion by 2010. A variety of functional dairy the acidification process for manufacture of fermented prod- foods are conquering the market worldwide. Examples include ucts and developed models to predict the acidification kinetics. probiotic, prebiotic, and symbiotic products, low cholesterol Mathematical models have been used to predict the influence fresh milk omega-3-milk, low lactose, and lactose free products of fermentation operating temperatures on cell growth rate, cell and milk products that can control or manage hypertension and concentration, substrate utilization rate and lactic acid produc- immune functions. The market for functional foods, nutraceu- tion rate. As for models, a number of them, purely or partially ticals, wellness foods, and beverages is fast growing and it is empirical, have been described in literature. Product inhibition estimated that the functional food industry could almost dou- is well-established feature of lactic fermentations. ble by 2007. An increasing sector of the public is quickly aging Boonmee et al. (2003) developed a model for batch and and purchasing functional food products. Today’s consumers are continuous fermentation of Lactococcus lactis strain NZ133. more concerned with weight loss and management, heart health, The growth kinetics of L. lactis is predominantly influenced by eye health, cancer, increasing energy and stamina, eye health, lactose limitation and lactate product inhibition with the growth and improved memory. Several categories of functional foods of this particular strain showing a relatively high sensitivity to and beverages have been developed to meet these challenges. lactate inhibition. The Leudeking-Piret equations for growth The scope of the present article is to provide an overview and lactate production were successfully incorporated into the of the kinetics of lactic acid fermentation in dairy products, model. The Leudeking–Piret model is given as the technology and nutritional significance of fermented milks popular in different countries, and the therapeutic properties of dx = μx (1) probiotic organisms involved in their manufacture. dt

dp dx LACTIC ACID FERMENTATION = α + βx dt dt (2) Fermentation Kinetics When this is modified to include the effects of lactose limi- tation and inhibition, as well as lactate inhibition the model is Mathematical analysis of the biokinetics of functional starter outlined as in Equatons (3)–(5). cultures can yield precious information about the relationship The rate of biomass production between the food environment and bacterial functionality and      may contribute to optimal strain selection and process design. dx s P − P K This may result in better process control, enhanced food safety = − ix × ix x dt K + s 1 P − P K + s (3) and quality, and reduction of economic losses. Kinetic data are sx mx ix ix needed to understand the fermentation process and to develop continuous fermentation systems. Lactic acid bacteria (LAB) The rate of lactate production have long been used in food industry as starter cultures for   the manufacture of fermented meat and dairy products. The dp dx s = α + qp,max key metabolite produced during such fermentation reactions is dt dt Ksp + s lactic acid, which is a commercially valuable product with ap-    plications in food manufacturing and pharmaceutical industries. p − Pip Kip × 1 − x (4) Both chemical and biotechnological methods are available for Pmp − Pip Kip + s lactic acid production, but the lactic acid from fermentative pro- cesses has increased its market share owing to the preference The rate of lactose utilization of consumers to products of natural origin (Chahal, 1989). The      commercial significance of dairy fermentation industry which ds s p − Pis Kis = qs,max 1 − × x (5) incorporates production of cheeses, fromage frais, sour cream, dt Kss + s Pms − Pis Kis + s etc. is well recognized and ranks second only to the alcoholic beverages (Daly et al., 1998). The processes for wood utiliza- where, tion can be directed toward lactic acid production (Moldes et al., −1 1999). The kinetics of milk fermentation by starter cultures Ki is lactate inhibition constant (gl ), −1 has been studied by several research workers. Response Sur- Ks is lactose limitation constant (gl ), 484 V. K. SHIBY AND H. N. MISHRA

P is lactate concentration (gl−1), 1996; de Vos, 1996). The homofermentation and heterofermen- −1 Pi is threshold lactate concentration (gl ), tation pathways are shown in Fig. 1. Both rods and cocci follow −1 Pm is maximum lactate concentration (gl ), different pathways of carbohydrate fermentation and achieve −1 −1 qp,max is maximum specific lactate production rate (gg h ), end products, which are at least 90 or 50%, lactate in the case −1 −1 qs,max is maximum specific lactose utilization (gg h ), of homo and hetero fermentative species respectively. Lactose s is lactose concentration (gl−1), is transported across the cell membrane either by lactose per- x is biomass concentration (gl−1), meate system or by phosphoenol pyruvate dependent phospho a is growth associated constant in Leudeking–Piret model transferase system (Lac PEP-PTS). Depending on the transport (gg−1), mechanism involved, unphosphorylated lactose (Lac permease) b is nongrowth associated constant in Leudeking–Piret model is hydrolyzed into glucose and galactose by β-galactosidase (gg−1h−1), or phosphorylated lactose is hydrolysed by phosphorylated β- μ is specific growth rate in Leudeking-Piret model (h−1), and galactosidase into glucose and galactose-6-phosphate. All of −1 μmax is maximum specific rate (h ) the dairy lactococci and some mesophilic lactobacilli oper- ate the Lac PEP-PTS system (Fig. 2) while leuconostoc and some industrially significant thermophilic organisms; S. ther- Common Organisms and Pathways mophilus and Lb delbrueckii subsp. bulgaricus possess a perme- ase system (Fig. 3) Subsequent metabolic pathways include the The group of LAB plays a central role in fermentation pro- glycolytic Embden-Meyerhof-Parnas(EMP), the phosphoketo- cesses, and has a long and safe history of application and con- lase pathways for glucose, the tagatose-6-phosphate pathway sumption in production of fermented foods and beverages. (Ray, for galactose-6-phosphate and the Leloir pathway for galac- 1992; Wood and Holzaphel, 1995; Wood, 1997; Caplice and tose (when it is not transported back into the environment). Fitzgerald, 1999) During fermentation of lactose to lactic acid LAB containing aldolase, that is, Streptococci, Pediococci, and the acidity of the milk rises and the growth conditions for mi- obligately homofermenative and facultative heterofermentative croorganisms other than LAB become increasingly unfavorable Lactobacilli have the homolactic fermentation with lactate as the (Driessen and Puhan, 1988). Reid et al. (2002) have studied the exclusive end product. LAB containing phosphoketolase can be LAB in fermented foods in South East Asia. They discussed divided into two groups. The first, that is, Leuconostocs and obli- the distribution and application of LAB in various products gately hetero fermentative lactobacilli, follows “6P—gluconate such as fermented milk, meat, fish, vegetable, or plant prod- pathway” with production of equimolar amounts of CO2, lac- ucts. Significant advances have been made in elucidating the tate and acetate. The others follow “bifidus pathway” with the genetic, biochemical land physiological basis of many of the formation of acetate and lactate in a molar ratio of 3:2. key technological traits of these bacteria (Daly et al., 1998). Among the LAB, lactose metabolism in lactococcus is prob- LAB are constituted of heterogenous group of Gram-positive ably the best understood in terms of its biochemical and ge- bacteria with a strictly fermentative metabolism (Temmermman netic make-up and also in terms of its regulation. The complete et al., 2004). One of the most important functional properties metabolic pathway is known and several important genes have common to all LAB is their ability to convert lactose and a va- been characterized (de Vos and Vaughan, 1994). The genes en- riety of other carbohydrates into the primary end product, lactic coding the PEP-PTS system and the tagatose pathway are all acid, by fermentation. The ability of LAB to transform food plasmid located in a single operon under the control of the into new products and to exert antagonistic action toward harm- repressor gene lacR. Another operon has also been identified ful microorganisms make them suitable for both domestic and in Lactococcus encoding a number of glycolytic enzymes The industrial productions Servin (2004). The LAB involved in the fermentative action of specific LAB strains may lead to the re- production of fermented milks are distributed in several phe- moval of toxic or antinutritive factors such as galactose and notypic and genotypic groups. These groups are characterized lactose from fermented milks to prevent lactose intolerance and by different nutritional requirements, metabolic, cultivational, accumulation of galactose (Wouters et al., 2002). and technological properties. Several authors have reported that LAB present in fermented milks may belong to species of Lac- Fermentation Process and Health tobacillus, Streptococcus, Pediococcus, Leuconostoc, and Lac- tococcus genera (Aucloir and Mocquot, 1974 ; Cogan, 1985; Fermented milks constitute important part of our food. In an- Gilliland, 1985; Sandine, 1985; Schleifer et al., 1985). The role cient days, human beings realized that fermentation occurred, of interaction between yeasts and LAB in African fermented without, however, knowing their cause. Originally milk fer- milks has been reviewed by Narvhus and Gadaja, 2003. mented spontaneously, and the reuse of fermentation vessels There are two main fermentation pathways in LAB; the ho- and tools contributed to a certain repeatability and stability in molactate pathway in which lactic acid is the major end product the fermentation process. This led to the use of specific microor- and heterolactate pathway in which other compounds such as ganisms for the manufacture of more or less refined products. acetic acid, carbon dioxide, ethanol etc. are produced in addi- Different countries or even different parts of the same country tion to lactic acid (Huggenholtz, 1993; Cocaign-Bous-quet et al., developed their own fermented milks. The best-known product FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODS—A REVIEW 485

Glucose

Fru-1,6 P Fru-6P Glc-6P

Acetyl-P+ Erythrose-4P 6P-Gluconate Fru-6P

Heptose-P Xylulose-5P +CO2 aldolase

+ Pentose-P

Phosphoketolase

Triose-3P Acetyl-P+ Triose-3P Triose-3P + Acetyl- P

ADP ADP ATP Pyruvate ATP Pyruvate Pyruvate

Acetate (Ethanol ) Lactate Acetate Lactate Lactate

Bifidus pathway 6P-Gluconate pathway Glycolysis

Phosphoketolase pathways

HOMOFERMENTATION HETEROFERMENTATION

Figure 1 Main pathways of hexose fermentation in lactic acid bacteria (Kandler, 1983). is the thermophilic fermented milk, yoghurt, which has enjoyed (Ram and Bhavadasan, 2002) LAB are natural inhabitants of increased popularity in the last three decades. The role of living gastrointestinal tract. These microorganisms have a number of microorganisms in fermented dairy products has gained consid- traits which make them particularly attractive to be used as erably increased interest for both the consumer and the producer. “probiotic”. During fermentation of lactose to lactic acid the Nature has provided a certain degree of beneficial association acidity of milk rises and the growth conditions of microorgan- for humans through the activity of lactic LAB. These bacte- isms other than LAB become increasingly unfavorable. Apart ria are widely used in foods and agricultural fermentations. In from the main metabolite lactic acid, fermentation microorgan- addition to their preservation, nutritional and therapeutic im- isms also produce bacteriostatic compounds. It has been sug- portance, these are known for their longevity of human life gested that the ingestion of LAB may counteract the effect of 486 V. K. SHIBY AND H. N. MISHRA

Figure 2 Scheme of lactose and galactose utilizati on by lactobacilli and streptococci (Kandler, 1983).

Escherichia coli outgrowth by a number of possible mechanisms constituents, inhibition to harmful bacteria of gastrointestinal such as anti-E. coli metabolites, detoxification of enterotoxins, tract, suppression of cancer, alleviation of lactose intolerance, prevention of toxic amine synthesis, and adhesion to the gut, thus and hypocholesterolaemic effect (Mathur et al., 2000). preventing colonization by pathogenic bacteria. These aspects Supplementation of infant formulas with Bifidobacterium are comprehensively reviewed by Gurr (1983). Homofermenta- lactis and S. thermophilus has been reported to be protective tive LAB convert the available energy source (Lactose) almost against nosocomical diahhroea in infants (Saavedra et al., 1994). completely to lactic acid via pyruvate to produce energy and to Pediatric beverage containing B. animalis, L. acidophilus, and equilibrate the redox balance. The fermentation action of spe- L. reuteri has been reported to be useful in prevention of ro- cific LAB strains may lead to removal of toxic or antinutritive tavirus diahhroea. Treatment with Lactobacillus GG promotes factors, such as lactose and galactose, from fermented milks to systemic local immune response to rotavirus, which may be of prevent lactose intolerance and accumulation of galactose. importance for protective immunity against infections (Kalia et al., 1992). Probiotics reported to reduce antibiotic induced diahhroea include B. longum, B. lactis, Lactobacillus GG, Culture Containing Milk Products in Prevention of Gastro L.acidophiluu La5, and Streptococcus faecum and yeast Saccha- Intestinal Infections romyces boulardii (Borgia et al., 1982; Colombel et al., 1987; Surawicz et al., 1989; Nord et al., 1997). Several strains of lacto- The beneficial effects of LAB and cultured milks have been bacillus have been reported to inhibit Salmonella typhimurium attributed to their ability to suppress the growth of pathogens (Hitchins et al., 1985). Helicobacter pylori is recognized as either directly or through the production of antibacterial sub- the main cause of anal gastritis. Inhibition of H. pylori NCTC stances such as lactic acid, peroxide, and bacteriocins (Kodama, 11637 by L. casei subsp. rhamnosus and several strains of 1952; Kansal, 2001). LAB are credited with imparting a number L. acidophilus and production of antihelicobacter factors by of nutritional and therapeutic attributes to fermented milk prod- these LAB have been reported (Kawamura et al., 1981; Lam- ucts such as improved digestion and bio availability of milk bert and Hull, 1996). FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODS—A REVIEW 487

producers (Driessen and Puhan, 1988). Mesophilic lactic cul- tures generally grow in the temperature range of 10–40◦C and contain group N streptococci and/or leuconostocs (Petterson, 1988). The final taste of cultured milk is the result of a mixture of compounds present in a certain ratio. For example, the di- acetyl flavor is associated with butter and buttermilk. Cultured milk should be mildly acid and slightly pricking. To meet these requirements, the content of lactic acid and carbohydrate has to be controlled during the manufacture of the product. By cool- ing the milk at the proper time, acidification can be limited, whereas the excess of the carbon dioxide in the product at the end of fermentation can be removed by stirring or de-aeration by vacuum. Milk for production of cultured milk has to be heat treated in order to inactivate the native substances which are inhibitory to the LAB and to improve the structure of the final product by denaturation of whey proteins. To obtain a coagulam that can be stirred easily to a smooth and viscous product, 805 or more of the whey proteins should be denatured (Snoeren et al., 1981; Richter, 1997) this can be reached by a heat treatment of 90◦C for3minor85◦C for 30 min (Harland et al., 1955; Hillier and Lyster, 1979). Lowering of pasteurization temperature of milk results in de- creasing firmness and retarded acidification. Ultra High Temper- ature (UHT) sterilized milk and other high temperature treated milks also result in lower viscosity, age-thickening and a cooked Figure 3 Lactose metabolism by Leuconostocs (Cogan, 1985). flavor in cultured milks. Homogenization of milk at 55◦C and 20 MPa is sufficient to get good distribution of fat. Decreas- TECHNOLOGY OF FERMENTED MILKS ing milk solids-not-fat content results in taste difference. The AND MILK PRODUCTS product may turn “flat” and “watery” and the defect known as “astringent” may occur. Increasing MSNF of milk leads to a The nutritional importance and technology of traditional fer- “full” taste, higher viscosity, and a stable cultured milk without mented dairy products popular in different parts of the world has wheying off during cold storage. been summarized in Table 1. Besides the traditional products which are popular in various countries, the development of pro- biotic products, dairy beverages, dietetic preparations, and dry Dry Cultured Milk Products cultured products are on progress due to the increasing demand for such value added products and convenience based ingredi- Extensive research has been carried out on various dry cul- ents. The process technology for different categories of such tured products including yoghurt, acidophilus milk, kumiss, products is described. The major categories include cultured and kefir, usually combined with additives that will enhance milks with mesophilic organisms and thermophilic milks. The the nutritive quality of the final product. Starters for dry cul- organisms involved in their manufacture, metabolites including tured beverages are streptococcus thermophilus, Lactobacillus flavor compounds produced and their proposed mechanism in bulgaricus, Lactobacillus acidophilus (LA), “Kefir grains”, and probiotic dairy products are given in Table 2 Dry cultured milk Bifidobacterium adolescens among others (Caric, 1994). Very products, whey based cultured beverages and several dietetic little scientific work has been published in this field and the preparations also find place in the booming health food market. developed processes are covered by patents (Pallansch, 1970; Hall and Hedrick, 1975; Shah et al., 1986; Usacheva et al., 1990). In general, the processing procedure for these products Cultured Milk differs somewhat from that for conventional cultured products (Krsev, 1989). Milk is heated to 90◦C–95◦C for 20 min prior Cultured milk is a collective name applied to a wide range to culturing. A total solids content of 30% has been found to of mesophilic fermented milks with a number of characteris- be most favorable. Concentration is accomplished either by tics in common. Mesophilic organisms are those with growth vacuum evaporation or ultra filtration. The advantage of us- optima between 20C and 30◦C. The starters used for fermenta- ing concentrated milk for culturing is volume reduction, and tion consist of homofermentative mesophilic LAB and of aroma certain stimulation is provided to microorganisms in this way. 488

Table 1 Traditional fermented milk products of different countries

Country/Region Product Technology and nutritional significance References

Southern and eastern Africa— Fermented milks and • Souring/coagulation of the raw milk in a smoked clay pot or bottle gourd, in warm Bekele and Kassaye, 1987; general concentrated fermented milks place, whey removed for concentration Kerven, 1987; Shalo, 1987. Southern and Eastern Africa—Ethiopia Irgo (fermented milk). • Milk utensils smoked by burning chips of Olea africana or Acacia busia. Hard fermented milk curd. • Similar to irgo except that there is daily removal of whey and the addition of fresh milk Bekele and Kassaye, 1987 until the vessel is filled with hard curd Arrera (sour butter milk). • Byproduct of butter making, a beverage with milk fat content 1 to 3%, rich in protein, lactose, minerals, and vitamins Middle-east Syria Laban • Cow, sheep, or goat milk heated to 80◦C, cooled to 37–40◦C, innoculated with LAB or with a small amount of a previous batch of laban, for about 4 h Labaneh (laban mousafa) • A drained laban or drained yoghurt with combined characteristics of laban and cheese http://www.fao.org/docrep/003/ (18–23% dry matter, pH 5 to 5.5) t0251e/T0251E04.htm#ch2 Shenineh • Prepared by shaking laban in a special bag made of sheep skin. sour taste and a very strong aroma and is very popular in the villages. Shenglish (Sorke) • Made from laban (45–50% dry matter), spices and chilli added for taste Keshkeh • Made by mixing laban with fine wheat. • The mixture is dried and ground into a powder West Africa—Mali. Kadam (fermented milk). • Popular traditional beverage or thirst quenching drink • Residual milk is accumulated and allowed to sour for few hours or several days depending on season Sour butter milk. • Soured milk churned to produce butter milk Southcone countries of latin Yoghurt. • Milk fermented with a mixture of Lactobacillus delbrueckii subsp. bulgaricus and america. Streptococcus thermophilus. The fermentation of lactose to lactic acid prevents milk spoilage due to the growth of contaminating bacteria India and neigh boring countries Dahi • Yoghurt-like product made from cow milk, buffalo milk, or mixture of two with De, 1980; Aneja, 1989 addition of starter into boiled and cooled milk with mild pleasant flavor, a clean acid taste, and a yellowish creamy-white color Mishti doi • Sweetened varety of dahi containing sugar, Artificial color, caramel, and jaggery. Chaas ((Buttermilk) • Produced by the churning of soured milk (dahi). Contains 1–2% fat and is rich in protein and lactose. Shrikhand • Concentrated dahi (Chakka) mixed with the required amount of sugar, condiments and flavor. Lassi • A refreshing beverage from dahi consumed sugared or salted Himalayan region—Nepal Mahi • Traditional drink made from whole or skimmed milk dahi fermented by natural souring and Bhutan or by “artificial” LAB., sweetened by the addition of sugar, diluting with water • Dahi sherbet made by diluting dahi 8 to 10 times its volume with water. FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODS—A REVIEW 489

Table 2 Probiotic microorganism, metabolites and proposed mechanism in dairy products

Product Microorganisms involved Metabolitesa,/flavorb compounds/probioticc property

Acidophilus milk L. acidophilus Maintenance of normal intestinal florac, acidophilina Acidophilus paste L. acidophilus Acidophilus buttermilk L. acidophilus -do- Acidophilus yoghurt L. acidophilus, S.thermophilus, L. Acetaldehydeb delbrueckii.subsp.bulgaricuss. Biogurt L. acidophilus, S. thermophilus Acidophilus—yeast milk L. acidophilus, lactose fermenting yeasts Probiotic dahi L. acidophilus, L. lactis, L lactis subsp diacetylactis Diacetylb enhanced digestibility, prevents constipation Bifidus milk Bifidobacterium bifidum, B. longum Removal of toxic aminesc, strengthening of host immune systemsc Bifighurt B. bifidum, S. thermpophilus Reduction of serum cholesterol Biogarde B. bifidum, L. acidophilus, S. thermophilus Biokys B. bifidum, L. acidophilus, P. acidilactici Special Yoghurt B. bifidum, L. acidophilus, S. thermophilus, L. delbrueckii subsp. bulgaricus Cultura B. bifidum, L. acidophilus Cultura drink B. bifidum, L. acidophilus Progurt S.lactis subsp. diacetylactis, S. lactis subsp.cremoris, Diacetyla Allieviates lactose maldigestionc l. acidophilus, and/or B. bifidum aMetabolites; bflavor compounds; cprobiotic property.

However, the desired amount of inoculam varies considerably drink contained 11.65–13.1% total solids, 11.27–11.65% total from 1–6% according to various authors. Even starter quantities sugar, 0.66–0.78% protein, 0.2–0.3% fat, and 0.42–0.46% min- as high as 10–15% have been reported. Various levels of lactic erals. Mango-molke mix, a popular whey beverage marketed acid in concentrated milk prior to spray drying were developed. in Europe contains bifidobacteria culture along with whey and Most often acid ranges from 0.6–1.1%. Sometimes treatments mango juice. Probiotic attributes of LAB may be incorporated intended to minimize the heat-induced changes and to increase to develop fermented whey beverages. Such beverages may be starter survival during drying are carried out as well. Spray dry- beneficial for the people suffering from gastro-intestinal tract ing temperatures are lower than those commonly used for milk disorders and it also provides nutritional and therapeutic soft drying and range from 145–175◦C (inlet air temperatures). Data drinks (Singh, 2001). Kumar and Tiwari (2003) showed that have been reported for drying cultured beverages by freeze- good quality whey based fermented milk beverage can be made drying on a laboratory scale. The resulting product is of good from a mixture of cheese whey and milk. The fermented bever- solubility and contains viable microflora after recombination. age made by admixing 70% of cheese-whey, 0.3% CMC with Kumar and Mishra (2003) developed mango soy fortified yo- the milk resulting in acceptable whey based fermented milk ghurt powder. The nutritional and therapeutic value of yoghurt beverage. was improved by supplementing buffalo milk with soymilk, thus incorporating in the product phytochemicals. By incorporating soymilk phenyl alanine, iron, thiamin, and niacin contents of Thermophilic Fermented Milks the product increased. The term thermophilic should be reserved for microorgan- isms whose optimum growth temperature lies between 55 and Whey Based Cultured Dairy Products 75◦C. In dairy industry, it tends to be employed to describe cultures that are most active between 35 and 40◦C. According Current worldwide popularity of fruit flavored drinkable yo- to Bianchi-Salvadori (1981) thermophilic yoghurt starters do ghurt offers an excellent opportunity for incorporation of whey not form part of the natural intestinal flora of man nor do they into the development of cultured fruit flavored products (Singh, implant themselves in the intestines. It has, however, been sug- 2001). Proper amount of stabilizer coupled with heat processing gested that L. delbrueckii subsp. bulgaricus and S. thermophilus of the ingredients and homogenization are important aspects in can establish themselves in the intestine and gradually domi- the manufacture of fermentable cultured dairy drink (Dorde- nate the natural microflora. In vitro, studies have indicated that vic et al., 1982). For making drinks from sweet or acid whey, L. delbrueckii subsp. bulgaricus is inhibited by bile salts (Lem- the standardized method involves adding sugar to filtered whey, bke, 1963). However, these bacteria are also able to resist a high pasteurization at 80◦C for 5 min, homogenization at 70◦C, in- degree of acidity and so it is quite feasible that a proportion of cubation at 43◦C with 2% Lactobacillus helveticus starter for bacteria ingested will reach the intestine in a viable state (Acott 15–17 h to the pH 3.8–3.95, repasteurization at 85◦C with 5 min and Labuza, 1972). Mabbit (1977) supports the hypothesis that holding, addition of 4–7% fruit juice concentrate, rehomogeni- certain strains of L.delbrueckii subsp. bulgaricus could survive sation, cooling to 50◦C and packing into retail containers. The and compete in the human intestine. This possibility is of great 490 V. K. SHIBY AND H. N. MISHRA importance since it would ensure the absence of putrefactive teins, that is, sedimentation (Kang and Lee, 1984; Towler, 1984; microorganisms and hence protect the intestinal health of the Hege and Kessler, 1986). Slow acidifying starters having limited consumer (Dellaglio, 1984). after—acidification ability; good aroma production; low ropi- ness; and low carbon dioxide production are selected for use Fermented Dairy Beverages in fermented beverages. Streptococcal cultures are the best for plain beverages. Yeast containing cultures can give the bever- The demand for fermented milk beverages is on the rise due age excellent taste, but the gas production may lead to blowing to their positive health effects and nutritive value. The general of packages (Koroleva et al., 1983, 1984; Rasic and Kurmann, requirements of fermented milk beverages are that they should 1988). Fermentation results in acidification down to pH 4.6 for be light, low calorie, for example, drinking yoghurt has 30% a complete casein coagulation which prevents whey separation, less energy than conventional yoghurt, refreshing (not causing too strong an acidification masks aroma, sweetness, and causes thirst), tasteful of agreeable mouth feel, and smooth in tex- a possible destabilization of additions. Mixing of the coagulum may be carried out with a static turbine mixer or even bet- ture. Milk like soft drinks mainly prepared with yoghurt and ◦ mesophilic starter cultures and nonsoft drinks, for example, Ke- ter homogenizing at lower temperature, for example, 40–45 C fir and Kumiss with alcohol production fall in the category of without pressure, Supplementary dilution may be carried out by fermented milk beverages. Acidified milk drinks (AMDs) need addition of fruit juices, water, fresh milk, and vegetable juices, a stabilizer, for example, high methoxy pectin if whey forma- for example, coconut, soy, whey, etc.; carbonation of the product tion is to be avoided. A stabilizer can act in different ways. is also possible (Choi and Kosikowski, 1985). An increased steric repulsion between the casein micelles may be introduced, thus preventing flocculation. Alternatively, a ki- Yogurt Beverages netic barrier may be imposed against extensive aggregation. Casein micelles in milk (pH 6.7) are generally assumed to stay Drinking yogurt is essentially stirred yogurt which has to- in the suspended state as the result of steric repulsive interac- tal solids content not exceeding 11% and which has undergone tions between the micelles. On acidification of milk to a pH homogenization to further reduce the viscosity; flavoring and value around 4, as is done during the preparation of yoghurt, coloring are invariably added. Heat treatment may be applied to the native mechanism of stabilization of casein micelles fails. extend the storage life. High Temperature Short Time (HTST) This failure is believed to be related to the collapse of the ex- κ pasteurization with aseptic processing will give a shelf life of tended conformation of -casein chains (Holt, 1982 and De several weeks at 2–4◦C, which UHT processes with aseptic Kruif, 1998). At pH 6.7 these chains protrude from the surface packaging will give a shelf life of several weeks at room tem- of the casein micelle in order to maximise their entropy. This perature. same tendency to maximize entropy of κ-casein chains causes the micelles to have a repulsive mutual interaction because over- lap of κ-casein chains of neighboring micelles would result in a Cultured Buttermilk loss of entropy of the chains. This phenomenon is called steric stabilization. In order to stabilize an AMD of 8.5% milk solids This product was originally the fermented byproduct of but- (not fat), high methoxy pectin has to be added at concentrations ter manufacture, but today, it is more common to produce cul- around 0.3% w/w (Trompa et al., 2004). It was found that up tured buttermilks from skim or whole milk. The culture most to 90% of this pectin added as a stabilizer to AMDs is not di- frequently used is S. lactis, perhaps also spp. cremoris. Milk is rectly interacting with the milk gel particles (largely consisting usually heated to 95◦C and cooled to 20–25◦C before the ad- of casein micelles). This nonadsorbing fraction of pectin, which dition of the starter culture. Starter is added at 1–2% and the is, however, necessary to produce a stable AMD can be taken fermentation is allowed to proceed for 16–20 h, to an acidity of out of the stable system without loss of stability. Another way 0.9% lactic acid. This product is frequently used as an ingredient to decrease the amount of ineffective pectin in the AMD is to in the baking industry, in addition to being packaged for sale in increase the energy input during the homogenization step, that the retail trade. is, after the addition of pectin. This will increase the adsorption rate of the pectin, and therefore allows for a smaller overall pectin concentration. Acidophilus Milk The steps in the manufacture of fermented dairy beverages include selection of a milk base with low total solids and low Acidophilus milk is traditional milk fermented with LA, proteins (Rossi and Clementi, 1983; Dellaglo, 1984), selection which has been thought to have therapeutic benefits in the gas- of additives such as fruit juice concentrate, colors, artificial trointestinal tract. Skim or whole milk may be used. The milk sweetener, sugar stabilizers, etc. taking into consideration their is heated to high temperature, for example, 95◦Cfor1h,tore- interactions with fermented milk components (Rasic and Kur- duce the microbial load and favor the slow growing LA culture. mann, 1988), Low temperature (e.g., <75◦C) and short time Milk is inoculated at a level of 2–5% and incubated at 37◦C treatment in order to prevent deposit formation by whey pro- until coagulated. Some acidophilus milk has acidity as high as FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODS—A REVIEW 491

1% lactic acid, but for therapeutic purposes 0.6–0.7% is more products will be an expanding product area. Sarkar and Misra common. (2001) attempted to incorporate Bifidobacterium bifidum NDRI Another variation has been the introduction of a sweet aci- and propionibacterium freudenreichii subsp. Shermanii MTCC dophilus milk, one in which the LA culture has been added but 1371 along with Yoghurt- YH-3 to obtain dietetic yoghurt with there has been no incubation. It is thought that the culture will enhanced nutritional and therapeutic characteristics. Dieteic yo- reach the gastro intestinal (GI) tract where its therapeutic ef- ghurt was obtained from skim milk (0.5% fat, 7.64% SNF), fects will be realized, but the milk has no fermented qualities, heated to 95◦C for 30 min at 1% level each and incubated at thus delivering the benefits without the high acidity and flavor, 42◦C. The dietetic yoghurt possess desirable technological and considered undesirable by some people. dietetic characteristics including antibacterial activity against pathogenic test organisms. The viable cell populations obtained in the product were within the range required for successful Sour Cream implantation in the intestine.

Cultured cream usually has a fat content between 12–30%, depending on the required properties. The starter is similar to FUNCTIONAL ASPECTS OF FERMENTED that used for cultured buttermilk. The cream after standardiza- MILK PRODUCTS tion is usually heated to 75–80◦C and is homogenized at >13 MPa to improve the texture. Inoculation and fermentation con- Fermented Products as Vehicles for Fortification ditions are also similar to those for cultured buttermilk, but the fermentation is stopped at an acidity of 0.6%. Fortification of foods can be an efficient tool to combat mi- cronutrient deficiencies. The successful application of food for- tification technology is based on consideration of compatibility Others of vehicle, fortificant, and process. Modified foods including those that have been fortified with nutrients also fall within the There are a great many other fermented dairy products, in- realm of functional foods (ADA reports). According to Amer- cluding Kefir, Kumiss, beverages based on bulgaricus or bifidus ican Dietetic Association (ADA) functional foods including strains, labneh, and a host of others. Many of these have devel- whole foods, fortified enriched or enhanced foods have poten- oped in regional areas and, depending on the starter organisms tially beneficial effect on the health when consumed as apart used, have various flavors, textures, and components from the of varied diet on a regular basis at effective levels. Fermented fermentation process, such as gas or ethanol. dairy products, such as yoghurt and soft cheeses, have been used in iron fortification programmes (Lysionek et al., 2002). In the iron fortification of powdered nonfat dry milk, ferrous Fermented Dietetic Preparations sulfate at a level of 10 ppm was found to be stable for a period of 12 months. Ferric ammonium citrate and ferric chloride at a Dietetic foods are manufactured to meet particular nutri- level of 20-ppm iron in the reconstituted product gave accept- tional needs of people whose normal processes of assimilation able results (Coccodrilli and Shah, 1985). Enrichment has been or metabolism are changed, or for whom a particular effect is used interchangeably with fortification (FAO/WHO, 1994), but obtained by a controlled intake of food or certain nutrients. elsewhere it has been defined as the restoration of vitamins and They may be formulated for people suffering from physiologi- minerals lost during processing (Hoffpauer and Wright, 1994). cal disorders or for healthy people with additional needs (Ben- der, 1975). The manufacture of dieteic-fermented milks causes problems with texture (correction with ropy starter cultures and Probiotic Applications hydrocolloids) and with flavor (correction with mild acidifying and aroma forming cultures, lactose- hydrolysis, skim-milk con- The claimed beneficial effects from the consumption of fer- centrate, fruit concentrates, sweeteners, etc.). Fermented milk mented milks were once a debated issue. Research conducted products fortified with some dietary components (fiber, vita- since the turn of the century has however, enhanced the under- mins, phospholipids, minerals, other bioactive substances). At standing of the therapeutic effects resulting from the consump- present, the most frequently produced fermented dietetic prod- tion of these products. The probiotic products are now consid- ucts are calorie reduced and dietary fiber fortified (separated and ered helpful in maintaining good health, restoring body vigor, combined ones). A small number of dietetic products have been and in combating intestinal and other disease disorders (Mital developed for adults (obesity, sports activity, etc.) and for el- and Garg, 1992). Most scientific papers refer to research using derly people. Only a few of the presently manufactured dietetic L. acidophilus and bifidobacterium species as dietary cultures. preparations are fermented, a factor which certainly become of Nearly all probiotics currently on the market contain Lacto- more significance in the future. The use of selected intestinal bacilli, Streptococci, Enterococci,orBifidobacteria. In contrast bacteria starter cultures for the preparation of fermented milk to Japan, where freeze-dried microorganisms are consumed by 492 V. K. SHIBY AND H. N. MISHRA a substantial part of the human population, in Europe, probi- gastrointestinal tract of the host, should not be pathogenic and, otic action toward humans is only claimed for certain fermented last but not least, must be capable of exerting a growth promot- dairy products (e.g., yoghurts). Those species that have been ing effect or a resistance to infectious diseases (Kalantzopoulos, extensively studied so far, with several experimental inocula- 1997). Protection of probiotics by microencapsulation in hydro- tion of milk for yoghurt manufacture (Prevost & Divies, 1988). colloid beads has been investigated for improving their viability Additional benefits of microencapsulation of cells include: pro- in food products and the intestinal tract (Rao et al., 1989). This tection of cells inside the beads from bacteriophages (Steen- has been proposed for various dairy fermentations (Champagne son et al., 1987); increased survival during freeze drying and et al., 1992a, 1992b, 1994) such as fermentation of whey (Audet freezing (Kearney et al., 1990; Sheu and Marshall, 1993; Sung, et al., 1989) and continuous Kim and Yoon, 1995); and greater 1997) The trials on man were mainly carried out with the two stability during storage (Kim et al., 1988; Reuter, 1990; Kebary yoghurt bacteria Streptococcus thermophilus and Lactobacillus et al., 1998). Many health benefits have been attributed to fer- bulgaricus. L. casei, Bifidobacteria, and L. acidophilus has also mented dairy products and probiotic microorganisms (Salminen received important scientific interest, however, only a few hu- et al., 1998). man studies have been reported. From the technological point The therapeutic significance of probiotic organisms is sum- of view a good probiotic should be stable and viable for long marized in Table 3. In order to exert positive health effects, it periods under storage, should be able to survive the low pH is generally assumed that the microorganisms need to be vi- levels of the stomach, be able to colonize the epithelium of the able. Therefore, the International Dairy Federation (1997) has

Table 3 Fermented products and therapeutic significance

Clinical condition/symptoms Health benefit of fermented products Reference

Lactose maldigestion • Viable yoghurt well tolerated by lactose-deficient Morley, 1979; Gilliland, 1989; Kim and Gilliland, 1983 subjects, L.acidophilus aids lactose digestion. • Manifested by the presence of breath • The presence of bacterial b-galactosidase in the hydrogen derived from fermentation viable yoghurt culture. of the lactose in the large intestine, abdominal pain, meteorism, bloating, flatulence and diarrhea. Hepatic encephalopathy • A neurological disorder where • Alteration of the intestinal microflora Macbeth et al., 1965; Kavasnikov and Sodenko, 1967; Detoxification of ammonia produced • A decrease in faecal urease, a lowering of blood Read et al., 1968 Loguerolo et al., 1987 in the intestine is impaired in patients ammonia and clinical improvement when treated with liver failure. individually with L. acidophilus, Lactobacillus GG,andE. faecum. SF68 Side effects of radiotherapy • Radiotherapy alters the intestinal • Treatment with fermented milk containing NCFB Salminen et al., 1998 ; Kansal, 2001 microflora, vascular permeability of 1748 significantly decrease pelvic radiotherapy the mucosa and intestinal motility. associated diarrhea Tumor or defective immune systems • Lactobacilli and their metabolic products modify Kansal, 2001 both the immune responses and antitumor activities. • Enhanced mainly by activating macrophage Varnam and Sutherland (1994). Anand et al., 1985 functions and increasing the activity of natural killer cells and T-cells, maintenance of normal intestinal flora • Help removal of dietary procarcinogens. Benno et al., 1984 High serum cholesterol levels • L.acidophilus strains and some bifidobacteria Mann and Spoerry, 1974; Kawamura et al., 1981; species lower cholesterol Gilliland et al., 1985; Gilliland, 1989; Walker and Gilliland, 1993; Hosona and Tono-oka, 1995; Gopal et al., 1996; Marshall, 1996; Usman and Hosono, 2000; Gupta and Prabhu (2004) Renal mal function • Effect of fermented milk product on cholesterol metabolizing enzymes systems in liver • Promotion of excretion of cholesterol through faeces, • Inhibition of cholesterol adsorption by the binding of cholesterol to cells of LAB. • The promotion of excretion by binding of bile salts to lactic acid bacterial cells. • Bifidobacterium spp.; Lactobacillus acidophilus • Reduce level of toxic amines. FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODS—A REVIEW 493 defined fermented milk as a milk product fermented by the ac- Future Research Prospects tion of specific microorganisms and resulting in reduction of pH and coagulation. These specific microorganisms shall be The development of more probiotic products by the incor- viable, active, and abundant (at least 107 cfu/g) in the prod- poration of probiotic organisms into the manufacturing process uct to the date of minimum durability. Probiotics are defined as for well-accepted traditional dairy products is to be explored live microbial food supplements which beneficially influence the significantly. The development of convenience based dry cul- host by improving its intestinal microbial balance (Fuller, 1989; tured products containing viable bacteria by various techniques Ziemer and Gibson, 1998). Both definitions emphasize the vi- such as microencapsulation and the fortification of such powders ability of microorganisms. Whether viable microorganisms are or concentrated products with minerals and vitamins are gain- necessary for specific health benefits remains unclear. Health ing importance. The preparation of suitable blends containing benefits discussed are: alleviation of lactose maldigestion, ef- healthful ingredients such as dietary fiber, natural vitamins and fects on diarrhoea, immune-stimulation, antitumor activity, an- folic acid also offers new possibilities for this widely expanding timutagenic activity, reduction of serum cholesterol, and effects research area. The formulation of various health drinks and di- on candidiasis. Many of the studies discussed here were not etetic preparations as value added products based on traditional conducted for the purpose of determining the efficacy of non- fermented products will definitely bring more opportunities to viable bacteria or fermented milks, but killed microorganisms the beverage industry. There is a need to intensify research to have often been used as placebo. The results from these studies distinguish the therapeutic benefits of viable and nonviable or- give an indication of the activity of viable versus nonviable mi- ganisms in different fermented products apart from the general croorganisms and assist in defining the need for probiotics to be nutrient enhancement achieved. viable.

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