Traditional Fermented Foods and Beverages from

a Microbiological and Nutritional Perspective:

The Colombian Heritage
Clemencia Chaves-López, Annalisa Serio, Carlos David Grande-Tovar, Raul Cuervo-Mulet, Johannes Delgado-Ospina,
and Antonello Paparella

Abstract: Fermentation has been used for preserving foods for centuries prior to the invention of pasteurization and
sterilization, and every culture has a variety of fermented products as part of its diet. This paper reviews the diversity of
fermented foods and beverages from Latin America; these fermented products are produced by traditional methods that
exploit mixed cultures of various nonpathogenic microorganisms. Fermented foods covered in this review include maize,
cassava, palm sap, sugar cane juice, cocoa, and milk. We explore the history of some Colombian fermented foods and
beverages, which are today part of the tradition of some ethnic groups, and evaluate their technology, microbiology, the
presence of some nutritional factors, and safety concerns. To the best of our knowledge, this is the 1st systematic review
on Colombian fermented beverages and foods, and we believe that it may contribute to valorize these products that are
still part of the Latin America tradition.
Keywords: beverages, cereal products, dairy products, fermentation, functional foods

Introduction In Colombia, local agricultural commodities are generally used

Fermentation is one of the ancient methods to preserve foods.
Due to its nutritional value and to the variety of sensory attributes,
it became popular in many cultures in which even today fermented
foods are part of the daily intake. In fact, fermentation is a rel-
atively cost-effective, low-energy preservation process, which is
essential to ensure food shelf-life and safety (Liu and others 2011).
Moreover, it remains the major technology for important food
production, even though other manufacturing technologies are
available nowadays (Plessas and others 2011).
In traditional fermented products, the process of fermentation
is spontaneous and uncontrolled. The products are often obtained
under local climatic conditions, and therefore the sensory charac-
teristics and the quality are variable. In addition, as indicated by
Simango (1997), fermentation provides a natural way to reduce
the volume of the material to be transported, to destroy undesir-
able components, to enhance the nutritive value and appearance
of the food, to reduce the energy required for cooking, as well as
to make a safer product.
MS 20140460 Submitted 3/20/2014, Accepted 6/11/2014. Authors Chaves-
López, Serio, and Paparella are with Faculty of Bioscience and Technology for Food,
Agriculture and Environment, Univ. of Teramo, Via C.R. Lerici, 1, 64023 Mosciano
Stazione, Italy. Authors Chaves-López, Grande-Tovar, Cuervo-Mullet, and Delgado-
Ospina are with Grupo de Biotecnologia Universidad de San Buenaventura Sede Cali,
Avenida 10 de Mayo, La Umbrı́a, Vı́a a Pance, Colombia. Direct inquiries to author
Clemencia Chaves-López (E-mail: chaves@unite.it).
as raw material for the production of traditional fermented foods,
by using traditional manufacturing procedures. Although some
fermented foods and beverages are industrially produced, many are
from household production for daily domestic consumption, and
even today some tribes produce fermented beverages as stimulant
and for medical purpose.
Since pre-Hispanic times, fermented products from maize (Zea
mais), cacao (Theobroma cacao), and cassava (Manihot esculenta) have
been the most widely used products in Colombia, and indigenous
populations developed and established processes for transforming
them into different types of products that are produced even today
(Lorence-Quiñones and others 1999), although microbial and en-
zymatic processes involved in food manufacturing have not been
completely elucidated until now. Actually, progress in fermenta-
tion technology could provide interesting opportunities to solve
the problem of food safety and malnutrition in some countries
where poverty, malnutrition, and infant mortality are widely seen
(Chelule and others 2010).
The aim of this review was to describe the main characteristics
of the most common traditional fermented foods and beverages
from Colombia, produced using autochtonous microorganisms to
ferment different raw materials: nutrient-rich crops (cereals and
roots), sugar cane, palm sap, cocoa, and animal products (milk).
In detail, the main microbiological and nutritional properties of
fermented foods, as well as the technological improvements that
have been achieved in manufacturing, will be highlighted. Al-
though many fermented foods and beverages have a long history of


C 2014 Institute of Food Technologists®

doi: 10.1111/1541-4337.12098 Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1031
Colombian fermented foods and beverages . . .
providing good, even exceptional, health benefits, some com-
pounds formed during fermentation provide no health benefit at
all. For this reason, we will consider both beneficial and detrimen-
tal effects.
Cassava-Derived Products
Cassava or manioc is an American original crop, spread across
South America. According to an Indian legend, the aborigines
were able to eliminate the poison from this root, make it edible
when cooked, and therefore cassava symbolizes the conversion of
death into life. Although cassava roots are rich in calories, they
are grossly deficient in proteins, fat, and some of the minerals and
vitamins (Charles and others 2005). Cassava contains potentially
toxic substances, lotaustralin and linamarin, both cyanogenic gly-
cosides, which generate hydrocyanic acid (HCN) by means of an
enzyme, linamarase, present in the tuber tissue. Cassava also con-
tains substances such as phytate, fiber, nitrate, polyphenols, oxalate,
and saponins that can reduce nutrient bioavailability (Montagnac
and others 2009).
The presence of HCN (also called hydrogen cyanide and for-
merly Prussic acid) ranges from 150 to 1000 mg/kg (Acosta-
Muñoz and Mazamorra-Valderrama 2004) in fresh tubers. Two
cassava varieties are recognized according to the concentration of
cyanogenic glycosides: “bitter cassava,” rich in glycosides, espe-
cially if grown in nutrient-poor areas, and “sweet cassava,” which
has lower amounts of these glycosides, which are located primar-
ily in the rind (Montoya-Henao 2007). Their inactivation occurs
when cooking is carried out at 75 °C, at conditions able to in-
activate the linamarase, and can be increased by using enzymatic
hydrolysis. Moreover, the cassava fermentation process results in
a reduction of its toxic products and an increase of product taste
and aroma (Holzapfel 1997). The lethal dose for HCN in an adult
depends on body weight and is considered to be between 30 and
210 mg (Tylleskar and others 1992).
In Colombia, cassava is mainly used for the production of starch
and its extraction is carried out since ancient times; today the
extraction is a business that began about 6 decades ago, principally
in Southwest Colombia, in places known as “rallanderı́as.”
Either a chemical or an enzymatic process can be used to extract
cassava starch. This starch is appreciated in the food, paper, textile,
adhesive, and pharmaceutical industries, but it must be modified
to reduce its toxicity due to the presence of cyanogenic substances.
Most modifications occur in the starch granule by means of phys-
ical, chemical, and enzymatic processes, which cause changes at
the molecular level, affecting its swelling ability, bonding power,
fluidity, pH, and temperature stability (Vargas-Aguilar 2010).
Sour Starch
The fermented sour starch of cassava known as “Almidón agrio” is
obtained by starch fermentation before drying. This 2-step process
is important to obtain a sour starch of high quality, expressed as
bread-making potential (BMP) (Laurent 1992). In fact, it has been
reported that BMP increases from 2 cm3 /g to at least 5 cm3 /g in
4 h of sun-drying (Larsonneur 1993).
To produce fermented sour starch of cassava (Figure 1), the
roots are washed to remove all foreign matter and grit or coating.
Subsequently, they should be grated to obtain a dough containing
the starch, which is washed, filtered, and decanted into open set-
tling tanks. The starch precipitates and is introduced into closed
containers under anaerobic conditions to carry out a natural fer-
mentation process for a long period (approximately 20 to 30 d,
depending on climatic conditions), with the final pH ranging
1032 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
Cassava roots
Water
Washing
Crushing
Water
Sieving Cassava bran
Drying Sedimentation (6-24 hours)
Fermentation
(20-30 days environmental
Sun drying (8-10 hours)
Storage Storage
Native starch Sour starch
Figure 1–Schematic diagram of the traditional process for Colombian
cassava starch production.
between 3.5 and 4.0. In some areas, especially those with warm
climates, the fermentation tanks are buried to maintain a constant
temperature.
Natural fermentation is characterized by a succession of mi-
croorganisms (Figueroa and others 1995; Ampe and others 2001)
in which the predominant microbial groups are lactic acid bacteria
(LAB) (108 to 109 log CFU/g) and yeasts (101 to 104 log CFU/g)
(Cadena and others 2006). In Colombian sour starch, a large di-
versity of LAB species, and namely Lactobacillus manihotivorans and
L. plantarum (the most frequent species), L. casei, L. hilgardii, L.
buchneri, L. fermentum, Leuconostoc mesenteroides, and Pediococcus spp.,
have been reported (Ben Omar and others 2000). Several strains
of these species have been shown to have high amylolytic activity
thus they have an ecological advantage in fermented sour cas-
sava as they can partially hydrolyze raw starch (Rodriguez-Sanoja
and others 2000) to provide sugars such as glucose or maltose
that can be used as an energy source by other microorganisms.
While L. manihotivorans is present only during the 1st period of
fermentation, when it may participate in accelerating the rate of
degrading starch (Ampe and others 2001), L. plantarum, is present
during all the steps of the fermentative process and contribute
to acidify the substrate. By using denaturing gradient gel elec-
trophoresis (DGGE) followed by 16S rDNA sequencing, close
relatives of Lactococcus lactis, Streptococcus spp., Bifidobacterium mini-
mum, and Enterococcus saccharolyticus were detected during Colom-
bian cassava starch fermentation (Ampe and others 2001). The
last 2 species, which were found in high quantities, might be a
sign of fecal contamination of the water used to wash cassava.
Although Ampe and others (2001) suggested that these species
do not participate in spontaneous lactic acid fermentation, the
large arsenal of Bifidobacterium genes involved in the breakdown

C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .
of carbohydrates (for example, fructo-oligosaccharides, gluco-
oligosaccharides, xylo-oligosaccharides, lactulose, and raffinose)
(Ventura and others 2011) may suggest a possible role of this genus
in starch fermentation. Moreover, although the relevance and spe-
cific role of E. saccharolyticus in cassava fermentation remains to be
defined, Enterococcus spp. could contribute to the development of
the sensory characteristics during fermentation.
The yeast role in cassava starch fermentation is poorly under-
stood. Some authors suggested that yeasts growth depends on
the degradation of cassava starch by other organisms (Lacerda
and others 2005), while others suggested that yeasts contribute
to starch hydrolysis, as well as to the production of enzymes
such as linamarase and polygalacturonase, and aldehydes and es-
ters that impart a pleasant aroma to the final product (Oyewole
and Odunfa 1990; Oyewole 2001). In Brazilian cassava fermenta-
tion, the presence of Galactomyces geotrichum, Issatchenkia spp., and
a Candida ethanolica-like species throughout the process has been
documented (Larsonneur and others 1999; Lacerda and others
2005). Geotrichum candidum, the anamorph of G. geotrichum, is an
oxidative species, and only a few strains with amylase activity have
been reported by Arotupin (2007). The presence of Issatchenkia spp.
and a C. ethanolica-like species in advanced stages of the process
suggested a higher acid tolerance of these yeasts (Halm and others
2004).
In Colombian rallanderı́as, the water used in a previous fermen-
tation is used as inoculum for successive fermentations. According
to Kimaryo and others (2000), inoculation of cassava with one or
several selected LAB species or strains would provide improved
fermentation control and better product quality. Also, the use of
Aspergillus niger gives good characteristics to cassava starch during
fermentation (Quintero and others 2012).
Fermentation of cassava root flour enhances its nutrient con-
tent through the biosynthesis of vitamins, essential amino acids,
and proteins, (improving protein quality), and fiber digestibility.
It also enhances micronutrient bioavailability and helps degrade
antinutritional factors (Achinewhu and others 1998). In fact, hy-
drolysis of cyanogenic glucosides partially increases during cassava
root fermentation by the action of both endogenous linamarase
and linamarase produced by LAB, notably Leuconostoc mesenteroides
and Lactococcus lactis (Kobawila and others 2005). It is to under-
line that during sour starch production, from 40% to 70% of the
cyanide content is released in the water used to wash cassava, while
5% to 10% is present in the cassava bran that is usually used for
animal feed, and finally about 4% is reduced after fermentation
and sun-drying to less than 1% (1 to 5 ppm) (Arguedas and Cooke
1982). On the other hand, it has been reported that unfermented
cassava flour from medium-cyanide content variety had a sig-
nificantly higher (P < 0.05) phytate content in comparison with
low-cyanide content variety (Oboh and Elusiyan 2007). However,
cassava root fermentation minimizes the antinutritional value of
phytate; as it can interact with multivalent cations and/or proteins,
forming insoluble complexes, which impair the bioavailability of
many essential minerals. Therefore the presence of phytates in
foods is a concern (Cheryan and Rackis 1980; Marfo and others
1990; Hellström and others 2010). In particular, it affects zinc
homeostasis and may change the bioavailability of other essential
minerals (Pariza and others 2000). However, cassava mash fermen-
tation significantly decreases phytate content. Microbial species
such as Saccharomyces cerevisiae, Issatchenkia orientalis, Hanseniaspora
guilliermondii, Lactobacillus pentosus, and Rhizopus oryzae are effec-
tive in reducing the phytate content of cassava (Oboh and Elusiyan
2007; Montagnac and others 2009; Hellström and others 2010).

C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1033
Table 1–Some characteristics of the native and sour starch of Colombian
cassava.
Cadena and others (2006) Villada and others (2011)
Native starch Sour starch Native starch Sour starch
R.H. (%) 12.10 10.73 8.5 7.9
Lipids (%) 0.27 0.33 0.31 0.22
Ash (%) 0.42 0.37 0.15 0.15
Fiber (%) 0.45 0.61 0.55 0.55
Proteins (%) 0.84 0.98 0.60 0.62
Lactic acid (%) 0.11 0.72 0.11 0.72
pH 5.52 3.85 5.9 3.3
R.H., relative humidity.
This microbial activity is crucial for undernutrition control in in-
fants and adults, since “almidón agrio” serves as a staple food in
many local communities.
As seen in Table 1, after fermentation the pH of cassava starch
decreases below 4.0, with variations depending either on the fer-
mentation type or on manufacturing conditions. The process is
characterized by an increase of both lactic acid and protein con-
tent, due to microbial biomass. The microbiota present in the
fermenting medium converts starch and sugars into organic acids
(particularly acetic, propionic, succinic, and valeric acids), which
impart the characteristic odor and taste to the different fermented
products (Rincón-Suárez and Villamil-Novoa 2005). Although
lactic acid is one of the common acids reported in almost all types
of fermentation, many short-chain and long-chain fatty acids, es-
ters, and aldehydes could be detected (Moorthy 1998). From the
technological point of view, it is important to underline that after
fermentation sour starch is sun-dried to obtain a stable product
with 10% to 25% moisture content (Brabet and Dufour 1996).
Upon completion of the drying process, the starch in the form of
dough is ground and sifted through sieves of pore size between
100 and 120 US mesh, to form a fine powder. Lactic acidification
together with sufficient UV energy resulted in partial depoly-
merization of the cassava starch molecules, which provided small
linear fragments and facilitated formation of radicals that will help
cross-linking of the remaining starch molecules, due to their high
activity, forming a 3-dimensional network that results in the un-
usual baking expansion properties of fermented sour starch during
baking (Dufour 1995; Vatanasuchart and others 2005). Moreover,
after sun-drying, linamarase activity is higher, with a degradation
of 60% of the cyanogen content (Gómez and Valdivieso 1984).
It has been shown that sweet, sour, and acid-treated starches
are different in molecular weight and in surface appearance under
scanning electron microscopy. In fact, while native starch gran-
ules have a smooth and homogeneous surface, fermented starch
granules are partially broken and the surface is rougher (Putri and
others 2011), due to the action of microbial metabolites during
fermentation. Although sour starch gelatinization properties are
not much affected by fermentation, the physical characteristics of
the starch granules can modify the thermo-mechanical properties
of the dough, with noticeable effects on the baking properties
(Mestres and Rouau 1997; Putri and others 2011). In the Colom-
bian baking industry, this starch is sought for the manufacture of
pandebono, pandeyuca, and snacks, due to its typical flavor and
texture (Montoya-Henao 2007).
Maize-Derived Products
The main food contributors to daily diet in Latin American
countries are represented by cereals. Although the effects of glob-
alization and urbanization have influenced dietary patterns and
lifestyle, maize is still widely consumed (Bermudez and Tucker
Colombian fermented foods and beverages . . .
2003). Maize is the most widely consumed cereal in Colombia
and is an excellent source of metabolizable energy, while the
protein content is both quantitatively and qualitatively poor. In
particular, the content in tryptophan and lysine is low. Moreover,
maize contains antinutritional factors such as phytates, condensed
tannins, α-amylase, and trypsin inhibitors as well as lectins (Ejigui
and others 2005). In particular, phytate is the major storage form
of phosphorus in mature grains and legumes (Kumar and others
2010), and only animals possessing intestinal phytases or microbial
populations able to degrade it can utilize phosphorus in this form
(Holm and others 2002); therefore, the phytate–mineral complex
is not hydrolyzable in the human gut (Sandberg and Andersson
1988). As large amounts of iron and zinc are required during
early life due to accelerated growth (Dallman 1992), the inter-
actions between phytate and minerals have important nutritional
implications.
To improve storage possibilities and increase product value, dif-
ferent traditional processes based on spontaneous fermentations
have been developed over time. Fermentation boosts the nutri-
tional value of maize-derived products by increasing the content
of nutrients that are deficient in maize, such as vitamin A, vitamin
B12, and the amino acids arginine and methionine (Steinkraus
1997; Chelule and others 2010). Fermentation has been ascribed
as a potential way to reduce the risk of mineral deficiency among
populations, especially in developing countries where unrefined
cereals and/or pulses are highly consumed (Kumar and others
2010).
Three principal fermented maize-based products are consumed
in Colombia: chicha, champús, and masa agria. In spite of the dif-
ferent manufacturing procedures, a stable co-metabolism between
LAB and yeasts exists in the fermentation of maize products, as in
many cereal fermented products.
Chicha
Chicha is a traditional alcoholic beverage produced in Colom-
bia and other South American countries such as Ecuador, Peru,
and Bolivia. Since pre-Hispanic times, beer or chicha made pri-
marily from maize, but also from other grains or fruits, has been
a source of refreshment and nutrition, as well as a key element
in social, political, and ritual exchanges (Hayashida 2008; Ramos
2011). Moreover, this drink was used during celebrations in the
planting season to predict harvest success. Today, its use is com-
mon among Indians and peasants in many regions, who use
it to quench thirst and prepare it with corn, its original base,
or other products such as cassava (manioc) or fresh fruit like
pineapple.
Chicha is still consumed in many areas of Colombia on holidays
and as a ceremonial beverage for the Indian population. The main
festivities of the community, when Chicha is consumed, are wed-
dings and great “mingas,” which are community work occasions
aimed at improving the village infrastructures that usually culmi-
nate with dancing (Nullvalue 2003; Mincanquer-Cuatı́n 2007).
Chicha manufacturing is generally performed as a social event
by groups of old women, sometimes with the help of young
girls, though the contexts, meanings, and technologies of brewing
have undergone challenges and changes throughout time (Ramos
2011). This beverage has an alcohol content of 2% to 12%, v/v.
Although new techniques are available for chicha manufacturing,
the old traditional process still exists in some Indian populations.
As reported by Lorence-Quiñones and others (1999), in the
manufacturing process (Figure 2), corn grains are ground using
a mortar to produce a corn meal that is slightly moistened with
1034 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
water and rolled into a ball of appropriate size. Then the balls
are subjected to a prefermentation process that is an essential step
in the ancestral chicha; in this phase, starch is hydrolyzed by either
amylases generated during the malting (germination) of maize ker-
nels or by the chewing/salivation process, which utilizes salivary
amylase (diastase) for the conversion of starch to fermentable sug-
ars (Escobar and others 1993). The pot is then filled with water
and boiled for 2 or 3 h; after cooling, the product is pressed and
filtered, and the filtrate thus obtained is allowed to ferment for
2 or 6 d, depending on temperature. Before fermentation, cane
molasses may be added to increase sweetness and alcohol content.
The beverage is ready for consumption when the sweetness disap-
pears and the taste becomes semisharp. Steinkraus (1997) reported
that chicha is also rich in B vitamins, with a doubled riboflavine
concentration, while thiamine and niacin remain fairly constant.
From the microbiological point of view, chicha fermentation
is a spontaneous process carried out by natural microflora at
room temperature, and particularly by yeasts. The role of yeasts in
Colombian chicha fermentation needs additional research, to eval-
uate their possible impact on starch degradation, aroma, and free
amino acid production. Different species of yeasts, bacteria, and
molds are present in Colombian chicha. Steinkraus (1997) reported
that S. cerevisiae, S. pastorianus, Mycoderma vini, Oidium lactis, and
Monilia candida as well as bacteria of the genera Leuconostoc, Lac-
tobacillus, Acetobacter, and various molds including Aspergillus and
Penicillium are present and presumably active. The major function
of Leuconostoc and Lactobacillus species is to reduce pH (3.5 to 4.6)
by means of amylolytic enzymes. Some yeasts also contribute to
the degradation of starch, which cannot be carried out by LAB,
and produce carbon dioxide that plays a significant role in effer-
vescence. Moreover, yeasts produce other volatile compounds that
contribute to the sensory attributes of chicha.
The microbiota involved in Colombian chicha can be different
depending on environment, fermentation vessels, as well as other
factors such as type of prefermention process. Recently, the yeast
population in chicha at the end of fermentation has been isolated
and identified (Cuervo-Mulet 2013, unpublished data). The iden-
tification based on the sequencing of 5.8-ITS, rDNA, and D1/D2
domains of the 26S rDNA, suggested that ancient chicha made with
the salivation process, harbored a wider variety of species that can
be divided in 2 main categories: (1) oxidative or weakly fermen-
tative yeasts such as Candida spp. (the most frequent genus), Pichia
spp., Hanseniaspora uvarum, and Issatchenkia spp., which might in-
fluence the chicha aroma with the production of esters, aldehydes,
and ketons; and (2) strongly fermentative yeasts such as Wicker-
hamomyces anomalus (formerly Pichia anomala) and S. cerevisiae that
contribute largely to ethanol and carbon dioxide production, as
well as to the flavor and the preservation of the final product. Seven
different Candida species were identified (Table 2): C. oleophila, C.
spandovensis, C. parapsilosis, C. sergipensis, C. ethanolica, C. pomicola,
and C. railenensis. The genus Candida is an extremely heteroge-
nous group of yeasts, which is commonly associated with plants,
rotting vegetation, insects that feed on plants, or different foods
and beverages (Laitila and others 2006). While the presence of
human-associated species such as C. parapsilosis is the possible evi-
dence of human saliva used to hydrolyze corn starch, other species
derive from different flavoring substrates such as fruits. In par-
ticular, C. oleophila is widely distributed on fruits (Glushakova
and others 2007) and produces lytic enzymes such as 1,3-β-
glucanase, chitinase, and protease (Bar-Shimon and others 2004).
Moreover, C. sergipensis that produces high percentages of alcohol
in grape must (de Melo and others 2007), and its sister species

C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .

Maize kernels
Dry grinding Soakening (12-18 hours)

Moistening with water

Draining

Rolled in balls
Germination in dark conditions
(environmental temperature for 3-12 days)
Chewing/salivation
Water
Sun driyng Boiling (3-7 hours)
Water
Heating in pots (about Cooling

Mixing thoroughly (1 hour) Filtering with a cloth

Sugar cane molasse
Cooling/decanting
Fermentation (2-6 days at
Upper layer Botton layer
Traditional chicha
Heating/concentration

Cooling

Fermentation (2-6 days at

Ancestral chicha

Figure 2–Process to obtain Colombian ancestral and traditional chicha.

Table 2–Yeast species in Colombian chicha made with 2 different prefer- a certain extent (De Vuyst and others 2014); these characteristics
mentation treatments. might be considered as an advantage for these species. It has been
With salivation Without salivation reported that the natural mixture of organisms found in chicha has
S. cerevisiae S. cerevisiae
a greater ability to utilize starches, dextrins, and sugars than pure
Candida oleophila Hanseniaspora opuntiae cultures of S. cerevisiae (Steinkraus 1997).
Candida spandovensis Hanseniaspora uvarum Although traditional chicha is made with maize, other cereals
Candida parapsilosis Kodamaea ohmeri
Candida sergipensis Lodderomyces elongisporus
(rice), fruits (pineapple), and roots (cassava and “arracacha” [Ar-
C. ethanolica Pichia guilliermondii racacia xanthorrhiza]) are also used to produce homemade chicha.
Candida pomicola Metschnikowia koreensis López-Arboleda and others (2010) isolated and identified yeast
Candida parapsilosis Wicherhamomyces anomalus
Candida railenensis
associated with corn, pineapple, and arracacha made into chicha.
Hanseniaspora uvarum They observed that S. cerevisiae, Pichia guilliermondii, and Can-
Kazachstania exigua dida tropicalis were the most abundant species in the 3 types of
Issatchenckia sp.
Pichia kluyveri chicha. Moreover the fermentation of these 3 types was char-
Wicherhamomyces anomalus acterized by the presence of different yeast species: for exam-
Wickerhamomyces pijperi ple, in pineapple chicha, Aureobasidium pullulans was present at
Cuervo Mullet (2013, unpublished data). the beginning of the fermentation and Kluyveromyces marxianus,
Candida spp. and Pichia spp., during the vigorous phase. In the
arracacha-type Hanseniapora uvarum, and P. kluyveri, were present
C. spandovensis has been associated with frozen fruit pulps in all 3 phases of fermentation and Kazachstania martiniae, as well
(Trindade and others 2002). On the other hand, Candida raile- as K. exigua, during the vigorous phase; in addition, in maize-
nensis is a typical endophytic yeast of starch-containing storage type the presence of Rhodotorula glutinis, Candida maltosa, Pichia
tissues of seeds (Isaeva and others 2010). The non fermenting fermentans, and Torulaspora delbrueckii characterized the vigorous
maltose species Kazachstania exigua, formerly Saccharomyces exiguus, phase.
anamorph Candida (Torulopsis) holmii, and W. anomalus have been The above-mentioned species suggest that the manufacturing
linked with sourdough fermentation (De Vuyst and others 2014). of chicha leads to a selection of a well-defined microbial commu-
In samples obtained without salivation, a minor variety of species nity, based on the association between maltose-fermenting lactic
was found, with S. cerevisiae as the preponderant species, followed bacteria and yeasts.
by W. anomalus. Both species strongly assimilate maltose and su- Although homemade manufacturing of maize Chicha has been
crose, and are tolerant to low pH and high osmotic pressure to forbidden by Colombian legislation since 1948, in some cities


C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1035
Colombian fermented foods and beverages . . .

this production continues in the “chicherı́as,” which are basically medium such as champús, by synthesizing both nutrients (amino
the equivalent of a local beer joint, where people of mixed-race acids and vitamins) and flavor volatile compounds.
heritage get together to socialize. The particular traits of the yeast isolated from champús have been
evidenced in a research conducted by Chaves-López and others
(2009), in which it became evident that S. cerevisiae strains isolated
Champús from this beverage can be an important source for new tropical
Champús is a low-alcoholic (2.5% to 4.2%) beverage with a yeast biotypes with potential winemaking applications, producing
sweet/sour taste obtained by a natural fermentation of heat-treated a wide range of aroma compounds, such as ethyl hexanoate, 2-
maize. As reported by Osorio-Cadavid and others (2008), to pro- phenlyethanol, 2- phenyl ethyl acetate, and geraniol.
duce champús, 2 steps are involved (Figure 3). In the 1st step, after
washing and peeling, kernels are boiled for 2 to 3 h, and after cool- Masa Agria
ing (2nd step), fruits such as pineapple or “lulo” (Solanum quitoense Masa agria can be either home made or prepared on a small
Lam.) together with “panela” (a natural sweetener obtained after commercial scale, according to traditional procedures (Figure 3).
drying the unrefined whole sugar cane juice) syrup and spices such The conversion of maize into “masa agria” involves a process in
as clove, cinnamon, and orange tree leaves are added. Then, the which preferably yellow maize is peeled until the pericarp is re-
beverage is left to ferment at 12 to 15 °C for about 12 to 24 h moved. The kernels are placed in a container, covered with water,
(3rd step). and buried for 4 d in a hot place (35 to 40 ° C); during this period,
The popularity of this drink is due to its pleasant taste and a spontaneous fermentation takes place. Successively, the maize is
flavor, in particular ethanol, methyl butanoate, 2-phenylethyl ac- washed, milled, and a dough is formed and allowed to stand for 3
etate, ethyl acetate, isoamyl acetate, 2-hexenal, and linanool have or 5 d, during which a dehydration occurs and the aw goes down
been identified as the principal aromatic volatile compounds. to near 0.91 depending of the producers. After fermentation, the
These volatiles are derived from the fruits and also from the yeast pH is reduced from 6.6 to 4.4 to 3.8.
metabolism. Since a mixture of microorganisms carries out fermentation, the
The nutritional properties of the maize in champús are increased quality and the sensory characteristics of the masa agria can be vari-
with the addition of fruits and sugar cane. In particular, there able and are related to fermentation time, as well as to the place of
is an increase in vitamins C and A, as well as minerals such as production. In fact, in this ecosystem different enzymes (amylases,
calcium, iron, phosphorus, and potassium that are derived from proteases, phytases, and lipases) are active and lead to products
panela (Osorio-Cadavid and others 2008). Moreover, during the with desirable traits such as enhanced taste, aroma, texture, and
fermentation, the nutritional value of maize is enhanced because increased stability at room temperature.
some antinutritional factors such as phitic acid and tannins are Table 3 reports some microbiological and physicochemical char-
reduced (Chitra and others 1996; Onyango and others 2004). acteristics of masa agria obtained from 10 different artisanal pro-
Although the majority of the microorganisms associated with ducers of the Valle del Cauca region (Chaves-López and Delgado-
corn kernels are destroyed by the heat treatment during processing, Ospina 2013, unpublished data). Masa agria samples contain high
fruits act as an inoculum of yeasts and LAB in champús. While yeasts levels of soluble starch and low concentrations of mono- or dis-
are present at levels of 105 to 107 log CFU/mL, LAB from 103 accharides as glucose, fructose, sucrose, and maltose. Moreover,
to 105 log CFU/mL. Osorio-Cadavid and others (2008) reported fermentation products that are responsible for the sour taste, such
the following yeast species isolated from champús: S. cerevisiae, I. as lactic acid (the major fermentation product) and acetic acid,
orientalis (Pichia kudriavzevii), Pichia fermentans, Pichia kluyveri var. were also detected. It is to underline that the monosaccharides
kluyveri, Zygosaccharomyces fermentati, Torulospora delbrueckii, Galac- in maize are between 4.5 and 14 mg/g, (Dı́az de León-Sánchez
tomyces geotrichum, and Hanseniaspora spp. The first 4 species were and others 2006) and a great amount of them is lost during starch
the most frequently isolated. washing. On the other hand, LAB are the predominant micro-
In starchy substrates such as cereal grains, it is necessary that bial groups in this product, followed by yeasts. The coexistence
amylases convert some of the starch to fermentable sugars that of LAB and yeasts is unavoidable, LAB usually secrete enzymes to
are rapidly converted to ethanol. The yeasts mentioned above are hydrolyze either polysaccharides or other high molecular weight
not able to ferment maltose, thus it is probable that they ferment compounds (Furukawa and others 2013). Also some yeasts pos-
sugars deriving from molasses and fruit. As evidenced by the same sess active amylases, increase the levels of B group vitamins and
authors, the volatile aroma compounds pattern (determined by free amino acids (Soni and Sandhu 1991), produce gas and other
SPME, solid-phase microextraction), produced by champús yeasts volatile compounds that give a contribution to sensory qualities
indicates that this beverage harbored 2 groups of fermenting yeasts. (Aidoo and others 2006).
The 1st group was characterized by high-fermentative species such LAB communities in the masa agria samples are composed
as S. cerevisiae and P. fermentans that played a vital role through mainly of Lactobacillus species, in particular L. plantarum and L. fer-
the production of ethanol and low quantities of esters and other mentum (Vanegas-Gamboa and others 2009). By using a polyphasic
volatile compounds. The 2nd group was formed by yeasts with approach to study the ecology of Pozol (a traditional fermented
a scarce fermentative activity and a strong capability to produce maize dough from Mexico and Guatemala), Ben Omar and oth-
esters, such as P. kluyveri var. kluyveri that produced high quantities ers (2000) suggested that during maize dough fermentation, mi-
of 2-phenylethyl acetate in a champús model systems (containing croorganisms act in proper succession in which 3 phases can be
5% of panela syrup, 3% boiled corn, 3% filtered lulo and pineapple evidenced. The first phase (0 to 24 h) started with a large initial
juice in water), with effects on the quality and aromatic profile of epiphytic aerobic microbial community (Enterococcus, Streptococcus,
champús. and Exiguobacterium species) that consumed monosaccharides and
The growth of the oxidative G. geotrichum, which contributes to available oxygen and favored the presence of amylolitic hetero-
aroma development and plays an important role in the production fermentative and homofermentative LAB. The 2nd phase (24 to
of some dairy products, might have a similar role on a complex 48 h) was marked by the presence of heterofermentative LAB

1036 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014 
C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .

Yellow Maize kernels

Cleaning-washing

Peelling

Boiling in water 2-3 hours Covering with water

Cooling (environmental temperature) Fermentation 3-5 days

(environmental
Addition of pulp fruit
Draining
Sugar cane molasse,
cinnamon, cloves,
Washing/draining
orange tree leaves

Grinding
Fermentation/storage

Dough formation/Drying

Masa Agria

Figure 3–Flow diagram for the production of traditional Colombian champús and masa agria.

Table 3–Microbiological and physico-chemical characteristics of masa Table 4–Antinutritional factors in unfermented and fermented maize
agria obtained from 10 different artisanal producers of the Valle del Cauca grains.
region.
Parameters Unfermented Fermented
Characteristic Concentration Phytates (g/100 g) 2.30 ± 0.07 0.84 ± 0.08
Lactic acid bacteria (Log CFU/g) 8.8 ± 0.4 Oxalates (g/100 g) 2.32 ± 0.01 0.34 ± 0.07
Yeast (Log CFU/g) 6.8 ± 0.8 Tannins (g/100 g) 2.62 ± 0.01 0.42 ± 0.04
Mesophilic aerobic bacteria (Log CFU/g) 6.5 ± 0.5 Adapted from Gernah and others (2010).
aw 0.94 ± 0.03
pH 3.85 ± 0.21
Lactic acid (g/L) 0.387 ± 0.035
Acetic acid (g/L) 0.018 ± 0.010
Glucose (g/L) 0.525 ± 0.879
Maltose (g/L) 0.008 ± 0.014 potential in the enhancement nutritional characteristics of many
Fructose (g/L) 0.005 ± 0.009 such foods and ingredients as well as health effects (Poutanen and
Chaves-López and Delgado-Ospina (2013, unpublished data). others 2009). In addition, maize fermentation modulates levels
and bioaccessibility of bioactive compounds and improves mineral
bioavailability. In this respect, Gernah and others (2010) reported
that produced high levels of ethanol and lactate, in particular Leu- a significant reduction of phytates, tannins, and oxalates during
conostoc species and L. fermentum. The latter seemed to be a key maize fermentation (Table 4). In addition, Poutanen and others
organism for maize fermentation, by making the large amounts of (2009) suggested that new bioactive compounds, such as prebiotic
starch available to the overall community. The 3rd phase (48 to oligosaccharides or other metabolites, may also be formed during
96 h) was characterized by a reduction of heterofermentative LAB cereal fermentation. These characteristics could be an advantage
and an increase of heterofermentative LAB with the presence of for people who do not have access to a variety of nutritional foods
L. plantarum, L. delbrueckii, and a Bifidobacterium species. or fail to eat a nutritionally balanced diet on a regular basis.
Recently, Betancour-Botero and others (2013) reported a strain During maize fermentation, the role of some microorganisms
of Lactobacillus plantarum (CPQBA 087–11 DRM) in masa agria in aflatoxin detoxification has been reported. Chelule and oth-
that possessed high amylolitic activity as well as high inhibitory ers (2010) studied the reduction of the mycotoxins aflatoxin B1
potential against pathogenic bacteria and molds. Fermentation (AFB1) and zearalenone (ZEA) in maize inoculated with yeasts,
also affects the dough hardness of masa agria in fact, Vanegas- and reported undetectable levels in homemade African amahewu.
Gamboa and others (2009) observed great differences in swelling Similar results had been previously reported, since a higher reduc-
power, solubility, water binding capacity, and pasting properties of tion of ZEA and AFB1 was observed in fermented maize products
the fermented flours. Moreover, as mentioned above, fermenta- than in unfermented products (Mokoena and others 2005). In
tion of cereals increases protein quality, in particular the level of the last several decades, mycotoxin contents in Colombia have
available lysine (Katongole 2008) and, therefore, has a significant been increasing, especially for the maize grains (Scussel 2004;


C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1037
Colombian fermented foods and beverages . . .

Selection of the palm and cutting Sugar cane

Cleaning and horizontally placing the steam

pressing bagasse

Boring a box-shaped cavity

Sugar cane juice
Sap collection( every 12 hours )
filtering
Fermentation
(12 hours ambiental
Fermentation
(environmental
Filtering

Bottling Storage

Guarapo
Palm wine
Figure 5–Flow diagram to produce Colombian guarapo.
Figure 4–Traditional process to obtain vino de palma.

Castilla–Pinedo and others 2011; Morris Navarro 2011), but data and bacteria are present in the sap, ferment part of the avail-
on derived fermented products are still lacking. able carbohydrates, and carry out a concurrent alcoholic, lactic
acid, and acetic acid fermentation (Bassir 1962; Amoa-Awua and
Palm Wine others 2007). While yeasts (in particular S. cerevisiae that is invari-
Data from chronicles of the 16th century narrate that several ably present) and LAB are important during fermentation because
Colombian Indian tribes produced a fermented drink from the sap they produce ethanol, carbon dioxide, and other volatile com-
of the palm tree, and particularly from the Acrocomia and Attalea pounds, the acetic acid bacteria can be responsible for a vinegary
genera (Patiño 1990). Nowadays, its production is confined to taste (Amoa-Awua and others 2007). In taberna, a traditional palm
only a few regions, and even today, on the Caribbean lowlands, sap (Acrocomia aculeate) beverage from the southern part of Mex-
people believe that palm wine “strengthens blood” and acts as an ico, Zymomonas mobilis represented an important proportion of
aphrodisiac. the bacterial community (60% to 80%). This species performs a
Atalea butyraceae, Scheelea magdalenica, and Ceroxylon alpinum are highly productive ethanolic fermentation, producing an equimo-
the most used species to produce “palm wine.” As palm sap extrac- lar mixture of ethanol and CO2 (Alcántara-Hernandez and others
tion involves cutting the palm, leading to depletion of native trees, 2010).
various nondestructively harvest techniques have been developed, Colombian palm wine contains 83 mg/L of ascorbic acid, and
but they have not been implemented yet (Bernal and others 2010). during fermentation an increase of thiamine and riboflavin (from
In the process (Figure 4), the palm is cut near the tip of the stipe, 25 μg to 150 μg/L and from 4 to 18 μg/L, respectively) has been
by felling the palm tree, and boring a box-shaped cavity (20 × observed (Steinkraus 2006).
30 × 20 cm) in the meristematic area, using a machete to cause
flow of the sap, which is collected every day in pumpkins and Guarapo
allowed to ferment (Pulgarı́n and Bernal 2004). An 8-m-tall palm Guarapo is the name given to sugarcane (Saccharum officinarum)
produces about 1 L of sap per day over a period of 20 to 30 d. juice, a refreshing drink that has been consumed in the Andean
The sap has a whitish, turbid appearance, contains 11.7% sucrose regions of Colombia since the 16th century and that could be
(Pulgarı́n and Bernal 2004), and is an excellent substrate for mi- fermented or not (Mora de Tovar 1989). In Guarapo manufactur-
crobial growth. Spontaneous fermentation starts soon after the ing, a mill called “trapice” is used to press sugarcane to obtain
sap is collected, and within 2 h the beverage can contain 3% a juice with a high content of the reducing sugars glucose and
to 4% ethanol. The production of palm wine is achieved under fructose (Patiño 1990). Once the juice is taken out of the cane, it
nonaseptic conditions, thus the microorganisms involved in its is filtered through a sieve and poured into a bowl, usually made of
fermentation are those naturally occurring, as well as those incor- clay, which contains a starter named “cunchos” or “supias” able to
porated during its collection, transport, and manipulation. This ferment the juice, after a few hours, before serving it in glasses for
cloudy whitish beverage has a sweet alcoholic taste and a very consumption (Serna-Isaza 1976). The steps to produce guarapo
short shelf-life. are schematically presented in Figure 5.
There are no reports regarding the fermentative microbiota of The microbial composition of “chunchos” has not been doc-
Colombian “palm wine.” However, studies on the microbiology umented in the scientific literature, but it has been reported that
of African “palm wine” have shown that the fermentation pro- the most common yeasts isolated from guarapo belong to the gen-
cess may already start in the palm where naturally occurring yeasts era Candida (pelliculosa, inconspicua, kefir, glabrata, lypolytica, and

1038 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014 
C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .
rugosa), Criptococcus (laurentii), and Rhodotorula (minuta) with a great
capability to degrade xylose (Vanegas and others 2003), at a load
of 106 log CFU/mL. Although the authors did not report the
time of guarapo fermentation, it can be assumed that the beverage
was in the early stage of fermentation. In fact, as in grape-must
fermentation, during juice-cane fermentation a succession of yeast
species takes place, with a high presence of non-Saccharomyces yeasts
during the first 4 d of fermentation. After that, Saccharomyces spp.
and other high ethanol-tolerant yeasts predominate (Pataro and
others 2000). During fermentation, yeast cells produce a broad
spectrum of volatile molecules, such higher alcohols, aldehydes,
organic acids, esters, organic sulfides, and carbonyl compounds.
In a study conducted by Olarte and others (2007) on 46 samples
of Guarapo, ethanol concentration was reported between 0.50%
and 6.94% and 41 samples contained acetaldehyde at variable con-
centrations. The most frequent LAB genera in sugarcane juice are
Leuconostoc, Lactobacillus, and Pediococcus (Cuervo-Mulet and oth-
ers 2010), which influence the beverage flavor by means of the
secondary compounds produced. In Brazilian fermented sugar-
cane, Gomes and others (2010) reported that L. plantarum and L.
casei were the prevalent LAB, but other species such as L. ferin-
toshensis, L. fermentum, L. jensenii, L. murinus, Lc. lactis, Enterococcus
spp., and Weissella were present after 7 d at levels from 105 to
108 CFU/mL.
The chemical composition of Guarapo also includes organic acid
salts, polysaccharides, proteins, minerals, and other compounds
(Larrahondo 1995). In particular, potassium is present in high
quantities, followed by phosphorus, calcium, sodium, magnesium,
sulfur, iron, aluminum, copper, zinc, calcium, and iron. In addition
to ethanol and water, fermented cane juice contains esters, higher
alcohols, acids, and other valuable and interesting compounds,
which are produced during fermentation. There is a concern re-
lated to its consumption in high quantities and for long periods, as
this beverage has been associated with the development of hepatic
cirrhosis positively be related to the presence of the ethanol.
Cacao
Theobroma cacao L. is a tree native to tropical rainforests, on this
continent extending from the Amazonian basin of South Amer-
ica to southern Mexico. According to some authors, the place of
origin of cacao trees was the Upper Amazon near the Colombian–
Ecuadorian border, on the eastern flanks of the Andes (Cheesman
1944; Schultes 1984; Motamayor and others 2002). It was brought
to Mesoamerica by early humans, and the use and domestication
of this crop may have started 4000 y ago (Powis and others 2011).
Ecological conditions vary greatly in Colombia, and the cacao-
growing regions are very scattered through its territory, and the
wide variety of microclimates around the country leads to co-
coa production with high variability in its chemical composition
(Carrillo and others 2014).
Although the use of cacao in Colombia is mainly to produce
chocolate, some Colombian tribes eat the pulp surrounding cacao
beans and also make an alcoholic beverage from it, and occasionally
vinegar (Patiño-Rodriguez 2002). Even today, Colombians like to
partake of a hot sweet chocolate beverage first thing in the morning
and late at night, especially in cold mountain climates.
Moreover, in the last few years cacao by-products such as bean
husk have been proposed to be used in the biocontrol of Bacillus
cereus and Streptococcus agalactiae (Cuéllar and Guerrero 2012) and
the mucilage to be used for the clarification of cane juice (Pérez
Echeverry 2004).

C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1039
Harvest of ripe pods
Storage of pods for 0-10 days
(environmental temperature)
Pod opening and wet bean removal
Fermentation (4-7 days)
Sun Drying artificial Drying
Storage
cacao
Figure 6–Traditional proccesing of cacao production.
Cacao beans contain a significant amount of fat (40% to 50%)
and polyphenols (about 12% to 18% of the dry weight of grain),
and particularly catechins or flavan-3-ols (37%), anthocyanins
(4%), and proanthocyanidins (58%), and also protein (13% to 16%)
and the methylxanthines theobromine and caffeine, which both
together account for about 3.2% of defatted unsweetened choco-
late composition (Ortiz de Bertorelli and others 2009; Tinoco and
Ospina 2010; Zapata Bustamante and others 2013).
The process to obtain cacao beans in Colombia is summarized
in Figure 6. After opening the cacao pods at the plantation, the
collected fresh cacao pulp-bean mass undergoes a spontaneous
fermentation for several days (2 to 7 d) depending on: (1) variety of
cacao plant, (2) climate, (3) local practices of fermentation which
include heaps, wooden fermentation boxes, canoes made of thick
tree trunks called “pozuelos,” barrels, or baskets, (4) frequency
of bean mixing or turning, (5) volume of cocoa to ferment, (6)
maturity and the sanitary condition of the beans (Schwan 1998;
Cubillos and others 2008; Ortiz de Bertorelli and others 2009;
Moreira and others 2013; Zapata Bustamante and others 2013).
Traditionally, in all types of fermentation the mass of fermenting
beans is usually covered with jute or sisal bags.
During fermentation, important changes take place, which are
essential for the development of the characteristic future cocoa and
chocolate flavors: (a) detachment of the mucilage that surrounds
the bean to facilitate preservation; (b) death of the embryo that
prevents germination; and (c) a chain of biochemical reactions
inside the beans, which generate a volume increase and a char-
acteristic color change (Barros 1981; Schwan and Wheals 2004).
These processes are crucial for the development of the sensory
quality of cocoa beans. Aroma and flavor profiles develop predom-
inantly during drying and fermentation but also the later roasting
impacts flavor via the Maillard reaction. In general, soil composi-
tion, climatic conditions, and primarily farming practices are other
Colombian fermented foods and beverages . . .
fundamental factors that ensure the special chocolate aroma and
flavor (Federacion Nacional de Cacaoteros Colombianos 2004).
It is well known that the microorganisms involved in cocoa
fermentation carry out their activity in a well-defined temporal
succession (Figure 7). The pulp of cacao beans has a high sugar
content, low pH (close to 3.5), and a limited oxygen concen-
tration. These conditions favor the growth of yeasts that degrade
pectin, ferment glucose and fructose with the consequent accumu-
lation of ethanol (5 to 60 mg/g), acids (especially acetic acid), and
secondary products (including, organic acid, aldehydes, ketones,
higher alcohols, esters) that together with glycosidase production
are likely to be significant and should affect the beans and chocolate
quality (Ardhana and Fleet 2003).
Yeast growth and activity are essential for cocoa fermenta-
tion and development of chocolate characteristics (Ho and others
2014). Fungal contribution to fermentation is restricted to the
first 36 h of fermentation, because the increasing temperature
and ethanol concentration of the bean mass act as limiting factors
(Ardhana and Fleet 2003). Fungi can hydrolyze the pulp, produce
acids, and off flavors, and alter the taste of the cocoa beans (Schwan
and Wheals 2004), and some mold species can also produce my-
cotoxins (Copetti and others 2011).
Yeasts create anaerobic conditions that allow the growth of LAB,
which ferment sugars, produce lactic acid, and assimilate citric
acid. The role of LAB and whether or not they are essential to the
process is not clear (Ho and others 2014). Greater aeration of the
mass, due to the disappearance of the mucilage and to the manual
practices, allow acetic acid bacteria (AAB) to grow and metab-
olize the substrate (Barel 1997), mainly by oxidation of ethanol
produced by yeasts into acetic acid, and further oxidation of the
latter to carbon dioxide and water (Schwan and Wheals 2004).
Oxidation is a highly exothermic reaction (496 kJ by molecule of
ethanol converted into acetic acid), which raises the temperature
to 50 °C (Lagunes-Gálvez and others 2007). It is believed that
the conditions provoked by AAB are the cause of diffusion and
hydrolysis of proteins, and this suggests that AAB might play a key
role in the formation of flavor precursors (Saltini and others 2013).
The particular temperature conditions, in combination with
increased pH and aeration, favor the growth of aerobic spore-
forming Bacillus spp. (Thompson and others 2007). A study con-
ducted with 2 clones grown in Colombia, ICS 60 and TSH 565,
highlighted that after 60 h of fermentation, temperature increased
up to 47 °C and remained almost constant up to 108 h to finally
decrease down to 30 °C (Pineda and others 2012). The role of the
Bacillus group in cocoa fermentation has not been fully clarified,
but Nielsen and others (2007) suggested that they may play a big-
ger role in box fermentation than in heap fermentation. Moreover,
Ouattara and others (2008) suggested that pulp degradation dur-
ing cocoa fermentation is due to the action of enzymes produced
either by yeasts and Bacillus species or strains.
The drying process of cacao reduces acidity and astringency, and
it decreases volatile compounds (Afoakwa and others 2008). This
process is performed by sunlight or artificially under controlled
temperature, which should not exceed 60 °C. Although the great
part of Colombian small farmers uses sunlight for drying, the
artificial drying predominates in large-scale operations (Espinal
and others 2005). As pointed out in recent publications, drying is
the most important unit operation that affects polyphenols such
as flavonoids and their antioxidant activity (Di Mattia and others
2013).
The linkage between the consumption of cacao-derived prod-
ucts and health goes back many years. In fact, as pointed out
1040 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
by Dillinger and others (2000), in a complete review of the in-
digenous, colonial era and, early modern period uses of cocoa
or chocolate, their use for medicinal purposes was already docu-
mented by the Florentine Codex (1590), which describes the life
and culture of Aztecs. In Europe and New Spain from the 16th to
the early 20th century, more than 100 medicinal uses were known
for cocoa and/or chocolate.
The beneficial effects on human health of some functional ca-
cao constituents have been reported in the scientific literature,
particularly in relationship with the high content of monomeric
(epicatechin and catechin) and oligomeric (procyanidins) flavanols
(Rusconi and Conti 2010). Recently, some epidemiological stud-
ies have established an inverse correlation between flavonoid intake
and the appearance of chronic diseases, such as cardiovascular and
cerebrovascular diseases, cancer, and other disorders including di-
abetes and rheumatoid arthritis (Wollgast and Anklam 2000; Oth-
man and others 2007). The main flavan-3-ol compounds present in
cacao are the monomers catechin and epicatechin, and the dimer
procyanidin B2 (Lamuela-Raventós and others 2005). Although,
it can be suggested that the daily intake of flavonoids from mixed
food sources, together with the intake of small amounts polyphe-
nols from cocoa or chocolate (flavanols and procyanidins), could
improve individual health status including potential efficient can-
cer prevention with minimal toxicity (Martin and others 2013).
However, cancer preventive efficacy in humans remains to be de-
cisively demonstrated.
In a recent study on cacao beans from 11 different cacao-
growing areas of Colombia, a proportional relationship was
pointed out between polyphenol content and changes in the al-
titude of plant crops. In particular, the authors suggested that the
lower is the altitude, the more polyphenols, flavan-3-ols, and epi-
catechin are produced by the cacao plant (Carrillo and others
2014).
Although fermentation and drying are key points for the devel-
opment of the typical cacao flavor, the same steps can harbor the
risk of mycotoxin formation, in particular ochatoxin A and afla-
toxins. Moreover, the growth of xerophilic fungi during storage
can be considered a spoilage indicator at this stage (Copetti and
others 2011). In the last several years, in Colombia, an increas-
ing effort in the implementation of traceability systems has been
made to enhance product quality, maintain sensory acceptability,
preserve bioactive compounds, and promote food safety.
Milk-Derived Products
In Colombia, the origins of dairy products date back to the
end of the 16th century, when the Spanish colonizers imported
cattle and transmitted cheese manufacturing techniques to the
native population. Today’s fermented milk products can be either
industrial or homemade, and their manufacturing is still a complex
procedure, which combines science and tradition.
Kumis
Kumis is fermented cow milk, widely consumed in rural and ur-
ban areas in the Colombian southwest. A similar beverage (koumiss)
is produced in Central Asia but there it is mainly made from un-
pasteurized fresh mares’ milk, and it is considered not only as an
essential food, but also as a medicinal remedy (Ishii and Konagaya
2002).
As reported by Chaves-López and others (2011), to produce
traditional kumis (Figure 8), raw whole milk is left fermenting for
2 or 3 d at room temperature. After fermentation, the pH ranges
between 3.9 and 4.5 and the alcohol content between 1% and 2%.

C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .

9
8
7

Log cfu/g of bean

6
5
4
3
2
1
0
0 24 36 48 72 96 120 144
Time (hours)
Moulds Yeast Lactic acid bacteria Acetic acid bacteria Bacillus spp

Figure 7–Microbial temporal succession during cacao fermentation (adapted from Ardhana and Fleet 2003).

Whole raw milk

Salt addition (2-3%) Fermentation

days )

Fermentation
days ) Curd breaking

Sugar cane and

Curd breaking cinnamon
Homogenization

Separation of lactosuero
Storage (4-6 days

Salt addition (2-3%)

Kumis

Homogenization

Storage (6-8 days

Lactosuero

Figure 8–Flow diagram for the production of kumis and suero costeño.

This creamy and sparkling beverage is stored under refrigeration,
with sugar and cinnamon before serving it must be consumed
within 3 d.
Colombian traditional kumis has only been sparsely character-
ized microbiologically and biochemically. During manufacturing,
the main chemical changes through milk fermentation are lactic
acid production from lactose, and milk protein hydrolysis. Table 5
highlights some of the most important chemical characteristics of
the traditional Colombian kumis. The production of lactic and
acetic acids that contribute to the inhibition of pathogenic bacte-
ria is due to an intense metabolic activity of the microbiota. The
antimicrobial activity of Colombian kumis has not been docu-
mented yet, although an anti-Listeria bacteriocin produced by L.
plantarum LB-B1 isolated from Chinese koumiss has been charac-
terized (Xie and others 2011).
The Colombian kumis microbiota is composed of distinct mi-
crobial groups, with a prevalence of LAB and yeasts, ranging from
107 to 109 log CFU/mL and from 106 to 108 log CFU/mL,
respectively; Enterobacteriaceae were also found, although at low
numbers (log 102 to 103 CFU/mL) (Chaves-López and others
2012). LAB and yeasts act in synergy to give the texture and taste
of kumis. Not only do LAB produce lactic acid and hydrogen


C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1041
Colombian fermented foods and beverages . . .
Table 5–Chemical characteristics of traditional Colombian kumis.
Compound Concentration
Ethanol (g/100 g) 2.51 ± 0.53
Lactic acid (g/100 g) 1.14 ± 0.46
Acetic acid (g/100 g) 0.05 ± 0.01
Citric acid (g/100 g) 0.53 ± 0.06
Propionic acid (mg/100 g) 0.0044 ± 0.0012
Butyric acid (mg/100 g) 0.0089 ± 0.0017
Total peptides content (μg/mL) 252.23 ± 31.22
Total amino acid content (mM leucin/mL) 2.08 ± 0.12
Adapted from Rossi (2010).
peroxide, which contribute to reduce the number of some con-
taminant bacteria, but they also release galactose that favors the
growth of non–lactose-fermenting yeasts. Moreover, LAB pos-
sess a very complex proteolytic system that releases peptides and
amino acids, leading to the particular aromatic profile and texture
of kumis. On the other hand, yeasts produce CO2 that gives the
particular effervescence, contribute to product aroma by means
of lypolitic and proteolytic activities, and enhance LAB growth
through amino acids and vitamin production.
As shown in Table 6, different species of LAB and yeasts were
isolated from Colombian kumis and Asian koumiss. The differ-
ences are related to: (1) the environmental conditions during
milk fermentation which select the species; (2) milk composition,
mainly fat, protein, and lactose contents; (3) different procedures
of the process; and (4) changes during continuous propagation
that enable stable associations between some yeasts and bacterial
species.
During kumis production, proteolysis in the milk leads to the
production of peptides that have been reported to have differ-
ent biological activities, some of which have been associated with
health-promoting properties (Vinderola and others 2009). The
number, the potency, and the importance of bioactive compounds
in fermented milk products are probably greater than previously
thought (Ebringer and others 2008). They include certain vita-
mins, specific proteins, bioactive peptides, oligosaccharides, or-
ganic (including fatty) acids. Some of them are normal milk com-
ponents, others emerge during fermentation or human digestive
processes. Although Asian koumiss has some beneficial influence
on enhancing immunity, treating tuberculosis, and cardiovascu-
lar disease (Chen and others 2010; Wang and others 2012), and
in China the “koumiss therapy method” is used for the treat-
ment of hepatitis, chronic ulcers, and tuberculosis (Liu and oth-
ers 2011), the “healthy” properties of Colombian kumis are not
claimed yet. However, peptides with up to 65% inhibitory activity
against angiotensin converting enzyme (ACE) have been detected
in vitro (Chaves-López and others 2011). ACE plays a major role
in the regulation of blood pressure. In fact, within the renin–
angiotensin system, ACE catalyzes the conversion of angiotensin I
to angiotensin II, a potent vasoconstrictor (Riordan 2003), which
therefore also increases blood pressure.
Researchers have recognized the importance of formulated
starter culture in order to produce milk with bioactive compounds.
In a recent study (Chaves-López and others 2014), cocultures of
selected microorganisms have been evaluated for the production
of fermented milk enriched with ACE inhibitory peptides. The
authors underlined the importance of choosing the strain com-
binations carefully, in order to obtain a high yield of ACE in-
hibitory activity without a bitter taste. In their study it was reported
that a co-culture of Pichia kudriavzevii, L. plantarum LAT3, and
Enterococcus faecalis, was the most promising culture, producing
1042 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
the most potent ACE-inhibitory peptides (IC50 = 30.63 ± 1.11
μg/mL) and giving a product without bitter taste. Moreover, this
attribute was maintained during refrigerated storage for 7 d.
On the other hand, it has recently been reported that fermen-
tation of whole milk by selected kumis organisms can increase the
levels of conjugated linoleic acid (CLA) (C18:2c9t11), with values
ranging from 9.17 ± 0.70 to 22.62 ± 3.85 mg/g fat (Osorio and
others 2011). The term “conjugated linoleic acid” (CLA) refers to
a mixture of geometric and positional isomers of octadecadienoic
acid with conjugated double bonds (Castro 2009). Linoleic acid
can be converted to CLA when a microbial or chemical reac-
tion shifts the double bonds to form alternating double and sin-
gle bonds, hence the term CLA (Pariza and others 2000). CLA
is considered to possess potential health benefits such as anticar-
cinogenic, antiatherogenic, antidiabetic, and antiadipogenic effects
(Rainer and Heiss 2004; Panghyová and others 2006), in particular,
the cis-9 trans-11 isomer, the most abundant CLA, is considered to
have anticarcinogenic properties (Ip and others 1995). The scien-
tific literature mentioned may provide evidence for the beneficial
effects of Colombian kumis, especially on cardiovascular health.
Moreover, Mazo and Arias (2006) evaluated the efficacy of kumis
in acute undernourished children, and they found a higher and
faster weight gain and a reduction of the frequency and duration
of episodes of diarrhea.
Although the production of the above-mentioned compounds
and other antimicrobial components during fermentation may
promote consumer health or improve kumis safety and stabil-
ity, risks associated with other fermenting and contaminating
pathogenic microorganisms need to be explored. In particular,
enterococci loads ranging from 4.2 to 8.3 log CFU/mL have
been reported in Colombian kumis (Chaves-López and others
2011). The presence of these microorganisms as a consistent part
of the kumis microbiota could be a concern, as enterococci are
among the most common nosocomial pathogens, and they have
been implicated as an important cause of endocarditis, bacteremia,
and infections of the urinary tract, central nervous system, intra-
abdominal and pelvic infections, as well as of multiple antibiotic
resistances (Endtz and others 1999; Serio and others 2007). In
this context, Chaves-López and others (2011), reported that 42
out of 72 strains of enterococci isolated from 13 different ku-
mis samples were free of virulence factors, and 33 isolates har-
bored at least 1 gene, with esp gene encoding for enterococcal
surface protein, as the most frequent. However, it is important
to highlight that vancomycin resistance of the strains was very
limited.
Another important health issue can be the production of
biogenic amines (BA), and in particular histamine and tyra-
mine. The presence of these compounds can be particularly
harmful for susceptible consumers, but it is often unavoidable
in fermented foods (Stratton and others 1991). In particular,
tyramine, 2-phenylethylamine, and histamine can cause distress,
mainly due to the effects on nervous and vascular systems, which
can be particularly severe in sensitive people or when the en-
zymes naturally involved in their detoxification (the amine ox-
idases) are inhibited as by certain medications (Lanciotti and
others 2007). Data reported from Colombian kumis revealed
very low values of total BA content, ranging from not de-
tectable to 15.31 mg/L, with ethylamine, putrescine, cadaver-
ine, and spermidine being the only amines detected (Chaves-
López and others 2011). Nevertheless, these levels are far below
the limits that are recommended by health authorities in many
countries.

C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .

Table 6–Principal lactic acid bacteria (LAB) and yeasts reported in from Colombian kumis and Asian koumiss.

Colombian kumis Asian koumiss Reference

LAB Enterococcus faecalis Chaves-López and others (2011), E. faecalis Wang and others (2008), Uchida
E. faecium Rossi (2010) L. kefiranofaciens and others (2007)
E. seriolicida (Lactococcus garviae) L. acidophilus
Vagococcus penaei L. buchneri
L. plantarum L. casei
L. paracasei subsp. paracasei L. fermentum
L. delbrueckii subsp. delbrueckii L. helveticus
L. helveticus L. jensenii
L. lactis subsp. lactis L. kefiri
L. kitasatonis
L. lactis
L. paracasei
L. plantarum
Lc. mesenteroides
S. thermophilus

Yeast C. tropicalis Chaves-López and others (2012) Candida pararugosa Mu and others (2012), Danova and
C. lusitaniae Dekkera anomala others (2005), Watanabe and others
C. glabrata Geotrichum sp. (2008), Ni and others (2007)
C. pararugosa I. orientalis (Pichia kudriavzevii)
C. tropicalis/K. marxianus Kazachstania unispora
Kazachstania unispora Kluyveromyces marxianus
Kluyveromyces marxianus Pichia deserticola
G. geotrichum P. fermentans
Pichia kudriavzevii P. manshurica
R. mucilaginosa P. membranaefaciens
S. cerevisiae S. cerevisiae
Trichosporon insectorum T. delbrueckii
T. asakii
Torulaspora delbruekii
Wickerharmomyces pijperii

Suero costeño cess (Cruz-Martı́nez 2006). Moreover, yeasts seemed to have

Suero costeño is a traditional homemade cream cheese produced
along the Colombian Caribbean coast. Raw cow milk is fermented
in calabashes (the dried fruit of Lagenaria vulgaris) that are sealed
and subsequently placed in a warm site, at an average temperature
of 35 °C. Resident microbiota from the calabashes is a reservoir
microbial community transferred directly to suero costeño. The time
required for their manufacturing (1 to 3 d) depends on the desired
viscosity. During this period, a natural fermentation takes place
and the pH decreases to near 4.6. Fermentation is characterized
by a liquid–solid 2-phase system, where the liquid part is called
lactosuero; the other one, known as suero, has a cream-like consis-
tence and desiderable sensory properties (Cueto-Vigil and others
2010). Figure 8 illustrates 2 of the most common procedures used
for suero costeño production, where salt addition before or after
fermentation is the main difference.
During production, LAB and yeasts are involved and, as previ-
ously mentioned about kumis, the complex interaction between
these 2 microbial groups and the differences in species as well
as their balances, contribute to the product sensory attributes.
Cueto and others (2007) reported a succession of LAB during
fermentation, in which Lactobacillus paracasei, L. plantarum, and L.
lactis were predominant at the beginning of the process with a
load of 4.8 log CFU/mL; during the intermediate stage (5 to
8 h), LAB reached values of 5.5 log CFU/mL with L. paraca-
sei, subsp. paracasei, L. plantarum, L. lactis subsp. lactis, Leuconostoc
lactis subsp. lactis as predominant species. At the final stage (24
h), LAB reached values between 7 and 8 log CFU/mL, and a
high portion of Lactobacillus species (such as: acidophilus, brevis,
delbrueckii subsp. delbrueckii, paracasei subsp. paracasei, pentosus,
rhamnosus, and plantarum) was dominant. Also, Enterococcus fae-
cium and E. durans were isolated at the end of the pro-
an effect on fermentation, with an increase during the first
few hours of the process and maximum values from 2 to
5 log CFU/mL at the end of the manufacturing process (Farelo De
La Hoz 2002). In particular, the predominance of Candida krusei,
Torulopsis pintolopesii (Candida pintolopesii), Rhodotorula mucilaginosa,
Candida kefir, Candida glabrata, and S. cerevisiae has been reported
(Farelo De La Hoz 2002; Cruz-Martı́nez 2006).
The presence of Enterobacteriaceae has been reported at levels
from 0.8 to 4.8 log CFU/mL (Cruz-Martı́nez 2006), and Staphylo-
coccus aureus coagulase-positive was reported in 100% of 63 samples
collected in the Cordoba region (Northern Colombia) with levels
of 5 to 6 log CFU/mL (Chams and others 2012), implying poor
hygienic and manipulation conditions during the production pro-
cess and during storage of suero costeño.
After fermentation, suero costeño (thickness phase) is retrieved
from the calabashes, and NaCl (2% to 3%) is added to the product
packed in traditional containers. Differently from other Colom-
bian fermented dairy products, Suero Costeño, it is salted to reach
NaCl concentrations from 1% to 3%, and it is commonly used as a
food dressing. Commercial suero costeño is classified on the basis of
fat content as light, semilight, and fat, whereas homemade prod-
ucts vary with respect to NaCl concentration, type of fermenting
microbiota, and length time of fermentation. Table 7 reports the
main physico-chemical characteristics of suero costeño produced in
various locations of northern Colombia. It is to underline that the
comparison of the aw values reported by Farelo De La Hoz (2002)
with other fresh cream cheese described in literature resulted un-
usual for this kind of product.
The microbiota involved in suero costeño fermentation has been
evaluated for its antimicrobial and probiotic potential. In this
regard, Rodrı́guez-Peña and Torres-Lozano (2006) reported the


C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1043
Colombian fermented foods and beverages . . .
Table 7–Physico-Chemical parameters of traditional suero costeño.
Farelo De La Hoz (2002)
Mean Min
R.H. (%) 75.57 62.72
Fat (%) 10.0 4.5
Protein (%) 7.53 3.86
NaCl (%) 2.24 1.1
Acidity (%) 2.35 1.41
pH 3.72 3.41
aw 0.94 0.93
R.H., relative humidity; n.r, not reported.
antibacterial activity of strains of Lactobacillus fermentum, L. brevis, L.
plantarum, L. rhamnosus, and L. lactis subsp. lactis against Escherichia
coli and S. aureus. In addition, selected strains of L. fermentum
and L. rhamnosus showed good probiotic characteristics that might
be used for food or dairy fermentations (Acuña-Monsalve 2009).
Thus, suero costeño may offer advantages as a carrier of probiotic
microorganisms. The importance of these probiotic-containing
products, commonly regarded as functional foods, in the mainte-
nance of health and well-being is becoming a key factor affecting
consumer choice (Gardiner and others 1998).
Surprisingly, commercial suero costeño is not well accepted by
consumers, as it is different from the traditional product in flavor
and overall taste. However, when inoculum derived from the tra-
ditional product is used to ferment pasteurized milk, the taste and
texture are not significantly different from the traditional product
(Acevedo and others 2012).
Summarizing Comments
In Colombian traditional fermented beverages and foods, fer-
mentation is performed mainly by LAB and yeasts, which con-
tribute to product preservation. In addition, these fermented prod-
ucts contain ingredients and substances of microbial origin that
could be valuable for consumer health. For this reason, the cur-
rent challenges for the Colombian food industry include research
and development of new fermented foods and beverages with
health-promoting activities intended for consumers with specific
health requirements, preferably by means of multifunctional starter
cultures and process innovation.
On the other hand, several traditional Colombian fermented
foods and beverages are still prepared at home, where the temper-
ature applied for incubation cannot be easily kept under control,
with fluctuations between day and night. Therefore, the selective
pressure exerted by the environment consolidates the dominance
of selected species during fermentation. Moreover, the impact of
the process variables and their changes during continuous propa-
gation enable stable associations of microbial species.
Actually, the hygienic quality of natural fermented Colombian
products is highly variable, because it depends on many factors
such as the microbiological quality of raw materials and ingre-
dients, as well as hygiene conditions during fermentation and
storage. Therefore, the possible role of these products as vehicles
of foodborne diseases still needs to be recognized and investigated.
Furthermore, raw materials such as maize, cassava, and cocoa beans
are good substrates for fungal growth and mycotoxin production,
and also cow feed and raw milk can be contaminated by aflatoxins,
with a possible increase of mycotoxin risks in the finished product.
Unfortunately, except for cocoa, to our knowledge no studies have
been published on the presence of mycotoxins in these fermented
foods.
1044 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
Simanca and others (2010)
Max Mean Min Max
80.60 76.03 73.48 78.43
16.5 n.r n.r n.r
11.45 5.09 4.0 6.0
2.95 2.34 1.79 2.95
3.08 1.40 0.93 1.85
3.97 3.94 3.52 4.39
0.96 n.r n.r n.r
Conclusion
This review is the 1st collection of scientific and technical data
on the quality and safety of various typical Colombian beverages
and foods. In our study, we have analyzed both beneficial and
detrimental effects of these products, but most of all, we have
pointed out the missing data and therefore future research needs.
We believe that the data reported on the functional potential, in
terms of antinutritional factor degradation, increase of mineral
bioavailability, bioactive compounds, and increase of nutrient di-
gestibility, could be useful to enhance the value of these products
and promote new applications in the food industry worldwide.
In fact, fermented Colombian foods and beverages might become
important sources of new valuable microbial strains for biotech-
nology.
Author Contributions
Clemencia Chaves-López devised and drafted the manuscript,
Annalisa Serio contributed to draft the manuscript, Carlos David
Grande-Tovar prepared the literature overview of cassava products,
Raul Cuervo-Mulet prepared the literature overview concerning
Chicha beverage, Johannes Delgado-Ospina performed the analy-
ses of microbiological and physicochemical characteristics of Masa
agria, Antonello Paparella contributed to manuscript revision. All
authors read and approved the final manuscript.
References
Acevedo D, Rodrı́guez A, Fernández A. 2012. Low-amplitude oscilatory
determinations for Suero Costeño. Rev U.D.C.A Act Divul Cient
15:219–25.
Achinewhu SC, Barber LI, Ijeoma IO. 1998. Physicochemical properties and
garification (gari yield) of selected cassava cultivars in Rivers State, Nigeria.
Plant Foods Hum Nutr 52(2):133–40.
Acosta-Muñoz L, Mazamorra-Valderrama E. 2004. Enterramientos de masas
de yuca del pueblo Ticuna: tecnologı́a tradicional en la várzea del Amazonas
colombiano. Available from: http://cdam.minam.gob.pe:8080/
handle/123456789/766. Accessed 2014 March 11.
Acuña-Monsalve Y. 2009. Selección e identificación de BAL con potencial
probiótico aisladas del Suero Costeño [Master thesis]. Facultad de Ingenierı́a
Agro-Industrial, Universidad de la Sabana, Bogotá, Colombia. 112 p.
Afoakwa EO, Paterson A, Fowler M, Ryan A. 2008. Flavor formation and
character in cocoa and chocolate: a critical review. Crit Rev Food Sci Nutr
48(9):840–57.
Aidoo KE, Nout MJR, Sarkar PK. 2006. Occurrence and function of yeasts
in Asian indigenous fermented foods. FEMS Yeast Res 6(1):30–9.
Alcántara-Hernández RJ, Rodrı́guez-Álvarez JA, Valenzuela-Encinas C,
Gutiérrez-Miceli FA, Castañón-González H, Marsch R, Ayora-Talavera T,
Dendooven L. 2010. The bacterial community in “taberna” a traditional
beverage of Southern Mexico. Lett Appl Microbiol 51(5):558–63.
Amoa-Awua WK, Sampson E, Tano-Debrah K. 2007. Growth of yeasts,
lactic and acetic acid bacteria in palm wine during tapping and fermentation
from felled oil palm (Elaeis guineensis) in Ghana. J Appl Microbiol
102:599–606.
Ampe F, Sirvent A, Zakhia N. 2001. Dynamics of the microbial community
responsible for traditional sour cassava starch fermentation studied by

C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .
denaturing gradient gel electrophoresis and quantitative rRNA
hybridization. Int J Food Microbiol 65:45–54.
Ardhana M, Fleet G. 2003. The microbial ecology of cocoa bean
fermentations in Indonesia. Int J Food Microbiol 86:87–99.
Arguedas P, Cooke RD. 1982. Residual cyanide concentration during the
extraction of cassava starch. Int J Food Sci Tech 17(2):251–62.
Arotupin DJ. 2007. Evaluation of microorganisms from cassava waste water
for production of amylase and cellulase. Res J Microbiol 2:475–80.
Barel M. 1997. La fermentation du cacao: le moyen de l’apprécier et de la
maitriser. IAA. Industries Alimentaires et agricoles 114(4):211–4.
Barros NO. 1981. In: Cacao. Instituto Colombiano Agropecuario. Bogotà,
Colombia. p 179–96.
Bar-Shimon M, Yehuda H, Cohen L, Weiss B, Kobeshnikov A, Daus A,
Goldway M, Wisniewski M, Droby S. 2004. Characterization of
extracellular lytic enzymes produced by the yeast biocontrol agent Candida
oleophila. Curr Genet 45(3):140–8.
Bassir O. 1962. Observation of the fermentation of palm-wine. West Afr J
Biol Appl Chem 6:5–21.
Ben Omar N, Ampe F, Raimbault M, Guyot JP, Tailliez P. 2000. Molecular
diversity of lactic acid bacteria from cassava sour starch (Colombia). Syst
Appl Microbiol 23:285–91.
Bernal R, Galeano G, Garcı́a N, Olivares IL, Cocomá C. 2010. Uses and
commercial prospects for the wine palm, Attalea butyracea, in Colombia.
Ethnobot Res Applic 8:255–68.
Bermudez OI, Tucker KL. 2003. Tendencias en el consumo de alimentos en
poblaciones latinoamericanas. Cad Saúde Pública, Rio de Janeiro
19(1):S87–99.
Betancourt Botero SP, Bolı́var Escobar GA, Ramı́rez Toro C. 2013.
Fermentación de maı́z de alta calidad proteica con Lactobacillus plantarum
(CPQBA 087–11 DRM) aislado en Colombia de masas tradicionales
fermentadas. Rev Argent Microbiol 45(4):282–3.
Brabet C, Dufour D. 1996. El almidón agrio de yuca: producción y estudios
de las propiedades fı́sico quı́micas. Proceedings of the Simposio en
Carbohidratos, October 4–6, Quito, Ecuador. p 197–203.
Cadena MP, Villarraga EC, Luján DE, Salcedo JG. 2006. Evaluación de la
agroindustria del almidón agrio de yuca (Manihot esculenta Crantz) en
Cordoba y Sucre. Temas Agrarios 11:43–53.
Carrillo LC, Londoño-Londoño J, Gil A. 2014. Comparison of polyphenol,
methylxanthines and antioxidant activity in Theobroma cacao beans from
different cocoa-growing areas in Colombia. Food Res Int 60:273–80
Castilla Pinedo Y, Mercado Martı́nez ID, Mendoza Gutiérrez V, Monroy
ML. 2011. Determinación y cuantificación de los niveles de aflatoxinas en
bollos de mazorca producidos en Arjona (Departamento de Bolı́var –
Colombia). Avanc Investig Ing 8(1):71–6.
Castro T. 2009. Effects of dietary sources of vegetable fats on performance of
dairy ewes and conjugated linoleic acid (CLA) in milk. Small Rum Res
84(1–3):47–53.
Chams L, Cury K, Aguas Y. 2012. Evaluación microbiológica de suero
costeño y valoración higiénica en puntos de venta en monterı́a, Córdoba.
Rev Colombiana Cienc Anim 4(2):344–52.
Charles AL, Sriroth K, Huang T. 2005. Proximate composition, mineral
contents, hydrogen cyanide and phytic acid of 5 cassava genotypes. Food
Chem 92(4):615–20.
Chaves-López C, Serio A, Osorio-Cadavid E, Paparella A, Suzzi G. 2009.
Volatile compounds produced in wine by Colombian wild Saccharomyces
cerevisiae strains. Ann Microbiol 59(4):733–40.
Chaves-López C, Serio A, Martuscelli M, Paparella A, Osorio-Cadavid E,
Suzzi G. 2011. Microbiological characteristics of kumis, a traditional
fermented Colombian milk, with particular emphasis on enterococci
population. Food Microbiol 5:1041–7.
Chaves-López C, Tofalo R, Serio A, Paparella A, Sacchetti G, Suzzi G. 2012.
Yeasts from Colombian kumis as source of peptides with angiotensin
I-converting enzyme (ACE) inhibitory activity in milk. Int J Food
Microbiol 159:39–46.
Chaves-López C, Serio A, Paparella A, Martuscelli M, Corsetti A, Tofalo R,
Suzzi G. 2014. Impact of microbial cultures on proteolysis and release of
bioactive peptides in fermented milk. Food Microbiol 42:117–21
Cheesman EE. 1944. Notes on the nomenclature, classification and possible
relationships of cocoa populations. Trop Agric 21:144–59.
Chelule PK, Mbongwa HP, Carries S, Gqaleni N. 2010. Lactic acid
fermentation improves the quality of amahewu, a traditional South African
maize-based porridge. Food Chem 122(3):656–61.

C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1045
Chen Y, Wang Z, Chen X, Liu Y, Zhang H, Sun T. 2010. Identification of
angiotensin I-converting enzyme inhibitory peptides from koumiss, a
traditional fermented mare’s milk. J Dairy Sci 93(3):884–92.
Cheryan M, Rackis JJ. 1980. Phytic acid interactions in food systems. CRC
Crit Rev Food Sci Nutr 13(4):297–335.
Chitra U, Singh U, Venkateswara Rao P. 1996. In vitro protein digestibility,
dietary fiber, and minerals of pulses as influenced by processing methods.
Plant Foods Hum Nutr 49(4):307–16.
Copetti MV, Iamanaka BT, Frisvad JC, Pereira JL, Taniwaki MH. 2011.
Mycobiota of cocoa: from farm to chocolate. Food Microbiol 28:1499–504.
Cruz-Martı́nez JG. 2006. Aislamiento y carcterización biochı́mica de
levaduras y bacterias acido lácticas productoras de substancias
antimicrobianas de interés industrial presents en el Suero Costeño [Thesis].
Universidad de la Sabana, Facultad de Ingenieria, Bogotà. 108 p.
Cubillos G, Merizalde GJ, Correa E. 2008. Manual de Beneficio del Cacao
para: técnicos, profesionales del sector agropecuario y productores; Octubre
de 2008, Medellı́n (Antioquia), Colombia S.A.
Cuéllar O, Guerrero G. 2012. Actividad antibacteriana de la cáscara de cacao.
Theobroma cacao L Rev MVZ Córdoba 17(3):3176–83.
Cuervo Mullet RA, Ledesma JA, Duran Vanegas JA, Argote Vega FE. 2010.
Aislamiento y control biologico de Leuconostoc mesenteroides en un ingenio
para optimizar el rendimineto de azucar y etanol. Rev Biotecnol Sector
Agropec Agroindustrial 8(2):31–40.
Cueto C, Garcı́a D, Garcés F, Cruz J. 2007. Preliminary studies on the
microbiological characterization of lactic acid bacteria in suero costeño, a
Colombian traditional fermented milk product. Rev Latinoam Microbiol
49:12–8.
Cueto-Vigil MC, Acuña-Monsalve Y, Valenzuela-Riaño J. 2010. Evaluación
in vitro del potencial probiótico de bacterias ácido lácticas aisladas de suero
costeño. Actualidades Biológicas 32:129–38.
Dallman PR. 1992. Changing iron needs from birth through aolescence. In:
Fomon SJ, Zlotkin S, editors. Nutritional anemias. New York: Raven Press.
p 29–39.
Danova S, Petrov K, Pavlov P.Petrova P. 2005. Isolation and characterization
of Lactobacillus strains involved in koumiss fermentation. Int J Dairy Technol
58:100–5.
de Melo DLFM, Santos FC, Barbosa Junior AM, Oliveira Santos P,
Gutiér rez Carnelossi MA, Trindade RC. 2007. Identification of yeasts
isolated from the pulp in nature and the production of homemade “Umbu”
wine. Braz Arch Biol Technol 50(5):887–92.
De Vuyst L, Van Kerrebroeck S, Harth H, Huys G, Daniel H-M, Weckx S.
2014. Microbial ecology of sourdough fermentations: diverse of uniform?
Food Microbiol 37:11–29.
Dı́az de León Sánchez F, Carballo Carballo A, Capella Vizcaino S, Bernal
Lugo I. 2006. Contenido de azúcares en 4 culativares de maı́z (Zea mays) y
su velocidad de deterioro en almacén. Rev Iber Tecnol Postcosecha
8(1):38–47.
Di Mattia C, Martuscelli M, Sacchetti G, Scheirlinck I, Beheydt B,
Mastrocola D, Pittia P. 2013. Effect of fermentation and drying on
procyanidins, antiradical activity and reducing properties of cocoa beans.
Food Bioproc Techn 6:3420–32.
Dillinger TL, Barriga P, Escárcega S, Jimenez M, Salazar Lowe D, Grivetti
LE. 2000. Food of the Gods: cure for humanity? A cultural history of the
medicinal and ritual use of chocolate. J Nutr 130:2057S–72S.
Dufour D. 1995. El almidón agrio de yuca en Colombia: estudio de las
propiedades reológicas durante las etapas del proceso. In: Boucher F,
Muchnik J editors. Agroindustria Rural Recursos Técnicos y Alimentación.
San José: C.R. p 165–81.
Ebringer L, Fernčı́k M, Krajčovič J. 2008. Beneficial health effects of milk
and fermented dairy products: review. Folia Microbiol 53(5):378–94.
Ejigui J, Savoie L, Marin J, Desrosiers T. 2005. Beneficial changes and
drawbacks of a traditional fermentation process on chemical composition
and antinutritional factors of yellow maize (Zea mays). J Biol Sci 5(5):
590–6.
Endtz HP, Van den Braak N, Verbrugh HA, Van Bekum A. 1999.
Vancomycin resistance status quo and quo vadis. Eur J Clin Microbiol Infect
Dis 18:683–90.
Escobar A, Gardner A, Steinkraus KH. 1993. South American fermented
maise chicha. In: Steinkraus KH editor. Handbook of indigenous fermented
foods. New York: Marcel Dekker. p 402–6.
Espinal GCF, Martı́nez Covaleda HJ, Ortı́z Hermida L. 2005. La cadena del
cacao en Colombia una mirada global de su estructura y dinámica.
Colombian fermented foods and beverages . . .
1991–2005. Bogotá, Colombia: Ministerio de Agricultura Y Desarrollo
Rural Observatorio Agrocadenas.
Farelo De La Hoz HD. 2002. Caracterización microbiológica y de los
parámetros fı́sicos quı́micos relacionados con el proceso de fermentación
del “Suero Costeño” como producto final elaborado en el difı́cil
Ariguani [Thesis]. Universidad de la Sabana, facultad de
Ingenieria, Programa de Producción Agroindustrial. Chia,
Colombia. 149 p.
Federacion Nacional de Cacaoteros. 2004. El beneficio y caracteristicas
fisico-chimicas del Cacao. Bogotá, Colombia: Produmedios.
Figueroa C, Davila AM, Pourquié J. 1995. Lactic acid bacteria of the sour
cassava starch fermentation. Lett Appl Microbiol 21:126–30
Furukawa S, Watanabe T, Toyama H, Morinaga Y. 2013. Significance of
microbial symbiotic coexistence in traditional fermentation. J Biosci
Bioengin 116(5):533–9.
Gardiner G, Ross RP, Collins JK, Fitzgerald G, Stanton C. 1998.
Development of a probiotic Cheddar cheese containing human-derived
Lactobacillus paracasei strains. Appl Environm Microbiol 64(6):
2192–9.
Gernah DI, Ariahu, CC, Ingbian EK. 2010. Effects of malting and lactic
fermentation on some chemical and functional properties of maize (Zea
mays). American J Food Techn 5:404–12.
Glushakova AM, Yurkov Am, Cherov IY. 2007. Massive isolation of
anamorphous ascomycete yeasts Candida oleophila from plant phyllosphere.
Microbiol 76(6):799–803.
Gomes FCO, Silva CLC, Vianna CR, Lacerda ICA, Borelli BM, Nunes AC,
Franco GR, Mourão MM, Rosa CA. 2010. Identification of lactic acid
bacteria associated with traditional cachaça fermentations. Braz J Microbiol
41:486–92.
Gómez G, Valdivieso M. 1984. Effects of sun-drying on a concrete flour and
oven-drying on trays on elimination of cyanide from cassava whole-root
chips. J Food Technol 19:703–10.
Halm M, Hornbaek T, Arneborg N, Sefa-Dedeh S, Jespersen L. 2004. Lactic
acid tolerance determined by measurement of intracellular pH of single cells
of Candida krusei and Saccharomyces cerevisiae isolated from fermented maize
dough. Int J Food Microbiol 94(1):97–103.
Hayashida FM. 2008. Ancient beer and modern brewers: Ethno-archae-
ological observations of Chicha production in two regions of the North
Coast of Peru. J Anthropol Archaeol 27:161–74.
Hellström AM, Vázques-Juárez R, Svanberg U, Andlid TA. 2010.
Biodiversity and phytase capacity of yeasts isolated from Tanzanian togwa.
Int J Food Microbiol 136(3):352–8.
Ho VTT, Zhao J, Fleet G. 2014. Yeasts are essential for cocoa bean
fermentation. Int J Food Microbiol 174:72–87.
Holm PB, Kristiansen KN, Pedersen HB. 2002. Transgenic approaches in
commonly consumed cereals to improve iron and zinc content and
bioavailability. J Nutrition 132:514S–6S.
Holzapfel WH. 1997. Use of starter cultures in fermentation on a household
scale. Food Control 8:241–58.
Ip C, Scimeca JA, Thompson H. 1995. Effect of timing and duration of
dietary conjugated linoleic acid on mammary cancer prevention. Nutrition
Canc 26:149–57.
Isaeva OV, Glushakova AM, Garbuz SA, Kachalkin AV, Chernov I. 2010.
Endophytic yeast fungi in plant storage tissues. Izv Akad Nauk Ser Biol
1:34–43.
Ishii S, Konagaya Y. 2002. Beneficial role of koumiss intake of Mongolian
nomads. J Japn Soc Nutr Food Sci 55:281–5.
Katongole JN. 2008. The microbial succession in indigenous fermented
maize products [Thesis]. Faculty of Natural and Agricultural Sciences, Dept.
of Microbial, Biochemical and Food Biotechnology, Univ. of Free State,
Bloemfontein. 162 p.
Kimaryo VM, Massawe GA, Olasupo NA, Holpzapfel WH. 2000. The use of
a starter culture on the fermentation of cassava for the production of
‘kivunde’, a traditional Tanzanian food product. Int J Food Microbiol
56:179–90.
Kobawila SC, Louembe D, Keleke S, Hounhouigan J, Gamba C. 2005.
Reduction of the cyanide content during fermentation of cassava roots and
leaves to produce Bikedi and Ntoba Mbodi, two food products from
Congo. Afr J Biotechnol 4(7):689–96.
Kumar V, Sinha AK, Makkar HPS, Becker K. 2010. Dietary roles of phytate
and phytase in human nutrition: a review. Food Chem 120(4):
945–59.
1046 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
Lacerda CHF, Hayashi C, Soares CM, Boscolo WR, Kavata LCB. 2005.
Replacement of corn Zea mays L. by cassava Manihot esculenta crants meal in
grass-carp Ctenopharyngodon idella fingerlings diets. Acta Sci Anim Sci
27:241–5.
Lagunes Gálvez S, Loiseau G, Paredes JL, Barel M, Guiraud JP. 2007. Study
on the microflora and biochemistry of cocoa fermentation in the
Dominican Republic. Int J Food Microbiol 114(1):124–30.
Laitila A, Wilhelmson A, Kotaviita E, Olkku J, Home S, Juvonen R. 2006.
Yeasts in an industrial malting ecosystem. J Ind Microbiol Biotechnol
33(11):953–66.
Lamuela-Raventós RM, Romero-Pérez AI, Andrés-Lacueva C, Tornero A.
2005. Health effects of cocoa flavonoids. Food Sci Tech Int 11(3):159–76.
Lanciotti R, Patrignani F, Iucci L, Guerzoni ME, Suzzi G, Belletti N,
Gardini F. 2007. Effects of milk high-pressure homogenization on biogenic
amine accumulation during ripening of ovine and bovine Italian cheeses.
Food Chem 104:693–701.
Larrahondo JE. 1995. Calidad de la caña de azúcar. In: Cassalett C, Torres J,
Isaacs C, editors. El cultivo de la caña de azúcar en la zona azucarera de
Colombia. Cali, Colombia: Cenicaña. p 337–54.
Larsonneur S. 1993. Influence du séchage solaire sur la qualité de l’amidon
aigre de manioc. Memorie ingénieur. Cali, Colombia: Université
Tecnologique de Compiégne and CIAT. 88 p.
Larsonneur EP, Canhos VP, Vilela ER, Asqueri ER, Carvalho HP. 1999.
Determinación de la flora microbiana de la fécula de yuca fermentada
(polvilho azedo) durante las diferentes etapas de procesamiento. Alimentaria
305:97–103.
Laurent L. 1992. Qualité de l’almidon aigre de manioc: validation d’une
méthode d’evaluation du pouvoir de panification et mise en place d’une
épreuve descriptive d’analyse sensorrielle. Projet de fin d’études. Géenie
biologique, produits biologiques et alimentaires. France: Université de
technologie de Compiégne. 68 p.
Liu S, Han Y, Zhou Z. 2011. Lactic acid bacteria in traditional fermented
Chinese foods. Food Res Int 44:643–51.
López-Arboleda WA, Ramı́rez-Castrillón M, Mambuscay-Mena LA. 2010.
Diversidad de levaduras asociadas a chichas tradicionales de Colombia. Rev
Colomb Biotecnol 12(2):176–86.
Lorence-Quiñones A, Wacher-Rodarte C, Quintero-Ramı́rez R. 1999.
Cereal fermentations in Latin American countries. In: Haard NF, Odunfa
SA, Lee CH, editors. Fermented cereals: a global perspective FAO
Agricultural Support Systems Division. Rome: Food & Agriculture
Organization. Available from:
http://www.fao.org/docrep/x2184e/x2184e01.htm. Accessed 2013
December 12.
Marfo EK, Simpson BK, Idowu JS, Oke OL. 1990. Effect of local food
processing on phytate levels in cassava, cocoyam, yam, maize, sorghum, rice,
cowpea, and soybean. J Agric Food Chem 38:1580–5.
Martin MA, Goya L, Ramos S. 2013. Potential for preventive effects of cocoa
and cocoa polyphenols in cancer. Food Chem Toxicol 56:336–51.
Mazo SA, Arias SA. 2006. Eficacia y seguridad de leche fermentada por
lactobacilos (kumis) en la recuperación nutricional de niños desnutridos y
en el control de sus episodios de enfermedad diarreica. Rev Fac Nac Salud
Pública 24(2):83–97.
Mestres C, Rouau X. 1997. Influence of natural fermentation and drying
conditions on the physicochemical characteristics of cassava starch. J Sci
Food Agricul 74(2):147–55.
Mincanquer-Cuatı́n WO. 2007. Siguiendo las huellas de los mayores: la
educación propia para la defensa del territorio y la cultura. Rev Educ Pedag
19(49):91–4.
Mokoena MP, Chelule PK, Galeni N. 2005. Reduction of fumonisin B1 and
zearalenone by lactic acid bacteria in fermented maize meal. J Food Prot
68:2095–9.
Montagnac JA, Davis CR, Tanumihardjo SA. 2009. Processing techniques to
reduce toxicity and antinutrients of cassava for use as a staple food. Comp
Rev Food Sci Food Safety 8:17–27.
Montoya-Henao S. 2007. Industrialización de la Yuca: Obtención de
almidón y sus aplicaciones. In: Ramirez Navas JS, editor. Universidad del
Valle, Valle del Cauca. Cali, Columbia: Manejo de sólidos y fluı́dos. p 40
Moorthy SN. 1998. Cassava fermentation and associated changes in
physicochemical and functional properties. Crit Rev Food Sci Nutr
38(2):73–121.
Mora de Tovar G. 1989. Chicha, guarapo y presión fiscal en la sociedad
colonial del siglo XVIII. An Colomb Hist Soc Cult 16–17:15–47.

C 2014 Institute of Food Technologists®
Colombian fermented foods and beverages . . .
Moreira IM, Miguel MG, Duarte WF, Dias DR, Schwan RF. 2013.
Microbial succession and the dynamics of metabolites and sugars during the
fermentation of three different cocoa (Theobroma cacao L.) hybrids. Food Res
Int 54(1):9–17.
Morris Navarro LF. 2011. Determinación de aflatoxinas en muestras de maı́z
(Zea mays) y arroz (Oryza sativa) para consumo humano en cinco
departamentos de la Costa Caribe Colombiana mediante cromatografı́a de
alta eficiencia durante seis meses en 2011. Universidad Nacional de
Colombia [Master Thesis]. Bogotá, Colombia.
Motamayor C, Risterucci AM, Lopez PA, Ortiz C, Moreno A, Lanaud C.
2002 Cacao domestication I: the origin of the cacao cultivated by the
Mayas. Heredity 89:380–6.
Mu Z, Yang X, Yuan H. 2012. Detection and identification of wild yeast in
koumiss. Food Microbiol 31(2):301–8.
Ni HJ, Bao QH, Sun TS, Chen X, Zhang HP. 2007. Identification and
biodiversity of yeasts isolated from koumiss in Xinjiang of China. Acta
Microbiol Sinica 47(4):578–82.
Nielsen DS, Teniola OD, Ban-Koffi L, Owusu M, Andersson TS, Holzapfel
WH. 2007. The microbiology of Ghanaian cocoa fermentations analysed
using culture-dependent and culture-independent methods. Int J Food
Microbiol 114(2):168–86.
Nullvalue. 2003. Los secretos de la Chicha. Available from:
http://www.eltiempo.com/archivo/documento/MAM-1049564. Accessed
2013 December 18.
Oboh G, Elusiyan CA. 2007. Changes in the nutrient and anti-nutrient
contents of micro-fungi-fermented cassava flour produced from low- and
medium-cyanide variety of cassava tubers. Afr J Biotechnol 6(18):
2150–7.
Olarte OMF, Martı́nez MJD, Acosta PJ, Garzón OMA. 2007. Determination
of the ethanol, methanol and acetaldehyde levels in the guarapo prepared in
Cundinamarca’s municipalities. Rev Col Gastroenterol 22:97–103.
Onyango C, Noetzold H, Bley T, Henle T. 2004. Proximate composition
and digestibility of fermented and extruded uji from maize-finger millet
blend. LWT 37(8):827–32.
Ortiz de Bertorelli L, Graziani de Fariñas L, Gervaise Rovedas L. 2009.
Influencia de varios factores sobre caracterı́sticas del grano de cacao
fermentado y secado al sol. Agronomı́a Trop 59(2):119–27.
Osorio JA, Ramirez C, Novoa CF, Gutierrez LF. 2011. Conjugated linoleic
acid, fatty acid profile and process properties in kumis: fermented milk
consumed in Colombia. Vitae 18(2):144–52.
Osorio-Cadavid E, Chaves-Lopez C, Tofalo R, Paparella A, Suzzi G. 2008.
Detection and identification of wild yeasts in Champús, a fermented
Colombian maize beverage. Food Microbiol 25:771–7.
Othman A, Ismail A, Ghani AN, Adenan I. 2007. Antioxidant capacity and
phenolic content of cocoa beans. Food Chem 100:1523–30.
Ouattara HG, Koffi BL, Karou GT, Sangaré A, Niamke SL, Diopoh JK.
2008. Implication of Bacillus sp. in the production of pectinolytic enzymes
during cocoa fermentation. World J Microbiol Biotech 24(9):1753–60.
Oyewole OB. 2001. Characterization and significance of yeast involvement
in cassava fermentation for fufu production. Int J Food Microbiol 65:213–8.
Oyewole OB, Odunfa SA. 1990. Characterization and distribution of lactic
acid bacteria in cassava fermentation during fufu production. J Appl
Microbiol 68:145–52.
Panghyová E, Kačenová D, Hajdušková S, Matulová M, Kiss E. 2006.
Influence of free linoleic acid on the fatty acids profile of fermentation by
selected probiotic bacteria. J Food Nutr Res 45(4):159–65.
Pariza MW, Park Y, Cook ME. 2000. Mechanisms of action of conjugated
linoleic acid: evidence and speculation. Exp Biol Med 223:8–13.
Pataro C, Guerra JB, Petrillo-Peixoto ML, Mendonça-Hagler LC, Rosa CA.
2000. Yeast communities and genetic polymorphism of Saccharomyces
cerevisiae strains associated with artisanal fermentation in Brazil. J Appl
Microbiol 89:24–31.
Patiño VM. 1990. Historia de la cultura material en la América Equinoccial
(Tomo 1). Alimentación y alimentos Bogotá, Instituto Caro y Cuervo.
[http://www.banrepcultural.org/blaavirtual/historia/equinoccial_1_
alimentos/biblio htm]
Patiño-Rodriguez VM. 2002. Historia y dispersión de los frutales nativos del
Neotropico. Cali, Colombia: Centro Internacional de Agricultura Tropical.
265 p.
Pineda RDP, Chica MJ, Echeverri LF, Ortiz A, Olarte HH, Riaño NM.
2012. Influencia de da fermentación y el secado al sol sobre las
caracteristicas del grano de cacao TSH 565 y ICS 60. Vitae 19:S288–90.

C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1047
Pérez Echeverry P. 2004. Mucı́lago pulverizado obtenido a partir de la cáscara
de cacao, una alternativa en la clarificación de jugos en la industria panelera
[Thesis]. Sede Manizales: Universidad Nacional de Colombia. Available
from: http://www.bdigital.unal.edu.co/1168/#sthash.5lP6gWKn.dpuf
Plessas S, Alexopoulos A, Voidarou C, Stavropoulou E, Bezirtzoglou E.
2011. Microbial ecology and quality assurance in food fermentation systems.
The case of kefir grains application. Anaerobe 17:483–5.
Poutanen K, Flander L, Katina K. 2009. Sourdough and cereal fermentation
in a nutritional perspective. Food Microbiol 26(7):693–9.
Powis TG, Cyphers A, Gaikwad NW, Grivetti L, Cheong K. 2011. Cacao
use and the San Lorenzo Olmec. Proc Natl Acad Sci U S A 108:8595–
600.
Pulgarı́n N, Bernal R. 2004. El potencial de la palma de vino, Attalea
butyracea, como planta azucarera. In: Ramı́rez-Padilla BR, Macı́as-PD,
Varona-BG, editors. Libro de Resúmenes Tercer Congreso Colombiano de
Botánica. Popayán, Colombia: Universidad del Cauca. p 194.
Putri WDR, Haryadi DW, Marseno-Cahyanto MN. 2011. Effect of
biodegradation by lactic acid bacteria on physical properties of cassava
starch. Int Food Res J 18:1149–54.
Quintero V, Giraldo G, Lucas J. 2012. Modificacion del almidon de yucca
por A. niger. Viatae 19(1):S177–9.
Rainer L, Heiss CJ. 2004. Conjugated linoleic acid: health implications and
effects on body composition. J Am Diet Assoc 104:963–8.
Ramos O. 2011. Avatarres de la Chicha. Poligramas 27:1–15.
Rincón–Suárez LM, Villamil-Novoa ES. 2005. Obtención y caracterización
fisicoquı́mica del almidón agrio para el mejoramiento del proceso de
fermentación [Thesis]. Bucaramanga, Colombia: Universidad Industrial de
Santander, Escuela de Quı́mica. 67 p.
Riordan JF. 2003. Angiotensin-I-converting enzyme and its relatives.
Genome Biol 4(8):225.1-.5
Rodrı́guez-Peña JM, Torres-Lozano LM. 2006. Evaluación de sustancias
antimicrobianas presentes en los extractos obtenidos de bacterias acido
lácticas aisladas de Suero Costeño [Thesis]. Bogotá, Colombia: Facultad de
Ingenierı́a Agro-Industrial, Universidad de la Sabana. 76 p.
Rodrı́guez-Sanoja R, Morlon-Guyot J, Jore J, Pintado J, Juge N, Guyot JP.
2000.Compararive characterization of complete and truncated forms of
Lactobacillus amylovorus α-amylase and role of the C-terminal direct repeats
in raw-starch binding. Appl Environ Microbiol 66(8):3350–6.
Rossi C. 2010. Produzione di un latte fermentato funzionale con attività
ACE inibitoria “in vitro” [Thesis]. Teramo, Italy: Università degli Studi di
Teramo. 86 p.
Rusconi M, Conti A. 2010. Theobroma cacao L., the food of the Gods: a
scientific approach beyond myths and claims. Pharmacol Res 61:5–13.
Saltini R, Akkerman R, Frosch S. 2013. Optimizing chocolate production
through traceability: a review of the influence of farming practices on cocoa
bean quality. Food Contr 29(1):167–87.
Sandberg AS, Andersson H. 1988. Effect of dietary phytase on the digestion
of phytate in the stomach and small intestine of humans. J Nutr 118:
469–73.
Schultes RE. 1984. Amazonian cultigens and their northward and westward
migrations in pre-Columbian times. In: Stone D, editor. Pre-Columbian
plant migration. Papers of the Peabody Museum of Archaeology and
Ethnology. Vol 76: Cambridge: Harvard Univ. Press. pp 69–83.
Schwan RF. 1998. Cocoa fermentations conducted with a defined microbial
cocktail inoculum. Appl Environ Microbiol 64:1477–83.
Schwan RF, Wheals AE. 2004. The microbiology of cocoa fermentation and
its role in chocolate quality. Crit Rev Food Sci Nut 44(4):205–21.
Scussel VM. 2004. Aflatoxin and food safety: recent South American
perspectives. Toxins Rev 23(2–3):179–216.
Serio A, Paparella A, Chaves-Lopez C, Corsetti A, Suzzi G. 2007.
Enterococcus populations in pecorino Abruzzese cheese: biodiversity and
safety aspects. J Food Prot 70(7):1561–8.
Serna-Isaza A. 1976. El guarapo: análisis socioeconómico corregimiento de
San Lorenzo-Parcialidad indı́gena de Cañamomo y Lomaprieta,
Riosucio-Caldas. Bogotá: Universidad de Los Andes. 113 p.
Simanca M, Arteaga M, Pérez-Soto M, Salcedo J. 2010. Characterization and
study of spontaneous fermentation of fermented milk product (suero
costeño) produced in Monteria. Revista MVZ Córdoba 15(1):
1944–53.
Simango C. 1997. Potential use of traditional fermented foods for weaning in
Zimbawe. Soc Sci Med 44:1065–8.
Colombian fermented foods and beverages . . .
Soni SK, Sandhu DH. 1991. Role of yeast domination in Indian idli batter
fermentation. World J Microbiol Biotechnol 7:505–7.
Steinkraus KH. 1997. Bio-enrichment: production of vitamins in fermented
foods. In: Wood BJB, editor. Microbiology of fermented foods. New York:
Thomson Science. pp 603–21.
Steinkraus KH. 2006. Fermentations in world food processing. Compreh
Rev Food Sci Food Safety 1(1):23–32.
Stratton SS, Hutkins RW, Taylor SL. 1991. Biogenic amines in cheese and
other fermented foods: a review. J Food Prot 54:460–70.
Thompson SS, Miller KB, López AS. 2007. Cocoa and coffee. In: Doyle
MP, Beuchat LR, Montville TJ, editors. Food microbiology fundamentals
and frontiers. Washington: ASM Press. pp 837–50.
Tinoco HA, Ospina DY. 2010. Análisis del proceso de deshidratación de
cacao para la disminución del tiempo de secado. Revista EIA
3:53–63.
Trindade RC, Resende MA, Silva CM, Rosa CA. 2002. Yeasts associated
with fresh and frozen pulps of Brazilian tropical fruits system. Appl.
Microbiol 25:294–300.
Tylleskar T, Banea M.Bikangi N, Cooke R, Poulter N, Rosaling H. 1992.
Cassava cyanogens and konzo, an upper motor neuron disease found in
Africa. Lancet 339:208–11.
Uchida K, Hirata M, Motoshima H, Urashima T, Ara I. 2007. Microbiota of
‘airag’, ‘tarag’ and other kinds of fermented dairy products from nomad in
Mongolia. Anim Sci J 78(6):650–8.
Vanegas IAC, Yepes MDS, Duque MCR. 2003. Búsqueda de cepas
Colombiana de levaduras productoras de xilitol. Facultad de Ciencias
Agropecuarias 28(2):27–32.
Vanegas-Gamboa DC, Betancourt-Botero DP, Ramı́rez-Toro CMS, Bolı́var
G. 2009. Research of the inhibitory capacity of lactic acid bacteria isolated
from corn sourdough. III Simposio Internacional de Bacterias Lácticas.
September 15–17, 2009, Tucumán, Argentina. 155 p.
Vargas-Aguilar P. 2010. Obtención de almidón fermentado a partir de yuca
(Manihot esculenta Crantz) variedad valencia, factibilidad de uso en productos
de panaderı́a. Tecnol Marcha 23(3):15–23.
1048 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014
Vatanasuchart N, Naivikul O, Charoenrein S, Sriroth K. 2005. Molecular
properties of cassava starch modified with different UV irradiations to
enhance baking expansion. Carb Pol 61(1):80–7.
Ventura M, Margolles A, Turroni F, Zomer A, de los Reyes-Gavilan C, van
Sinder D. 2011. Stress responses of Bifidobacteria. In: Tsakalidou E,
Papadimitriou E, editors. Stress responses of lactic acid bacteria. New York:
Springer. pp 323–47.
Villada HS, Narváez EA, Acosta H. 2011. Elaboración, caracterización y
envejecimento de almidón termoplástico agrio de yuca extruido. Alimentos
Hoy 12(12):1–22.
Vinderola G, de los Reyes-Gavilán C, Reinheimer J. 2009. Probiotics and
prebiotics in fermented dairy products. In: Ribeiro CP, Passos ML, editors.
Contemporary food engineering. New York: CRC Press and Taylor &
Francis Group. pp 601–34.
Wang J, Chen X, Liu W, Yang M, Airidengcaicike, Zhang H. 2008.
Identification of Lactobacillus from koumiss by conventional and molecular
methods. Eur Food Res Technol 227:1555–61.
Wang J, Zhang H, Chen X, Chen Y, Menghebilige, Bao Q. 2012. Selection
of potential probiotic lactobacilli for cholesterol-lowering properties and
their effect on cholesterol metabolism in rats fed a high-lipid diet. J Dairy
Sci 95(4):1645–54.
Watanabe K, Fujimoto J, Sasamoto M, Dugersuren J, Tumursuh T,
Demberel S. 2008. Diversity of lactic acid bacteria and yeasts in airag and
tarag, traditional fermented milk products of Mongolia. World J Microbiol
Biotechnol 24:1313–25.
Wollgast J, Anklam E. 2000. Polyphenols in chocolate: is there a contribution
to human health? Food Res Int 33:449–59.
Xie Y, An H, Hao Y, Qin Q, Huang Y, Luo Y, Zhang L. 2011.
Characterization of an anti-Listeria bacteriocin produced by Lactobacillus
plantarum LB-B1 isolated from koumiss, a traditionally fermented dairy
product from China. Food Control 22(7):1027–31.
Zapata Bustamante S, Tamayo Tenorio A, Rojano AB. 2013. Efecto de la
fermentación sobre la actividad antioxidante de diferentes clones de cacao
colombiano. Rev Cubana Plant Med 18(3):391–404.

C 2014 Institute of Food Technologists®