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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. as raw material for the production of traditional fermented foods,
Due to its nutritional value and to the variety of sensory attributes, by using traditional manufacturing procedures. Although some
it became popular in many cultures in which even today fermented fermented foods and beverages are industrially produced, many are
foods are part of the daily intake. In fact, fermentation is a rel- from household production for daily domestic consumption, and
atively cost-effective, low-energy preservation process, which is even today some tribes produce fermented beverages as stimulant
essential to ensure food shelf-life and safety (Liu and others 2011). and for medical purpose.
Moreover, it remains the major technology for important food Since pre-Hispanic times, fermented products from maize (Zea
production, even though other manufacturing technologies are mais), cacao (Theobroma cacao), and cassava (Manihot esculenta) have
available nowadays (Plessas and others 2011). been the most widely used products in Colombia, and indigenous
In traditional fermented products, the process of fermentation populations developed and established processes for transforming
is spontaneous and uncontrolled. The products are often obtained them into different types of products that are produced even today
under local climatic conditions, and therefore the sensory charac- (Lorence-Quiñones and others 1999), although microbial and en-
teristics and the quality are variable. In addition, as indicated by zymatic processes involved in food manufacturing have not been
Simango (1997), fermentation provides a natural way to reduce completely elucidated until now. Actually, progress in fermenta-
the volume of the material to be transported, to destroy undesir- tion technology could provide interesting opportunities to solve
able components, to enhance the nutritive value and appearance the problem of food safety and malnutrition in some countries
of the food, to reduce the energy required for cooking, as well as where poverty, malnutrition, and infant mortality are widely seen
to make a safer product. (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
MS 20140460 Submitted 3/20/2014, Accepted 6/11/2014. Authors Chaves- ferment different raw materials: nutrient-rich crops (cereals and
López, Serio, and Paparella are with Faculty of Bioscience and Technology for Food, roots), sugar cane, palm sap, cocoa, and animal products (milk).
Agriculture and Environment, Univ. of Teramo, Via C.R. Lerici, 1, 64023 Mosciano
Stazione, Italy. Authors Chaves-López, Grande-Tovar, Cuervo-Mullet, and Delgado- In detail, the main microbiological and nutritional properties of
Ospina are with Grupo de Biotecnologia Universidad de San Buenaventura Sede Cali, fermented foods, as well as the technological improvements that
Avenida 10 de Mayo, La Umbrı́a, Vı́a a Pance, Colombia. Direct inquiries to author have been achieved in manufacturing, will be highlighted. Al-
Clemencia Chaves-López (E-mail: chaves@unite.it). 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 Cassava roots
all. For this reason, we will consider both beneficial and detrimen- Water
tal effects.
Washing
Cassava-Derived Products
Cassava or manioc is an American original crop, spread across
South America. According to an Indian legend, the aborigines Crushing
were able to eliminate the poison from this root, make it edible
when cooked, and therefore cassava symbolizes the conversion of Water
death into life. Although cassava roots are rich in calories, they Sieving Cassava bran
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-
Drying Sedimentation (6-24 hours)
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, Fermentation
and saponins that can reduce nutrient bioavailability (Montagnac (20-30 days environmental
and others 2009).
The presence of HCN (also called hydrogen cyanide and for-
merly Prussic acid) ranges from 150 to 1000 mg/kg (Acosta- Sun drying (8-10 hours)
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- Storage Storage
cially if grown in nutrient-poor areas, and “sweet cassava,” which
has lower amounts of these glycosides, which are located primar- Native starch Sour starch
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 Figure 1–Schematic diagram of the traditional process for Colombian
cassava starch production.
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 between 3.5 and 4.0. In some areas, especially those with warm
depends on body weight and is considered to be between 30 and climates, the fermentation tanks are buried to maintain a constant
210 mg (Tylleskar and others 1992). temperature.
In Colombia, cassava is mainly used for the production of starch Natural fermentation is characterized by a succession of mi-
and its extraction is carried out since ancient times; today the croorganisms (Figueroa and others 1995; Ampe and others 2001)
extraction is a business that began about 6 decades ago, principally in which the predominant microbial groups are lactic acid bacteria
in Southwest Colombia, in places known as “rallanderı́as.” (LAB) (108 to 109 log CFU/g) and yeasts (101 to 104 log CFU/g)
Either a chemical or an enzymatic process can be used to extract (Cadena and others 2006). In Colombian sour starch, a large di-
cassava starch. This starch is appreciated in the food, paper, textile, versity of LAB species, and namely Lactobacillus manihotivorans and
adhesive, and pharmaceutical industries, but it must be modified L. plantarum (the most frequent species), L. casei, L. hilgardii, L.
to reduce its toxicity due to the presence of cyanogenic substances. buchneri, L. fermentum, Leuconostoc mesenteroides, and Pediococcus spp.,
Most modifications occur in the starch granule by means of phys- have been reported (Ben Omar and others 2000). Several strains
ical, chemical, and enzymatic processes, which cause changes at of these species have been shown to have high amylolytic activity
the molecular level, affecting its swelling ability, bonding power, thus they have an ecological advantage in fermented sour cas-
fluidity, pH, and temperature stability (Vargas-Aguilar 2010). sava as they can partially hydrolyze raw starch (Rodriguez-Sanoja
and others 2000) to provide sugars such as glucose or maltose
Sour Starch that can be used as an energy source by other microorganisms.
The fermented sour starch of cassava known as “Almidón agrio” is While L. manihotivorans is present only during the 1st period of
obtained by starch fermentation before drying. This 2-step process fermentation, when it may participate in accelerating the rate of
is important to obtain a sour starch of high quality, expressed as degrading starch (Ampe and others 2001), L. plantarum, is present
bread-making potential (BMP) (Laurent 1992). In fact, it has been during all the steps of the fermentative process and contribute
reported that BMP increases from 2 cm3 /g to at least 5 cm3 /g in to acidify the substrate. By using denaturing gradient gel elec-
4 h of sun-drying (Larsonneur 1993). trophoresis (DGGE) followed by 16S rDNA sequencing, close
To produce fermented sour starch of cassava (Figure 1), the relatives of Lactococcus lactis, Streptococcus spp., Bifidobacterium mini-
roots are washed to remove all foreign matter and grit or coating. mum, and Enterococcus saccharolyticus were detected during Colom-
Subsequently, they should be grated to obtain a dough containing bian cassava starch fermentation (Ampe and others 2001). The
the starch, which is washed, filtered, and decanted into open set- last 2 species, which were found in high quantities, might be a
tling tanks. The starch precipitates and is introduced into closed sign of fecal contamination of the water used to wash cassava.
containers under anaerobic conditions to carry out a natural fer- Although Ampe and others (2001) suggested that these species
mentation process for a long period (approximately 20 to 30 d, do not participate in spontaneous lactic acid fermentation, the
depending on climatic conditions), with the final pH ranging large arsenal of Bifidobacterium genes involved in the breakdown

1032 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014 
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Colombian fermented foods and beverages . . .

of carbohydrates (for example, fructo-oligosaccharides, gluco- Table 1–Some characteristics of the native and sour starch of Colombian
oligosaccharides, xylo-oligosaccharides, lactulose, and raffinose) cassava.
(Ventura and others 2011) may suggest a possible role of this genus Cadena and others (2006) Villada and others (2011)
in starch fermentation. Moreover, although the relevance and spe- Native starch Sour starch Native starch Sour starch
cific role of E. saccharolyticus in cassava fermentation remains to be
R.H. (%) 12.10 10.73 8.5 7.9
defined, Enterococcus spp. could contribute to the development of Lipids (%) 0.27 0.33 0.31 0.22
the sensory characteristics during fermentation. Ash (%) 0.42 0.37 0.15 0.15
The yeast role in cassava starch fermentation is poorly under- Fiber (%) 0.45 0.61 0.55 0.55
Proteins (%) 0.84 0.98 0.60 0.62
stood. Some authors suggested that yeasts growth depends on Lactic acid (%) 0.11 0.72 0.11 0.72
the degradation of cassava starch by other organisms (Lacerda pH 5.52 3.85 5.9 3.3
and others 2005), while others suggested that yeasts contribute R.H., relative humidity.
to starch hydrolysis, as well as to the production of enzymes
such as linamarase and polygalacturonase, and aldehydes and es- This microbial activity is crucial for undernutrition control in in-
ters that impart a pleasant aroma to the final product (Oyewole fants and adults, since “almidón agrio” serves as a staple food in
and Odunfa 1990; Oyewole 2001). In Brazilian cassava fermenta- many local communities.
tion, the presence of Galactomyces geotrichum, Issatchenkia spp., and As seen in Table 1, after fermentation the pH of cassava starch
a Candida ethanolica-like species throughout the process has been decreases below 4.0, with variations depending either on the fer-
documented (Larsonneur and others 1999; Lacerda and others mentation type or on manufacturing conditions. The process is
2005). Geotrichum candidum, the anamorph of G. geotrichum, is an characterized by an increase of both lactic acid and protein con-
oxidative species, and only a few strains with amylase activity have tent, due to microbial biomass. The microbiota present in the
been reported by Arotupin (2007). The presence of Issatchenkia spp. fermenting medium converts starch and sugars into organic acids
and a C. ethanolica-like species in advanced stages of the process (particularly acetic, propionic, succinic, and valeric acids), which
suggested a higher acid tolerance of these yeasts (Halm and others impart the characteristic odor and taste to the different fermented
2004). products (Rincón-Suárez and Villamil-Novoa 2005). Although
In Colombian rallanderı́as, the water used in a previous fermen- lactic acid is one of the common acids reported in almost all types
tation is used as inoculum for successive fermentations. According of fermentation, many short-chain and long-chain fatty acids, es-
to Kimaryo and others (2000), inoculation of cassava with one or ters, and aldehydes could be detected (Moorthy 1998). From the
several selected LAB species or strains would provide improved technological point of view, it is important to underline that after
fermentation control and better product quality. Also, the use of fermentation sour starch is sun-dried to obtain a stable product
Aspergillus niger gives good characteristics to cassava starch during with 10% to 25% moisture content (Brabet and Dufour 1996).
fermentation (Quintero and others 2012). Upon completion of the drying process, the starch in the form of
Fermentation of cassava root flour enhances its nutrient con- dough is ground and sifted through sieves of pore size between
tent through the biosynthesis of vitamins, essential amino acids, 100 and 120 US mesh, to form a fine powder. Lactic acidification
and proteins, (improving protein quality), and fiber digestibility. together with sufficient UV energy resulted in partial depoly-
It also enhances micronutrient bioavailability and helps degrade merization of the cassava starch molecules, which provided small
antinutritional factors (Achinewhu and others 1998). In fact, hy- linear fragments and facilitated formation of radicals that will help
drolysis of cyanogenic glucosides partially increases during cassava cross-linking of the remaining starch molecules, due to their high
root fermentation by the action of both endogenous linamarase activity, forming a 3-dimensional network that results in the un-
and linamarase produced by LAB, notably Leuconostoc mesenteroides usual baking expansion properties of fermented sour starch during
and Lactococcus lactis (Kobawila and others 2005). It is to under- baking (Dufour 1995; Vatanasuchart and others 2005). Moreover,
line that during sour starch production, from 40% to 70% of the after sun-drying, linamarase activity is higher, with a degradation
cyanide content is released in the water used to wash cassava, while of 60% of the cyanogen content (Gómez and Valdivieso 1984).
5% to 10% is present in the cassava bran that is usually used for It has been shown that sweet, sour, and acid-treated starches
animal feed, and finally about 4% is reduced after fermentation are different in molecular weight and in surface appearance under
and sun-drying to less than 1% (1 to 5 ppm) (Arguedas and Cooke scanning electron microscopy. In fact, while native starch gran-
1982). On the other hand, it has been reported that unfermented ules have a smooth and homogeneous surface, fermented starch
cassava flour from medium-cyanide content variety had a sig- granules are partially broken and the surface is rougher (Putri and
nificantly higher (P < 0.05) phytate content in comparison with others 2011), due to the action of microbial metabolites during
low-cyanide content variety (Oboh and Elusiyan 2007). However, fermentation. Although sour starch gelatinization properties are
cassava root fermentation minimizes the antinutritional value of not much affected by fermentation, the physical characteristics of
phytate; as it can interact with multivalent cations and/or proteins, the starch granules can modify the thermo-mechanical properties
forming insoluble complexes, which impair the bioavailability of of the dough, with noticeable effects on the baking properties
many essential minerals. Therefore the presence of phytates in (Mestres and Rouau 1997; Putri and others 2011). In the Colom-
foods is a concern (Cheryan and Rackis 1980; Marfo and others bian baking industry, this starch is sought for the manufacture of
1990; Hellström and others 2010). In particular, it affects zinc pandebono, pandeyuca, and snacks, due to its typical flavor and
homeostasis and may change the bioavailability of other essential texture (Montoya-Henao 2007).
minerals (Pariza and others 2000). However, cassava mash fermen-
tation significantly decreases phytate content. Microbial species Maize-Derived Products
such as Saccharomyces cerevisiae, Issatchenkia orientalis, Hanseniaspora The main food contributors to daily diet in Latin American
guilliermondii, Lactobacillus pentosus, and Rhizopus oryzae are effec- countries are represented by cereals. Although the effects of glob-
tive in reducing the phytate content of cassava (Oboh and Elusiyan alization and urbanization have influenced dietary patterns and
2007; Montagnac and others 2009; Hellström and others 2010). lifestyle, maize is still widely consumed (Bermudez and Tucker


C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1033
Colombian fermented foods and beverages . . .

2003). Maize is the most widely consumed cereal in Colombia water and rolled into a ball of appropriate size. Then the balls
and is an excellent source of metabolizable energy, while the are subjected to a prefermentation process that is an essential step
protein content is both quantitatively and qualitatively poor. In in the ancestral chicha; in this phase, starch is hydrolyzed by either
particular, the content in tryptophan and lysine is low. Moreover, amylases generated during the malting (germination) of maize ker-
maize contains antinutritional factors such as phytates, condensed nels or by the chewing/salivation process, which utilizes salivary
tannins, α-amylase, and trypsin inhibitors as well as lectins (Ejigui amylase (diastase) for the conversion of starch to fermentable sug-
and others 2005). In particular, phytate is the major storage form ars (Escobar and others 1993). The pot is then filled with water
of phosphorus in mature grains and legumes (Kumar and others and boiled for 2 or 3 h; after cooling, the product is pressed and
2010), and only animals possessing intestinal phytases or microbial filtered, and the filtrate thus obtained is allowed to ferment for
populations able to degrade it can utilize phosphorus in this form 2 or 6 d, depending on temperature. Before fermentation, cane
(Holm and others 2002); therefore, the phytate–mineral complex molasses may be added to increase sweetness and alcohol content.
is not hydrolyzable in the human gut (Sandberg and Andersson The beverage is ready for consumption when the sweetness disap-
1988). As large amounts of iron and zinc are required during pears and the taste becomes semisharp. Steinkraus (1997) reported
early life due to accelerated growth (Dallman 1992), the inter- that chicha is also rich in B vitamins, with a doubled riboflavine
actions between phytate and minerals have important nutritional concentration, while thiamine and niacin remain fairly constant.
implications. From the microbiological point of view, chicha fermentation
To improve storage possibilities and increase product value, dif- is a spontaneous process carried out by natural microflora at
ferent traditional processes based on spontaneous fermentations room temperature, and particularly by yeasts. The role of yeasts in
have been developed over time. Fermentation boosts the nutri- Colombian chicha fermentation needs additional research, to eval-
tional value of maize-derived products by increasing the content uate their possible impact on starch degradation, aroma, and free
of nutrients that are deficient in maize, such as vitamin A, vitamin amino acid production. Different species of yeasts, bacteria, and
B12, and the amino acids arginine and methionine (Steinkraus molds are present in Colombian chicha. Steinkraus (1997) reported
1997; Chelule and others 2010). Fermentation has been ascribed that S. cerevisiae, S. pastorianus, Mycoderma vini, Oidium lactis, and
as a potential way to reduce the risk of mineral deficiency among Monilia candida as well as bacteria of the genera Leuconostoc, Lac-
populations, especially in developing countries where unrefined tobacillus, Acetobacter, and various molds including Aspergillus and
cereals and/or pulses are highly consumed (Kumar and others Penicillium are present and presumably active. The major function
2010). of Leuconostoc and Lactobacillus species is to reduce pH (3.5 to 4.6)
Three principal fermented maize-based products are consumed by means of amylolytic enzymes. Some yeasts also contribute to
in Colombia: chicha, champús, and masa agria. In spite of the dif- the degradation of starch, which cannot be carried out by LAB,
ferent manufacturing procedures, a stable co-metabolism between and produce carbon dioxide that plays a significant role in effer-
LAB and yeasts exists in the fermentation of maize products, as in vescence. Moreover, yeasts produce other volatile compounds that
many cereal fermented products. contribute to the sensory attributes of chicha.
The microbiota involved in Colombian chicha can be different
Chicha depending on environment, fermentation vessels, as well as other
Chicha is a traditional alcoholic beverage produced in Colom- factors such as type of prefermention process. Recently, the yeast
bia and other South American countries such as Ecuador, Peru, population in chicha at the end of fermentation has been isolated
and Bolivia. Since pre-Hispanic times, beer or chicha made pri- and identified (Cuervo-Mulet 2013, unpublished data). The iden-
marily from maize, but also from other grains or fruits, has been tification based on the sequencing of 5.8-ITS, rDNA, and D1/D2
a source of refreshment and nutrition, as well as a key element domains of the 26S rDNA, suggested that ancient chicha made with
in social, political, and ritual exchanges (Hayashida 2008; Ramos the salivation process, harbored a wider variety of species that can
2011). Moreover, this drink was used during celebrations in the be divided in 2 main categories: (1) oxidative or weakly fermen-
planting season to predict harvest success. Today, its use is com- tative yeasts such as Candida spp. (the most frequent genus), Pichia
mon among Indians and peasants in many regions, who use spp., Hanseniaspora uvarum, and Issatchenkia spp., which might in-
it to quench thirst and prepare it with corn, its original base, fluence the chicha aroma with the production of esters, aldehydes,
or other products such as cassava (manioc) or fresh fruit like and ketons; and (2) strongly fermentative yeasts such as Wicker-
pineapple. hamomyces anomalus (formerly Pichia anomala) and S. cerevisiae that
Chicha is still consumed in many areas of Colombia on holidays contribute largely to ethanol and carbon dioxide production, as
and as a ceremonial beverage for the Indian population. The main well as to the flavor and the preservation of the final product. Seven
festivities of the community, when Chicha is consumed, are wed- different Candida species were identified (Table 2): C. oleophila, C.
dings and great “mingas,” which are community work occasions spandovensis, C. parapsilosis, C. sergipensis, C. ethanolica, C. pomicola,
aimed at improving the village infrastructures that usually culmi- and C. railenensis. The genus Candida is an extremely heteroge-
nate with dancing (Nullvalue 2003; Mincanquer-Cuatı́n 2007). nous group of yeasts, which is commonly associated with plants,
Chicha manufacturing is generally performed as a social event rotting vegetation, insects that feed on plants, or different foods
by groups of old women, sometimes with the help of young and beverages (Laitila and others 2006). While the presence of
girls, though the contexts, meanings, and technologies of brewing human-associated species such as C. parapsilosis is the possible evi-
have undergone challenges and changes throughout time (Ramos dence of human saliva used to hydrolyze corn starch, other species
2011). This beverage has an alcohol content of 2% to 12%, v/v. derive from different flavoring substrates such as fruits. In par-
Although new techniques are available for chicha manufacturing, ticular, C. oleophila is widely distributed on fruits (Glushakova
the old traditional process still exists in some Indian populations. and others 2007) and produces lytic enzymes such as 1,3-β-
As reported by Lorence-Quiñones and others (1999), in the glucanase, chitinase, and protease (Bar-Shimon and others 2004).
manufacturing process (Figure 2), corn grains are ground using Moreover, C. sergipensis that produces high percentages of alcohol
a mortar to produce a corn meal that is slightly moistened with in grape must (de Melo and others 2007), and its sister species

1034 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014 
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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


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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 Harvest of ripe pods
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
Storage of pods for 0-10 days
fermentation, during juice-cane fermentation a succession of yeast
species takes place, with a high presence of non-Saccharomyces yeasts
(environmental temperature)
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 Pod opening and wet bean removal
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 Fermentation (4-7 days)
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 Sun Drying artificial Drying
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. Storage
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 cacao
108 CFU/mL.
The chemical composition of Guarapo also includes organic acid
salts, polysaccharides, proteins, minerals, and other compounds Figure 6–Traditional proccesing of cacao production.
(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 Cacao beans contain a significant amount of fat (40% to 50%)
alcohols, acids, and other valuable and interesting compounds, and polyphenols (about 12% to 18% of the dry weight of grain),
which are produced during fermentation. There is a concern re- and particularly catechins or flavan-3-ols (37%), anthocyanins
lated to its consumption in high quantities and for long periods, as (4%), and proanthocyanidins (58%), and also protein (13% to 16%)
this beverage has been associated with the development of hepatic and the methylxanthines theobromine and caffeine, which both
cirrhosis positively be related to the presence of the ethanol. 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).
Cacao The process to obtain cacao beans in Colombia is summarized
Theobroma cacao L. is a tree native to tropical rainforests, on this in Figure 6. After opening the cacao pods at the plantation, the
continent extending from the Amazonian basin of South Amer- collected fresh cacao pulp-bean mass undergoes a spontaneous
ica to southern Mexico. According to some authors, the place of fermentation for several days (2 to 7 d) depending on: (1) variety of
origin of cacao trees was the Upper Amazon near the Colombian– cacao plant, (2) climate, (3) local practices of fermentation which
Ecuadorian border, on the eastern flanks of the Andes (Cheesman include heaps, wooden fermentation boxes, canoes made of thick
1944; Schultes 1984; Motamayor and others 2002). It was brought tree trunks called “pozuelos,” barrels, or baskets, (4) frequency
to Mesoamerica by early humans, and the use and domestication of bean mixing or turning, (5) volume of cocoa to ferment, (6)
of this crop may have started 4000 y ago (Powis and others 2011). maturity and the sanitary condition of the beans (Schwan 1998;
Ecological conditions vary greatly in Colombia, and the cacao- Cubillos and others 2008; Ortiz de Bertorelli and others 2009;
growing regions are very scattered through its territory, and the Moreira and others 2013; Zapata Bustamante and others 2013).
wide variety of microclimates around the country leads to co- Traditionally, in all types of fermentation the mass of fermenting
coa production with high variability in its chemical composition beans is usually covered with jute or sisal bags.
(Carrillo and others 2014). During fermentation, important changes take place, which are
Although the use of cacao in Colombia is mainly to produce essential for the development of the characteristic future cocoa and
chocolate, some Colombian tribes eat the pulp surrounding cacao chocolate flavors: (a) detachment of the mucilage that surrounds
beans and also make an alcoholic beverage from it, and occasionally the bean to facilitate preservation; (b) death of the embryo that
vinegar (Patiño-Rodriguez 2002). Even today, Colombians like to prevents germination; and (c) a chain of biochemical reactions
partake of a hot sweet chocolate beverage first thing in the morning inside the beans, which generate a volume increase and a char-
and late at night, especially in cold mountain climates. acteristic color change (Barros 1981; Schwan and Wheals 2004).
Moreover, in the last few years cacao by-products such as bean These processes are crucial for the development of the sensory
husk have been proposed to be used in the biocontrol of Bacillus quality of cocoa beans. Aroma and flavor profiles develop predom-
cereus and Streptococcus agalactiae (Cuéllar and Guerrero 2012) and inantly during drying and fermentation but also the later roasting
the mucilage to be used for the clarification of cane juice (Pérez impacts flavor via the Maillard reaction. In general, soil composi-
Echeverry 2004). tion, climatic conditions, and primarily farming practices are other


C 2014 Institute of Food Technologists® Vol. 13, 2014 r Comprehensive Reviews in Food Science and Food Safety 1039
Colombian fermented foods and beverages . . .

fundamental factors that ensure the special chocolate aroma and by Dillinger and others (2000), in a complete review of the in-
flavor (Federacion Nacional de Cacaoteros Colombianos 2004). digenous, colonial era and, early modern period uses of cocoa
It is well known that the microorganisms involved in cocoa or chocolate, their use for medicinal purposes was already docu-
fermentation carry out their activity in a well-defined temporal mented by the Florentine Codex (1590), which describes the life
succession (Figure 7). The pulp of cacao beans has a high sugar and culture of Aztecs. In Europe and New Spain from the 16th to
content, low pH (close to 3.5), and a limited oxygen concen- the early 20th century, more than 100 medicinal uses were known
tration. These conditions favor the growth of yeasts that degrade for cocoa and/or chocolate.
pectin, ferment glucose and fructose with the consequent accumu- The beneficial effects on human health of some functional ca-
lation of ethanol (5 to 60 mg/g), acids (especially acetic acid), and cao constituents have been reported in the scientific literature,
secondary products (including, organic acid, aldehydes, ketones, particularly in relationship with the high content of monomeric
higher alcohols, esters) that together with glycosidase production (epicatechin and catechin) and oligomeric (procyanidins) flavanols
are likely to be significant and should affect the beans and chocolate (Rusconi and Conti 2010). Recently, some epidemiological stud-
quality (Ardhana and Fleet 2003). ies have established an inverse correlation between flavonoid intake
Yeast growth and activity are essential for cocoa fermenta- and the appearance of chronic diseases, such as cardiovascular and
tion and development of chocolate characteristics (Ho and others cerebrovascular diseases, cancer, and other disorders including di-
2014). Fungal contribution to fermentation is restricted to the abetes and rheumatoid arthritis (Wollgast and Anklam 2000; Oth-
first 36 h of fermentation, because the increasing temperature man and others 2007). The main flavan-3-ol compounds present in
and ethanol concentration of the bean mass act as limiting factors cacao are the monomers catechin and epicatechin, and the dimer
(Ardhana and Fleet 2003). Fungi can hydrolyze the pulp, produce procyanidin B2 (Lamuela-Raventós and others 2005). Although,
acids, and off flavors, and alter the taste of the cocoa beans (Schwan it can be suggested that the daily intake of flavonoids from mixed
and Wheals 2004), and some mold species can also produce my- food sources, together with the intake of small amounts polyphe-
cotoxins (Copetti and others 2011). nols from cocoa or chocolate (flavanols and procyanidins), could
Yeasts create anaerobic conditions that allow the growth of LAB, improve individual health status including potential efficient can-
which ferment sugars, produce lactic acid, and assimilate citric cer prevention with minimal toxicity (Martin and others 2013).
acid. The role of LAB and whether or not they are essential to the However, cancer preventive efficacy in humans remains to be de-
process is not clear (Ho and others 2014). Greater aeration of the cisively demonstrated.
mass, due to the disappearance of the mucilage and to the manual In a recent study on cacao beans from 11 different cacao-
practices, allow acetic acid bacteria (AAB) to grow and metab- growing areas of Colombia, a proportional relationship was
olize the substrate (Barel 1997), mainly by oxidation of ethanol pointed out between polyphenol content and changes in the al-
produced by yeasts into acetic acid, and further oxidation of the titude of plant crops. In particular, the authors suggested that the
latter to carbon dioxide and water (Schwan and Wheals 2004). lower is the altitude, the more polyphenols, flavan-3-ols, and epi-
Oxidation is a highly exothermic reaction (496 kJ by molecule of catechin are produced by the cacao plant (Carrillo and others
ethanol converted into acetic acid), which raises the temperature 2014).
to 50 °C (Lagunes-Gálvez and others 2007). It is believed that Although fermentation and drying are key points for the devel-
the conditions provoked by AAB are the cause of diffusion and opment of the typical cacao flavor, the same steps can harbor the
hydrolysis of proteins, and this suggests that AAB might play a key risk of mycotoxin formation, in particular ochatoxin A and afla-
role in the formation of flavor precursors (Saltini and others 2013). toxins. Moreover, the growth of xerophilic fungi during storage
The particular temperature conditions, in combination with can be considered a spoilage indicator at this stage (Copetti and
increased pH and aeration, favor the growth of aerobic spore- others 2011). In the last several years, in Colombia, an increas-
forming Bacillus spp. (Thompson and others 2007). A study con- ing effort in the implementation of traceability systems has been
ducted with 2 clones grown in Colombia, ICS 60 and TSH 565, made to enhance product quality, maintain sensory acceptability,
highlighted that after 60 h of fermentation, temperature increased preserve bioactive compounds, and promote food safety.
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 Milk-Derived Products
Bacillus group in cocoa fermentation has not been fully clarified, In Colombia, the origins of dairy products date back to the
but Nielsen and others (2007) suggested that they may play a big- end of the 16th century, when the Spanish colonizers imported
ger role in box fermentation than in heap fermentation. Moreover, cattle and transmitted cheese manufacturing techniques to the
Ouattara and others (2008) suggested that pulp degradation dur- native population. Today’s fermented milk products can be either
ing cocoa fermentation is due to the action of enzymes produced industrial or homemade, and their manufacturing is still a complex
either by yeasts and Bacillus species or strains. procedure, which combines science and tradition.
The drying process of cacao reduces acidity and astringency, and
it decreases volatile compounds (Afoakwa and others 2008). This Kumis
process is performed by sunlight or artificially under controlled Kumis is fermented cow milk, widely consumed in rural and ur-
temperature, which should not exceed 60 °C. Although the great ban areas in the Colombian southwest. A similar beverage (koumiss)
part of Colombian small farmers uses sunlight for drying, the is produced in Central Asia but there it is mainly made from un-
artificial drying predominates in large-scale operations (Espinal pasteurized fresh mares’ milk, and it is considered not only as an
and others 2005). As pointed out in recent publications, drying is essential food, but also as a medicinal remedy (Ishii and Konagaya
the most important unit operation that affects polyphenols such 2002).
as flavonoids and their antioxidant activity (Di Mattia and others As reported by Chaves-López and others (2011), to produce
2013). traditional kumis (Figure 8), raw whole milk is left fermenting for
The linkage between the consumption of cacao-derived prod- 2 or 3 d at room temperature. After fermentation, the pH ranges
ucts and health goes back many years. In fact, as pointed out between 3.9 and 4.5 and the alcohol content between 1% and 2%.

1040 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014 
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, antimicrobial activity of Colombian kumis has not been docu-
with sugar and cinnamon before serving it must be consumed mented yet, although an anti-Listeria bacteriocin produced by L.
within 3 d. plantarum LB-B1 isolated from Chinese koumiss has been charac-
Colombian traditional kumis has only been sparsely character- terized (Xie and others 2011).
ized microbiologically and biochemically. During manufacturing, The Colombian kumis microbiota is composed of distinct mi-
the main chemical changes through milk fermentation are lactic crobial groups, with a prevalence of LAB and yeasts, ranging from
acid production from lactose, and milk protein hydrolysis. Table 5 107 to 109 log CFU/mL and from 106 to 108 log CFU/mL,
highlights some of the most important chemical characteristics of respectively; Enterobacteriaceae were also found, although at low
the traditional Colombian kumis. The production of lactic and numbers (log 102 to 103 CFU/mL) (Chaves-López and others
acetic acids that contribute to the inhibition of pathogenic bacte- 2012). LAB and yeasts act in synergy to give the texture and taste
ria is due to an intense metabolic activity of the microbiota. The 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. the most potent ACE-inhibitory peptides (IC50 = 30.63 ± 1.11
μg/mL) and giving a product without bitter taste. Moreover, this
Compound Concentration
attribute was maintained during refrigerated storage for 7 d.
Ethanol (g/100 g) 2.51 ± 0.53
Lactic acid (g/100 g) 1.14 ± 0.46
On the other hand, it has recently been reported that fermen-
Acetic acid (g/100 g) 0.05 ± 0.01 tation of whole milk by selected kumis organisms can increase the
Citric acid (g/100 g) 0.53 ± 0.06 levels of conjugated linoleic acid (CLA) (C18:2c9t11), with values
Propionic acid (mg/100 g) 0.0044 ± 0.0012 ranging from 9.17 ± 0.70 to 22.62 ± 3.85 mg/g fat (Osorio and
Butyric acid (mg/100 g) 0.0089 ± 0.0017
Total peptides content (μg/mL) 252.23 ± 31.22 others 2011). The term “conjugated linoleic acid” (CLA) refers to
Total amino acid content (mM leucin/mL) 2.08 ± 0.12 a mixture of geometric and positional isomers of octadecadienoic
Adapted from Rossi (2010). 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-
peroxide, which contribute to reduce the number of some con- gle bonds, hence the term CLA (Pariza and others 2000). CLA
taminant bacteria, but they also release galactose that favors the is considered to possess potential health benefits such as anticar-
growth of non–lactose-fermenting yeasts. Moreover, LAB pos- cinogenic, antiatherogenic, antidiabetic, and antiadipogenic effects
sess a very complex proteolytic system that releases peptides and (Rainer and Heiss 2004; Panghyová and others 2006), in particular,
amino acids, leading to the particular aromatic profile and texture the cis-9 trans-11 isomer, the most abundant CLA, is considered to
of kumis. On the other hand, yeasts produce CO2 that gives the have anticarcinogenic properties (Ip and others 1995). The scien-
particular effervescence, contribute to product aroma by means tific literature mentioned may provide evidence for the beneficial
of lypolitic and proteolytic activities, and enhance LAB growth effects of Colombian kumis, especially on cardiovascular health.
through amino acids and vitamin production. Moreover, Mazo and Arias (2006) evaluated the efficacy of kumis
As shown in Table 6, different species of LAB and yeasts were in acute undernourished children, and they found a higher and
isolated from Colombian kumis and Asian koumiss. The differ- faster weight gain and a reduction of the frequency and duration
ences are related to: (1) the environmental conditions during of episodes of diarrhea.
milk fermentation which select the species; (2) milk composition, Although the production of the above-mentioned compounds
mainly fat, protein, and lactose contents; (3) different procedures and other antimicrobial components during fermentation may
of the process; and (4) changes during continuous propagation promote consumer health or improve kumis safety and stabil-
that enable stable associations between some yeasts and bacterial ity, risks associated with other fermenting and contaminating
species. pathogenic microorganisms need to be explored. In particular,
During kumis production, proteolysis in the milk leads to the enterococci loads ranging from 4.2 to 8.3 log CFU/mL have
production of peptides that have been reported to have differ- been reported in Colombian kumis (Chaves-López and others
ent biological activities, some of which have been associated with 2011). The presence of these microorganisms as a consistent part
health-promoting properties (Vinderola and others 2009). The of the kumis microbiota could be a concern, as enterococci are
number, the potency, and the importance of bioactive compounds among the most common nosocomial pathogens, and they have
in fermented milk products are probably greater than previously been implicated as an important cause of endocarditis, bacteremia,
thought (Ebringer and others 2008). They include certain vita- and infections of the urinary tract, central nervous system, intra-
mins, specific proteins, bioactive peptides, oligosaccharides, or- abdominal and pelvic infections, as well as of multiple antibiotic
ganic (including fatty) acids. Some of them are normal milk com- resistances (Endtz and others 1999; Serio and others 2007). In
ponents, others emerge during fermentation or human digestive this context, Chaves-López and others (2011), reported that 42
processes. Although Asian koumiss has some beneficial influence out of 72 strains of enterococci isolated from 13 different ku-
on enhancing immunity, treating tuberculosis, and cardiovascu- mis samples were free of virulence factors, and 33 isolates har-
lar disease (Chen and others 2010; Wang and others 2012), and bored at least 1 gene, with esp gene encoding for enterococcal
in China the “koumiss therapy method” is used for the treat- surface protein, as the most frequent. However, it is important
ment of hepatitis, chronic ulcers, and tuberculosis (Liu and oth- to highlight that vancomycin resistance of the strains was very
ers 2011), the “healthy” properties of Colombian kumis are not limited.
claimed yet. However, peptides with up to 65% inhibitory activity Another important health issue can be the production of
against angiotensin converting enzyme (ACE) have been detected biogenic amines (BA), and in particular histamine and tyra-
in vitro (Chaves-López and others 2011). ACE plays a major role mine. The presence of these compounds can be particularly
in the regulation of blood pressure. In fact, within the renin– harmful for susceptible consumers, but it is often unavoidable
angiotensin system, ACE catalyzes the conversion of angiotensin I in fermented foods (Stratton and others 1991). In particular,
to angiotensin II, a potent vasoconstrictor (Riordan 2003), which tyramine, 2-phenylethylamine, and histamine can cause distress,
therefore also increases blood pressure. mainly due to the effects on nervous and vascular systems, which
Researchers have recognized the importance of formulated can be particularly severe in sensitive people or when the en-
starter culture in order to produce milk with bioactive compounds. zymes naturally involved in their detoxification (the amine ox-
In a recent study (Chaves-López and others 2014), cocultures of idases) are inhibited as by certain medications (Lanciotti and
selected microorganisms have been evaluated for the production others 2007). Data reported from Colombian kumis revealed
of fermented milk enriched with ACE inhibitory peptides. The very low values of total BA content, ranging from not de-
authors underlined the importance of choosing the strain com- tectable to 15.31 mg/L, with ethylamine, putrescine, cadaver-
binations carefully, in order to obtain a high yield of ACE in- ine, and spermidine being the only amines detected (Chaves-
hibitory activity without a bitter taste. In their study it was reported López and others 2011). Nevertheless, these levels are far below
that a co-culture of Pichia kudriavzevii, L. plantarum LAT3, and the limits that are recommended by health authorities in many
Enterococcus faecalis, was the most promising culture, producing countries.

1042 Comprehensive Reviews in Food Science and Food Safety r Vol. 13, 2014 
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 an effect on fermentation, with an increase during the first
along the Colombian Caribbean coast. Raw cow milk is fermented few hours of the process and maximum values from 2 to
in calabashes (the dried fruit of Lagenaria vulgaris) that are sealed 5 log CFU/mL at the end of the manufacturing process (Farelo De
and subsequently placed in a warm site, at an average temperature La Hoz 2002). In particular, the predominance of Candida krusei,
of 35 °C. Resident microbiota from the calabashes is a reservoir Torulopsis pintolopesii (Candida pintolopesii), Rhodotorula mucilaginosa,
microbial community transferred directly to suero costeño. The time Candida kefir, Candida glabrata, and S. cerevisiae has been reported
required for their manufacturing (1 to 3 d) depends on the desired (Farelo De La Hoz 2002; Cruz-Martı́nez 2006).
viscosity. During this period, a natural fermentation takes place The presence of Enterobacteriaceae has been reported at levels
and the pH decreases to near 4.6. Fermentation is characterized from 0.8 to 4.8 log CFU/mL (Cruz-Martı́nez 2006), and Staphylo-
by a liquid–solid 2-phase system, where the liquid part is called coccus aureus coagulase-positive was reported in 100% of 63 samples
lactosuero; the other one, known as suero, has a cream-like consis- collected in the Cordoba region (Northern Colombia) with levels
tence and desiderable sensory properties (Cueto-Vigil and others of 5 to 6 log CFU/mL (Chams and others 2012), implying poor
2010). Figure 8 illustrates 2 of the most common procedures used hygienic and manipulation conditions during the production pro-
for suero costeño production, where salt addition before or after cess and during storage of suero costeño.
fermentation is the main difference. After fermentation, suero costeño (thickness phase) is retrieved
During production, LAB and yeasts are involved and, as previ- from the calabashes, and NaCl (2% to 3%) is added to the product
ously mentioned about kumis, the complex interaction between packed in traditional containers. Differently from other Colom-
these 2 microbial groups and the differences in species as well bian fermented dairy products, Suero Costeño, it is salted to reach
as their balances, contribute to the product sensory attributes. NaCl concentrations from 1% to 3%, and it is commonly used as a
Cueto and others (2007) reported a succession of LAB during food dressing. Commercial suero costeño is classified on the basis of
fermentation, in which Lactobacillus paracasei, L. plantarum, and L. fat content as light, semilight, and fat, whereas homemade prod-
lactis were predominant at the beginning of the process with a ucts vary with respect to NaCl concentration, type of fermenting
load of 4.8 log CFU/mL; during the intermediate stage (5 to microbiota, and length time of fermentation. Table 7 reports the
8 h), LAB reached values of 5.5 log CFU/mL with L. paraca- main physico-chemical characteristics of suero costeño produced in
sei, subsp. paracasei, L. plantarum, L. lactis subsp. lactis, Leuconostoc various locations of northern Colombia. It is to underline that the
lactis subsp. lactis as predominant species. At the final stage (24 comparison of the aw values reported by Farelo De La Hoz (2002)
h), LAB reached values between 7 and 8 log CFU/mL, and a with other fresh cream cheese described in literature resulted un-
high portion of Lactobacillus species (such as: acidophilus, brevis, usual for this kind of product.
delbrueckii subsp. delbrueckii, paracasei subsp. paracasei, pentosus, The microbiota involved in suero costeño fermentation has been
rhamnosus, and plantarum) was dominant. Also, Enterococcus fae- evaluated for its antimicrobial and probiotic potential. In this
cium and E. durans were isolated at the end of the pro- 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) Simanca and others (2010)


Mean Min Max Mean Min Max
R.H. (%) 75.57 62.72 80.60 76.03 73.48 78.43
Fat (%) 10.0 4.5 16.5 n.r n.r n.r
Protein (%) 7.53 3.86 11.45 5.09 4.0 6.0
NaCl (%) 2.24 1.1 2.95 2.34 1.79 2.95
Acidity (%) 2.35 1.41 3.08 1.40 0.93 1.85
pH 3.72 3.41 3.97 3.94 3.52 4.39
aw 0.94 0.93 0.96 n.r n.r n.r
R.H., relative humidity; n.r, not reported.

antibacterial activity of strains of Lactobacillus fermentum, L. brevis, L. Conclusion


plantarum, L. rhamnosus, and L. lactis subsp. lactis against Escherichia This review is the 1st collection of scientific and technical data
coli and S. aureus. In addition, selected strains of L. fermentum on the quality and safety of various typical Colombian beverages
and L. rhamnosus showed good probiotic characteristics that might and foods. In our study, we have analyzed both beneficial and
be used for food or dairy fermentations (Acuña-Monsalve 2009). detrimental effects of these products, but most of all, we have
Thus, suero costeño may offer advantages as a carrier of probiotic pointed out the missing data and therefore future research needs.
microorganisms. The importance of these probiotic-containing We believe that the data reported on the functional potential, in
products, commonly regarded as functional foods, in the mainte- terms of antinutritional factor degradation, increase of mineral
nance of health and well-being is becoming a key factor affecting bioavailability, bioactive compounds, and increase of nutrient di-
consumer choice (Gardiner and others 1998). gestibility, could be useful to enhance the value of these products
Surprisingly, commercial suero costeño is not well accepted by and promote new applications in the food industry worldwide.
consumers, as it is different from the traditional product in flavor In fact, fermented Colombian foods and beverages might become
and overall taste. However, when inoculum derived from the tra- important sources of new valuable microbial strains for biotech-
ditional product is used to ferment pasteurized milk, the taste and nology.
texture are not significantly different from the traditional product
(Acevedo and others 2012). 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,
Summarizing Comments Raul Cuervo-Mulet prepared the literature overview concerning
In Colombian traditional fermented beverages and foods, fer- Chicha beverage, Johannes Delgado-Ospina performed the analy-
mentation is performed mainly by LAB and yeasts, which con- ses of microbiological and physicochemical characteristics of Masa
tribute to product preservation. In addition, these fermented prod- agria, Antonello Paparella contributed to manuscript revision. All
ucts contain ingredients and substances of microbial origin that authors read and approved the final manuscript.
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 References
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