Milk Fermented Products 2013

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Fermented Milks and Milk Products as Functional

FoodsA Review
a
V. K. Shiby & H. N. Mishra
Freeze Drying and Animal Products Technology Discipline , Defence Food Research
Laboratory , Siddharthanagar , Mysore, India 570011
b
Department of Agricultural and Food Engineering , Post Harvest Technology Centre, Indian
institute of Technology , Kharagpur , India
Accepted author version posted online: 01 Aug 2012.Published online: 07 Feb 2013.
To cite this article: V. K. Shiby & H. N. Mishra (2013) Fermented Milks and Milk Products as Functional FoodsA Review,
Critical Reviews in Food Science and Nutrition, 53:5, 482-496, DOI: 10.1080/10408398.2010.547398
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DOI: 10.1080/10408398.2010.547398
Fermented Milks and Milk Products

as Functional FoodsA Review
V. K. SHIBY1 and H. N. MISHRA2
Downloaded by [UNAM Ciudad Universitaria] at 11:56 27 January 2014
Freeze Drying and Animal Products Technology Discipline, Defence Food Research Laboratory, Siddharthanagar, Mysore,
India 570011
2
Department 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
Healthiness is one of the most frequently mentioned reasons
behind food choices in EU countries (Lappalainen et al., 1998).
Individuals are considered responsible for their own state of
health. Diseases are seen more and more as consequences of
consumers own behavior rather than the result of environment
(Ogden, 1998). Diet may strongly influence an individuals risk
of obesity; cardiovascular diseases, cancer, and other life style
related diseases. Traditionally, the healthfulness has been associated with nutritional factors such as fat, fiber, salt, and vitamin contents of food. In addition to traditional healthiness
food may contain single components that may have a positive
impact on our well-being. Products that are claimed to have
special beneficial physiological effects in the body are usually
called functional foods (Bellisle et al., 1998; Roberfroid, 1999;
Hardy, 2000; Kwak and Jukes, 2001). A particular food may be
made more functional by increasing or adding a potential health
Address correspondence to Prof. H. N. Mishra, Department of Agricultural
and Food Engineering, Post Harvest Technology Centre, Indian Institute of
Technology, Kharagpur-721302, India. E-mail: hnm@agfe.iitkgp.ernet.in
promoting entity. Alternatively, concentration of adverse components may be reduced or there may be a partial interchange
between toxic and beneficial ingredients. Functional food may
be considered as a therapeutic aid without prescription. The
term nutraceutical was coined by Stephen De Felice, founder of
the Foundation for Innovation in Medicine, in 1989. He defined
a nutraceutical as a food, dietary supplement or medical food
that has a medical or health benefit including the prevention or
treatment of disease. Today the term nutraceutical is often used
interchangeably with functional food. An official definition for
the term functional foods is lacking in USA and Europe. According to EU concerted action a food can be considered as
functional if it has been satisfactorily demonstrated to affect
beneficially one or more target functions in the body beyond
adequate nutritional effects in a way that is relevant to either
an improved state of health and well-being and/or a reduction
of risk of disease. These functional foods may also be used as
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
purpose. Functional foods may be processed by modification
or they may be fortified with different substances and the
482
FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODSA REVIEW
functionality of a product can be targeted to a special disease or

just to improve overall well being (Roberfroid, 1999). Information relating health effects and the ways of communicating such
information are the key factors because the health effect cannot
be perceived from the product itself (Urala et al., 2003). Since
1989, the nutraceutical or functional food industry has evolved
into a market worth $20.2 billion in 2002. Functional beverages
reached $ 10.35 billion sales in 2002, up 10.7% and are projected
to reach $15.9 billion by 2010. A variety of functional dairy
foods are conquering the market worldwide. Examples include
probiotic, prebiotic, and symbiotic products, low cholesterol
fresh milk omega-3-milk, low lactose, and lactose free products
and milk products that can control or manage hypertension and
immune functions. The market for functional foods, nutraceuticals, wellness foods, and beverages is fast growing and it is
estimated that the functional food industry could almost double by 2007. An increasing sector of the public is quickly aging
and purchasing functional food products. Todays consumers are
more concerned with weight loss and management, heart health,
eye health, cancer, increasing energy and stamina, eye health,
and improved memory. Several categories of functional foods
and beverages have been developed to meet these challenges.
The scope of the present article is to provide an overview
of the kinetics of lactic acid fermentation in dairy products,
the technology and nutritional significance of fermented milks
popular in different countries, and the therapeutic properties of
probiotic organisms involved in their manufacture.
LACTIC ACID FERMENTATION
Fermentation Kinetics
Mathematical analysis of the biokinetics of functional starter
cultures can yield precious information about the relationship
between the food environment and bacterial functionality and
may contribute to optimal strain selection and process design.
This may result in better process control, enhanced food safety
and quality, and reduction of economic losses. Kinetic data are
needed to understand the fermentation process and to develop
continuous fermentation systems. Lactic acid bacteria (LAB)
have long been used in food industry as starter cultures for
the manufacture of fermented meat and dairy products. The
key metabolite produced during such fermentation reactions is
lactic acid, which is a commercially valuable product with applications in food manufacturing and pharmaceutical industries.
Both chemical and biotechnological methods are available for
lactic acid production, but the lactic acid from fermentative processes has increased its market share owing to the preference
of consumers to products of natural origin (Chahal, 1989). The
commercial significance of dairy fermentation industry which
incorporates production of cheeses, fromage frais, sour cream,
etc. is well recognized and ranks second only to the alcoholic
beverages (Daly et al., 1998). The processes for wood utilization can be directed toward lactic acid production (Moldes et al.,
1999). The kinetics of milk fermentation by starter cultures
has been studied by several research workers. Response Sur-
483
face Methodology has been successfully used in modeling of

acidification rate and growth of starter bacteria as a function
of parameters such as fermentation temperature, fat and solid
content, inoculum size, and cocci/rods ratio on the fermentation process of yoghurt (Torriani et al., 1996). The pH measurement method described by Spinnler and Corrieu (1989) is
widely used in the determination of acidification kinetics during
gel formation. Several research workers have tried to optimize
the acidification process for manufacture of fermented products and developed models to predict the acidification kinetics.
Mathematical models have been used to predict the influence
of fermentation operating temperatures on cell growth rate, cell
concentration, substrate utilization rate and lactic acid production rate. As for models, a number of them, purely or partially
empirical, have been described in literature. Product inhibition
is well-established feature of lactic fermentations.
Boonmee et al. (2003) developed a model for batch and
continuous fermentation of Lactococcus lactis strain NZ133.
The growth kinetics of L. lactis is predominantly influenced by
lactose limitation and lactate product inhibition with the growth
of this particular strain showing a relatively high sensitivity to
lactate inhibition. The Leudeking-Piret equations for growth
and lactate production were successfully incorporated into the
model. The LeudekingPiret model is given as
dx
= x
dt
(1)
dx
dp
=
+ x
dt
dt
(2)
When this is modified to include the effects of lactose limitation and inhibition, as well as lactate inhibition the model is
outlined as in Equatons (3)(5).
The rate of biomass production
dx
=
dt
s
Ksx + s

Kix
P Pix
1
x
Pmx Pix
Kix + s
(3)
The rate of lactate production

dp
s
dx
=
+ qp,max
dt
dt
Ksp + s

Kip
p Pip
x
1
Pmp Pip
Kip + s
(4)
The rate of lactose utilization

ds
s
Kis
p Pis
= qs,max
1
x (5)
dt
Kss + s
Pms Pis
Kis + s
where,
Ki is lactate inhibition constant (gl1),
Ks is lactose limitation constant (gl1),
484
V. K. SHIBY AND H. N. MISHRA
P is lactate concentration (gl1),

Pi is threshold lactate concentration (gl1),
Pm is maximum lactate concentration (gl1),
qp,max is maximum specific lactate production rate (gg1h1),
qs,max is maximum specific lactose utilization (gg1h1),
s is lactose concentration (gl1),
x is biomass concentration (gl1),
a is growth associated constant in LeudekingPiret model
(gg1),
b is nongrowth associated constant in LeudekingPiret model
(gg1h1),
is specific growth rate in Leudeking-Piret model (h1), and
max is maximum specific rate (h1)
Common Organisms and Pathways

The group of LAB plays a central role in fermentation processes, and has a long and safe history of application and consumption in production of fermented foods and beverages. (Ray,
1992; Wood and Holzaphel, 1995; Wood, 1997; Caplice and
Fitzgerald, 1999) During fermentation of lactose to lactic acid
the acidity of the milk rises and the growth conditions for microorganisms other than LAB become increasingly unfavorable
(Driessen and Puhan, 1988). Reid et al. (2002) have studied the
LAB in fermented foods in South East Asia. They discussed
the distribution and application of LAB in various products
such as fermented milk, meat, fish, vegetable, or plant products. Significant advances have been made in elucidating the
genetic, biochemical land physiological basis of many of the
key technological traits of these bacteria (Daly et al., 1998).
LAB are constituted of heterogenous group of Gram-positive
bacteria with a strictly fermentative metabolism (Temmermman
et al., 2004). One of the most important functional properties
common to all LAB is their ability to convert lactose and a variety of other carbohydrates into the primary end product, lactic
acid, by fermentation. The ability of LAB to transform food
into new products and to exert antagonistic action toward harmful microorganisms make them suitable for both domestic and
industrial productions Servin (2004). The LAB involved in the
production of fermented milks are distributed in several phenotypic and genotypic groups. These groups are characterized
by different nutritional requirements, metabolic, cultivational,
and technological properties. Several authors have reported that
LAB present in fermented milks may belong to species of Lactobacillus, Streptococcus, Pediococcus, Leuconostoc, and Lactococcus genera (Aucloir and Mocquot, 1974 ; Cogan, 1985;
Gilliland, 1985; Sandine, 1985; Schleifer et al., 1985). The role
of interaction between yeasts and LAB in African fermented
milks has been reviewed by Narvhus and Gadaja, 2003.
There are two main fermentation pathways in LAB; the homolactate pathway in which lactic acid is the major end product
and heterolactate pathway in which other compounds such as
acetic acid, carbon dioxide, ethanol etc. are produced in addition to lactic acid (Huggenholtz, 1993; Cocaign-Bous-quet et al.,
1996; de Vos, 1996). The homofermentation and heterofermentation pathways are shown in Fig. 1. Both rods and cocci follow
different pathways of carbohydrate fermentation and achieve
end products, which are at least 90 or 50%, lactate in the case
of homo and hetero fermentative species respectively. Lactose
is transported across the cell membrane either by lactose permeate system or by phosphoenol pyruvate dependent phospho
transferase system (Lac PEP-PTS). Depending on the transport
mechanism involved, unphosphorylated lactose (Lac permease)
is hydrolyzed into glucose and galactose by -galactosidase
or phosphorylated lactose is hydrolysed by phosphorylated galactosidase into glucose and galactose-6-phosphate. All of
the dairy lactococci and some mesophilic lactobacilli operate the Lac PEP-PTS system (Fig. 2) while leuconostoc and
some industrially significant thermophilic organisms; S. thermophilus and Lb delbrueckii subsp. bulgaricus possess a permease system (Fig. 3) Subsequent metabolic pathways include the
glycolytic Embden-Meyerhof-Parnas(EMP), the phosphoketolase pathways for glucose, the tagatose-6-phosphate pathway
for galactose-6-phosphate and the Leloir pathway for galactose (when it is not transported back into the environment).
LAB containing aldolase, that is, Streptococci, Pediococci, and
obligately homofermenative and facultative heterofermentative
Lactobacilli have the homolactic fermentation with lactate as the
exclusive end product. LAB containing phosphoketolase can be
divided into two groups. The first, that is, Leuconostocs and obligately hetero fermentative lactobacilli, follows 6Pgluconate
pathway with production of equimolar amounts of CO2 , lactate and acetate. The others follow bifidus pathway with the
formation of acetate and lactate in a molar ratio of 3:2.
Among the LAB, lactose metabolism in lactococcus is probably the best understood in terms of its biochemical and genetic make-up and also in terms of its regulation. The complete
metabolic pathway is known and several important genes have
been characterized (de Vos and Vaughan, 1994). The genes encoding the PEP-PTS system and the tagatose pathway are all
plasmid located in a single operon under the control of the
repressor gene lacR. Another operon has also been identified
in Lactococcus encoding a number of glycolytic enzymes The
fermentative action of specific LAB strains may lead to the removal of toxic or antinutritive factors such as galactose and
lactose from fermented milks to prevent lactose intolerance and
accumulation of galactose (Wouters et al., 2002).
Fermentation Process and Health
Fermented milks constitute important part of our food. In ancient days, human beings realized that fermentation occurred,
without, however, knowing their cause. Originally milk fermented spontaneously, and the reuse of fermentation vessels
and tools contributed to a certain repeatability and stability in
the fermentation process. This led to the use of specific microorganisms for the manufacture of more or less refined products.
Different countries or even different parts of the same country
developed their own fermented milks. The best-known product
485
Glucose
Fru-1,6 P
Fru-6P
Glc-6P
Acetyl-P+ Erythrose-4P
Fru-6P
Xylulose-5P +CO2
Heptose-P
aldolase
6P-Gluconate
+
Pentose-P
Phosphoketolase
Triose-3P
Acetyl-P+ Triose-3P
Triose-3P
ADP
Acetyl- P
ADP
ATP
Pyruvate
Pyruvate
Lactate
Acetate
Lactate
ATP
Pyruvate
Lactate
Bifidus pathway
Glycolysis
Acetate (Ethanol )
6P-Gluconate pathway
Phosphoketolase pathways
HOMOFERMENTATION
Figure 1
HETEROFERMENTATION
Main pathways of hexose fermentation in lactic acid bacteria (Kandler, 1983).
is the thermophilic fermented milk, yoghurt, which has enjoyed

increased popularity in the last three decades. The role of living
microorganisms in fermented dairy products has gained considerably increased interest for both the consumer and the producer.
Nature has provided a certain degree of beneficial association
for humans through the activity of lactic LAB. These bacteria are widely used in foods and agricultural fermentations. In
addition to their preservation, nutritional and therapeutic importance, these are known for their longevity of human life
(Ram and Bhavadasan, 2002) LAB are natural inhabitants of

gastrointestinal tract. These microorganisms have a number of
traits which make them particularly attractive to be used as
probiotic. During fermentation of lactose to lactic acid the
acidity of milk rises and the growth conditions of microorganisms other than LAB become increasingly unfavorable. Apart
from the main metabolite lactic acid, fermentation microorganisms also produce bacteriostatic compounds. It has been suggested that the ingestion of LAB may counteract the effect of
486
Figure 2
Scheme of lactose and galactose utilizati on by lactobacilli and streptococci (Kandler, 1983).
Escherichia coli outgrowth by a number of possible mechanisms

such as anti-E. coli metabolites, detoxification of enterotoxins,
prevention of toxic amine synthesis, and adhesion to the gut, thus
preventing colonization by pathogenic bacteria. These aspects
are comprehensively reviewed by Gurr (1983). Homofermentative LAB convert the available energy source (Lactose) almost
completely to lactic acid via pyruvate to produce energy and to
equilibrate the redox balance. The fermentation action of specific LAB strains may lead to removal of toxic or antinutritive
factors, such as lactose and galactose, from fermented milks to
prevent lactose intolerance and accumulation of galactose.
Culture Containing Milk Products in Prevention of Gastro
Intestinal Infections
The beneficial effects of LAB and cultured milks have been
attributed to their ability to suppress the growth of pathogens
either directly or through the production of antibacterial substances such as lactic acid, peroxide, and bacteriocins (Kodama,
1952; Kansal, 2001). LAB are credited with imparting a number
of nutritional and therapeutic attributes to fermented milk products such as improved digestion and bio availability of milk
constituents, inhibition to harmful bacteria of gastrointestinal

tract, suppression of cancer, alleviation of lactose intolerance,
and hypocholesterolaemic effect (Mathur et al., 2000).
Supplementation of infant formulas with Bifidobacterium
lactis and S. thermophilus has been reported to be protective
against nosocomical diahhroea in infants (Saavedra et al., 1994).
Pediatric beverage containing B. animalis, L. acidophilus, and
L. reuteri has been reported to be useful in prevention of rotavirus diahhroea. Treatment with Lactobacillus GG promotes
systemic local immune response to rotavirus, which may be of
importance for protective immunity against infections (Kalia
et al., 1992). Probiotics reported to reduce antibiotic induced
diahhroea include B. longum, B. lactis, Lactobacillus GG,
L.acidophiluu La5, and Streptococcus faecum and yeast Saccharomyces boulardii (Borgia et al., 1982; Colombel et al., 1987;
Surawicz et al., 1989; Nord et al., 1997). Several strains of lactobacillus have been reported to inhibit Salmonella typhimurium
(Hitchins et al., 1985). Helicobacter pylori is recognized as
the main cause of anal gastritis. Inhibition of H. pylori NCTC
11637 by L. casei subsp. rhamnosus and several strains of
L. acidophilus and production of antihelicobacter factors by
these LAB have been reported (Kawamura et al., 1981; Lambert and Hull, 1996).
Figure 3
Lactose metabolism by Leuconostocs (Cogan, 1985).
TECHNOLOGY OF FERMENTED MILKS

AND MILK PRODUCTS
The nutritional importance and technology of traditional fermented dairy products popular in different parts of the world has
been summarized in Table 1. Besides the traditional products
which are popular in various countries, the development of probiotic products, dairy beverages, dietetic preparations, and dry
cultured products are on progress due to the increasing demand
for such value added products and convenience based ingredients. The process technology for different categories of such
products is described. The major categories include cultured
milks with mesophilic organisms and thermophilic milks. The
organisms involved in their manufacture, metabolites including
flavor compounds produced and their proposed mechanism in
probiotic dairy products are given in Table 2 Dry cultured milk
products, whey based cultured beverages and several dietetic
preparations also find place in the booming health food market.
Cultured Milk
Cultured milk is a collective name applied to a wide range
of mesophilic fermented milks with a number of characteristics in common. Mesophilic organisms are those with growth
optima between 20C and 30 C. The starters used for fermentation consist of homofermentative mesophilic LAB and of aroma
487
producers (Driessen and Puhan, 1988). Mesophilic lactic cultures generally grow in the temperature range of 1040 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 diacetyl 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 cooling 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
for 3 min or 85 C for 30 min (Harland et al., 1955; Hillier and
Lyster, 1979).
Lowering of pasteurization temperature of milk results in decreasing firmness and retarded acidification. Ultra High Temperature (UHT) sterilized milk and other high temperature treated
milks also result in lower viscosity, age-thickening and a cooked
flavor in cultured milks. Homogenization of milk at 55 C and
20 MPa is sufficient to get good distribution of fat. Decreasing milk solids-not-fat content results in taste difference. The
product may turn flat and watery and the defect known as
astringent may occur. Increasing MSNF of milk leads to a
full taste, higher viscosity, and a stable cultured milk without
wheying off during cold storage.
Dry Cultured Milk Products

Extensive research has been carried out on various dry cultured products including yoghurt, acidophilus milk, kumiss,
and kefir, usually combined with additives that will enhance
the nutritive quality of the final product. Starters for dry cultured beverages are streptococcus thermophilus, Lactobacillus
bulgaricus, Lactobacillus acidophilus (LA), Kefir grains, and
Bifidobacterium adolescens among others (Caric, 1994). Very
little scientific work has been published in this field and the
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
differs somewhat from that for conventional cultured products
(Krsev, 1989). Milk is heated to 90 C95 C for 20 min prior
to culturing. A total solids content of 30% has been found to
be most favorable. Concentration is accomplished either by
vacuum evaporation or ultra filtration. The advantage of using concentrated milk for culturing is volume reduction, and
certain stimulation is provided to microorganisms in this way.
488
Himalayan regionNepal
and Bhutan
India and neigh boring countries
Southcone countries of latin

america.
West AfricaMali.
Middle-east Syria
Southern and eastern Africa

general
Southern and Eastern AfricaEthiopia
Lassi
Mahi
Shrikhand
Mishti doi
Chaas ((Buttermilk)
Dahi
Sour butter milk.

Yoghurt.
Kadam (fermented milk).
Shenglish (Sorke)
Keshkeh
Shenineh
Labaneh (laban mousafa)
Laban
Arrera (sour butter milk).
Fermented milks and

concentrated fermented milks
Irgo (fermented milk).
Hard fermented milk curd.
Product
Traditional fermented milk products of different countries
Country/Region
Table 1
Souring/coagulation of the raw milk in a smoked clay pot or bottle gourd, in warm
place, whey removed for concentration
Milk utensils smoked by burning chips of Olea africana or Acacia busia.
Similar to irgo except that there is daily removal of whey and the addition of fresh milk
until the vessel is filled with hard curd
Byproduct of butter making, a beverage with milk fat content 1 to 3%, rich in protein,
lactose, minerals, and vitamins
Cow, sheep, or goat milk heated to 80 C, cooled to 3740 C, innoculated with LAB
or with a small amount of a previous batch of laban, for about 4 h
A drained laban or drained yoghurt with combined characteristics of laban and cheese
(1823% dry matter, pH 5 to 5.5)
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.
Made from laban (4550% dry matter), spices and chilli added for taste
Made by mixing laban with fine wheat.
The mixture is dried and ground into a powder
Popular traditional beverage or thirst quenching drink
Residual milk is accumulated and allowed to sour for few hours or several days
depending on season
Soured milk churned to produce butter milk
Milk fermented with a mixture of Lactobacillus delbrueckii subsp. bulgaricus and
Streptococcus thermophilus. The fermentation of lactose to lactic acid prevents milk
spoilage due to the growth of contaminating bacteria
Yoghurt-like product made from cow milk, buffalo milk, or mixture of two with
addition of starter into boiled and cooled milk with mild pleasant flavor, a clean acid
taste, and a yellowish creamy-white color
Sweetened varety of dahi containing sugar, Artificial color, caramel, and jaggery.
Produced by the churning of soured milk (dahi). Contains 12% fat and is rich in
protein and lactose.
Concentrated dahi (Chakka) mixed with the required amount of sugar, condiments
and flavor.
A refreshing beverage from dahi consumed sugared or salted
Traditional drink made from whole or skimmed milk dahi fermented by natural souring
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.
Technology and nutritional significance
De, 1980; Aneja, 1989
http://www.fao.org/docrep/003/
t0251e/T0251E04.htm#ch2
Bekele and Kassaye, 1987
Bekele and Kassaye, 1987;

Kerven, 1987; Shalo, 1987.
References

Table 2
Probiotic microorganism, metabolites and proposed mechanism in dairy products
Product
Biogurt
Acidophilusyeast milk
Probiotic dahi
Bifidus milk
Bifighurt
Biogarde
Biokys
Special Yoghurt
Cultura
Cultura drink
Progurt
aMetabolites; bflavor
Metabolitesa,/flavorb compounds/probioticc property
Microorganisms involved
Acidophilus milk
Acidophilus paste
Acidophilus buttermilk
Acidophilus yoghurt
489
L. acidophilus
L. acidophilus
L. acidophilus
L. acidophilus, S.thermophilus, L.
delbrueckii.subsp.bulgaricuss.
L. acidophilus, S. thermophilus
L. acidophilus, lactose fermenting yeasts
L. acidophilus, L. lactis, L lactis subsp diacetylactis
Bifidobacterium bifidum, B. longum
B. bifidum, S. thermpophilus
B. bifidum, L. acidophilus, S. thermophilus
B. bifidum, L. acidophilus, P. acidilactici
B. bifidum, L. acidophilus, S. thermophilus, L.
delbrueckii subsp. bulgaricus
B. bifidum, L. acidophilus
B. bifidum, L. acidophilus
S.lactis subsp. diacetylactis, S. lactis subsp.cremoris,
l. acidophilus, and/or B. bifidum
Maintenance of normal intestinal florac, acidophilina

-doAcetaldehydeb
Diacetylb enhanced digestibility, prevents constipation

Removal of toxic aminesc, strengthening of host immune systemsc
Reduction of serum cholesterol
Diacetyla Allieviates lactose maldigestionc
compounds; cprobiotic property.
However, the desired amount of inoculam varies considerably

from 16% according to various authors. Even starter quantities
as high as 1015% have been reported. Various levels of lactic
acid in concentrated milk prior to spray drying were developed.
Most often acid ranges from 0.61.1%. Sometimes treatments
intended to minimize the heat-induced changes and to increase
starter survival during drying are carried out as well. Spray drying temperatures are lower than those commonly used for milk
drying and range from 145175 C (inlet air temperatures). Data
have been reported for drying cultured beverages by freezedrying on a laboratory scale. The resulting product is of good
solubility and contains viable microflora after recombination.
Kumar and Mishra (2003) developed mango soy fortified yoghurt powder. The nutritional and therapeutic value of yoghurt
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
the product increased.
Whey Based Cultured Dairy Products

Current worldwide popularity of fruit flavored drinkable yoghurt offers an excellent opportunity for incorporation of whey
into the development of cultured fruit flavored products (Singh,
2001). Proper amount of stabilizer coupled with heat processing
of the ingredients and homogenization are important aspects in
the manufacture of fermentable cultured dairy drink (Dordevic et al., 1982). For making drinks from sweet or acid whey,
the standardized method involves adding sugar to filtered whey,
pasteurization at 80 C for 5 min, homogenization at 70 C, incubation at 43 C with 2% Lactobacillus helveticus starter for
1517 h to the pH 3.83.95, repasteurization at 85 C with 5 min
holding, addition of 47% fruit juice concentrate, rehomogenisation, cooling to 50 C and packing into retail containers. The
drink contained 11.6513.1% total solids, 11.2711.65% total

sugar, 0.660.78% protein, 0.20.3% fat, and 0.420.46% minerals. Mango-molke mix, a popular whey beverage marketed
in Europe contains bifidobacteria culture along with whey and
mango juice. Probiotic attributes of LAB may be incorporated
to develop fermented whey beverages. Such beverages may be
beneficial for the people suffering from gastro-intestinal tract
disorders and it also provides nutritional and therapeutic soft
drinks (Singh, 2001). Kumar and Tiwari (2003) showed that
good quality whey based fermented milk beverage can be made
from a mixture of cheese whey and milk. The fermented beverage made by admixing 70% of cheese-whey, 0.3% CMC with
the milk resulting in acceptable whey based fermented milk
beverage.
Thermophilic Fermented Milks

The term thermophilic should be reserved for microorganisms whose optimum growth temperature lies between 55 and
75 C. In dairy industry, it tends to be employed to describe
cultures that are most active between 35 and 40 C. According
to Bianchi-Salvadori (1981) thermophilic yoghurt starters do
not form part of the natural intestinal flora of man nor do they
implant themselves in the intestines. It has, however, been suggested that L. delbrueckii subsp. bulgaricus and S. thermophilus
can establish themselves in the intestine and gradually dominate the natural microflora. In vitro, studies have indicated that
L. delbrueckii subsp. bulgaricus is inhibited by bile salts (Lembke, 1963). However, these bacteria are also able to resist a high
degree of acidity and so it is quite feasible that a proportion of
bacteria ingested will reach the intestine in a viable state (Acott
and Labuza, 1972). Mabbit (1977) supports the hypothesis that
certain strains of L.delbrueckii subsp. bulgaricus could survive
and compete in the human intestine. This possibility is of great
490
importance since it would ensure the absence of putrefactive

microorganisms and hence protect the intestinal health of the
consumer (Dellaglio, 1984).
Fermented Dairy Beverages

The demand for fermented milk beverages is on the rise due
to their positive health effects and nutritive value. The general
requirements of fermented milk beverages are that they should
be light, low calorie, for example, drinking yoghurt has 30%
less energy than conventional yoghurt, refreshing (not causing
thirst), tasteful of agreeable mouth feel, and smooth in texture. Milk like soft drinks mainly prepared with yoghurt and
mesophilic starter cultures and nonsoft drinks, for example, Kefir and Kumiss with alcohol production fall in the category of
fermented milk beverages. Acidified milk drinks (AMDs) need
a stabilizer, for example, high methoxy pectin if whey formation is to be avoided. A stabilizer can act in different ways.
An increased steric repulsion between the casein micelles may
be introduced, thus preventing flocculation. Alternatively, a kinetic barrier may be imposed against extensive aggregation.
Casein micelles in milk (pH 6.7) are generally assumed to stay
in the suspended state as the result of steric repulsive interactions between the micelles. On acidification of milk to a pH
value around 4, as is done during the preparation of yoghurt,
the native mechanism of stabilization of casein micelles fails.
This failure is believed to be related to the collapse of the extended conformation of -casein chains (Holt, 1982 and De
Kruif, 1998). At pH 6.7 these chains protrude from the surface
of the casein micelle in order to maximise their entropy. This
same tendency to maximize entropy of -casein chains causes
the micelles to have a repulsive mutual interaction because overlap of -casein chains of neighboring micelles would result in a
loss of entropy of the chains. This phenomenon is called steric
stabilization. In order to stabilize an AMD of 8.5% milk solids
(not fat), high methoxy pectin has to be added at concentrations
around 0.3% w/w (Trompa et al., 2004). It was found that up
to 90% of this pectin added as a stabilizer to AMDs is not directly interacting with the milk gel particles (largely consisting
of casein micelles). This nonadsorbing fraction of pectin, which
is, however, necessary to produce a stable AMD can be taken
out of the stable system without loss of stability. Another way
to decrease the amount of ineffective pectin in the AMD is to
increase the energy input during the homogenization step, that
is, after the addition of pectin. This will increase the adsorption
rate of the pectin, and therefore allows for a smaller overall
pectin concentration.
The steps in the manufacture of fermented dairy beverages
include selection of a milk base with low total solids and low
proteins (Rossi and Clementi, 1983; Dellaglo, 1984), selection
of additives such as fruit juice concentrate, colors, artificial
sweetener, sugar stabilizers, etc. taking into consideration their
interactions with fermented milk components (Rasic and Kurmann, 1988), Low temperature (e.g., <75 C) and short time
treatment in order to prevent deposit formation by whey pro-
teins, that is, sedimentation (Kang and Lee, 1984; Towler, 1984;
Hege and Kessler, 1986). Slow acidifying starters having limited
afteracidification ability; good aroma production; low ropiness; and low carbon dioxide production are selected for use
in fermented beverages. Streptococcal cultures are the best for
plain beverages. Yeast containing cultures can give the beverage excellent taste, but the gas production may lead to blowing
of packages (Koroleva et al., 1983, 1984; Rasic and Kurmann,
1988). Fermentation results in acidification down to pH 4.6 for
a complete casein coagulation which prevents whey separation,
too strong an acidification masks aroma, sweetness, and causes
a possible destabilization of additions. Mixing of the coagulum
may be carried out with a static turbine mixer or even better homogenizing at lower temperature, for example, 4045 C
without pressure, Supplementary dilution may be carried out by
addition of fruit juices, water, fresh milk, and vegetable juices,
for example, coconut, soy, whey, etc.; carbonation of the product
is also possible (Choi and Kosikowski, 1985).
Yogurt Beverages
Drinking yogurt is essentially stirred yogurt which has total solids content not exceeding 11% and which has undergone
homogenization to further reduce the viscosity; flavoring and
coloring are invariably added. Heat treatment may be applied to
extend the storage life. High Temperature Short Time (HTST)
pasteurization with aseptic processing will give a shelf life of
several weeks at 24 C, which UHT processes with aseptic
packaging will give a shelf life of several weeks at room temperature.
Cultured Buttermilk
This product was originally the fermented byproduct of butter manufacture, but today, it is more common to produce cultured buttermilks from skim or whole milk. The culture most
frequently used is S. lactis, perhaps also spp. cremoris. Milk is
usually heated to 95 C and cooled to 2025 C before the addition of the starter culture. Starter is added at 12% and the
fermentation is allowed to proceed for 1620 h, to an acidity of
0.9% lactic acid. This product is frequently used as an ingredient
in the baking industry, in addition to being packaged for sale in
the retail trade.
Acidophilus Milk
Acidophilus milk is traditional milk fermented with LA,
which has been thought to have therapeutic benefits in the gastrointestinal tract. Skim or whole milk may be used. The milk
is heated to high temperature, for example, 95 C for 1 h, to reduce the microbial load and favor the slow growing LA culture.
Milk is inoculated at a level of 25% and incubated at 37 C
until coagulated. Some acidophilus milk has acidity as high as
1% lactic acid, but for therapeutic purposes 0.60.7% is more

common.
Another variation has been the introduction of a sweet acidophilus milk, one in which the LA culture has been added but
there has been no incubation. It is thought that the culture will
reach the gastro intestinal (GI) tract where its therapeutic effects will be realized, but the milk has no fermented qualities,
thus delivering the benefits without the high acidity and flavor,
considered undesirable by some people.
Sour Cream
Cultured cream usually has a fat content between 1230%,
depending on the required properties. The starter is similar to
that used for cultured buttermilk. The cream after standardization is usually heated to 7580 C and is homogenized at >13
MPa to improve the texture. Inoculation and fermentation conditions are also similar to those for cultured buttermilk, but the
fermentation is stopped at an acidity of 0.6%.
Others
There are a great many other fermented dairy products, including Kefir, Kumiss, beverages based on bulgaricus or bifidus
strains, labneh, and a host of others. Many of these have developed in regional areas and, depending on the starter organisms
used, have various flavors, textures, and components from the
fermentation process, such as gas or ethanol.
Fermented Dietetic Preparations

Dietetic foods are manufactured to meet particular nutritional needs of people whose normal processes of assimilation
or metabolism are changed, or for whom a particular effect is
obtained by a controlled intake of food or certain nutrients.
They may be formulated for people suffering from physiological disorders or for healthy people with additional needs (Bender, 1975). The manufacture of dieteic-fermented milks causes
problems with texture (correction with ropy starter cultures and
hydrocolloids) and with flavor (correction with mild acidifying
and aroma forming cultures, lactose- hydrolysis, skim-milk concentrate, fruit concentrates, sweeteners, etc.). Fermented milk
products fortified with some dietary components (fiber, vitamins, phospholipids, minerals, other bioactive substances). At
present, the most frequently produced fermented dietetic products are calorie reduced and dietary fiber fortified (separated and
combined ones). A small number of dietetic products have been
developed for adults (obesity, sports activity, etc.) and for elderly people. Only a few of the presently manufactured dietetic
preparations are fermented, a factor which certainly become of
more significance in the future. The use of selected intestinal
bacteria starter cultures for the preparation of fermented milk
491
products will be an expanding product area. Sarkar and Misra

(2001) attempted to incorporate Bifidobacterium bifidum NDRI
and propionibacterium freudenreichii subsp. Shermanii MTCC
1371 along with Yoghurt- YH-3 to obtain dietetic yoghurt with
enhanced nutritional and therapeutic characteristics. Dieteic yoghurt was obtained from skim milk (0.5% fat, 7.64% SNF),
heated to 95 C for 30 min at 1% level each and incubated at
42 C. The dietetic yoghurt possess desirable technological and
dietetic characteristics including antibacterial activity against
pathogenic test organisms. The viable cell populations obtained
in the product were within the range required for successful
implantation in the intestine.
FUNCTIONAL ASPECTS OF FERMENTED

MILK PRODUCTS
Fermented Products as Vehicles for Fortification
Fortification of foods can be an efficient tool to combat micronutrient deficiencies. The successful application of food fortification technology is based on consideration of compatibility
of vehicle, fortificant, and process. Modified foods including
those that have been fortified with nutrients also fall within the
realm of functional foods (ADA reports). According to American Dietetic Association (ADA) functional foods including
whole foods, fortified enriched or enhanced foods have potentially beneficial effect on the health when consumed as apart
of varied diet on a regular basis at effective levels. Fermented
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
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
level of 20-ppm iron in the reconstituted product gave acceptable results (Coccodrilli and Shah, 1985). Enrichment has been
used interchangeably with fortification (FAO/WHO, 1994), but
elsewhere it has been defined as the restoration of vitamins and
minerals lost during processing (Hoffpauer and Wright, 1994).
Probiotic Applications
The claimed beneficial effects from the consumption of fermented milks were once a debated issue. Research conducted
since the turn of the century has however, enhanced the understanding of the therapeutic effects resulting from the consumption of these products. The probiotic products are now considered helpful in maintaining good health, restoring body vigor,
and in combating intestinal and other disease disorders (Mital
and Garg, 1992). Most scientific papers refer to research using
L. acidophilus and bifidobacterium species as dietary cultures.
Nearly all probiotics currently on the market contain Lactobacilli, Streptococci, Enterococci, or Bifidobacteria. In contrast
to Japan, where freeze-dried microorganisms are consumed by
492
a substantial part of the human population, in Europe, probiotic action toward humans is only claimed for certain fermented
dairy products (e.g., yoghurts). Those species that have been
extensively studied so far, with several experimental inoculation of milk for yoghurt manufacture (Prevost & Divies, 1988).
Additional benefits of microencapsulation of cells include: protection of cells inside the beads from bacteriophages (Steenson et al., 1987); increased survival during freeze drying and
freezing (Kearney et al., 1990; Sheu and Marshall, 1993; Sung,
1997) The trials on man were mainly carried out with the two
yoghurt bacteria Streptococcus thermophilus and Lactobacillus
bulgaricus. L. casei, Bifidobacteria, and L. acidophilus has also
received important scientific interest, however, only a few human studies have been reported. From the technological point
of view a good probiotic should be stable and viable for long
periods under storage, should be able to survive the low pH
levels of the stomach, be able to colonize the epithelium of the
Table 3
gastrointestinal tract of the host, should not be pathogenic and,

last but not least, must be capable of exerting a growth promoting effect or a resistance to infectious diseases (Kalantzopoulos,
1997). Protection of probiotics by microencapsulation in hydrocolloid beads has been investigated for improving their viability
in food products and the intestinal tract (Rao et al., 1989). This
has been proposed for various dairy fermentations (Champagne
et al., 1992a, 1992b, 1994) such as fermentation of whey (Audet
et al., 1989) and continuous Kim and Yoon, 1995); and greater
stability during storage (Kim et al., 1988; Reuter, 1990; Kebary
et al., 1998). Many health benefits have been attributed to fermented dairy products and probiotic microorganisms (Salminen
et al., 1998).
The therapeutic significance of probiotic organisms is summarized in Table 3. In order to exert positive health effects, it
is generally assumed that the microorganisms need to be viable. Therefore, the International Dairy Federation (1997) has
Fermented products and therapeutic significance
Clinical condition/symptoms
Lactose maldigestion
Manifested by the presence of breath
hydrogen derived from fermentation
of the lactose in the large intestine,
abdominal pain, meteorism, bloating,
flatulence and diarrhea.
Hepatic encephalopathy
A neurological disorder where
Detoxification of ammonia produced
in the intestine is impaired in patients
with liver failure.
Side effects of radiotherapy
Radiotherapy alters the intestinal
microflora, vascular permeability of
the mucosa and intestinal motility.
Tumor or defective immune systems
High serum cholesterol levels
Renal mal function
Health benefit of fermented products
Reference
Viable yoghurt well tolerated by lactose-deficient

subjects, L.acidophilus aids lactose digestion.
The presence of bacterial b-galactosidase in the
viable yoghurt culture.
Morley, 1979; Gilliland, 1989; Kim and Gilliland, 1983
Alteration of the intestinal microflora

A decrease in faecal urease, a lowering of blood
ammonia and clinical improvement when treated
individually with L. acidophilus, Lactobacillus
GG, and E. faecum. SF68
Macbeth et al., 1965; Kavasnikov and Sodenko, 1967;

Read et al., 1968 Loguerolo et al., 1987
Treatment with fermented milk containing NCFB

1748 significantly decrease pelvic radiotherapy
associated diarrhea
Lactobacilli and their metabolic products modify
both the immune responses and antitumor
activities.
Enhanced mainly by activating macrophage
functions and increasing the activity of natural
killer cells and T-cells, maintenance of normal
intestinal flora
Help removal of dietary procarcinogens.
L.acidophilus strains and some bifidobacteria
species lower cholesterol
Salminen et al., 1998 ; Kansal, 2001
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.
Kansal, 2001
Varnam and Sutherland (1994). Anand et al., 1985
Benno et al., 1984

Mann and Spoerry, 1974; Kawamura et al., 1981;
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)
defined fermented milk as a milk product fermented by the action of specific microorganisms and resulting in reduction of
pH and coagulation. These specific microorganisms shall be
viable, active, and abundant (at least 107 cfu/g) in the product to the date of minimum durability. Probiotics are defined as
live microbial food supplements which beneficially influence the
host by improving its intestinal microbial balance (Fuller, 1989;
Ziemer and Gibson, 1998). Both definitions emphasize the viability of microorganisms. Whether viable microorganisms are
necessary for specific health benefits remains unclear. Health
benefits discussed are: alleviation of lactose maldigestion, effects on diarrhoea, immune-stimulation, antitumor activity, antimutagenic activity, reduction of serum cholesterol, and effects
on candidiasis. Many of the studies discussed here were not
conducted for the purpose of determining the efficacy of nonviable bacteria or fermented milks, but killed microorganisms
have often been used as placebo. The results from these studies
give an indication of the activity of viable versus nonviable microorganisms and assist in defining the need for probiotics to be
viable.
493
Future Research Prospects

The development of more probiotic products by the incorporation of probiotic organisms into the manufacturing process
for well-accepted traditional dairy products is to be explored
significantly. The development of convenience based dry cultured products containing viable bacteria by various techniques
such as microencapsulation and the fortification of such powders
or concentrated products with minerals and vitamins are gaining importance. The preparation of suitable blends containing
healthful ingredients such as dietary fiber, natural vitamins and
folic acid also offers new possibilities for this widely expanding
research area. The formulation of various health drinks and dietetic preparations as value added products based on traditional
fermented products will definitely bring more opportunities to
the beverage industry. There is a need to intensify research to
distinguish the therapeutic benefits of viable and nonviable organisms in different fermented products apart from the general
nutrient enhancement achieved.
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Critical Reviews in Food Science and Nutrition

Fermented Milks and Milk Products as Functional

V. K. Shiby & H. N. Mishra

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Critical Reviews in Food Science and Nutrition, 53:482496 (2013)

Fermented Milks and Milk Products

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FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODSA REVIEW

functionality of a product can be targeted to a special disease or

face Methodology has been successfully used in modeling of

The rate of lactate production

The rate of lactose utilization

V. K. SHIBY AND H. N. MISHRA

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P is lactate concentration (gl1),

Common Organisms and Pathways

FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODSA REVIEW

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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

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V. K. SHIBY AND H. N. MISHRA

Escherichia coli outgrowth by a number of possible mechanisms

constituents, inhibition to harmful bacteria of gastrointestinal

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FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODSA REVIEW

Lactose metabolism by Leuconostocs (Cogan, 1985).

TECHNOLOGY OF FERMENTED MILKS

Dry Cultured Milk Products

India and neigh boring countries

Southcone countries of latin

Southern and eastern Africa

Sour butter milk.

Kadam (fermented milk).

Labaneh (laban mousafa)

Arrera (sour butter milk).

Fermented milks and

Traditional fermented milk products of different countries

Technology and nutritional significance

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De, 1980; Aneja, 1989

Bekele and Kassaye, 1987

Bekele and Kassaye, 1987;

FERMENTED MILKS AND MILK PRODUCTS AS FUNCTIONAL FOODSA REVIEW

Probiotic microorganism, metabolites and proposed mechanism in dairy products

Metabolitesa,/flavorb compounds/probioticc property

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Maintenance of normal intestinal florac, acidophilina

Diacetylb enhanced digestibility, prevents constipation

Diacetyla Allieviates lactose maldigestionc

compounds; cprobiotic property.

However, the desired amount of inoculam varies considerably

Whey Based Cultured Dairy Products

drink contained 11.6513.1% total solids, 11.2711.65% total

Thermophilic Fermented Milks

V. K. SHIBY AND H. N. MISHRA

importance since it would ensure the absence of putrefactive

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Fermented Dairy Beverages