Anaerobe (1997) 3, 185190

Fermented Products with Probiotic Qualities

G. Kalantzopoulos
Agricultural University of
Athens, , Botanikos, 11855
Athens, Greece
(Received 14 October 1996,
accepted in revised form 6 May
1997)
Key Words: fermented
products, probiotics,
Bifidobacteria, lactic acid
bacteria

For several centuries, fermented products derived from plant or animal

materials have been an acceptable and essential part of the diet in most parts
of the world. Health benefits have also often been associated with them.
Probiotics can be defined as fermented food containing specific live
microorganisms or a live microbial food or feed supplement, which
beneficially effects the human or the host animal by improving its intestinal
microbial balance.
Nearly all probiotics currently on the market contain Lactobacilli, Streptococci,
Enterococci or Bifidobacteria. In contrast to Japan, where freeze-dried
microorganisms are consumed by a substantial part of the human
population, in Europe, probiotic action towards humans are only claimed
for certain fermented dairy products (e.g. yoghurts). Those species that have
been extensively studied so far, with several experimental trials on man, are
the two yoghurt bacteria Streptocaccus thermophilus and Lactobacillus bulgaricus, L. casei and Bifidobacteria. L. acidophilus has also received important
scientific interest, however, only a few human studies have been carried
out.
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 colonise the epithelium of the 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.
The beneficial effects of probiotics are mainly contributed to a direct
antagonistic effect against specific groups of microorganisms (Enteropathogenes), by an effect on the metabolism in the gut or by a stimulation
of systemic or mucosal immunity.
We will present major proven health benefits of milks fermented with those
bacterial species and discuss, where possible, the impact of the specific
selection and utilisation of particular strains.
1997 Academic Press

Introduction
Fermented products have been consumed for thouE.mail: kalatz@auadec.aua.ariadne-t. r

1075-9964/97/020185 + 06 $25.00/0/an970099

sands of years and various health benefits have been

associated with these products for many years. However, it was only in the 1970s that the possible
probiotic effects related to the consumption of fermented products aroused increased scientific
interest.
1997 Academic Press

186

G. Kalantzopoulos

Fermented foods derived from plant or animal

materials are an acceptable and essential part of the
diet in most parts of the world. They include wide
diversity of raw materials such substrates by using
technology from the most primitive to the most
advanced and achieving an astounding range of
sensory and textural qualities in the final products.

Why Fermented Products?

The fundamental reasons for the development and
acceptance of fermented foods can be variably
ascribed to preservation, improved nutritional properties, better flavour/aroma, upgrading of substrates to
higher value products and improved health aspects. In
more recent times, in many affluent communities
novelty and/or trendiness played a role. All these
properties are the result of the activity of a population
of bacteria strains, mainly of lactic acid bacteria or
microbial combinations with pro- and prebiotic potential in different organic substrates.
The contribution of biotechnology, has been very
important during the last few years as it offers the
possibility of selecting and using new sources, to
increase the yield of sources already used, to introduce
specific functional properties in raw materials or
ingredients, to improve the nutritional value and the
bioavailability of nutrients and flavour.
The predominant microflora in these products is
composed by strains of Lactobacilli, anaerobic or semiaerobic.

Health Advantages
The nutritional value of a particular food depends on
its digestibility and its content of essential nutrients.
Both digestibility and nutrient content may be
improved by fermentation. During fermentation the
enzymatic activity of microbial culture may predigest
the macronutrients [1].
The beneficial effect of predigesting proteins is
relatively small for healthy people, with normal
gastrointestinal function. Nevertheless, it is known,
that the clots of curd that form in the stomach after the
ingestion of yoghurt are notably smaller than after the
ingestion of milk and this will increase proteolysis in
the stomach.
Predigesting carbohydrates may greatly improve
the tolerance for certain foods. For example, it is a
well-known fact that due to the low lactose content of
yoghurt in combination with the lactase activity of the
microbial culture, yoghurt is better tolerated than milk

by lactose-deficient individuals. The lactase activity of

the culture of Lactobacillus bulgaricus and Streptococcus
thermophilus resists passage through the stomach and
assists in the digestion of lactose in the intestine.
Several lactobacilli, such as strains of Lactobacillus
buchneri, L. brevis, L. cellobiosis, L. fermentum and L.
salivarius; produce alpha-galactosidic activity and can
therefore breakdown alpha-galactosidic bounds in
raffinose and stachyose. Therefore, they can be used to
eliminate the gas-producing carbohydrate fraction in
legumes and soya bean milks. The acid formed during
fermentation of the carbohydrates may help in lowering the pH of the gastric contents and this is
certainly beneficial for elderly people, who often have
a reduced gastric acid secretion.
With regard to fats, yeasts, many bacteria and
moulds used in fermentation display lipolytic activity,
the nutritional significance of this is probably small.
Fermentation may reduce the content of nondigestible material in plant foods, like cellulose,
hemicellulose and polygalacturonic and glucuronic
acids. Breakdown of these compounds may lead to an
improved bioavailability of mineral and trace elements. During fermentation extra essential nutrients
may be synthesized, such as vitamins, amino acids
and proteins.
Fermented milks are claimed to contain a number of
biologically active compounds which may contribute
to human health. These compounds include bacteria
used for fermentation, their metabolic products and
components derived from milk. Certain strains of
lactic acid bacteria, have been found probiotic in vivo
as such, but in fermented milks the peptides derived
from hydrolysed milk proteins could contribute to the
probiotic properties. In fact peptides of different
activities have been detected in various milk proteins
on proteolysis with digestive enzymes or starter
bacteria.
These peptides include opioid, antimicrobial, anticancer, anti-hypertensive, immunomodulatory and
mineral carriers. Both casein fractions and whey
proteins are known to act as precursors for the above
bioactive peptides [2].
Several clinical studies have shown that the Lactobacillus GG strain has beneficial health effects, for
example, in the treatment of gastrointestinal infections. The factors or mechanisms producing such
effects are not fully understood but stimulation of the
mucosal immune system has been implicated. It was,
therefore, interesting to investigate whether immunoactive peptides would be formed during fermentation of milk with Lactobacillus GG.
These preliminary results would suggest that lactic
acid bacteria [3], used in fermented milks alter the
immunogenic properties of milk proteins. This finding
may be of importance for example in the selection of

Fermented Products with Probiotic Qualities

probiotic strains of lactic acid bacteria, development of
hypoallergenic infant formulas and functional foods.

Therapeutic properties of fermented products

At the beginning of the century, Metchnikoff attributed almost magical health-giving properties to fermented milk, including prolongation of life and
reduction of the effect of the putrefractive process in
the intestine [4].
After a long period of inactivity, a lot of research has
been carried out over the last decade. This involves
the following topics.

Reduction of serum cholesterol

A high serum cholesterol concentration is generally
considered as high risk factor in the development of
cardiovascular disease. Fermented foods may reduce
the serum cholesterol concentration by reducing the
intestinal absorption of dietary and endogenous cholesterol or inhibiting cholesterol synthesis in liver.
It has been shown [5] that certain strains of
Lactobacillus acidophilus might assimilate cholesterol in
the intestine and reduce its absorption. Also deconjugation of bile acids by L. acidophilus might enhance the
fecal excretion of steroids and reduce serum cholesterol. Unfortunately, no data have yet been presented
to provide the desirable effect in man. Therefore,
careful selection of strains, with good technological
properties and preferentially isolated from the indigenous human intestinal flora are required.

Anti-tumor activity and effects on the immune system

Recent case-control studies in France [6] and in the
Netherlands [7] have presented results strongly suggesting a protective effect of yoghurt, buttermilk and
curd on the risk of breast cancer. Another study [8]
demonstrated that Lactobacillus acidophilus supplementation in man changed the intestinal bacteria
activity, leading to a reduction of beta-glucurinidase,
nitro-reductase and azo-reductase activity and bacterial enzymes that are associated with the conversion of
procarcinogens to proximal carcinogens. Indigenous
or ingested bacteria or their antigens can penetrate the
epithelial barrier of the intestinal wall and stimulate
the immuno- competent cells of the intestinal lamina
itself of the mesenteric lymph nodes and the spleen. In
this way, lactobacilli from yoghurt or bacteria from
other fermented foods might trigger the local and
immune systemic system. In this respect it was
demonstrated that small quantities of yoghurt and
especially Lactobacillus bulgaricus, from yoghurt cul-

187

ture, potentiate gamma- interferon production by

Con-A stimulated human peripheral blood lymphocytes in vitro [9]. In return gamma-interferon, a
cytokine with antiviral and anti proliferative effects,
can activate natural killer cells. Furthermore, lactobacilli from yoghurt were found to have antimutagenic
properties on chemical and fecal mutagens in vitro
[10]

Bacteriocins Activity
Many bacteria used in fermentation are known to
produce bacteriocins, which can exert a beneficial
effect by inhibiting the growth of pathogens in food in
the intestine. Lactobacillus acidophilus and Streptococcus
thermophilus can neutralize the action of enterotoxins
produced by pathogenic strains of Escherichia coli. The
production of specific bacteriocins, due to ingestion of
lactobacilli and particularly those that have the
capacity to adhere to the intestinal wall, could bring
about an extra defensive effect that facilitates the
resistance to infection by enteropathogenic bacteria
(colonization resistance). Experimental evidence for
such a role of Lactobacilli in animals is increasing, but
so far only circumstantial evidence for human situation is available [11].

Competition with Pathogens

Fermentation with lactic acid bacteria is one of the
oldest methods of food processing and preservation
used by mankind. It affords a vital means of preserving highly perishable foods [1].
Food products may be contaminated with a variety
of spoilage organisms and pathogens. Lactic acid
bacteria have a strong inhibitory effect against the
growth and toxin production of most other bacteria.
This antagonistic activity can be the result of:
(i) the competition for the available nutrients;
(ii) the decrease in redox potential;
(iii) the production of lactic acid and acetic acid and
the resulting decrease in pH;
(iv) the production of other inhibitory primary
metabolites, such as hydrogen peroxide,
carbon dioxide or diacetyl;
(v) the production of special antimicrobial
compounds, like bacteriocins and antibiotics.
Each of these properties and especially a combination of some of them, can be used to extend the shelf
life and safety of food products. In the past decade,
encouraging results have been obtained with fish,

188

G. Kalantzopoulos

meat, poultry and dairy products for the inhibition of

Staphylococcus, Salmonella, Pseudomonas, Clostridium
and other organisms by the use of several strains of
lactic acid bacteria, which produced bacteriocins or
antimicrobial substances [1214].

Some Facts About Fermented Milks with

Probiotics Properties

uted to a direct antagonistic effect against specific

groups of microorganisms (Enteropathogens), by an
effect on the metabolism in the gut or by a stimulation
of systemic or mucosal immunity.
We will present major proven health benefits of
milks fermented with those bacteria species and
discuss whenever possible the impact of the specific
selection and utilization of particular strains.

Yoghurt
In Europe probiotic action towards humans has only
been claimed for certain fermented dairy products
(yoghurt).
Fermented milk with probiotics properties, can be
defined as fermented milk, which beneficially effects
humans by improving our intestinal microbial balance
and by re-establishing an optimal microbial ecology of
the gut. An extensive literature [15,16], exists on the
impact of cultured products on the ecology of the
intestinal tract of man and animals.
Probiotic preparations which are currently available
contain a wide range of Lactobacillus and Bifidobacterium species. The Lactobacilli currently being used as
probiotics comprise [4]: L. casei, L. acidophilus, L.
delbreuckii subsp. bulgaricus, L. brevis, L. cellibiosus, L.
lactis, L. fermentum, L. plantarum, L. reuteri
The Bifidobacteria currently being used as probiotics
comprise: B. bifidum, B. longum, B. infantis, B. adolescentis, B. thermophilum, B. animalis.
The desirable characteristics of a good probiotic
strain are listed below.
(i) Normal habitat of the human intestinal tract.
(ii) Easy proliferation in vitro (production).
(iii) Remaining viable during processing, storage
and mixing in food/feed.
(iv) Survive the upper gastro-intestinal tract (to
reach in the intestine e.g. acid and bile
resistant).
(v) Colonization and/or proliferation in the
gastro-intestinal tract e.g. by the production of
bacteriocins, lactic acid.
(vi) Non- pathogenic and non-toxic/carcinogenic,
not absorbed in digestive tract/not invasive,
no tissue residues.
(vii) Genetically stable, no mutations and lack of
potential for making with pathogenic
bacteria.
(viii) Improvement of growth and efficiency in
animals.
(ix) Prevention of intestinal infection, compete with
pathogenic microorganisms.
(x) (Pre) digestion of lactose (lactose intolerance).
(xi) Anticholesterolaemic effects.
(xii) Antitumour activity.
The beneficial effect of probiotics are mainly attrib-

The most factual health benefit linked to yoghurt

consumption is the reduction of lactose malabsorption. This effect is endorsed by both observation and
clinical trials, but the mechanism involved is not yet
fully understood. Some specificity among lactic acid
bacteria species has been shown, with L. bulgaricus
giving the highest level of activity and Bifidobacteria
being on the low activity side. Heat-treated yoghurt
will not show the some level of activity toward lactose
digestion as live yoghurt.
The first mass production of yoghurt was started by
the pharmacist Isaac Carasso, with the goal of combating intestinal infections. This idea was built on
common knowledge in the Balkanian populations. A
few studies [17] give statistical data on the effect of
yoghurt on diarrhea in man. In a recent study yoghurt
was tested with both Str. thermophilus and Bifidobacterium bifidum. However, whether one or both bacteria
were responsible for the observed effect cannot be
assessed.
Yoghurt bacteria show some influence on immunological parameters. The consumption of yoghurt has
been associated with a decrease in allergic symptoms
in the elderly. Recent studies have demonstrated the
adjuvant effect of yoghurt and a special strain of L.
casei in fermented milk on the vaccinal anti-choleric
immunity response in mice. This effect was also
obtained with heat-treated yoghurt, but not with milk
alone, suggesting that cell components or fermentation products rather than active organisms are more
essential for this specific action.

Milk fermented with Bifidobacteria

Certain strains of Bifidobacteria survive intestinal transit and reach the colon in significant numbers. Because
they are one of the major species present in the colon,
Bifidobacteria can influence the indigenous intestinal
microflora, which results in such physiological effects
as the alteration of enzyme activities of the microflora
and regulation of gut transit [18].
Bifidobacteria also help in some diarrhea and constipation cases. A recent crossover and double-blind
study conducted on 36 women has indicated the

Fermented Products with Probiotic Qualities

189

specific action of milk fermented with yoghurt bacteria and Bifidobacterium Bio strain D-173010 a strain
selected for its good survival rate in fermented milk
and throughout the gastrointestinal transit time, compared to yoghurt. Previously this effect was observed
with live Bifidobacteria cells only.
Bifidobacteria are reported to improve digestive
parameters and demonstrate some antipathogen
action in man [19]. They also exert an action on parts
of the immune system [20].
Several strains reduce the levels of some colonic
enzymes connected with the conversion of procarcinogens to carcinogens in humans [21].
Fermented milk with viable yoghurt strains of L.
helveticus or Bifidobacterium sp. but not with L. acidophilus, have shown an effect on colon cancer cell
growth and differentiation with co-culture in vitro
[22].
Bifidobacterium sp. along with L. helveticus, was most
effective in reducing human HT-29 cell growth rate
and in increasing the activity of dipeptidyl peptidase
IV, a specific marker of cell differentiation. These
results are indicative of some specificity among
various lactic acid bacteria [23].
Major effects have been found with populations of
Bifidobacteria in fermented milk of 10 3 8 cells/g.
Bifidobacteria are not well adapted to fermented milk
and suffer in the presence of oxygen. Therefore, an
important selection criteria for specific strains is the
growth and survival in acidified and partly aerobic
conditions.
Some studies involve milks fermented with a
combination of Bifidobacteria and L. acidophilus.
Whether or not this combination gives additional or
altered health benefits is not known [24].

alter the activity of the intestinal microflora thus

preventing the development of potentially undesirable microorganisms. But the real mechanisms for
specific actions are complex and not fully understood.
Studies on animals have demonstrated both a stimulation of the non-specific and specific immune systems.
It was found that increased levels of several immunoglobulins in children with acute diarrhea when treated
with L. casei strain GG. In this study a dosage
10 3 1011 L. casei per day was utilized. The effect
was not observed with heat-treated fermented milk
[26].
The effects on L. casei on Salmonella were studied as
part of a recent research program. As a result of the
random study, researchers found that the survival
yield after Salmonella infection was 90% with a milk
fermented with yoghurt bacteria and several strains of
L. casei and only 10% with milk. This observation
demonstrates some level of strain specificity and
shows that a combination of different strains can give
additional benefits. A requirement for the adhesion of
bacteria cells to have an effect of diarrhea or on the
modulation of the immune system has been postulated but it has not yet been proven.
Lactobacillus casei has been shown to decrease the
activity of enzymes related to the risk of colon cancer
and to inhibit mutagenicity [27]. It was also found to
decrease the recurrence of superficial bladder cancer
in humans [28]. The mechanism of action may be
associated with both in the formation of carcinogenic
compounds in the intestines and immunomodulating
effect. Additional studies [29] are needed to further
investigate the effect of L. casei, as well as that of
Bifidobacteria and other lactic acid bacteria, in reducing
the risk of cancer.

Milk fermented with Lactobacillous casei

Milk fermented with Lactobacillus acidophilus

Lactobacillus casei is mainly found in the small intestine

of man. Some strains of L. casei can survive the transit
through the stomach and reach the ileum in sufficient
quantities to produce a physiological effect. In recent
in vivo study [25], it was shown that the ileum survival
rate of several strains of L. casei was 510% (except for
one strain: 0.5%) compared with Bifidobacteria
(1030%) or Str. thermophilus (0.5%) if associated with
L. casei.
Among lactic acid bacteria, L. casei is the most
studied species for its effects on the reduction of
incidence and duration of several types of diarrhea
and its capacity to modulate the immune system. It
can aid in the prevention and treatment of antibioticrelated diarrhea and travellers diarrhea and can have
a strong effect on infantile diarrhea.
Lactobacillus caseis ability to ameliorate or prevent
certain types of diarrhea seems related to its ability to

Lactobacillus acidophilus is one of the Lactobacillus sp,

that survive the gastrointestinal transit well. Like L.
casei it is most often found in the small intestine. It also
constitutes the dominant flora of the urinary tract in
women. Among the possible involvements of L.
acidophilus in human health, is the reduction of blood
cholesterol and the fight against vaginal Candida
infections. Additional carefully controlled clinical
studies are needed to confirm these observations.
Many L. acidophilus strains do not grow well in milk
and survive poorly in fermented products. In selecting
a specific strain one must consider this point.

Conclusion
A substantial amount of evidence indicates that

190

G. Kalantzopoulos

fermentation, in addition to preservation and

improvement of the sensorial acceptability, may offer
possibilities for the development of novel products
with improved nutritional as well as possible therapeutical properties. While studies on the effects of
consuming fermented milks with live bacteria are
becoming more numerous, more rigorous well-structured, double-blind trials with appropriate controls
are needed to guarantee the reality of the potential
health benefits. For a better selection of specific strains
and a better understanding of interactions between
food, microorganisms and host, more studies are
needed to establish the mechanisms by which these
bacteria exert a pro- or prebiotic effect and determine,
which properties are responsible for this activity. The
presence of viable bacteria in large numbers, together
with good survival throughout the gastrointestinal
transit, are very often a prerequisite for optimal
activity. All the other health oriented properties of
microorganisms utilized in fermented milk stay at the
level of a working hypothesis as no correlation
between a specific structural or metabolic property
and a health benefit has so far been clearly shown in
man.
Due to difficulties in carrying out accurate controlled clinical studies, a strain specificity has rarely
been proven in vivo. Nevertheless, some strain specificity has now been shown in vitro or with animal
studies. In addition to the growth and survival of each
strain, it is essential that the organoleptic properties
resulting from the fermentation of milk stay a good
food. Traditional fermented milks are so numerous in
the world that they constitute an immense source for
searching for appropriate bacteria with specific properties. By these means we have create the first Greek
collection from traditional fermented products known
with the acronym ACADC.
The food industry already uses the specificity of
lactic acid bacteria strains to improve existing fermented products and to develop new ones. Strains
specificity can be used for food products with specific
health benefits, which will answer to the needs of the
consumers.
Finally the transfer of beneficial properties from
laboratory strains to industrial strains, by recombinant-DNA technology, will be possible in the near
future and may result in improved, healthier and safe
food products.

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