Download Nutritional attributes of lactic acid fermented fruits

Peer-reviewed article
Nutritional attributes of lactic
acid fermented fruits and
vegetables
ELEFTHERIOS H. DROSINOS, SPIROS PARAMITHIOTIS*
Spiros Paramithiotis
*Corresponding author
Agricultural University of Athens Laboratory of Food Quality Control and Hygiene,
Department of Food Science and Technology, Iera Odos 75, Athens, GR-11855, Greece
AgroFOOD industry hi-tech - September/October 2012 - vol 23 n 5
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KEYWORDS: Fermented vegetables, antinutrient compounds, bioactive compounds, starter cultures.
ABSTRACT: Lactic acid fermentation of fruits and vegetables is worldwide. Depending on the geographical area, the
availability of raw materials as well as the ambient temperatures, a wide range of spontaneously fermented foods has been
produced, which today are recognized as characteristic for each region. The effect of lactic acid fermentation on the
nutritional value of fruits and vegetables has been the subject of limited research, compared to the respective of other
substrates incorporating animal-derived materials. However, significant modifications in the level and bioavailability of
nutrients, as well as interactions with antinutrient compounds, the gut microbiota and even the human immune system
have been recognized. In the present article, the effect of lactic acid fermentation on nutrient and antinutrient content of
fruits and vegetables are presented.
INTRODUCTION
A wide variety of fruits and vegetables have been traditionally
utilized as a substrate for fermentation but only a few of them
undergo lactic acid fermentation. The majority of them are
performed on a small scale, mainly by entrepreneurs, and
only fermented olives, cucumbers, sauerkraut and kimchi
have met worldwide commercial significance. The production
of fermented fruits and vegetables is characterized by
substrate-specific steps. Lye-treatment, which is an essential
initial treatment of olives with a NaOH solution that aims in
hydrolysis of oleuropein, a phenolic glucoside that is largely
responsible for the bitterness of olive fruits, is such an example.
Salting distinguishes fermented fruits and vegetables into
three categories: dry-salted, brine-salted and non-salted.
With dry salting, vegetables are treated with dry salt and
brine is formed due to osmotic extraction of water from
the already cut tissue. Brine formation is enhanced by the
mechanical pressure that is applied in some cases. This brine
contains fermentable carbohydrates and all the nutrients
necessary for microbial growth. When the substrate contains
less moisture is not dry-salted, instead is immersed into brine
solution. Then carbohydrates and other nutrients are extracted
and fermentation begins. Some vegetables are fermented
by lactic acid bacteria without prior treatment with salt. In
that case, the rapid colonization of the food by lactic acid
bacteria is crucial in order to inhibit growth of other genera
by lowering of the pH value and restriction of the oxygen. A
variation of this technique is the so-called “pit fermentation”,
an ancient method for preserving excess starchy vegetables
and fruits and currently applied in many places such as South
Pacific, Ethiopia and Himalaya. Lactic acid fermentation has
multiple effects on the nutritional value of food by modifying
the level and bioavailability of nutrients, by interacting with
antinutrient compounds or the gut microbiota and even the
human immune system. In the next paragraphs, the advances
regarding the effect of lactic acid fermentation on nutrient and
antinutrient content of fruits and vegetables are presented.
EFFECT ON ANTINUTRIENT COMPOUNDS
Plant foods contain a series of compounds, collectively
referred to as antinutrients, which generally interfere with the
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assimilation of some nutrients and in some cases may even
confer toxic or undesirable physiological effects.
Such antinutrients include oxalate, protease and a-amylase
inhibitors, lectins, condensed tannins and phytic acid.
Numerous processing and cooking methods have been shown
to possibly reduce the amount of these antinutrients and hence
their adverse effects. It has been concluded that the way food
is prepared and cooked is equally important as the identity of
the food itself. Research is currently focused on identifying the
antinutrient effect of several constituents rather than studying
their fate during lactic acid fermentation.
Regarding the oxalate content of cereal grains, legumes and
their products, very little is known. They are very poorly absorbed
under normal non-fasting conditions in humans; however
excess ingestion may interfere with calcium metabolism and
may result in chronic disease such as renal damage and stone
formation.
Antinutritional and chronic problems that can be
linked to the above mentioned reason are minimal (1).
There is only one report that correlates fermentation and
oxalate levels and refer to the nutritive status of dawadawa,
an African alkaline fermented food made by locust bean, and
have reported a decrease up to 43 percent of oxalates during
its production without, though, making clear whether this
reduction is due to processing steps before fermentation such as
soaking, dehulling and washing or to the fermentation itself (2).
Lectins are a group of bioactive proteins found in almost all
organisms and thus are ubiquitous to human food. Some
lectins originating from legumes and cereals have been found
to be highly toxic to humans and animals after oral ingestion,
most likely due to their binding to specific receptor sites on the
surface of the intestinal epithelial cells, which seriously impair
their ability to absorb nutrients from the gastrointestinal tract,
thus causing serious growth retardation (3). However, other
lectins, such as those of tomatoes, lentils, peas and other
common foods, are not toxic. Furthermore several plant
lectins have been shown to be important tools in cell biology
and immunology, with potential for clinical applications
such as antitumor and anticarcinogenic activity (4).
Lectins of animal origin, such as galectins have also emerged
as bioactive molecules that may possess immune-system
modulation properties.
The removal of the lectins with antinutritional and toxic effects
has been the subject of some research.
EFFECT ON NUTRIENTS AND BIOACTIVE COMPOUNDS
Lactic acid fermentation generally increases the digestibility
and the nutrient content of fermented foods. Folate is
produced by various green leafy vegetables, cereals, legumes
and by some microorganisms and is an essential component
in the human diet. Moreover, it has a preventative role against
several disorders including the development of neural tube
defects, risk of coronary heart disease, some types of cancer
and neuropsychiatric disorders (5). Vegetables as well as
some fermented milk products, especially yoghurt, buttermilk
and several cheese varieties are already recognized as good
dietary sources of folates. However, folate production by lactic
acid bacteria seems to be a strain depended property, e.g.
strains of Lb. acidophilus may produce or deplete folates in
dairy products (6, 7).
It is, though, possible to select folate producing starter cultures,
for effective supplementation of fermented vegetables (8).
Several other compounds, with quite interesting properties, such
as flavonoids, alkylresorcinols, glucosinolates and soyasaponins,
are also present in the raw materials and scarce information
exists regarding their fate during lactic acid fermentation.
Flavonoids are phenol derivatives widely distributed in plants.
A series of attractive biochemical effects have been assigned
to them, including action against cardiovascular diseases,
cancer, inflammation and allergy (9).
Alkylresorcinols
are
amphiphillic
1,3-dihydroxybenzene
derivatives, with an odd-numbered alkyl chain at position 5
of the benzene ring. Among others, they have been reported
to be present in high levels in cereals, more accurately in the
outer layers of the grains (10).
It has been stated that they have many biological effects,
among them anticancer and antioxidant activities (11).
Glucosinolates are a group of sulphur-containing plant
secondary metabolites found in plant families of the order
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t has been stated that lectins are heat labile molecules and
therefore can be detoxified by traditional cooking.
As a result, fermented foods that are prepared using raw
materials containing lectins, and a cooking step is incorporated,
either as such or as steaming, before or after fermentation, can
be lectin free.
Moreover, limited hydrolysis of lectins has also been found to
occur during lactic acid fermentation.
A Leuconostoc mesenteroides strain, isolated from Indian
fermented food batter (rice-soy idli batter), has been found
to hydrolyze lectins from soy beans, navy beans, black
beans and others, by excreting a mixture of protease, betaN-acetylglucosaminidase and alpha-D-mannosidase that
are involved in their hydrolysis (1). Condensed tannins are
the predominant class of polyphenols that occur widely
in food grains and legumes.They are considered to have
antinutritional effect due to their interaction with proteins that
lead to complex formation, resulting in decrease in protein
digestibility and digestive enzyme inactivation. However this
is of limited concern as they occur mainly in the outer layers
or seed coats that are mostly removed from the substrate
before fermentation (1). Phytic acid occurs primarily as a salt
of monovalent and divalent cations in discrete regions of
cereal grains, legumes, some roots and tubers. The presence
of phytate in foods causes concern because it decreases
the bioavailability of minerals such as phosphorus, zinc, iron,
calcium and magnesium and the solubility, functionality
and digestibility of proteins by forming complexes. Phytate
also interacts with enzymes, such as trypsin, pepsin, alphaamylase, and β-galactosidase, resulting in a decrease of their
activity. Lactic acid fermentation of cereals, legumes, and
tubers provides the optimum pH for enzymatic degradation
of phytates primarily as a result of the activity of endogenous
phytases and secondarily due to microbial phytases,
abrogating all the above mentioned negative effects.
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AgroFOOD industry hi-tech - September/October 2012 - vol 23 n 5
Capparales, which includes the Brassicaceae family, widely
used as raw material for vegetable fermentation. Their major
hydrolysis products, isothiocyanates, have been found to act
protectively against cancer, particularly in the bladder, colon
and lung (12, 13).
Soyasaponins are triterpenoid glycosides that occur in many
edible legumes, such as lupins, lentils, chickpeas, as well
as soybean. Ingestion of saponin-containing plant foods
by humans and animals has been associated with both
deleterious and beneficial effects.
Regarding the latter, reduced risk of cardiovascular disease
and some cancers has been reported. Moreover, although a
hypocholestoremic effect in animals has been recognized, it is
more speculative in humans.
Some studies suggest that saponins may reduce cholesterol
through the formation of insoluble complex with cholesterol,
thus preventing absorption in the intestine. It has been reported
that soyasapogenols are more cytotoxic toward cultured
cancer cells compared to soyasaponin glycosides or DDMPconjugated soyasaponins (14).
Lactic acid fermentation resulted in an increase in the
concentration of soyasapogenol B most probably due to
the conversion of soyasaponins I and III by β-glucosidase
activity of lactic acid bacteria; it has been also speculated
that the bioactivities of group B soyasaponins extracts will be
accordingly increased (15).
Utilization of proper starter culture can effectively prevent
biogenic amines accumulation, with particular emphasis on
histamine and putrescine; the former due to the high toxicity
and the latter due to higher abundance (17). The main field
for probiotic culture application has been the dairy products.
However, considerable amount of research has taken
place regarding the use of probiotic bacteria as fermenting
agents in fruit and vegetables or their juices resulting in very
promising outcome. The main vehicle has been table olive
fermentation, due to the relatively high economic importance.
It has been exhibited that probiotic strains of Lb. rhamnosus,
Bifidobacterium bifidum and Bf. longum are able to survive
at levels of 106 cfu/g after 30 days at room temperature.
Moreover, high viability with more than 107 cfu/g was reported
throughout 3-month period for Lb. paracasei (18).
Regarding fermentation of fruit juices by probiotic bacteria,
two major problems have been identified: lose of viability
due to the acidic environment and consumer acceptance.
One method of raising the pH in a fruit juice is to blend in milk
ingredients. However, not much is known regarding stability
of probiotics in such products (19). Regarding consumer
acceptance, it has been reported that consumers prefer the
organoleptic characheristics of conventional juices. However,
the perceptible off-flavors caused by probiotics that often
contribute to consumer dissatisfaction may be masked by
adding 10 percent v/v of tropical fruit juices (20).
STARTER CULTURE SELECTION
CONCLUSION
Starter cultures should ensure fast and adequate acidification.
Moreover, absence of amino acid decarboxylase activity as
well as bacteriocin production and probiotic potential are
desirable characteristics. Finally, the ability to prevail with
lower NaCl levels and the production of only L(+) lactic acid
are also advantageous properties. However, special attention
should be given to specific attributes of various products, e.g.
sauerkraut and cauliflower fermentation are characterized by
a specific microbial sequence.
Leuconostoc mesenteroides dominates the first stage, mainly
due to its comparatively higher initial numbers and shorter
generation time. Developed acidity along with the added
NaCl inhibits undesirable Gram-negative microorganisms.
Moreover, the carbon dioxide that is produced replaces air
and creates an anaerobic atmosphere, that facilitates growth
of other lactic acid bacteria and helps to prevent oxidation
of ascorbic acid and darkening of the natural colour of
the vegetable.
As the fermentation proceeds, the relatively sensitive to acidic
conditions Leu. mesenteroides is replaced sequentially by
Lactobacillus brevis and, at the final stage of fermentation, by
Lb. plantarum. During this final stage, large quantities of lactic
acid are formed by the remaining carbohydrates, leading
to further lowering of the pH value. The biogenic amine
content of fermented vegetables in general and sauerkraut
in particular drew the attention very early (16). Many authors
have surveyed biogenic amine content in sauerkraut and
have reported presence of tyramine and putrescine in much
higher levels than histamine, tryptamine and spermine.
Furthermore, it has been exhibited that accumulation of
biogenic amines takes place during both
fermentation and storage.
Lactic acid fermentation of fruits and vegetables has been
the subject of intensive study over the last decades. Research
has mainly focused on the development of the microbial
microecosystem as well as safety assessment from both
microbiological and chemical points of view, and secondarily
to the effect of lactic acid fermentation on specific nutrients,
bioactive compounds and antinutrients. Although important
conclusions have been drawn, a lot of research is still necessary.
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