Critical Reviews in Food Science and Nutrition

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/bfsn20

Spontaneously fermented traditional beverages as

a source of bioactive compounds: an overview

R. B. Cuvas-Limon , Clarisse Nobre , Mario Cruz , Rosa M. Rodriguez-Jasso ,

Héctor A. Ruíz , Araceli Loredo-Treviño , J. A. Texeira & Ruth Belmares

To cite this article: R. B. Cuvas-Limon , Clarisse Nobre , Mario Cruz , Rosa M. Rodriguez-Jasso ,
Héctor A. Ruíz , Araceli Loredo-Treviño , J. A. Texeira & Ruth Belmares (2020): Spontaneously
fermented traditional beverages as a source of bioactive compounds: an overview, Critical Reviews
in Food Science and Nutrition, DOI: 10.1080/10408398.2020.1791050

To link to this article: https://doi.org/10.1080/10408398.2020.1791050

Published online: 14 Jul 2020.

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CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION
https://doi.org/10.1080/10408398.2020.1791050

REVIEW

Spontaneously fermented traditional beverages as a source of

bioactive compounds: an overview
R. B. Cuvas-Limona,b, Clarisse Nobreb , Mario Cruzc, Rosa M. Rodriguez-Jassoa , He
ctor A. Ru
ıza ,
~oa , J. A. Texeirab, and Ruth Belmaresa
Araceli Loredo-Trevin
a
Food Research Department, School of Chemical Sciences, Autonomous University of Coahuila, Saltillo Coahuila, Saltillo, Coahuila, Mexico;
b
Centre of Biological Engineering, University of Minho, Braga, Portugal; cDepartment of Food Science and Technology, Antonio Narro
Autonomous Agricultural University, Saltillo, Coahuila, Mexico

ABSTRACT KEYWORDS
Fermented food has been present throughout history, since fermentation not only helps preserv- Bioactive compounds;
ing food, but also provides specific organoleptic characteristics typically associated to these foods. fermentation process
Most of the traditional fermented foods and artisanal beverages are produced by spontaneous Mexican fermented
beverages; traditional
generation, meaning no control of the microbiota, or the substrate used. Nevertheless, even not fermented beverages
being standardized, they are an important source of bioactive compounds, such as antioxidant
compounds, bioactive beeps, short chain fatty acids, amino acids, vitamins, and minerals. This
review compiles a list of relevant traditional fermented beverages around the world, aiming to
detail the fermentation process itself—including source of microorganisms, substrates, produced
metabolites and the operational conditions involved. As well as to list the bioactive compounds
present in each fermented food, together with their impact in the human health. Traditional fer-
mented beverages from Mexico will be highlighted. These compounds are of high interest for the
food, pharmaceutical and cosmetics industry. To scale-up the home fermentation processes, it is
necessary to fully understand the microbiology and biochemistry behind these traditional prod-
ucts. The use of good quality raw materials with standardized methodologies and defined microor-
ganisms, may improve and increase the production of the desirable bioactive compounds and
open a market for novel functional products.

Introduction The fermentation process involves two main factors: the

first factor is the type of microorganisms used and the
In the past, food processing was empirical, but over the
second factor is the substrate. Microorganisms are respon-
years this area has been extensively studied and innovated.
sible to initiate the fermentation process of the food, which
Fermentative processes were firstly used by the population
involves the chemical transformation of primary compounds
to prolong the shelf life of perishable agricultural products.
This provided a wide variety of new fermented foods and into new secondary metabolites, that generate organoleptic
beverages, that remain nowadays as the main part of the changes in the product, and thereby, extending the shelf life
diet of many underdeveloped countries and most Southeast of the product (Tamang, Watanabe, et al. 2016). These
Asian countries (Hugenholtz 2013). microorganisms can be yeasts, fungi or bacteria (Bourdichon
Fermentation is a cost-efficient bioprocess that improves et al. 2012), depending on the substrate to degrade, since
quality, nutritional value and organoleptic properties of the mechanism of the fermentation process varies according
many perishable foods (Blandino et al. 2003). Fermented to the substrate. The substrates can be meat, fish, dairy, veg-
foods are commonly described as foods or beverages proc- etables, cereals, and fruits, including food wastes such as
essed through controlled microbial growth and enzymatic fruit peels (Cifelli et al. 2017).
changes of primary and secondary components of foods During the fermentation process, primary and secondary
(Cifelli et al. 2017). Among the products derived from the metabolites are produced, such as antibiotics, antimicrobial
most common fermentations marketed worldwide are the peptides, carbon dioxide, alcohol, vitamins, folates, and
fermented alcoholic beverages, such as beer, wine, cider and, organic acids, that are considered bioactive compounds
particularly in Mexico, tequila, mezcal, pulque, and sotol; (Cifelli et al. 2017). Bioactive compounds are molecules with
and the products derived from fermented milk, such as therapeutic potential, that may promote health benefits by
cheese (a wide variety), yogurt, kefir and, particularly in decreasing excessive oxidative stress, pro-inflammatory state
Mexico, jocoque (Tamang, Shin, et al. 2016). and metabolism disorders (Siriwardhana et al. 2013). An

CONTACT Ruth Belmares [email protected] Food Research Department, School of Chemical Sciences, Autonomous University of Coahuila,
Saltillo Coahuila, Boulevard Venustiano Carranza e Ing, Jos
e C
ardenas s/n Col. Rep
ublica C.P. 25280, Saltillo, Coahuila, Mexico; Clarisse Nobre
[email protected] Centre of Biological Engineering, University of Minho, Braga, Portugal.
ß 2020 Taylor & Francis Group, LLC
2 R. B. CUVAS-LIMON ET AL.

example are the short chain fatty acids (SCFAs) that reduce First factor: indigenous microorganisms in
and prevent gastrointestinal disorders and colon cancer (Roy spontaneously fermented food
et al. 2006; Soret et al. 2010). Currently, the fermentation
The diversity of the microorganisms initiating the fermenta-
process is being used to develop emerging food products
tion is directly related to the substrate availability. In food
with health related benefits, the so called functional foods;
fermentation the presence of microorganisms can be
in addition to their natural properties these new foods can
achieved spontaneously or induced. Spontaneous fermenta-
provide extra benefits by helping in the prevention of dis-
tions are based on the presence of microorganisms indigen-
eases or strengthening the human body immune system
ous to raw materials that exhibit remarkable technological
(Sir

o et al. 2008). Thus, bioactive compounds are a trend as characteristics. However, these microorganisms must have
new ingredients in functional foods. the capacity to grow at high levels, in short time, and act as
Most food fermentation processes applied around the starter cultures preventing the development of pathogenic
world are neither standardized nor studied in depth. bacteria and undesirable decomposition (Holzapfel 2002;
Nevertheless, final fermented food has been consumed regu- Montel et al. 2014; Franciosa et al. 2018; Settanni et al.
larly by the population. Thus, the objective of this review is 2020). Traditional fermented foods and beverages are gener-
to describe the most relevant traditional fermentative proc- ally non-standardized products and are based on spontan-
esses used in food modification and preservation. Also, eous fermentations. In these products indigenous
detail as much as possible the process itself and how it microorganisms are generally a consortia of microorganisms
affects final food. Food physical and chemical modifications rather than pure cultures (Smid and Lacroix 2013). The con-
will be detailed, emphasizing the availability of bioactive sortia may consist in bacteria of different species, for
compounds. Mexican fermented food will be highlighted. example, lactic acid bacteria (LAB) and acetic acid bacteria
The following topics are covered in this review: operational (AAB), or a mix of bacteria, fungi, or yeasts. Consortia of
conditions of the fermentation processes, including the microorganisms are more versatile and robust compared to
microorganisms involved and the substrate source, second- pure cultures, and have even greater resistance against bac-
ary metabolites generated, bioactive compounds, and health teriophages present in the medium (Garc
ıa, Rendueles, and
benefits associated to the fermented food. D
ıaz 2019). However, the coexistence of microorganisms in
the same medium reduces growth, adaptation, morpho-
logical development and capacity to synthesize proteins and
Factors involved in the fermentation process secondary metabolites, since some of the produced metabo-
lites are used as chemical signals for competition communi-
Traditional fermented beverages turned out to be a great
cation (Nai and Meyer 2018). The use of microorganism
source of bioactive compounds. Their matrix constitutes the
consortia in the artisanal products generally induces a differ-
perfect environment for interactions between substrate and
ent variety of sensory properties on the same final product
microorganisms involved. Fermentation is a biotransform-
(Smid and Kleerebezem 2014).
ation process involving two main factors: the starter culture
Currently, scientific research has been focused on
or indigenous microorganisms and the substrate, as well as
improving productivity and underlying pathways by meta-
inherent factors such as the temperature and the pH condi- bolic engineering, or selecting spontaneous or induced
tions (Yunita and Dodd 2018). Nevertheless, traditional fer- mutants (van Hylckama Vlieg et al. 2011). By inducing
mentations occur generally spontaneously, and operational starter cultures, it has been possible to obtain the same trad-
conditions are not fully controlled, that is, the temperature itional fermented food but with improved organoleptic
is usually the room temperature and the initial pH is properties. Several species of microorganisms have been iso-
dependent on the raw material (food matrix). In spontan- lated from artisanal fermented products (S
aez, Flomenbaum,
eously fermentation, the microorganisms involved are gener- and Z
arate 2018). Selected species from the isolated ones
ally a consortia of bacteria, fungi and/or yeasts, which have been used to induce fermentation. The selection of spe-
provides the typical sensory characteristics of the products cific microorganisms as starter cultures allows to improve
obtained (Smid and Kleerebezem 2014). The type of micro- the quality of the organoleptic properties and eliminates the
organisms and the substrate have a major role on the sort of presence of pathogenic microorganisms (Siroli et al. 2015).
products obtained, since primary and secondary metabolites Between the different microorganisms responsible for the
generated are dependent on them. The interaction between fermentation process are the fungi, yeasts, and bacteria.
these two factors, under controlled conditions, is therefore Yeasts such as Saccharomyces cerevisiae are commonly used
key to achieve new differentiated products with interesting to produce fermented alcoholic beverages, while LAB have
chemical composition modification and new bioactive sub- been used mainly in dairy products (Tamang et al. 2015).
stances. Even the fermentations can be classified according Between the most common foods that rely on bacterial con-
to the type of microorganisms used: bacterial, based on yeast sortia are cheeses with eyes, where the starter culture are
or fungi fermentations. Other classification, based in the bacterial consortia of LAB and AAB (Tamang and
food nature, divides it into eight groups, such as fermented Kailasapathy 2010). Fermented beverages such as kefir is
cereals, vegetables, fruits, legumes, roots/tubers, milk, meat, another example of food from bacterial consortia. Pulque is
and fish products (Tamang, Shin, et al. 2016). an example of an alcoholic fermented beverage based on a
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 3

consortium of microorganisms with bacteria and yeasts acids, aldehydes, or ketones, in a process designated
(Escalante et al. 2008). “oxidative fermentation,” which is a source of energy to the
The probiotic properties of many fermented foods are cells. Oxidative fermentation is a process of incomplete oxi-
given by the presence of these starter cultures or indigenous dation of substrates, which are oxidized by primary dehy-
microorganisms. Many authors have been reporting that cer- drogenases of a respiratory chain, with the concomitant
tain yeasts present in fermented food, turn out to have pro- release of oxidized products into the surrounding medium
biotic activity (Tamang et al. 2015; Lu, Putra, and Liu 2018). (Matsushita and Matsutani 2016; Lynch et al. 2019).
Bacteria of the lactic acid genus are characterized by provid- Fermented foods are very well-known around the world, a
ing such benefits by producing bacteriocines and bioactive good example is yogurt. Yogurt is probably one of the most
peptides. For these reasons, the production of bioactive studied fermented food over time. It is well-known that the
compounds is dependent on the type of microorganisms starter cultures of yogurt correspond to a bi-culture of two
contained in food, as well as the substrate to be fermented. species, each represented by one strain, the Streptococcus
Microorganisms biotransform the chemical components of thermophilus and the Lactobacillus delbrueckii subsp. bulgari-
the substrates, imparting biopreservative effects and improv- cus. On the other hand, other foods are characterized by an
ing the viability of the nutrients. During fermentation, toxic
undefined microbial consortia constituted by multiple
components and anti-nutritional factors are degraded and
eukaryotic and prokaryotic species, such as the case of
antimicrobial, antioxidants compounds, peptides, and
cheese and bread obtained through sourdough fermentation
enzymes are produced. Microorganisms enzymes, in turn,
(van Hylckama Vlieg et al. 2011).
degrade complex compounds into simple ones. The bio-
The search in SCOPUS database, for the last 10 years
active compounds are promoted by increasing flavonoids
(2009
2019), using the keywords "Isolated of lactic acid
and saponins. This process helps to improve sensory quality
bacteria and traditional fermented beverages" yielded 41
in food and food safety (Tamang et al. 2009; Farhad,
Kailasapathy, and Tamang 2010; Bourdichon et al. 2012; documents, being 2016 the year with the highest number of
Tamang et al. 2015). publications (9 articles). Between the traditional fermented
beverages are Cauim, Boza, Shalgam, Leben, Pulque, Pozol,
Atole agrio, Chal, Chhang, and Bhaati jaanr, that will be fol-
Bacteria lowing described.
Among the group of microorganisms initiating fermentation Cauim, also called Kawi, is a beverage produced by
are bacteria. Bacteria can be classified by genus or end prod- Brazilian Indians of the Tapirap
e tribe. Cauim is a nonalco-
ucts generated, that is, LAB are responsible for lactic fer- holic beverage produced from diverse substrates like rice,
mentations while AAB for acetic acid production. In corn, peanut, cotton seed, banana, pumpkin, and cassava
fermented foods and even in spontaneously fermented foods (C
ıntia et al. 2010). Cassava is used as substrate in many fer-
the most isolated microorganisms are the LAB ones. LAB mented foods widely consumed not only in Brazil, but also
produce lactic acid as the main final product during sugar in Asia and Africa (Almeida, Rachid, and Schwan 2007). To
fermentation. LAB are gram positive, catalase negative with- prepare Cauim, raw materials are cooked for approximately
out cytochromes, non-spore forming, non-aerobic or aeroto- 2 hours and then cooled at room temperature. Further the
lerant, fastidious, acid-tolerant bacteria (Axelsson 1998). inoculum is added to the porridge to start the fermentation
LAB are key in the fermentation process due to their process (Almeida, Rachid, and Schwan 2007). The species
physiological characteristics such as substrate utilization,
more predominant in Cauim are LAB from the genus
metabolic capacities and functional properties (Ramos and
Lactobacillus. Ramos et al. (2011) studied the microbial
Schwan 2017). Chemically, LAB are fermenting microorgan-
communities involved in the fermentation of a beverage
isms that modify the carbohydrate content of foods, decrease
made with cotton seed and rice. They reported 81 yeast and
pH by production of organic acids, synthesize amino acids,
162 bacteria, 57% LAB (e.g. Lactobacillus plantarum,
improve the availability of B-group vitamins, degrade anti-
Lactobacillus brevis, Lactobacillus paracasei, Leuconostoc lac-
nutrients, and increase the availability of some minerals like
iron, zinc and calcium (Blandino et al. 2003). By lowering tis, Leuconostoc mesenteroides, Lactococcus lactis), 21%
the pH, LAB prevent and inhibit the growth of undesirable Bacillus (Bacillus subtilis, Bacillus cereus), 14%
microorganisms, such as pathogenic microorganisms, rotten Corynebacterium, and 9% Enterobacteriaceae. These micro-
and toxicogenic bacteria (Wood and Holzapfel 1995). organisms are responsible for chemical and physical changes
AAB are gram-negative, obligate aerobes, and are classi- in food, and to produce antimicrobial substances, creating
fied in the family of the Acetobacteraceae. They are non- unfavorable conditions for the growth of pathogens.
spore forming, ellipsoidal to rod-shaped cells that can occur Furthermore, they play an important role by fermenting car-
singly, in pairs or in short chains (Malimas et al. 2018; bohydrates such as glucose, maltose, sucrose, and raffinose.
Lynch et al. 2019). The most important genres of AAB used It has been reported that Bacillus genus has strong protease
to ferment foods are Acetobacter, Gluconobacter, and amylolytic activity and provides growth factors like vita-
Gluconacetobacter, and Komagataeibacter (Giudici, De Vero, mins and soluble nitrogen compounds. Also produces anti-
and Gullo 2017). AAB are characterized by their ability to microbial compounds and acids during fermentation which
oxidize carbohydrates, alcohols, and sugar alcohols (polyhy- promotes increased security, stability, and shelf life of the
dric alcohols or polyols) into their corresponding organic final product (Ramos and Schwan 2017).
4 R. B. CUVAS-LIMON ET AL.

Boza, is a traditional fermented beverage consumed in fructivorans, Lactobacillus reuteri, and L. fermentum (Erten,
Turkey, Bulgaria, Albania, Romania, South Russia, Fyrom, Tanguler, and Canbaş 2008; Panghal et al. 2018). The micro-
Anatolia, Middle East an Northern Persia (Arici and biology of Shalgam is complex and not known in detail.
Daglioglu 2002; Blandino et al. 2003; Vijaya Kumar, Depends on the microorganisms that are present on the sur-
Vijayendra, and Reddy 2015). Boza is based on lactic acid faces of the raw materials and vessels, where the product is
and yeast fermentation of cereals such as millet, maize, produced and stored, and in the sourdough extract. The fer-
wheat, and rice semolina (Panghal et al. 2018). Boza is a vis- mentation is carried out spontaneously and involves mixed
cous drink in the form of a colloidal suspension and pale cultures of mainly LAB and yeast (Erten, Tanguler, and
yellow or light to dark beige. Its characteristic smell is typic- Canbaş 2008).
ally acidic-alcoholic, and it holds a slightly acidic or sweet In Tunisia, there is a spontaneously traditional fermented
taste (depending on the acid content). The smell and taste drink called Leben, based on the lactic acid fermentation of
are thus, affected by metabolites derived from alcoholic fer- milk. Leben is consumed as a fresh drink or as an ingredient
mentation (Baschali et al. 2017). Boza preparation involves of some foods such as a brad couscous (Samet-Bali et al.
six stages: preparation of raw materials, boiling, cooling, 2017). Leben is produced with raw milk from cows, goats,
straining, addition of sugar, and fermentation (Arici and ewes, and camels. To prepare Leben, the raw milk is left to
Daglioglu 2002). Between the microorganisms identified as ferment spontaneously overnight or more, and then the sour
indigenous microorganisms of Boza are yeast and LAB such fermented milk is churned in a sac made of goat skin. By
as Lactobacillus, Lactococcus, Pediococcus, and Leuconostoc churning, the milk is separated into an aqueous fraction the
(Botes et al. 2007). Specifically, L. plantarum, Lactobacillus Leben itself, and into a fatty fraction called raw butter
acidophilus, Lactobacillus fermentum, Lactobacillus coprophi- (Samet-Bali et al. 2017). The microorganisms responsible for
lus, Leuconostoc raffinolactis, L. mesenteroides, and Leben fermentation are LAB predominant, mainly
Leuconostoc brevis (Baschali et al. 2017). It has been Lactobacillus sp. and Leuconostoc sp., Candida sp., and
reported that LAB present in this drink produce bacterio- Saccharomyces sp. (Oyewole 1997). Specifically, Lactococcus
cines with probiotic properties. Todorov et al. (2008) lactis subsp. lactis, Streptococcus salivaricus subsp. thermo-
reported that L. plantarum ST284BZ strain holds antiviral philus, L. delbrueckii subsp. bulgaricus and yeasts involved in
and antibacterial (bacteriocin) capacity being a great pro- lactic acid fermentations (Candida krusei) (Khedkar,
biotic. While L. plantarum ST194BZ has high activity Kalyankar, and Deosarkar 2016). To standardize product
against Mycobacterium tuberculosis which may be used as a characteristics, selected bacterial cultures composed of L. lac-
bacteriocin to control tuberculosis (Todorov et al. 2008). tis species are used to produce an industrial Leben in
Busa is other beverage similar to Boza, that uses similar Tunisia (Samet-Bali et al. 2017). Other traditional beverage
indigenous microorganisms but includes cocoa in the stand- from Tunisia is Rayeb that is produced by spontaneous fer-
ard Boza recipe. Busa is consumed in the Balkans (Baschali mentation of milk by LAB. This fermented drink, considered
et al. 2017). healthy since it helps digestion, has been consumed for cen-
Shalgam juice is another traditional Turkish drink, also turies. Enterocin A, which is a bacteriocin produced by
known as Shalgam. It is originally from the Cukurova prov- Enterococcus faecium MMRA, was detected in Rayeb
ince of Turkey but consumed throughout the country. It is (Rehaiem et al. 2010).
made of juice of black or purple carrots (Daucus carota) or Chal is a traditional drink obtained by spontaneous fer-
turnips (Brassica rapa), sourdough, salt, bulgur (broken mentation of camel milk, it is consumed in Turkman Sahra,
wheat) flour, and drinkable water (Erten, Tanguler, and in Golestan province, Iran. The preparation of Chal consists
Canbaş 2008). The black carrot, responsible for the red color of mixing fermented camel milk and sour milk previously
of the juice, is the main raw material of Shalgam. During fermented as inoculum. The mixture is placed in earthen-
fermentation, sugars from the carrot are transformed into ware pots about 1 or 2 days (Soleymanzadeh, Mirdamadi,
lactic acid. Turnip is a minor raw material, as it is added and Kianirad 2016). Several bacteria have been isolated from
only in amounts up to 2% (w/v). Bulgur flour provides Chal such as L. plantarum, Lactobacillus paraplantarum,
nutrients to microorganisms during fermentation. Lactobacillus kefiri, L. paracasei, L. lactis, Weissella cibaria
Sourdough is obtained by using yeast dough fermented at and E. faecium, Lactobacillus rhamnosus (Fitzgerald and
room temperature during the night. The added salt is com- Murray 2006; Hayes et al. 2006).
mercial salt or sea salt (Erten, Tanguler, and Canbaş 2008; Chhang is a traditional Indian drink made from cooked
Tanguler and Erten 2012). The elaboration of Shalgam by rice, and Jau Chhang from cooked barley. Chhang and Jau
the traditional method includes two stages. A first fermenta- Chhang are mild alcoholic sweet beverages prepared using
tion is carried out to enrich dough with lactic bacteria and traditional inoculum “Phab” in the tribal areas of Himachal
yeast, and then, the main fermentation takes place with the Pradesh (Thakur and Chand Bhalla 2004). What is known
carrots (Hasan, Gulden, and Huseyin 2014). Several strains about Phab is that it is prepared by people from the Nubra
have been identified and isolated from this drink, such as valley in the Ladakh region using coarse flour from husked
Lactobacillus, Leuconostoc and Pediococcus, specifically L. roasted barley (Hordeum vulgare). Artemisia sp. available
plantarum, L. brevis, L. paracasei, L. acidophilus, locally in Ladakh is used to incubate the fresh tablet of
Lactobacillus casei, Lactobacillus sanfranciscensis, Phabs (Angmo and Bhalla 2014). Chhang microbiota is a
Lactobacillus pontis, Lactobacillus alimentarius, Lactobacillus consortium of different microorganisms that include LAB,
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 5

yeast and molds, such as Pediococcus pentosaceus, L. planta- a nonalcoholic drink derived from fermented corn. Atole
rum, E. faecium, L. casei, Enterococcus lactis, Bacillus amylo- agrio is traditionally prepared by spontaneous fermentation.
liquefaciens, S. cerevisiae, Saccharomyces fibuligera, Candida This beverage can be prepared either by liquid or solid state
tropicalis, Pichia kudriavzevii, Serratia proteamaculans, fermentation. Manufacturing process has only few steps,
Aspergillus sp., Mucur sp., and Rhizopus sp. (Thakur et al. maize is not boiled nor soaked prior to fermentation, the
2015). Isolates from traditional inoculum of Chhang (Phap duration of fermentation is only hours instead of days, and
and Dheli) are L. plantarum, P. pentosaceus, E. faecium, and the end product is boiled prior to the consumption (Ampe
S. fibuligera (Thakur and Chand Bhalla 2004). and Miambi 2000; Castillo-Morales, Wacher-Rodarte, and
Pulque is a traditional non-distilled alcoholic fermented Hern
andez-S
anchez 2005). The elaboration process of Atole
beverage of Mexico made from cactus plant (Agave salmiana, agrio has been described in detail by (Valderrama 2012;
Agave atrovireins, and Agave mapisaga) (Tamang, Shin, et al. V€akev€ainen et al. 2018). Succinctly, first the grains are cut
2016). It is based on the fermentation of mead that is off from the corn cobs with a knifr and grounded and
obtained from agave. The process has four stages: (1) castra- mixed with water to obtain a white dough. For the solid state
tion, (2) pit scraping and aguamiel (mead) extraction, (3) fermentation, the dough is molded manually into balls of
seed preparation, and (4) fermentation (Escalante et al. 2016). 100 g. Then balls are let to ferment for 12 h at 34  C. Finally,
Pulque fermentation is a batch non-stirred process, performed it is added 1 L of water and the maize-water slurry is homo-
under non-aseptic conditions. It is a spontaneous fermenta- genized by hand. For the liquid fermentation, 750 g of dough
tion, traditionally carried on by the natural microbiota pre- are mixed with 750 mL of water prior to the fermentation
sent in the sap (indigenous microorganisms). The fermenting and the slurry is allowed to ferment for 6 h, at 34  C. The fer-
microbiota is based on LAB. The indigenous microorganisms mentation time were selected based on the traditional manu-
identified in Pulque were L. lactis subsp. lactis, L. plantarum, facturing process of Atole agrio. The suspension is sieved and
Lactobacillus acetotolerans, L. acidophilus, Lactobacillus hilgar- pasteurized for 10 min at 100  C. In case of solid state fer-
dii, L. kefir, Leuconostoc citreum, Leuconostoc kimchii, L. mes- mentation there is a slight modification in the process. After
enteroides, Leuconostoc pseudomesenteroides, Zymomonas the formation of balls, these are fermented 12 hours at 34  C,
mobilis, Acetobacter malorum, Acetobacter pomorum, and then, the same process is performed. V€akev€ainen et al.
Microbacterium arborescens, Flavobacterium johnsoniae, (2018), identified and characterized LAB of Atole agrio, find-
Gluconobacter oxydans, and Hafnia alvei (Escalante et al. ing the presence of Enterococcus (5.8%), Weissella (29.2%),
2008; Escalante et al. 2016; Tamang, Watanabe, et al. 2016). Pediococcus (24.0%), Lactococcus (17.8%), Leuconostoc (6.7%)
Pozol is another traditional Mexican drink, consumed in and Lactobacillus (16.4%). Other microorganisms involved in
the Mexican southeast, comprising the states of Tabasco, these fermentations are LAB such as L. acidophilus, L. planta-
Chiapas, Yucatan, and Campeche. The consumption of rum, L. acetotolerans, L. kefir, L. lactis. subsp. lactis, L. cit-
Pozol began many years ago by the Mexican Indians, in fact reum, L. kimchii, L. mesenteroides, an alcohol-producing
the word Pozol comes from Aztec pozolli. This beverage is a bacteria (Z. mobilis) (Lappe-Oliveras et al. 2008).
refreshing nonalcoholic drink (M
endez-Albores et al. 2004). Chorote is other fermented beverage commonly consumed
The first step to elaborate Pozol is to cook white or yellow in the South of Mexico, especially in the states of Tabasco,
maize in 1% (w/v) lime solution. The corn can be used Chiapas, and Oaxaca. It is made from corn and cocoa (Quero
alone or mixed with roasted cocoa paste or ground cocoa 2000). The fermentation of this drink is based on the fermen-
beans, depending a lot on the region. The second step is to tation with corn dough treated with lime and cocoa beans.
wash it with water and ground it to a mass known as nixta- Traditionally, the elaboration of the Chorote starts by making
balls of approximately 5–10 cm diameter with the corn dough.
mal. Next step is to mold it into balls in a range from 10 to
Later it is suspended in water like a refreshing drink. The
12 cm length and 5 to 8 cm diameter, which weigh 70–170 g.
Chorote is a fermentation in solid state, the cocoa beans are
Balls are wrapped in banana leaves and fermented at room
roasted and ground and finally add to the corn dough.
temperature for an average of four days (Nuraida, Wacher,
Isolated microorganisms in Chorote were mainly LAB. The
and Owens 1995; Tamang, Shin, et al. 2016).
fermentation time takes approximately nine days at room
Microorganisms involved in the primary fermentation are
temperature. In Mexico it is considered as popular as Pozol, a
mainly LAB, molds and yeasts (Nuraida, Wacher, and
drink based on fermented nixtamal (Wacher et al. 1993). In
Owens 1995). The predominant microorganism isolated
fact, Chorote, Pozol and sour Atole agrio are very similar trad-
were Leuconostoc spp., Streptococcus spp., Enterococcus,
itional drinks. Table 1 shows some traditional fermented bev-
Exiguobacterium, Lactobacilli homofermentative, and
erages consumed in different parts of the world, including the
Lactococci heterofermentative. Different authors have
substrate used, the microorganisms involved in the fermenta-
reported microorganisms such as Streptococcus suis,
tions, which are generally consortia of bacteria and yeasts,
Streptococcus bovis, L. lactis, L. raffinolactis, Lactobacillus
and the metabolites produced in these fermentations.
confuses, L. fermentum, L. plantarum, L. casei, L. delbrueckii,
L. alimentarius, and Bifidobacterium (Wacher et al. 1993;
Nuraida, Wacher, and Owens 1995; Wacher et al. 2000; Yeasts and molds
Escalante, Wacher, and Farr
es 2001; D
ıaz-Ruiz et al. 2003). Yeasts are defined as unicellular ascomycetous or basidiomy-
In the southeastern states of Mexico such as Tabasco, cetous fungi (Kurtzman, Fell, and Boekhout 2011;
Chiapas and southern Veracruz, Atole Agrio is consumed as Lambrechts and Pretorius 2019). Yeast monocultures are
6 R. B. CUVAS-LIMON ET AL.

Table 1. Traditional fermented beverages consumed in different parts of the world, including information on the substrate, microorganisms involved and metab-
olites produced.
Microorganism
Product Substrate Bacteria Yeast Metabolites Reference
Boza Cereals like bulgur, Lactobacillus plantarum, Saccharomyces uvarum, Lactic acid, ethanol plus Blandino et al. (2003);
maize, chickpea, Lactobacillus fermentum, Saccharomyces cerevisiae esters, lipid, protein, Dogan and
millet, wheat, or rice Lactobacillus sanfranciscensis, vitamin B, amino acids, Ozpinar (2017)
Lactobacillus coryniformis, phenolic acid, ferulic acid,
Lactobacillus confuses, vanillic acid, protocatechuic
Leuconostoc acid, y-oryzanol, phytic
paramesenteroides, acid, and inositol.
Leuconostoc mesenteroides,
Lactobacillus brevis.
Turnip juice Black carrots Enterococcus faecalis, Acetic acid, lactic acid, Wu and Li (2018); Erten,
Lactobacillus bavaricus, propionic acid, ammonia, Tanguler, and
L. brevis, amines, aldehydes, Canbaş (2008)
L. plantarum, phenols, indole, alcohols,
Lactococcus lactis, amino acids (cysteine,
L. mesenteroides, methionine).
Pediococcus pentosaceus.
Leben Milk L. lactis, Candida sp., Acetic acid, lactic acid, Odunfa and Oyewole
L. mesenteroides. Saccharomyces sp. propionic acid, malic acid, (1998); Holzapfel and
formic acid, bacteriocins, Schillinger (2002);
antimicrobial peptides, Even et al. (2010);
phenolic acids, ferulic acid, Ramos et al. (2011)
antioxidants compounds,
aromatic compounds,
organic and fatty acid.

Chhang Rice L. plantarum, Acetic acid, lactic acid, Handa and Sharma
Lactobacillus. propionic acid, malic, acid, (2016)
formic acid, bacteriocins,
antimicrobial peptides,
phenolic acids, ferulic acid.

Sundug Black Grape wine Lactobacillus, S. cerevisiae, Ethanol, phenolic compounds, Rib
ereau-Gayon (2000);
Streptococcae, Kloeckera, Hanseniaspora, anthocyanins, Tamang, Watanabe,
Oenococcus, Candida, hydroxybenzoic acid, et al. (2016)
Pediococcus sp. Pichia, hydroxycinnamic acid,
Metschnikowia, Torulaspora, flavonoids.
Kluyveromyces,
Schizosacchaomyces,
Zygosaccharomyces,
Brettanomyces
Pozol Corn Leuconostoc sp., Candida sp., Folate, phytic acid, acetic Nuraida, Wacher, and
Heterofermentative, Trichosporon cutaneum. acid, lactic acid, succinic Owens (1995);
Lactobacillus sp., acid, esters, higher V€akev€ainen et al.
Homofermentative. alcohols, glycerol, (2018)
acetaldehyde.

Pulque Agave Lactobacillus acidophilus, S. cerevisiae, Oxalic, saccharic, keto- Escalante et al. (2004);
Aguamiel L. mesenteroides, Zymomonas mobilis. glucconic, vitamins, and Correa-Ascencio et al.
Acetobacter hydrolytic enzymes, (2014); Escalante
pomorium,Gluconobacter ethanol, minerals, organic et al. (2016); De Roos
oxydans. acids, and phytates. and De Vuyst (2018)
Tejuino Corn dough L. acidophilus, Mannitol, fructose, Freire et al. (2017)
L. mesenteroides. antimicrobial peptides,
organic acids, amino acids.

Kefir Milk and Kefir grains Lactobacillus, Kluyveromyces marxianus Antimicrobial peptides, amino G€
uzel-Seydim et al.
Lactococcus, subsp. lactis, acids, acetic acid, lactic (2000); Simova et al.
Leuconostoc, S. cerevisiae, acid, and other organic (2002); Wu and Li
Acetobacter. Candida inconspicua, acids and vitamins (folic (2018)
Candida maris. acid, riboflavin, cobalamin)
Kimchi Meat, fish and cabbage Alkalibacterium, Halococcus spp., Antimicrobial peptides, amino Collins et al. (1993);
L. mesenteroides, Natronococcus spp., acids, propionic acid, Chang et al. (2008);
Weissella. Natrialba spp., carbon dioxide, hydrogen Wu and Li (2018)
Haloterrigena spp., peroxide, bacteriocins,
Lodderomyces spp., antifungical peptides.
Trichosporon spp., Candida
spp., Saccharomyces spp.,
Pichia spp.,
Sporisorium spp.,
Kluyveromyces spp.
Wine, beer Grapes, barley
(continued)
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 7

Table 1. Continued.
Microorganism
Product Substrate Bacteria Yeast Metabolites Reference
Lactobacillus, S. cerevisiae, Saccharomyces Alcohol. carbon dioxide, Veli
canski et al. (2014);
Streptococcus, unisporus, ethanol, gluconic acid, Petruzzi et al. (2016);
Pediococcus. Candida pelliculosa, Candida ethyl gluconate, phenolic Vilela (2019)
glabrata, Candida sake, compounds, tyrosol,
Candida guilliermondii. hydroxytyrosol, tryptophol,
glutathione, cysteine,
glycine, melatonin,
tryptophan, caffeic acid,
folates, sterols, lignans, free
ferulic acids and
alkylresorcinols.
Kombucha Fungus or mushroom Acetobacter xylinum, Saccharomyces spp., Torulopsis Sugars, ethyl gluconate, Tamang and Fleet
Acetobacter xylinoides, spp., oxalic, lactic, keto- gluconic (2009); Veli
canski
Bacterium gluconicum. Pichia spp., Brettanomyces and amino acids, vitamins, et al. (2014); Petruzzi
spp., Zygosaccharo tea components (catekhins, et al. (2016)
myceskombuchaensis. flavonols) hydrolytic
enzymes, acetaldehyde,
acetic acid, succinic acids,
glycerol, terpenoids, esters.
Bhaati jaanr Rice P. pentosaceus, Saccharomyces fibuligera, Phenolic compounds, Tamang and
Lactobacillus bifermentans. Pichia anomala, flavonoids, coumarins, Thapa (2006)
S. cerevisiae, lignans, tannins, terpenes,
C. glabrata. tocopherols, phospholipids,
aldehydes, ketones and
ply-functional organic
acids, volatiles compounds,
ethyl esters and fatty acids.
Alcoholic Fruits, cereals Lactobacillus, Brettamomyces intermedius, Antibiotics, antimicrobial Tamang and Fleet
beverages and vegetables Streptococcus, Candida lodderae, compounds, antimicrobial (2009); Petruzzi et al.
and non- Pediococcus. Debarymyces dekkera, peptides, amino acids, (2016); Caulier et al.
food Kluyveromyces delphensis, ribosomal peptides, (2019); Vilela (2019)
mixed S. cerevisiae, bacteriocins (I, II, II),
amylolytic S. fibuligera, enzymes and polyketides
astarter Zygosaccharomyces. (acetogenins, ansamycins,
enediynes, macrolids,
polynes, polythers,
tetracycline), fatty acids
and derivates (benzenoids,
furans, esters, alcohols,
aldehydes, alkanes), volatile
compounds (nitrogen-
containing volatile organic
compounds , terpenoids,
sulphur- containing),
lipopeptides (fegycins,
iturins, surfactins, kurtakins)
Cheese Milk Lactobacillus, Bifidobacterium, Organic acid, aromatic Falchero et al. (2010);
Lactococcus, Brachybacterium, compounds, fatty acids, Bourdichon
Enterococcus, Brevibacterium, sensorial properties. et al. (2012)
Leuconostoc. Propionibacterium.

frequently used to create fermented alcoholic and nonalco- amylolytic starters, such as: Brettanomyces anomalus,
holic beverages and foods, such as cheeses, breads, and other Candida javanica, Geotrichum candidum, Hansenula
products (Hittinger, Steele, and Ryder 2018). an
omala, Pichia burtonii, Rhodotorula glutinis,
Yeast play an important role during fermentation, since they Saccharomycopsis fibuligera, S. cerevisiae, Saccharomyces
are responsible for the production of organic acids and alcohol, dairensis, Saccharomyces globosus, Saccharomyces kluyveri,
providing flavor, texture and aroma to fermented foods. Saccharomyces sak
e, Torulopsis versatilis, Trichosporon pullu-
However, the organoleptic properties provided depend on lans, Zygosaccharomyces rouxii (Tamang and Fleet 2009;
nutritional content and toxin-reducing factors (Rai and Table 1).
Jeyaram 2017). For example, fermentation of cereal by yeast In spontaneously fermented foods, yeasts have been iden-
promotes high levels of total sugars, sterols, lignans, free ferulic tified as indigenous microorganisms that initiate the fermen-
acids, and alkylresorcinols, as well as total phenolic content and tation process, such as in Kombucha, Shalgam, Leben, Boza,
aroma formation (Vieria-Dalod
e et al. 2008; Yeo and Bhaati jaanr, Chhang, Pozol and Atole agrio, which will be
Ewe 2015). further detailed.
The most common yeast in fermented food is S. cerevi- Kombucha is a traditional fermented beverage, based on a
siae. Nevertheless, many other yeasts have been isolated consortium of AAB and yeasts. Yeasts that have been iso-
from traditional fermented foods and non-food mixed lated from Kombucha are Brettanomyces bruxellensis,
8 R. B. CUVAS-LIMON ET AL.

Candida stellada, Schizosaccharomyces pombe, Torulaspora Yeasts involved in Pozol fermentations are a diversity of spe-
delbrueckii, and Zygosaccharomyces baili. In fermentation of cies of the genus Candida and filamentous yeast such as
Shalgam S. cerevisiae is used (Hasan, Gulden, and Huseyin Trichosporon cutaneum and G. candidum (Nuraida, Wacher,
2014). Samet-Bali et al. (2017), isolated Candida lusitanie, C. and Owens 1995). Others species identified are Rhodotorula
tropicalis and C. krusei from Leben fermentation. An minuta, R. mucilaginosa, Debaryomyces hansenii, Candida guil-
amount of 4.61 ± 0.21 Log count (Log10 CFU/mL) of yeasts liermondii subsp. guilliermondii, Kluyveromyces lactis subsp. lac-
and molds were determined in Leben. tis, Clodosporium cladosporioides, Phoma glomerata, Phoma
Boza is produced by simultaneous fermentation with bac- fimeti, G. candidum, Penicillum fellutanum (Wacher et al. 2000).
teria and yeast. Yeasts are responsible for the alcoholic fermen- The yeasts involved in Atole agrio are mainly Saccharomyces,
tation, producing carbon dioxide bubbles and increasing the the most common is the S. cerevisiae. Other yeasts found were
volume, while bacteria produces lactic acid and gives the acidic Candida spp. and C. lusitaniae (Cervantes Contreras and
character to Boza in the lactic acid fermentation. Yeasts isolated Pedroza Rodr
ıguez 2007; Lappe-Oliveras et al. 2008).
and identified from Boza were Saccharomyces carlsbergensis, S.
cerevisiae, Saccharomyces uvarum (Arici and Daglioglu 2002)
Second factor: substrate
and, C. tropicalis, Candida glabrata, Geotrichum penicillum and
G. candidum (Baschali et al. 2017). Fermentation can occur as a natural and spontaneous phe-
Bhaati jaanr is a traditional fermented rice paste. It is com- nomenon as long as there is a raw material (substrate) avail-
monly consumed as a mild-alcoholic sweet-beverage in the able, either animal or vegetable, and a microorganism
rural areas of the Darjeeling hills, Sikkim and Northeast in consortium naturally present in the substrates to begin fer-
India, Nepal and Bhutan. To produce Bhaati jaanr, glutinous mentation activity (Septembre-Malaterre, Remize, and
rice is cooked for about 15 min in an open cooker, excess Poucheret 2018).
water is drained off, and cooked rice is spread on a bamboo The type of by-products that are obtained, as well as the
mat for cooling. A dry mixed starter culture called marcha is development of textures, flavors and odors depends on the
powdered, and about 2% of it is sprinkled over the cooked substrate and microorganisms involved. The substrate must
rice, mixed well and kept in a vessel or an earthen pot for have a rich chemical composition, including high concentra-
1–2 days at room temperature for saccharification. tions of mono and di-saccharides and the minerals necessary
Filamentous molds identified in Bhaati jaanr, were Mucor cir- to start the microbial metabolism. But at the same time, it
cinelloides, Rhizopus chinensis, and Rhizopus stolonifera. Yeasts must not contain inhibitors such as toxins that inhibit the
identified were S. fibuligera, Pichia anomala, S. cerevisiae, and growth of these microorganisms. It is true that environmen-
C. glabrata (Tamang and Thapa 2006). Rhizopus strains play tal conditions influence the fermentation process, but trad-
an important role in the saccharification process of rice. itional fermented foods are not standardized processes,
Tamang and Thapa (2006) reported the physicochemical which means that these conditions are not always the same.
changes occurring during fermentation of Bhaati jaanr, such Microorganisms usually grow at room temperature
as pH (3.5), acidity (0.24%), moisture (83.4%), and alcohol (25–27  C) and not always under ideal conditions of sterility.
(5.9%) during fermentation. Yeasts increased significantly Nevertheless, the conditions provided by the natural envir-
(p < 0.05) from 105 to 108 CFU g
1 on day 2 and decreased onment extensively influence the characteristics of the final
to a level of 105 CFU g
1 on day 10. product. In this way, research on fermentable food seeks to
Yeasts isolated in Chhang and Jau Chhangbeverages, standardize traditional fermented food and beverages to
which fermentation process was described in the previous improve their organoleptic properties and optimize the time
section, and Sura were S. cerevisiae, S. fibuligera, C. tropica- of the fermentation. Table 2 shows different raw materials
lis, and P. kudriavzevii (Thakur et al. 2015). Molds and used as substrates in traditional food beverages.
fungi as Bacillus are usually employed for starch saccharifi- The most commonly used substrates are fruits, vegetables,
cation or proteolysis, or as secondary ripening microbiota meat, and cereals. Between the traditional alcoholic fermen-
after a primary fermentation (Cifelli et al. 2017). It has been tations based on fruits are the well-known wine and cider.
reported that species of Bacillus have been isolated from fer- They are firstly fermented by S. cerevisiae, with a secondary
mented foods based on legumes. malolactic fermentation induced by LAB, which improves
Between the yeasts detected during Pulque fermentation the flavor and aroma of the final product (Alexandre et al.
are Saccharomyces and other yeast, which during the fer- 2004). Lactobacillus, Oenococcus, Pediococcus, and
mentative process produce ethanol, amino acids, vitamins, Leuconostoc have been reported as the predominant genera
and volatile flavor compounds (Lappe-Oliveras et al. 2008). during malolactic fermentation in winemaking (Garc
ıa,
The microbial diversity of Pulque includes Saccharomyces Rendueles, and D
ıaz 2019).
cerevisiae subsp. chevalieri, Saccharomyces cerevisiae subsp. Vegetables are another important substrate. Vegetables
capensis, Saccharomyces bayanus, Saccharomyces pastorianus, are rich in carbohydrates, proteins, minerals, amino acids,
Kluyveromyces marxianus, Kluyveromyces lactis, Candida val- and phytochemicals. Around the world, vegetables are a sub-
ida, Candida parapsilosis, Clavispora lusitaniae, strate of different fermented beverages. The chemical com-
Debaryomices carsonii, Hanseniaspora uvarum, G. candidum, position of the substrate depends on the geographical
Pichia guilliermondii, Pichia membranifaciens, Rhodotorula location and climatic conditions where the crop is obtained.
mucilaginosa (Escalante et al. 2016). Also, the harvesting time and consequently the degree of
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 9

Table 2. Classification of raw materials in fermented food substrates.

Raw material Fermented beverage Reference
Cereals Rice Ang-Kak Steinkraus (1996); Tamang and Kailasapathy (2010)
Boza Blandino et al. (2003); Tamang and Kailasapathy (2010)
Dosa Soni et al. (1986); Tamang and Kailasapathy (2010)
idli Tamang and Kailasapathy (2010)
Khamak Alexandraki et al. (2013)
Lao-chao Blandino et al. (2003); Tamang and Kailasapathy (2010)
Puto Steinkraus (2004); Tamang and Kailasapathy (2010)
Selroti Yonzan and Tamang (2010, 2013)
Tape Steinkraus (1996); Tamang and Kailasapathy (2010)
Ketan
Maize Busa lu and Karapinar (1997); Altay et al. (2013)
Hanciog
Boza
Bosa
Gow
e Greppi et al. (2013)
Kenkey Oguntoyinbo et al. (2011)
Kunu-zaki Olasupo et al. (2010); Oguntoyinbo et al. (2011)
Koko Blandino et al. (2003); Tamang and Kailasapathy (2010)
Mawe Greppi et al. (2013)
Ogi Greppi et al. (2013)
Poto poto Abriouel et al. (2006); Tamang and Kailasapathy (2010)
Pozol D
ıaz-Ruiz et al. (2003); Castillo-Morales, Wacher-Rodarte,
and Hern
andez-S
anchez (2005)
Sorghum Hussuwa Yousif et al. (2010)
Kunu-zaki Oguntoyinbo et al. (2011)
Togwa Mugula et al. (2003); Tamang and Kailasapathy (2010)
Vegetables Cucumbers Cucumbers fermented Tamang and Kailasapathy (2010)
Jiang-gua Chen et al. (2012)
Khalpi Tamang and Kailasapathy (2010)
Cabbage Paocai Yan et al. (2008)
Sauerkraut Johanningsmeier et al. (2007)
Turnip Sunki Watanabe et al. (2009)
Shalgam
Soybean Bekang Chettri and Tamang (2014)
Douchi Wang et al. (2006)
Fruits Grape Wine Bahiru, Mehari, and Ashenafi (2006); Tamang and
Kailasapathy (2010)
Apple Cider Tamang and Kailasapathy (2010)
Plants Agave Tequila Escalante et al. (2004); Aldrete-Tapia et al. (2020)
Pulque Escalante et al. (2004, 2016); Torres-Maravilla et al. (2016)

maturity of the raw material used is not always exactly the to protect against free radical damage that can lead to cancer,
same for every processing.The substrate of Shalgam is black heart attack, and stroke, so it is a source of nutrition. Agave
carrot (Erten, Tanguler, and Canbaş 2008). Black carrot con- sap has a high diversity of microorganisms, which determine
tain sugars such as a sucrose, glucose, and fructose the attributes of Pulque. It is rich in different compounds favor-
(1.20–3.31, 1.10–5.60, 1.00–34.36 g/100 g, respectively), that able for microorganisms naturally associated with agaves.
are fermented by LAB and yeasts (Kammerer, Carle, and Microorganisms are transported to the scraped cavities of the
Schieber 2004). An important component of black carrots stems through the air or the action of scrapers and other uten-
are carotenoids, the most important being anthocyanins,

sils used for collecting agave sap (Alvarez-R
ıos, Figueredo-
and cyanidine glycosides (acylated with p-coumaric, ferulic, Urbina, and Casas 2020).
p-hydroxybenzoic and synapic acids), peonidine and Cereals are other substrate used in fermented beverages.
pelargonidine glycosides (Kammerer, Carle, and Schieber Between the mostly common products obtained by fermen-
2003). In fact, the purple-red coloring of the Shalgam is tation of cereals is the traditional beer, which is mainly
related to the pigments of the anthocyanins of the black fermented by the action of S. cerevisiae. Nevertheless, other
carrot and b-carotenes found in carrots. Mineral content in microorganisms may also be involved. For example, Belgian
black carrot includes sodium, potassium, calcium, magne- lambic beer is traditionally produced by spontaneous
sium, and phosphorus. These compounds available are used fermentation involving Enterobacteriaceae and LAB species
for the microorganisms growth, transforming biochemically (Spitaels et al. 2015; De Roos and De Vuyst 2018). In
and organoleptically the substrates, and producing different this case, the cereals have adequate nutrients that become
metabolites that enrich the food with different micro- a viable medium for the growth of LAB. This influences
nutrients (vitamins, minerals, amino acids, etc.) (Ghosh the organoleptic properties of the final product, since it
et al. 2015). eliminates the "green" and unpleasant taste associated with
Pulque is a fermented beverage that use as substrate a plant raw cereals in the beer (Peyer, Zannini, and Arendt 2016).
(Agave). Agave sap contains sugars (sucrose, fructose, and glu- A wide diversity of cereals such as millet, oats, barley,
cose), vitamins, minerals, and amino acids. It has been reported rice, corn, and others have been used. Their rich chemical
10 R. B. CUVAS-LIMON ET AL.

composition makes them feasible to be used as substrates in the corn part of the conventional yellow corn. The major
different fermented foods and beverages. Cereals have been physical structures of maize are: endosperm (82–83%), germ
used as raw materials for many years to develop products (10–11%), pericarp (5–6%), and tip cap (0.8–1.0%). Gross
through fermentation in different countries. In general, the maize grain composition is 68–74% starch, 8–11.5% protein,
cereal contain water, vitamins, minerals, carbohydrates, diet- and 4–5.5% fat. The pericarp is source of crude fiber (87%),
ary fiber (DF) and proteins (Blandino et al. 2003). consisting mainly of hemicellulose (67%) and cellulose
Cereals are important source of hemicelluloses, which (23%), with only a small fraction of lignin (0.1%) (L
opez-
include arabinoxylans, b-glucans, and arabinogalactans, also Hern
andez et al. 2018). Corn contains phenolic acids and
called DF (Saulnier et al. 2007). DF are non-digestible com- anthocyanins. Phenolic acids are the most effective natural
ponents consisting of non-starch polysaccharides, resistant antioxidants. In vitro and in vivo studies have shown that
starch, oligosaccharides (mainly fructans), and carbohydrate- phenolic acids have various biological properties, such as
free polyphenolic ether lignin. These polymers are present in free radical scavenging, ulcer control, allergy, anti-inflamma-
the cell walls along with lignin, lignans, phenolic acids and tory, and anti-tumor activities (Chen et al. 2017). Corn is
small amounts of protein (McDougall et al. 1996). The cell the substrate of different fermented beverages, such as Boza,
walls of the outer part of the nucleus are thick and hydro- Atole agrio, and Pozol. During the fermentation of the Pozol
phobic and are composed of cellulose, xylans, and significant the polysaccharides are hydrolyzed by the LAB. These drinks
amounts of lignin (Bach Knudsen et al. 2017). are considered prebiotic because of their DF. Cereal fiber
Vitamins in cereals are micronutrients that are essential has been reported to stimulate the growth of beneficial
for the metabolism of all living organisms. They are found colonic microbiota (De Munter et al. 2007). On the other
as precursors of intracellular coenzymes that are necessary hand, LAB are responsible for the characteristic flavor and
to regulate vital biochemical reactions in the cell. It has been aroma of the sour Atole agrio, that is directly related to the
identified as a major source of thiamin in cereals (Capozzi volatile organic compounds produced during fermentation
et al. 2012). Cereals are also important sources of folates (V€akev€ainen et al. 2020). Volatile organic compounds are
(Katan et al. 2009). Folate is mainly concentrated in the derived from amino acids, peptides, and fatty acids. Some of
bran fractions (Kariluoto et al. 2006). the volatile organic compounds responsible for generating
Minerals are micronutrients defined as chemical elements aroma are acetaldehyde, acetone, butan-2-one, butane-2,3-
required by organisms to perform vital functions. The prin- dione (diacetyl), and 3-hydroxybutan-2-one (acetoin) (Lee
cipal minerals in cereals are iron, zinc, copper, manganese, et al. 2019).
calcium, magnesium, potassium, and phosphorus (Berdanier,
Dwyer, and Herber 2013).
Compounds from fermented beverages with
All these components are used by the microorganisms as
bioactive potential
substrateto initiate the fermentation process. Boza is a trad-
itional fermented beverage made of millet, cooked maize, The transformation of the natural components of the raw
wheat, or rice (Akpinar-Bayizit, Yilmaz-Ersan, and material takes place during the fermentation process.
Ozcan 2010). Microorganisms involved in the fermentation produce
Millet are a rich source of carbohydrate, DF, protein, enzymes, such as proteinase, amylase, mannase, cellulase,
phytochemicals (phenolic acids, flavonoids, catechins, phytic and catalase, able to decouple complex compounds into sim-
acid, phytosterols, tocopherols, and tocotrienols), fat, cal- ple bio molecules. By alteration of the nutritional and bio-
cium, iron, and Vitamin E (Rousseau et al. 2019). It has active properties of the food matrices, new compounds with
been reported to contain a low glycemic index. Since the biological activities are synthesized, which may affect benefi-
release of glucose from millet into the blood is slow, this cially the human health (Tamang and Nikkuni 1996; Chettri
reduces the absorption of glucose. It also has low phytic and Tamang 2014; Cifelli et al. 2017).
acid, which helps reduce type 2 diabetes, weight loss, and The nutritional quality of foods obtained by fermentation
the risk of heart disease (Malli and Tripathi 2015). involve three factors: the microorganisms, the substrate and
Another Boza substrate is a wheat bran that is a by-product the environmental conditions. Changes occurring during the
of conventional wheat milling. Wheat contains several essential fermentation due to the action of LAB may be classified
nutrients, including the B vitamin group (Capozzi et al. 2012). into five stages (Figure 1). In a first stage, sugars are trans-
It is high in DF and contains phenolic compounds and flavo- formed into end products, such as simpler acids, carbon
noids. These compounds promote health by reducing the risk dioxide and alcohols. This in turn leads to an increase of
of diabetes, hypertension and colon cancer (Kong et al. 2020). the nutrients available in the food. In a second stage, poly-
Rice is another substrate of Boza, Chhang, and Bhaati jaanr. mers are hydrolyzed and bioactive compounds are enzymati-
Rice is a cereal cultivated in India. This cereal contain carbohy- cally synthesized, such as antioxidants. In a third stage the
drates, proteins, vitamins, mineral, and phytochemicals. Studies bioavailability of nutritive compounds and the concentration
suggest that rice contains rice proteins and peptide fractions of vitamins and amino acids is enhanced, and there is a
with antioxidant, hypertensive, anticarcinogenic and anti-obesity greater bioavailability of phytochemicals and minerals. Later,
effect (Amagliani et al. 2017). in stage 4, the toxic and anti-nutritional compounds are
Corn is a plant of American origin that is consumed degraded. Finally, the synthesis of promoters for absorption
worldwide (Velu et al. 2006). There are different varieties of and uptake occurs (van Hylckama Vlieg et al. 2011).
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 11

Figure 1. Fermentation process of food.

Figure 2. Beverage fermentation process and including the relationship between microorganisms and the primary metabolites found.

Studies have shown that the secondary metabolites may the compound is absorbed and made available to the host
bring specific benefits to the human health. The biogenic cell metabolism is trigged. During the process of gastrointes-
effect is related with the specific metabolic pathway of the tinal digestion, compounds are released from food, followed
microorganisms, so that different biochemical mechanisms by absorption by epithelial cells, tissue distribution and bio-
allow them to fulfill their role as efficient cellular factories activity. For example, bioactive peptides released by the pro-
for the synthesis and release of health promoting com- biotic bacteria have an antimicrobial effect, by acting against
pounds (Figure 2). pathogenic bacteria, that in turn improve the immune sys-
Another factor resulting from the fermentation process is tem (Septembre-Malaterre, Remize, and Poucheret 2018).
the increased bioavailability of nutritional compounds. The nutritional properties are also modified with fermen-
Meaning that by fermentation, the rate and extent to which tation, as there is a reduction in the level of carbohydrates
12 R. B. CUVAS-LIMON ET AL.

such as polysaccharides and non-digestible oligosaccharides. inhibiting peptides have been the most studied for their
The presence of amino acids and their availability is altered potential in the prevention and treatment of hypertension.
with the fermentation conditions, such as low pH, which is ACE is a key enzyme for the regulation of blood pressure
optimal to begins enzymatic activity. For example, in the through the renin-angiotensin system (Wu, Liao, and
fermentation of cereals when the pH decreases, the present Udenigwe 2017). Whole grain consumption has been associ-
phytate begins to degrade; when the phytate is reduced, the ated with a reduced risk of developing several chronic dis-
bioavailability of iron and other minerals increases eases, such as coronary heart disease, arteriosclerosis, type 2
(Blandino et al. 2003). diabetes and some types of cancer (Cho et al. 2013). Cereals
Yeasts are part of bacterial consortiums in fermented are a source of DF and a wide variety of phytochemicals.
foods. Which play a key role in the production of bioactive Physiologically, non-starch soluble polysaccharides contrib-
metabolites such as single-cell proteins, nanoparticles etha- ute to increased viscosity in the small intestine, as this can
nol, aldehydes, isobutanol, isoamyl alcohol, esters, free oils, influence the rate and extent of digestion and absorption.
aromatics compounds, such as a 4-ethylguiacol and 4-ethyl- Cereals contain phenolic and lignan phytochemicals.
phenol folate, carotenoids, Y-amino, butyric acid, antimicro- Phenolics are absorbed in the small intestine, and another
bial peptides, melatonin, 4-hydroxy-2(or5)-ethyl-5(or 2)- macronutrient passes to the large intestine, where the micro-
methyl-3(2H)-furanone (HEMF) and phenolic compounds. biota, which degrades and metabolizes DF into SCFAs and
They also produce hydrolytic enzymes responsible for the gases, also converts phenolic compounds into a few other
transformation of bioactive molecules such as amylase, lac- metabolites. These metabolites are absorbed by the body and
tase, xylanase, cellulase, phytase, lipase, inulinase, and super- have the ability to influence metabolism at the cellular level
oxide dismutase, b-glucosidase, b-galactosidase, and (Bach Knudsen et al. 2017).
fructosyl transferase (Chaves-L
opez et al. 2012; Mu, Yang, Arslan-Tontul and Erbas (2019) enriched the protein
and Yuan 2012; Akabanda et al. 2013; Chi et al. 2016). content of probiotic Boza by the addition of gluten, zein,
When yeasts degrade the substrate of fermented beverages and chickpea flour. Its probiotic potential was evaluated by
there is a production of oligosaccharides, polyphenols lactu- co-culture fermentation of the cereal medium with L. acid-
lose oligosaccharides and xylo-oligosaccharides and carote- ophilus, Bifidobacterium bifidum, and Saccharomyces boular-
noids, showing the potential of yeasts for the development dii. Chickpea added to Boza provided the highest cell counts
of biotechnological foods by creating new products with of L. acidophilus (7.92 log CFU/g), B. bifidum (7.32 log
nutraceutical value (Bhataya, Schmidt-Dannert, and Lee CFU/g), and S. boulardii (3.26 log CFU/g during storage.
2009; Rai et al. 2016; Han et al. 2017; Rodriguez et al. 2017). With the addition of gluten, the protein content of the sam-
Research has shown that traditional fermented beverages, ple was enriched four times as compared with control Boza.
such as Boza fermented drink, are a source of bioactive During fermentation and storage, a total of 36 different
compounds, which makes the drink a beverage with func- compounds were identified with the major compounds as 9,
tional properties (Botes et al. 2007). Boza is a source of pro- 12-octadecadienoic acid, 9-octadecenoic acid, hexadecanoic
biotics, prebiotics (from exopolysaccharides (EPS) produced acid and hexadecanoic acid, 2-hydroxyl-1-(hydroxymethyl)
by LAB), bioactive peptides (with anti-hypertension activity), ethyl ester. The concentration of volatile compounds gener-
and DF (from the cereals used as substrate). Probiotics and ally decreased during storage of samples.
prebiotics have been extensively reported to prevent and Shalgam is made from black carrots and its bioactive
treat gastrointestinal health diseases, colon cancer, allergies, compounds are provided by the raw material, which is rich
obesity, insulin resistance syndrome, type 2 diabetes, hyper- in anthocyanins, phenolic compounds, vitamins and miner-
tension, osteoporosis, among others (Nobre et al. 2015; als. The anthocyanins are flavonoids with recognized anti-
Markowiak and
Sli_zewska 2017; Salmer
on 2017). oxidant properties (Tanriseven et al. 2020). These
LAB have the ability to produce extracellular polymers antioxidants have anti-cancer, anti-tumor, and anti-inflam-
known as microbial (EPS) (Vu et al. 2009). EPS are pro- matory properties which may prevent cardiovascular diseases
duced during the growth of bacteria and have a generally (Kong et al. 2003). Anthocyanins as cyanidin-3-glycoside
recognized safe status (GRAS); these substances contain cer- were quantified in Shalgam in a concentration up to
tain antibiotic peptides and bioactive compounds with 114.1 mg/L (Erten, Tanguler, and Canbaş 2008). Other phen-
nutraceutical properties and functions (Abedfar et al. 2020). olic compounds present in black carrot are chlorogenic
EPS can be used to improve the rheological properties, tex- acids, which are derivatives of hydroxycinnamic acid gener-
ture and stabilization of foods. They have been used as good ated by the esterification of cinnamic acids (caffeic, ferulic,
viscosity agents, stabilizers, emulsifiers, as well as gelling p-coumaric, and (-)-quinic acids) (Mizgier et al. 2015). On
agents in foods and pharmaceutical products (Sanalibaba the other hand, LAB also help to increase the immunity
and Cakmak 2016). against pathogenic bacteria, as well as regulating the intes-
Peptides are derived from proteins. These proteins are tinal microbiota. It has been reported that in Shalgam, the
often cryptic and dormant until proteolytic release of the most important compound formed is the lactic acid or lac-
active peptides. The release can occur by enzymatic activity tate, which results from lactic fermentation. Lactic acid is
during gastrointestinal digestion or during ripening and fer- produced in an average concentration of 6.81 g/L. It pro-
mentation (Amorim et al. 2019). Among the various types vides changes in the taste and aroma of the drink (Erten,
of bioactive peptides, angiotensin converting enzyme (ACE) Tanguler, and Canbaş 2008).
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 13

In the case of Leben, it is the substrate (milk) that gives Pozol has a great microbiological diversity, thus, the pro-
the chemical, microbiological and sensory properties to the duction of bioactive compounds from microorganisms iso-
fermented food. Through the interaction of milk with LAB, lated from Pozol has been studied. Phister, O’Sullivan, and
bioactive compounds (sterols, fibers, vitamins, minerals, McKay (2004), identified three antimicrobial compounds
organic acids) are obtained. In addition to the production of produced by a Bacillus sp. strain CS93 isolated from Pozol,
bacteriocins (Bach Knudsen et al. 2017). In Leben, organic named bacilysin, chlorotetaine, and iturin. These compounds
acids are produced during fermentation, which potentially were associated to the medicinal properties attributed to
inhibits the proliferation of Escherichia coli and other coli- Pozol. Later, it was found that the same bacteria is able to
forms. A proteolytic activity has also been reported in Leben produces also bioactive lipopeptides, which are versatile
associated to the yeasts (Samet-Bali et al. 2017). molecules, in which peptides are attached to lipid chains.
Chhang is a rice-based drink. Rice contains vitamins, pro- These lipopetides may also have medicinal properties and
teins, polyphenolic compounds (phytic acid, ferulic acid, have been used as antibiotics (Moran et al. 2010).
and oryzanols). During fermentation of rice produced, bio- Several bioactive compounds produced from Pulque fermen-
logically active metabolites such as amino acids, organic tation have been reported, highlighting the presence of vitamin
acids, phenolic acid, ferulic acid, vanillic acid, protocatechuic C (Raca~ no 2000), but also other vitamins such as pantothenic
acid, phytic acid, inositol, and antimicrobial metabolites. acid, thiamin, p-amino benzoic acid, pyridoxine, biotin ascorbic
Many plant phenols are often biologically unavailable after acid and riboflavin (Sanchez-Marroquin and Hope 1953). It has
intake, such as ferulic acid, thus, fermentation can improve also been reported that Pulque is a source of amino acids such
antioxidant potential of food (Sindhu and Khetarpaul 2002). as Ile, Leu, Lys, Cys, Phe, Tyr, Thr, Trp, Val. It has also been
Antimicrobial metabolites have been identified in Chhang, reported that Pulque provides a significant amount of iron
including organic acids, diacetyl, hydrogen peroxide, antibi- (Morales de Le
on, Bourges, and Camacho 2005).
otics, and bacteriocytes related to the indigenous microor- Giles-G
omez et al. (2016) evaluated in vitro and in vivo
ganisms (usually LAB). In vitro studies shown that L. the probiotic potential of the L. mesenteroides P45 strain iso-
plantarum F22 isolated from Chhang holds probiotic fea- lated from Pulque. The strain showed resistance to lysozyme,
tures, since it showed resistance to the extreme conditions low pH conditions (3.5) and bile salts (0.1 and 0.3% oxgall).
of the gastric simulation (Handa and Sharma 2016). It also showed antibacterial activity against pathogenic strains,
In the case of Chal, which is a milk-based fermented bev- such as Listeria monocytogenes, E. coli, Salmonella ent
erica
erage, the functional properties are derived from the inter- serovar Typhi and Salmonella ent
erica serovar Typhimurium.
action of the substrate with the LAB. Tamang and Thapa In vivo tests run with a mice model showed an anti-infectious
(2006) investigated the isolation and identification of LAB activity of L. mesenteroides P45 against S. ent
erica serovar
from Chal and studied the antioxidant activity of camel and Typhimurium. Torres-Maravilla et al. (2016) isolated L. san-
bovine milk fermented with LAB. Post-fermentation results franciscensis LBH1068 from Pulque and evaluated its potential
showed that fermented camel milk has higher antioxidant as a novel anti-inflammatory probiotic strain.
activity than bovine milk. The fermented milk of camel with Although traditional spontaneous fermented beverages,
L. lactis SM10 showed better organoleptic properties and which are consumed worldwide, have shown an interesting
higher values of antioxidant activities—DPPH (57.90 mm) potentialas a source of bioactive compounds,, they are not
and ABTS (148.35 mm)—as compared to other strains standardized beverages and are their bioactive compounds
(Soleymanzadeh, Mirdamadi, and Kianirad 2016). content may significantly vary for the same product produced
It has been reported, that from the 88 LAB strains isolated in different batches. Thus, they are not produced by the food
from Atole agrio, 87.5% were identified as folates producers, industry and are not for sale in the functional food market. It
71.6% degraded phytates, 38.6% produced exopolysaccharides, is true that studies arguing their functionality as such are
12.5% showed amylolytic activity, and 81.8% were resistant to lacking, but traditional fermented beverages are still a source
antibiotics. Atole agrio has been used by indigenous and mes- of bioactive compounds.
tizo groups from South-East Mexico not only for its nutri-
tional value, but also for medicinal and ceremonial purposes
Bioactive compounds: beneficial health effects
(V€akev€ainen et al. 2018). It has been reported that low pH in
sour Atole agrio is related to antimicrobial activity against As mentioned in the previous section, fermented beverages
gram-negative microorganisms. are a source of bioactive compounds because through bio-
Microbiological and biochemical changes produced dur- synthesis and biotransformation new derived compounds
ing the fermentation of the Chorote have been reported. At with bioactive potential are generated. These bioactive com-
the end of the process there is a decrease in pH (up to 4.2), pounds fulfill specific functions in the human body. These
which is related to the production of lactic acid, an increase are exerted by the active principles of the substances. They
in total protein (103.0–152.7 g/kg) and soluble protein influence the cellular activity and the mechanisms in the
(6.1–31.9 g/kg), and an increase in available amino acids, body, which help to promote health (Figure 3).
such as lysine and tryptophan. Fungi, yeasts, lactic amylo- Bioactive compounds produced from these fermentations
lytic acid, and nitrogen-fixing bacteria have been observed have several positive applications in human health. These
to increase during fermentation (Castillo-Morales, Wacher- bioactive compounds have been studied in vitro and in vivo
Rodarte, and Hern
andez-S
anchez 2005). to demonstrate their relationship with the improvement of
14 R. B. CUVAS-LIMON ET AL.

growth effect that inhibits the multiplication of pathogenic

bacteria. During fermentation, probiotics create a favorable
environment (lowering the pH and reducing the availability
of oxygen), that allows the release of bacteriocins which
counteract the growth of pathogenic microorganisms
(Koebnick et al. 2003; Bekkali et al. 2007; Turan et al. 2015).
In addition, some studies suggest that probiotics can play a
beneficial role in relieving the symptoms of constipation, at
least with certain strains of probiotics. Due to the fermenta-
tion of fiber in the intestine, the synthesis of essential micro-
nutrients such as vitamins, amino acids and enzymes takes
place, improving the metabolic activity of carbohydrates
(Chugh and Kamal-Eldin 2020).
Cervantes Elizarr
as et al. (2019) studied isolated and
identified LAB from Aguamiel and Pulque and evaluate their
probiotic potential and effect against Helicobacter pylori.
They reported that 60% of the isolates exhibited antimicro-
bial activity against E. coli and Staphylococcus aureus. The
growth of H. pylori ATCC 43504 was suppressed by all the
LAB, and the urease activity from all the H. pylori strains
was inhibited, which may decrease its chances for survival
Figure 3. Heal benefits of fermented foods. in the stomach. The results suggest that LAB isolated from
Pulque and Aguamiel could be an option to establish a
chronic degenerative diseases. Some of the activities pro- harmless relationship between the host and H. pylori, help-
vided by microorganisms isolated from fermented beverages ing in their eradication therapy.
are summarized in Table 3. The probiotic potential of 14 strains isolated from Pulque
One of the most important degenerative diseases, affect- was recently tested. The isolates belonged from the following
ing about a quarter of the world’s population, is hyperten- phylogenetic groups: L. plantarum, L. paracasei, L. brevis, and
sion, which is a major but controllable risk factor in Lactobacillus composti. Bacteria resistance for lysozyme, low
cardiovascular disease and related complications. pH, and bile acid was evaluated. Strains adherence to human
Compounds that play a role in the regulation of blood pres- intestinal epithelial cells and respective immunomodulatory
sure by reducing ACE activity are known as ACE inhibitors. properties were also evaluated. Bacterial strains with anti-
Inhibition of ACE, which is one of the health effects of bio- inflammatory properties were then tested in vivo using an
active peptides, is considered a useful therapeutic approach
induced chronic colitis mouse model. A reduction of weight
in the treatment of hypertension (Korhonen and Pihlanto
loss, significant decreased in gut permeability, and cytokine
2006; Akıllıoglu and Karakaya 2009).
modulation was found for mice treated with the lactobacilli
There are many studies concerning ACE-inhibitory pepti-
isolated from Pulque. In particular, the L. sanfranciscensis
des and ACE-inhibitory activities of meat, fish, milk, fer-
LBH1068, shown high potential as a probiotic to treat inflam-
mented dairy products and eggs (He, Liu, and Ma 2013).
matory bowel diseases (Torres-Maravilla et al. 2016).
Kancabaş and Karakaya (2013), studied ACE inhibitory
Based on the Brazilian indigenous beverage Cauim, a
activity of protein hydrolysate and protein fractions obtained
from Boza, and determined the effect of in vitro digestion blend of cassava and rice was fermented with indigenous
on the ACE inhibitory activity of Boza. The protein content strains L. plantarum from Cauim and T. delbrueckii from
of the hydrolysate obtained after digestion was found to be Tarub
a, and the commercial probiotic L. acidophilus.
lower than that of the Boza, but the inhibitory activity of Fermentation with the co-culture of the LAB strains shown
the hydrolysate ACE was significantly higher (p < 0.05). The to confers potential health benefits to the fermented prod-
protein hydrolysate was separated into three fractions uct. It has been reported that L. plantarum can decrease
according to molecular weight, and the separate protein intestinal heavy metal absorption, reduce metal accumula-
fractions inhibited ACE activity. The IC50 values of the frac- tion in tissues, and alleviate hepatic oxidative stress (Behera,
tions revealed that the ACE-inhibitory activity of Boza Ray, and Zdolec 2018). In addition, L. plantarum has anti-
increased 3.5-fold after stomach digestion. Results showed oxidant properties. These bacteria colonize the intestinal
that Boza can be considered a good source of ACE-inhibit- tract and play a key role in protecting against free radicals.
ing peptides. L. plantarum also contributes to the preservation of various
Other studies on the beneficial effects provided by bio- disorders such as diabetes, cardiovascular disease, and ulcers
active compounds have been exploring its antimicrobial of the gastrointestinal tract (Kaushik et al. 2009). Safety of
activity. Antimicrobial activity is related with the probiotic the food was improved by the resultant acidification and
microorganisms. The mechanism of action that results in production of organic acids. The yeast strain T. delbrueckii
the antimicrobial activity is described by the competitive showed to improve the product’s digestibility by reducing
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 15

Table 3. Bioactive compounds and functional properties of fermented foods.

Synthesized in
Functional properties Bioactive compounds Microorganisms fermented foods Health benefits Reference
Antimicrobial Properties Antimicrobial compounds LAB Vegetables Tamang et al. (2009);
(Bacteriocin) Milk Protection of the Khan, Flint, and Yu
gastrointestinal tract by (2010); Gaggia et al.
SCFAs production, pH (2011); Grosu-Tudor
modulation, hydrogen and Zamfir (2013)
Lactococcus lactis BH5, peroxide, and production Chang et al. (2008); Hur
Bacteriocin Leuconostoc citreum GJ7, Kimchi of bacterial type et al. (2000); Shin
Pediococcus pentosaceus. inhibitory substances. et al. (2008)
Pediocin Anticancer effects

Nisin Z Lactococcus lactis. Dahi (India) Antiviral effects Mitra, Chakrabartty, and
Biswas (2010)
Antimicrobial compounds Weisella cibaria. Fermented cabbage Patel et al. (2014)
product
Antioxidant Antioxidants compounds, Bacillus, Asian fermented Modulate circulatory King et al. (2012)
Properties Peptides, Lactobacillus, soybean foods oxidative stress Mishra et al. (2015);
Enzymes. Bifidobacterium. Gaisawat et al. (2019)
Soybean food of India Protect cells against Moktan, Saha, and
and Nepal carcinogen-induced Sarkar (2008);
damage Tamang et al. (2015)
Antioxidant
Anti-inflammatory
Anticancer
Immunomodulatory Bioactive peptides, Proteolytic Fermented beverages Immune modulating De Mejia and Dia
Properties Amino acids. microorganisms effects (2010); Chugh and
(Bacillus), Kamal-Eldin (2020)
LAB. Maintain the energy
balance
Contribute to antioxidant
effects
Anti-inflammatory effects
Inhibitory properties Producing peptides and Enzyme (ACE) K
efir Minimize the risk of Quir

os et al. (2005)
amino acids. developing chronic or
Koumiss degenerative diseases. Chen et al. (2010)
Yogurt Papadimitriou
et al. (2007)
Fermented camel milk He, Liu, and Ma (2013)
Cheese Meyer et al. (2009)
Fermented fish products Ichimura et al. (2003)
Enhancement of Lipases, LAB, Fermented beverages Help to improve the Den Besten et al.
metabolic functions Proteases, Bifidobacterium. metabolism (2013); Chugh and
Esterases, Kamal-Eldin (2020)
Amylases Improve nutrient
b-galactosidase, absorption
Lactase
Mitigate lactose
intolerance
Production of SCFAs Acetate, LAB Fermented beverages Provides 60–70% of the Topping and Clifton
Butyrate, energy needed by the (2001); Gill
Propionate. colon, muscle and et al. (2018)
brain cells
Therapeutic effects
Anti-inflammatory bowel
Anti-colon cancer
Help to heart diseases
protection against obesity
and diabetes,
Production of vitamins Vitamin B12, Bifidobacterium, Fermented beverages Help to synthesize DNA Mohammed et al.
Vitamin K, Lactobacillus. Combat (2014); Piwowarek
Vitamin B6, cardiovascular disease et al. (2018)
Cobalamin,
Folate,
Thiamin.

starch, increasing the antioxidant activity, and further stimu- having key role in wide range of biological and pharmaco-
lating LAB growth during fermentation (Freire et al. 2017). logical properties, such as anti-inflammatory, anticancer,
Polyphenols derivate from secondary metabolites origi- antimicrobial, antiallergic, antiviral, antithrombotic, hepato-
nates from primary metabolites (carbohydrates, amino acids, protective, food additive, signaling molecules, and many
and lipids). They are known as strong natural antioxidants, more. Hence the importance of being studied and
16 R. B. CUVAS-LIMON ET AL.

incorporated into food beverages (Kumar and Goel 2019; functional properties, as well as in the optimization and
Kumar et al. 2019). Changes in polyphenols during Shalgam design of new food bioprocesses.
fermentation was recently studied. It was observed that total As a final remark, although it has been reported that fer-
phenolic content, anthocyanins content and total antioxidant mented foods are a good source of bioactive compounds,
capacity greatly increase in the first 12 days of fermentation. very few studies have been conducted to disclose the rela-
The recovery of the Shalgam drink was largely identical to tionship between the intake of traditional fermented foods
the black carrot results in terms of flavonoids, phenols and and their impact on human health.
anthocyanins (identified as cyanidin), and antioxidant cap-
acity, after in vitro digestion. The amount of beneficial com-
Disclosure statement
pounds in the early fermentation stage was found
significantly less than with the final product. The degrad- The authors declare no conflict of interest.
ation of phenolics and anthocyanins was observed after the
€
bioaccessibility tests (Toktaş, Bildik, and Ozçelik 2018). Abbreviations
The SCFAs that are produced during fermentation with
AAC Acetic acid bacteria
LAB, specifically the butyrate, have been associated to integ- ABTS 2,20 -azinobis-(3-ethylbenzothiazoline-6-sulfonic acid)
rity maintenance of the intestinal mucosa (Kort et al. 2015). ACE Angiotensin converting enzyme
Butyrate may reduce the risk of developing colon cancer, by CFU Colony forming units
reducing cell proliferation and stimulating cell differenti- DPPH 2,2-diphenyl-1-picrylhydrazyl
DF Dietary fiber
ation. It is also associated with maturation of the enteric
EPS Exopolysaccharide
neurons. In addition, SCFAs have been identified as import- LAB Lactic acid bacteria
ant modulators of the immune system, helping chronic SCFAs Short chain fatty acids
inflammation (Lee et al. 2015). w/v weight/volume
Through the review conducted, it was observed that there
are many studies discussing bioactive compounds (phenolic
Funding
compounds, antioxidants, bioactive peptides, etc.) and their
beneficial effects on human health. However, few studies The authors acknowledge the National Council of Science and
approach the relationship between traditional fermented foods, Technology (CONACYT, Mexico) for the financial support (CVU
559365). This study was also supported by the Portuguese Foundation
bioavailability and bioaccessibility of these bioactive compounds. for Science and Technology under the scope of the strategic funding of
The scientific challenge is to perform in vitro and in vivo UID/BIO/04469/2019 unit and BioTecNorte operation (NORTE-01-
studies, in addition to study the interactions of the com- 0145-FEDER-000004) funded by the European Regional Development
pounds, the digestion, absorption and metabolism pathways. Fund under the scope of Norte2020 - Programa Operacional Regional
Also to understand the bioaccessibility and bioavailability of do Norte also, Project ColOsH 02/SAICT/2017 (POCI-01-0145-
FEDER-030071).
the functional properties of the traditional fermented food-
s,as a source of bioactive compounds, and its impact on the
human health. This knowledge will certainly expand the
market for traditional fermented beverages con- ORCID
sumed worldwide.
Clarisse Nobre http://orcid.org/0000-0001-9693-2395
Rosa M. Rodriguez-Jasso http://orcid.org/0000-0001-8971-0639
H
ector A. Ru
ız http://orcid.org/0000-0003-0917-0324
Future trends and conclusions Araceli Loredo-Trevi~
no http://orcid.org/0000-0002-2857-3340
Currently, science and technology face a major challenge in Ruth Belmares http://orcid.org/0000-0003-1362-4691
the creation, development and improvement of foods with
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