Nutritional Properties of Fermented Milk Products

Download as pdf or txt
Download as pdf or txt
You are on page 1of 7
At a glance
Powered by AI
The document discusses the nutritional properties and potential health benefits of fermented milk products like yogurt. It mentions evidence that fermented milks may help with lactose intolerance and could potentially reduce cancer risk.

The document discusses evidence that fermented milks may help improve tolerance to lactose for those who are lactose intolerant. It also mentions potential for certain cultures to reduce cancer risk, though evidence is still limited.

Examples of fermented milk products mentioned include yogurt, viili, koumiss, kefir, and milk products containing Lactobacillus acidophilus.

Vol50, N o 1 February 1997

International Journal of Dairy Technology

Nutritional properties of fermented milk products


JUDITH BUTTRISS
5-7 John Princes Street, London W l M OAP, UK

Fermented milk products such as yogurts have been consumed for several thousand years and the
belief that they are beneficial to health is probably equally ancient. But it is only in recent years
that scientific support for these beliefs has begun to build. Fermented milk products, like the milk
fr-om which they are made, are rich in protein, vitamins and minerals. However, in addition to
these purely nutritional properties, there is increasing support for a number of other health
advantages. The evidence for some of these is stronger than for others. For example, while the
support for improvement in tolerance of lactose b y maldigesters of this disaccharide is now very
robust, evidence to support the alleged ability of fermented milk products containing particular
bacterial cultures to reduce cuncer risk is still in its infancy. This paper focuses on the products
recognized by Consumers as yogurts. It includes a comparison of the nutritional value of milk and
yogurt, consideration of consumption trends and their impact on nutrition, and summarizes the
strengths and weaknesses of the evidence associated with a number of suggested health benefits
of hioferniented milks.

INTRODUCTION
Fermented milk products have been consumed
in Europe for perhaps 4000 years and yogurt is
one of the oldest and most popular of these
products worldwide. Many of the products
available today are derived from the results of
spontaneous lactic acid bacteria fermentation of
milk that arose centuries ago through the
influence of climatic conditions and local
traditions in the handling of milk. A number of
types of fermented milk products are listed in
Table 1 but mostly this paper will focus on
those recognized by consumers as yogurts.
Fermented milk products were originally
developed as a means of preserving the nutrients. Also, by fermenting milk with different
microorganisms, it has proved possible to
develop a wide range of products with different
flavours, textures, consistencies and functions.
Details of the different bacterial species used to
make fermented milk products can be found in
a review by Robinson. Yogurt is by far the
most commonly found fermented milk in the
UK. Yogurts are produced by a lactic acid
fermentation process using thermophilic strains
of bacteria. Other products such as viili, popular
in Finland, are also made via a lactic acid
fermentation process but mesophilic bacteria
are used and a mould added to give viili its
characteristic slimy consistency through a process which partially hydrolyses the fat. Other

products such as koumiss and kefir are made by


processes in which lactic acid and alcohol
fermentations are combined by use of a combination of yeast and bacteria (thermophiles in the
case of koumiss and mesophiles for kefir) (see
Korolevo2 for details). Milk products incorporating Lactobacillus acidophilus are discussed
in detail by S e l l a r ~Some
. ~ of these are referred
to as culture-containing rather than cultured
because the former do not undergo a true
fermentation process during their production.
Within the past few decades, yogurt has
gained wide consumer acceptance in Britain,
helped no doubt by its image as a healthy
food. However, its popularity must also be due
to its taste, the wide variety of types on the
market and its convenience as a dessert or snack
food. Yogurt is the most frequently consumed
chilled dessert in households in the United
Kingdom and, increasingly, consumers are
becoming aware of its versatility in cooking.
Table 2 and Fig. 1 show overall consumption
of yogurt in the UK and provide an indication of
the most popular types purchased. Consistent

Paper given at
symposium on The
current status of biofermented milks-foc US
on Europe, London,
29 October 1996.
0 1997 Society of
Dairy Technology
21

Vol50, N o I February 1997

International Journal of Dairy Technology

with consumers strong interest in health, a


variety of low fat and virtually fat free yogurts
are now available, as are products with a
reduced calorie and sugar content through the
use of artificial sweeteners.
ATTRIBUTES
NUTRITIONAL
Nutritionally, plain yogurt has a similar composition to that of the milk from which it is made
and so is an excellent source of high quality
protein, calcium, phosphorus, magnesium, zinc
and the B vitamins riboflavin, B12 and niacin.
However, there are a few subtle differences,
particularly with respect to yogbrts vitamin
content (Table 3).
Nutritional properties remain similar regardless of the method of production, eg, stirred

The UK Yoghurt Market by Sector, 1992

!t 21%

Fig. 1. Segmentation of the yogurt market, 1992. Based on Milk Marketing Board Trade
Estimates for 1992.

compared with set yogurts. However, the


composition can be modified by changes
brought about by the bacteria in the starter
culture during the fermentation process, by
synthesis or release of nutrients or other
substances by the bacteria in the starter culture,
by addition of other ingredients during manufacture, eg, skimmed milk powder, fruit or fruit
juice, and by storage conditions. There is also
the suggestion that the health properties of
fermented milks may be determined by the
nature of the culture used in their production.

Lactose
An example of how the nutritional composition
is modified by the presence of the culture
concerns the milk sugar, lactose. During fermentation, 20-30% of milks lactose is hydrolysed to its component sugars, glucose and
galactose, by the culture b a ~ t e r i a .Conse~
quently, the lactose levels in yogurt can be
lower than in milk, although this is not always
the case as skimmed milk powder or non-fat
milk solids are sometimes added during manufacture. A lower lactose content would presumably help tolerance of the product by those
with a reduced ability to digest lactose. But
clearly the explanation is not this simple
because yogurts with a fairly high lactose
content also seem to be better tolerated by such
individuals than the equivalent amount of
lactose as milk (see below).
Lactic acid is produced as a byproduct of the
fermentation process. This may act as a preservative by reducing pH. It has also been
suggested that it influences the physical properties of the casein curd (eg, to induce a finer
suspension) so as to promote digestibility, to
improve utilization of calcium and other minerals and to inhibit the growth of potentially
harmful bacteria (see G ~ r r and
, ~ Alm,6 for
reviews).
Protein
Protein is composed of amino acids. Although
the overall amino acid concentration is similar
in yogurt and the milk from which it is derived,
there is a greater proportion of free amino acids
in yogurt because of the proteolytic activity of
the bacterial culture which partially digests the
protein during fermentation. However, this
characteristic is unlikely to be of major importance as most people already digest protein
efficiently.
Fat
It has been proposed that the digestibility of fat
is improved via the action of the bacteria
present during the fermentation process, but
whether this effect really exists is highly
debatable.5,7 The overall energy (calorie) content of yogurt reflects both the fat content of the
milk from which it was made and whether or
not there has been the addition of ingredients
such as cream or sugar.

22

lnrernurionrrl Joirrnol of Dairy Technolo,qy

Vol50, N o 1 Fehruary 1997

Vitamins
The vitamin content of yogurt varies with the
type of milk used (particularly the fat content of
the milk, which influences the amount of
vitamin A and other fat soluble vitamins
present), with the strain of bacteria and with
fermentation conditions. In addition, whenever
milk is processed there is likely to be an effect
on the concentration of the more labile water
soluble vitamins, concentrations of which are
influenced by heat and/or light. Yogurt manufacture is no exception. Vitamin C is heat and
light labile, but it is more stable in the acid
conditions of fermented milk than in nmnal
milk.7
Levels of some B vitamins are reduced due to
the requirement of some lactic acid bacteria for
vitamin B12, for e ~ a n i p l e . Losses
~ . ~ of up to
90% of vitamin B12 have been reported with
specific bacterial strains, but losses are not
always this great and can be reduced considerably by use of a supplementary culture
capable of synthesizing significant amounts of
vitamin B 12.
On the other hand, several cultures are able to
synthesize the B vitamin, folk acid, increasing
the level of this vitamin present in the final
p r ~ d u c tIn
. ~ the current climate in which there
are concerns about the folate intake of women
in the early stages of pregnancy, this aspect may
prove to be a nutritional advantage.
Minerals
The fermentation process has little effect on the
mineral content of milk. Yogurt is an excellent
source of a number of minerals, especially
calcium, zinc, phosphorus and magnesium (see
Table 4). Not only are the concentrations of
these minerals high, but the bioavailability is
also generally good (ie, the proportion available
for absorption and utilization within the body).
Table 5 demonstrates this point. It lists the
number of servings of calcium containing foods
which would need to be consumed to match the
amount of calcium available from a single small
pot of yogurt (or from a glass of milk).

Some researchers have speculated that bioavailability of minerals from yogurt might even
be enhanced, compared with milk, because of
the lower (more acid) gastric pH induced by
yogurt, but scientific support for this is inconclusive and, generally, findings do not support
superior bioavailability.9

SUGGESTED
HEALTH PROPERTIES
The belief that yogurt consumption is beneficial
to health is ancient and part of folklore, having
been passed from generation to generation in
many parts of Europe. Recently, the term
probiotic has been coined to describe some of
these benefits.
An oral probiotic was defined at a special
workshop in Frankfurt as living micro-organisms which upon ingestion in certain numbers,
exert health benefits beyond inherent basic
nutrition. Probiotics may be consumed either as
a food component or as a non-food preparation.
Many health benefits have been attributed to
fermented milk products over the years, some
of which are listed in Table 6. For some of these
eg, improved lactose tolerance, a considerable
amount of evidence has been amassed as
discussed below, but others remain little more
than speculation and are far from well-established from a scientific point of view.
The job of attempting to make sense of the
available evidence is confounded by a number

23

VoI 50, N o I February 1997

of factors9 Not all the data are derived from


well designed studies and not all interpretations
are based on statistically significant data. Much
of the data concerns animal models and in vitro
experimentation, and this cannot be extrapolated directly to humans. Furthermore, it is
difficult to generalize because of the large
number of strains of microorganisms involved
which may differ considerably in their properties and effects.
Central to a number of these is the ability of
viable bacteria in 'live' yogurt and other
fermented milk products to survive passage
through the stomach. The term 'live' refers to
products which retain live bacteria after manufacture because the milk from which they were
made was heat treated prior to the addition of
the bacterial culture (heat treatment kills the
bacteria). This applies to the majority of the
brands of yogurt available today.

Complexity of the gut microflora


Many of the suggested health benefits are
associated with the concept that the gut microflora is involved in resistance to disease,"" and
that its balance can become deranged by
environmental factors and stress, thus compromising resistance. It has been suggested that
under such conditions probiotics have the
potential to manifest a beneficial effect.
This concept serves to emphasize the role of
the intestinal microflora in human health and
the complexity of the microflora ecosystem. It
is now evident that the intestinal microflora can
influence health in a number of ways-both
positive and negative. l 2 These include impacts
on nutrition, physiological function, eg, one of
the short chain fatty acids produced by colonic
bacteria (butyrate) is important in determining
the rate of colonic cell growth and differentiation,I3 drug efficacy, carcinogenesis, immunological responses, resistance to infection and
responses to endotoxins and other stresses. The
several hundred types of bacteria which comprise the microflora each contain a series of
different enzymes capable of a range of different functions, eg, conversion of substances
present in the gut to different compounds,
which may be beneficial or detrimental. Also
toxins and other substances produced by bacteria present in the gut can modify the host's
response, eg, to infection or stress. However,
beneficial microorganisms can protect against
the proliferation of harmful pathogenic ones.
So any bacteria-harmful or otherwiseentering the intestine via food are arriving in an
already very complex system. To be potentially
influential in the gut, bacteria need to be able to
survive passage through the stomach with its
extremely acid pH, and to survive the actions of
bile acids and the immune system. Other factors
that affect the ability of bacteria to grow
successfully in the colon (large bowel) include
availability of substrates and competition for
these, substrate versatility and efficiency of use,
24

International Journal

of

Dairy Technology

ability to adhere to the gut epithelium or


particle surfaces in order to remain in the
environment, and ability to produce substances,
eg, antimicrobial agents, which adversely influence the growth of bacteria already present in
the gut. There is evidence that bacteria that are
indigenous to the human gut are highly adapted
and so well able to tolerate these obstacles. l4
The extent to which diet and items within the
diet can modify microbial ecology is a question
on which little general agreement exists. This is
in part due to the difficulties associated with
defining the indigenous flora and the variability
from one person to the next. The theoretical
effects of diet are via provision of substrate, via
antibacterial or bacteriostatic effects of food
components, via an influence on gut physiology, eg, bile and acid secretion, motility etc
and, fourthly, the introduction of microorganisms via the diet may influence the existing
ecology.

Which microorganisms are involved?


The belief that fermented dairy products confer
health benefits is associated with various fermented products made using a diversity of
cultures. Most cultures used to produce yogurt
contain strains of bacteria from either or both of
the lactic acid generating genera known as
Lactobacillus spp and Lactococci spp, eg,
streptococci and enterococci. Standard cultures
contain mainly Lactobacillus bulgaricus and
Streptococcus thermophilus. Other species are
used to impart flavour (see Robinson' for a
review), It is thought that these classic yogurt
bacteria are likely to have little or no probiotic
potential as they are probably killed in the
intestine. l S
However, recently there has been particular
interest in the possible health benefits of
yogurts produced using cultures containing
Lactobacillus acidophilus and bifidobacteria,
both of which are found naturally in the human
gut. This interest probably arose initially from
the finding that infants who are entirely breast
fed have a totally different microflora in their
colons compared with bottle fed infants. In
breast fed infants up to 99% of the bacteria
present are bifidobacteria, whereas infants
receiving formula have a much more diverse
microflora.16 Gum suggests that an explanation
of this might be linked to the presence in human
milk of antibacterial substances which inhibit
pathogens but not bifid~bacteria.'~Another
explanation, also discussed by Gurr, is that the
difference in composition between human and
cows' milk (eg, differences in protein) might
induce differences in transit time of the milk
through the gut. The more rapid transit time of
human milk may result in conditions ideal for
the fermentation of lactose in the colon,
providing an acid environment inhibitory to the
growth of pathogens such as Escherichia coli
but tolerated by bifidobacteria. Whether or not
bifidobacteria are a significant advantage to the

Vol50,No 1 February 1997

baby has yet to be vigorously tested, but it is


well established that breast fed babies are less
susceptible to infection than those who have
been solely formula fed. Compared with infants, the gut and faecal microflora of older
children and adults seem to be relatively
unaffected by diet.

IMPROVED
LACTOSE INTOLERANCE
Numerous studies appear to indicate that
yogurt, particularly products containing live
bacteria, is well tolerated compared to milk by
individuals who have lactose intolerance. Such
individuals experience gastrointestinal symptoms due to a reduced ability to digest lactose,
the sugar (a disaccharide) in milk, into its
component sugars-glucose and galactosewhich can then be absorbed readily in the small
intestine. Undigested lactose cannot be absorbed and travels to the large bowel (colon)
where it is digested by the resident microorganisms, causing excess gas production,
intestinal discomfort and diarrhoea. In humans
lactase levels peak in early infancy to enable
digestion of human milk to take place efficiently. In most white Europeans levels remain
high during childhood and into adulthood,
perhaps stimulated by cows' milk consumption.
However, in as many as 70% of the world's
population (mainly non-Europeans), activity of
the enzyme, and hence ability to digest lactose
effectively, declines rapidly after weaning. This
is genetically determined and is considered to
be linked with the absence of a tradition of
dairying in Africa, India and Asia because of
adverse climatic conditions.
Lactose intolerance is not an all or nothing
phenomenon and the condition can exist to
varying degrees, depending on the extent of
loss of enzyme activity. The most likely
explanation for an improved tolerance of lactose when it is consumed as part of yogurt is the
presence of microbial (3-galactosidase derived
from the bacterial culture used in yogurt
production, which like intestinal lactase can
break down lactose to its component sugars.
Being intracellular, this enzyme survives its
passage through the stomach so long as the cell
wall of the bacteria remains intact, and so
potentially reaches the small intestine in its
active form. Kuhn and colleagues'8 suggest that
the enzyme can survive passage into the small
intestine even in non-viable but intact bacteria.
Pasteurization (and freezing) destroy the enzyme, but usually yogurt cultures are added to
the milk after it has been heat treated rather than
before.
However, the hypothesis is confounded by
the finding that lactose maldigesters tolerate
yogurts with varying levels of (3-galactosidase
equally well.I9 This suggests that factors in
addition to lactase activity, including rate of
gastrointestinal transit, may contribute. It has
been suggested that the presence in the gut of
bacterial lactase might stimulate residual in-

International Journal of Dairy Technology

testinal lactase activity. However, the results of


a double blind study provide no evidence to
support this.*'
Gurr' proposes that cultured products such as
yogurt, because of their acidity and the consequent finer dispersion of protein in the
stomach, retard the emptying of the stomach's
contents into the small intestine. Any capacity
to breakdown lactose, whether it be of microbial or indigenous origin, would then have
longer to take effect and consequently lactose
digestion would theoretically be more efficient,
even when the specific activity of the enzyme
was low.
Recent work has also suggested that the
regular consumption of gradually increasing
amounts of lactose might actually stimulate
changes in the microflora of the colon, thus
improving tolerance.*'

OTHERSUGGESTED BENEFITS
A number of other claims of health or probiotic
effects of fermented milks have been made
(Table 6).
Protection against gastrointestinal infections
Gastrointestinal infections, including diarrhoea, can result from a change in the gut
microflora caused by an invading pathogen.
Before the problem manifests itself, however,
the pathogen usually needs to establish itself in
sufficient numbers within the gut.
At the beginning of this century it was
suggested that consumption of fermented milk
products containing viable lactic acid bacteria
might interfere with the colonization and subsequent proliferation of foodborne pathogens,
thus preventing manifestation of
L hulgaricus, S therrnophilus, L acidophilus6
and also Bifdobacteriurn b i f d ~ r nhave
~ , ~ all
~
been implicated in this effect. In addition, it has
been suggested that lactic acid bacteria can
protect against antibiotic induced diarrhoea in
patients taking antibiotics capable of destroying
natural antagonists to disease producing organisms.26 Various mechanisms have been suggested including the ability of these cultures to
lower intestinal pH, which favours growth of
lactic acid bacteria, and their ability to produce
acids such as lactic, acetic, formic and propionic acids, which create an unfavourable
environment for the multiplication of pathogenic bacteria.
However, most of the evidence supporting a
role for cultured or culture containing dairy
products is derived from animal experiments
and in vitro s t ~ d i e s , ~ , ' and
~ > *findings
~
tend to
be i n c o n ~ i s t e n t But
. ~ ~ one
~ ~ promising line of
research concerns treatment of young children
with severe diarrhoea associated with various
conditions including rotavirus in f e c ti~ n.*~.~'
In
several studies, ingestion of fermented products
has reduced the duration of diarrhoea associated with rotavirus infection. There are also
25

Vol50, No 1 February 1997

reports of benefit to sufferers of travellers'


d i a r r h ~ e a . ~ .Proposed
~'
mechanisms include
immunomodulatory effects, influence on bacterial enzyme activity and competition for
receptor binding sites.3'

Relief of constipation
The administration of fermented milk products
containing lactobacilli to severely constipated
elderly patients has been reported to have
beneficial effects on bowel movement in several s t ~ d i e s . ~ , ~ '
Improved immunity
Studies in experimental animals and in vitro
have suggested that consumption of live, active
bacteria via products such as yogurt enhance
specific and non-specific immune mechanisms,
and as a consequence provide protection
against pathogens and viruses.'5 It has been
suggested that gamma-interferon may be instrumental in this
But to date,
evidence is not sufficiently strong to justify
claims that fermented milks enhance the immune response or reduce the risk of infection in
humans. In particular, it is not clear what the
implications of the experimental findings in
animal models and in vitro are for normal
healthy people.
Cholesterol reduction
Having a high blood cholesterol concentration
is considered to be one of the four major risk
factors for coronary heart disease. Interest is
growing in the possibility that some fermented
milk products may facilitate a reduction in
blood cholesterol level, specifically the low
density lipoprotein (LDL) fraction. This interest initially derived from the observation that
Masai tribesmen in East Africa consume large
quantities of yogurt like foods and have low
blood cholesterol in spite of a diet largely based
on animal products. A number of studies have
since provided support for a hypocholesterolaemic effect, although others have failed to
provide confirmation. The conflicting reports in
the literature may be explained by factors such
as differences in experimental design and in the
species and strains of bacteria used. For
example, Agerbaek and colleagues34 have reported a 10% reduction in LDL-cholesterol
after regular consumption of a fermented
product carrying a specific bacterial culture
(which included Enterococcus faecium) for 6
weeks. There was criticism of a number of
aspects of this short study, however, including
the type of placebo used-it
was not a fermented product. There was also a high initial
level of LDL-cholesterol in the treated group of
middle aged men. Other studies reviewed by
Renner9 and Schaafsma" have also demonstrated reductions in LDL-cholesterol of a
similar magnitude4.2% and 5-6%. Additional studies are underway, in which some of
the shortcomings of earlier studies are being
26

Internatioiial Journal of Dairy Technology

addressed. But further work is needed to


attempt to identify the mechanism of the
hypocholesterolaemic response, whether a
dose-response relationship exists and whether
these effects persist or are merely transient.
Such work will help assess the clinical importance of these findings."

Protection against cancer


There are reports suggesting that fermented
milk products may protect against certain types
of cancer.y There is a small amount of epidemiological support for this,3s although the
data are inconsistent. In animal models yogurt,
lactobacilli and bifidobacteria have all been
reported to inhibit the growth or cause regression of tumours which have been transplanted
or chemically induced.
Again, various mechanisms have been suggested including the potential of some strains of
lactic acid bacteria to reduce the activity of
faecal (bacterial) enzymes known to promote
the synthesis of carcinogens from available
substrates, or stimulate the host's immune
~ y s t e mHowever,
.~
there is little or no evidence
to show that these mechanisms operate in
humans, although some findings from experimental animals and in vitro studies support
these ideas. It can be concluded that, although
there are some indications of possible underlying mechanisms, evidence to date is still very
preliminary and is restricted to an indication of
changes in bacterial enzyme activity. As yet
there is no evidence that this results in a
reduction in cancer incidence and much more
work is needed before such claims can be
made.
Adverse effects
There is much interest in the potential role of
probiotics such as dairy cultures in promoting
human health, but it is important to recognize
that there might also be some adverse effects.36
It is as yet unclear whether probiotics might be
disadvantageous in young children (under the
age of 2) who are yet to establish fully an adult
gut flora. There may also be detrimental effects
in patients with autoimmune disease or certain
other underlying diseases. There is additionally
a concern about the potential to transfer to the
host the property of antibiotic resistance which
some bacterial strains carry.37

CONCLUSIONS
Regular consumption of cultured and culture
containing milk products have been claimed to
confer a wide range of health benefits. It can be
concluded that a number of investigations
support the view that yogurt (particularly 'live'
yogurt) is a well tolerated alternative to milk for
those with a reduced ability to digest lactose.
This improved tolerance is considered to be
partly due to the presence of the enzyme (3galactosidase in the bacterial culture within the

International Journal of Dairy Technology

Vol SO,No 1 February 1997

yogurt, and partly due to other factors such as


effects on transit time.
There is also growing evidence of a role for
fermented products, perhaps containing specific strains, in reducing the duration of diarrhoea in conditions such as rotavirus infection.
There is also the possibility, which still needs
substantiation, that cholesterol reducing potential exists. However, data relating to most of the
other alleged health related benefits, such as
beneficial
influences on cancer and
immunocompetence, are conflicting. Differences in experimental design and in the strain
and species of bacteria used may help explain
these inconsistencies, but as most of the work to
date has been conducted in animal models and
in vitro, the applicability of these findings to
humans remains to be established. In particular,
it is important to establish whether probiotics
can improve the health of already healthy
individuals.
Regardless of the current deficiencies in our
knowledge, fermented milk products provide a
wide range of important nutrients, and are
palatable, widely available at an affordable
price and versatile. In addition to these qualities, evidence of health benefits associated with
the presence of specific strains of live bacteria
is no longer anecdotal, and is gradually gaining
established scientific credibility.
REFERENCES
1 Robinson R K (199 I ) Micro-organisms of fermented milk.
In Therapeutic Properties of Fermented Milk Products, pp
2 3 4 4 . Robinson R K, ed. London: Elsevier Applied
Science.
2 Koroleva N S (1991) Products prepared with lactic acid
bacteria and yeasts. In Therapeutic Properties of Fermented Milk Products, pp 159-180. Robinson R K, ed.
London: Elsevier Applied Science.
3 Sellars R L (1991) Acidophilus products. In Therapeutic
Properties of Fermented Milk Products, pp 81-1 16.
Robinson R K, ed. London: Elsevier Applied Science.
4 Bourlioux P and Pochart P (1988) Nutritional and health
properties of yogurt. World Review of Nutrition and
Dietetics 56 217-258.
5 Gurr M I (1987) Nutritional aspects of fermented milk
products. FEMS Microbiology Reviews 46 337-342.
6 Alm L (1991) The therapeutic effects of various culturesan overview. In Therapeutic Properties of Fermented Milk
Prnducts, pp 4 5 4 4 . Robinson R K, ed. London: Elsevier
Applied Science.
7 IDF (1983) The effect of feeding cultured dairy products
on health. In Cultured Dairy Foods in Human Health.
Document 159, pp 18-28. Brussels: International Dairy
Federation.
8 Department of Health (1991) Dietary Reference Valuesfor
Food Energy and Nutrients .for the United Kingdom.
Report on Health and Social Subjects 41. London:
HMSO.
9 Renner L G (1991) Cultured dairy products in human
nutrition. In Bulletin of the International Dairy Frderation, No 255. Brussels: IDF.
10 Weaver C M and Plawecki K L (1994) Dietary calcium:
adequacy of a vegetarian diet. American Journal of
Clinical Nutrition 59 12388-1 241 8.
11 Schaafsma G (1996) State of the art concerning probiotic
strains in milk products. Paper given at IDF Nutrition
Week in Potsdam, Germany. Newsletter of the International Dairy Federation 145, 23-24. Brussels: IDF.
1l a Fuller R (1996) Probiotics-panacea or nostrum? Nutrition Bulletin 79, vol 21, pp 204-208. London: British
Nutrition Foundation.
12 Gurr M I, Marshall V M E and Fuller R (1984) Fermented
milks, intestinal microflora and nutrition. International

13
14

15

16

17
18

19

20

21

22
23
24
25
26
27
28
29

30

31

32

33

34

35
36

37

Dai1.y Federarion Bulletin, Document 179, pp 54-59,


Brussels: IDF.
OSullivan M G (1996) Metabolism of bifidogenic factors
by gut flora-an overview. Bulletin of the Inter-national
Dairy Feder-ation 313 23-30.
Salminen S (1996) Uniqueness of probiotic strains. Paper
given at IDF Nutrition Week in Potsdam, Germany.
Newsletter of the International Dairy Federation 145.
18-19. Brussels: IDF.
Hamilton-Miller J M T (1996) Probiotics-panacea or
nostrum? Nutrition Bulletin 79, vol 21, pp 199-203.
London: British Nutrition Foundation.
Kurman J A and Rasic J L (1991j The health potential of
products containing bifidobacteria. In Therapeutic Proprrties ($Fermented MilkProducrs, pp 117-158. Robinson R
K, ed. London: Elsevier Applied Science.
G u n M I (1981j Human and artificial milks for infant
feeding. Jour-nal of Dairy Research 48 5 19-554.
Kuhn C rt a/ (1996) Lactose intolerance-importance of
viability of lactobacilli in fermented milk products. Paper
given at IDF Nutrition Week in Potsdam, Germany.
Newsletter of the International Dairy Federation 145, 38.
Brussels: IDF.
Savaino D A (1989). In Fermented Milks: Current
Research (Proceedings of an International Congress.
14-16 December 1989, Paris). London: John Libbey
Eurotext.
Lerebours E et a1 (1989) Yogurt and fermented-thenpasteurised milk: effects of short-term and long-term
ingestion on lactose absorption and its mucosal lactase
activity in lactase-deficient subjects. American Journal uf
Clinical Nutrition 49 823-827.
Hertzler S R and Savaiano D A (1996) Colonic adaptation
to daily lactose feeding in lactose maldigesters reduces
lactose intolerance. American Journal of Clinical Nutritioti
6 4 232-236.
Metchnikoff E (1908) The Prolungarron nf Life. New
York: Putnam.
Kopeloff N ( 1926) Lactobacillus acidophilus. Baltimore
MD: Williams and Wilkins.
Rettger L G, Levy M N and Weiss J E ( 1935)Lactobacillus
acidophilus and its therapeutic applications. New Haven
CT: Yale University Press.
Yaeshima T (1996) Benefits of bifidobacteria to human
health. Bulletin of the International Dairy Federation 313
3w2.
Matalon M E and Sandine W E (1986) Lactohacillrrs
bulgaricus, Streptococcus themophilus and yogurt: a
review. Cultured Dairy Products Journal 21 (4) 6-12.
Gilliland S E (1989) Acidophilus milk products: a review
of potential benefits. Journal of Dairy Science 72
2483-2494.
Hitchins A D and McDonough F E (1989) Prophylactic
and therapeutic aspects of fermented milk. American
Journal of Clinical Nutrition 49 675484.
Saavedra J M et a1 (1994) Feeding of B$dohacterium
hifdium and Streptococcus thermophilus to infants in
hospital for prevention of diarrhoea and shedding of
rotavirus. Lancet 344 1046-1049.
Salminen S and Tanaka R (1996) Role of cultured and
culture-containing dairy products and probiotic bacteria in
health and disease. Newsletter of the International Dairy
Federation 145, 32-34. Brussels: IDF.
Tvede M (1996) Potential of probiotic strains in stabilizing
intestinal microflora to prevent gastrointestinal infection.
Paper given at IDF Nutrition Week in Potsdam, Germany.
Newsletter of the International Dairy Federation 145, 30.
Brussels: IDF.
Andrews P J and Borody T J (1992) Putting back the
bugs; bacterial treatment relieves chronic constipation
and symptoms of initable bowel syndrome. Medical
.lour-nu1 of Australia 159 6 3 3 4 3 4 .
De Simone C eta/ (1986) The adjuvant effect of yogurt on
production of gamma-interferon by Con A-stimulated
human peripheral blood lymphocytes. Nutrition Reports
International33 419433.
Agerbaek M, Gerdes L V and Richelsen B (1995)
Hypocholesterolaemic effect of a new fermented milk
product in healthy middle-aged men. Eurnpean Journal of
Clinical Nutrition 49 346-352.
vant Veer P et a / (1989) Fermented milk products and
r
49 402W023.
breast cancer. C a r ~ e Research
van der Kamp, J (1996) Safety considerations regarding
probiotic strains. Paper given at IDF Nutrition Week in
Potsdam, Germany. Newsletter of the International Dairy
Federation 145, 27-28. Brussels: IDF.
Jett B D et a1 (1994) Virulence of enterococci. Clinical
Microbiology Revieux 7 462478.

27

You might also like